Prof Paul Burgess

Prof Paul Burgess
Institute of Cognitive Neuroscience, UCL
17 Queen Square
London
WC1N 3AR
[email protected]
Tel: 0208 679 1139
Fax: 020 7813 2835
http://www.icn.ucl.ac.uk/StaffLists/MemberDetails.php?Title=Prof&FirstName=Paul&LastName=Burgess
Profile
Appointment
-
Professor of Cognitive Neuroscience
Institute of Cognitive Neuroscience
Div of Psychology & Lang Sciences
Faculty of Brain Sciences
Research Groups:
Research Themes
Executive Functions Group
Basic Life Sciences
Neuroscience
Research Summary
My interests lie in five overlapping areas. They all concern themselves with discovering the
role that the frontal lobes of the brain play in enabling us to decide what we want to achieve,
and then organise our behaviour to that end, often over long time periods. I am also interested
in how we can measure and treat executive function problems in people who have suffered
brain damage, and the neuropsychiatric sequelae of frontal lobe dysfunction.
1. The functions of rostral prefrontal cortex (Area 10)
My recent research is indicating a special role for a large part of the frontal lobes known as
Area 10 in many functions important to human cognition. Up until now, virtually nothing has
been known about the functions of this area, and my group is trying to discover what it is
there for and how it works. This is an especially exciting topic because so little is known: it is
likely that the next few years will see rapid scientific advance.
2. Functional organisation of the frontal lobe cognitive system
My group and I build and test information processing models of how the cognitive processes
supported (at least in part) by the frontal lobes work together to perform various functions.
The experiments I carry out vary from e.g. theoretical studies of simple inhibition or initiation
processes, to studies of complex behaviours in real life (e.g. shopping).
3. Memory control processes
I am interested in how people recall events that have happened to them, which is a very
complex process of reconstruction and memory for "source". One insight into how this
process operates is to look at what happens when it fails, and I study these mistakes both in
healthy people (e.g. Burgess and Shallice, 1996) and in neurological patients, where the
syndrome of gross memory errors is known as "confabulation."
4. Behavioural organisation
I carry out studies which aim to discover how we form plans, schedule our activities (known
as "multitasking"), remember to carry out intended actions after a delay ("prospective
memory") and assess the consequences of our actions. These use functional imaging (PET or
fMRI), human neuropsychology, and experimental psychology methods, as well as others (e.g.
verbal protocol analysis; individual differences; ageing; developmental studies).
5. Assessment and rehabilitation of executive function deficits
Deficits in executive functions may be devastating to someone's ability to cope with everyday
life, work and relationships. It is very important therefore that we can understand these
problems, measure them, and develop ways of helping people to overcome their deficits. I am
inventor or co-inventor of a number of neuropsychological tests of executive function which
are now used in clinics throughout the world (e.g. the Hayling and Brixton Tests; BADS
battery; Six Element Test; Multiple Errands Test) and have, through collaborations with my
clinical colleagues, a long-standing research interest in developing rehabilitation techniques.
6. Frontal lobe function and mental health.
I am interested in finding out the role that purturbation or atypical development of frontal lobe
structures might play in the presentation of psychiatric and psychosocial disorders such as
schizophrenia and autistic spectrum disorders (especially Asperger Syndrome).
Academic Background
1992 PhD
1983 BA Hons
Doctor of Philosophy – Neuropsychology
Bachelor of Arts (Honours) – Psychology
Institute of Neurology
University of Nottingham
Research Activities:






Biological influences on social competence, and neurodevelopmental disorders of social
cognition
Active
Cognitive heterogeneity in autism
Active
Cognitive neuroscience of executive functions
Active
Eating Disorders, in particular cognition, motivation and personality in anorexia nervosa
Active
Executive functions of the frontal lobes
Neural bases of human long-term memory
Active
Achievements
Title
Type
Organisation
Fellow
Fellow
British Psychological Society
Member
Member
IASSID (International Association for
the Scientific Study of Intellectual &
Developmental Disabailities)
President's Award for
Distinguished Contributions
to Psychological Knowledge
Award
British Psycholological Society
Member
Member
Experimental Psychology Society
Member
Member
Memory Disorders Research Society
Publications
Bolton, H. M., Burgess, P. W., Gilbert, S. J., & Serpell, L. (2014). Increased set shifting
costs in fasted healthy volunteers. PLoS One, 9 (7), e101946-?.
doi:10.1371/journal.pone.0101946
Volle, E., de Lacy Costello, A., Coates, L. M., McGuire, C., Towgood, K., Gilbert, S., . . .
Burgess, P. W. (2012). Dissociation between verbal response initiation and suppression
after prefrontal lesions. Cereb Cortex, 22 (10), 2428-2440. doi:10.1093/cercor/bhr322
Gilbert, S. J., Bird, G., Frith, C. D., & Burgess, P. W. (2012). Does "task difficulty" explain
"task-induced deactivation?". Front Psychol, 3, 125-?. doi:10.3389/fpsyg.2012.00125
Gonen-Yaacovi, G., & Burgess, P. W. (2012). PROSPECTIVE MEMORY: THE
FUTURE FOR FUTURE INTENTIONS. PSYCHOLOGICA BELGICA, 52 (2-3), 173-204.
Benoit, R. G., Gilbert, S. J., Frith, C. D., & Burgess, P. W. (2012). Rostral Prefrontal
Cortex and the Focus of Attention in Prospective Memory. CEREBRAL CORTEX, 22 (8),
1876-1886. doi:10.1093/cercor/bhr264
Castiel, M., Alderman, N., Jenkins, K., Knight, C., & Burgess, P. (2012). Use of the Multiple
Errands Test - Simplified Version in the assessment of suboptimal effort.
NEUROPSYCHOLOGICAL REHABILITATION, 22 (5), 734-751.
doi:10.1080/09602011.2012.686884
Benoit, R. G., Gilbert, S. J., & Burgess, P. W. (2011). A neural mechanism mediating the
impact of episodic prospection on farsighted decisions. J Neurosci, 31 (18), 6771-6779.
doi:10.1523/JNEUROSCI.6559-10.2011
Burgess, P. W. (2011). Frontopolar cortex: constraints for theorizing. Trends Cogn Sci, 15
(6), 242-?. doi:10.1016/j.tics.2011.04.006
Burgess, P. W., Gonen-Yaacovi, G., & Volle, E. (2011). Functional neuroimaging studies
of prospective memory: what have we learnt so far?. Neuropsychologia, 49 (8), 2246-2257.
doi:10.1016/j.neuropsychologia.2011.02.014
Okuda, J., Gilbert, S. J., Burgess, P. W., Frith, C. D., & Simons, J. S. (2011). Looking to the
future: Automatic regulation of attention between current performance and future
plans. NEUROPSYCHOLOGIA, 49 (8), 2258-2271.
doi:10.1016/j.neuropsychologia.2011.02.005
Burgess, P. W., Gonen-Yaacovi, G., & Volle, E. (2011). Rostral prefrontal cortex: What
neuroimaging can learn from human neuropsychology. In B. Levine, F. CRAIK (Eds.),
Mind and the frontal lobes (pp. 47-92). New York: USA: Oxford Univ Pr.
Volle, E., Gonen-Yaacovi, G., Costello, A. D. E. L., Gilbert, S. J., & Burgess, P. W. (2011).
The role of rostral prefrontal cortex in prospective memory: a voxel-based lesion study.
Neuropsychologia, 49 (8), 2185-2198. doi:10.1016/j.neuropsychologia.2011.02.045
Gilbert, S. J., Gonen-Yaacovi, G., Benoit, R. G., Volle, E., & Burgess, P. W. (2010). Distinct
functional connectivity associated with lateral versus medial rostral prefrontal cortex: a
meta-analysis. Neuroimage, 53 (4), 1359-1367. doi:10.1016/j.neuroimage.2010.07.032
Dumontheil, I., Gilbert, S. J., Burgess, P. W., & Otten, L. J. (2010). Neural correlates of
task and source switching: similar or different?. Biological Psychology, 83 (3), 239-249.
doi:10.1016/j.biopsycho.2010.01.008
Dumontheil, I., Gilbert, S. J., Frith, C. D., & Burgess, P. W. (2010). Recruitment of lateral
rostral prefrontal cortex in spontaneous and task-related thoughts. The Quarterly
Journal of Experimental Psychology, 69 (3), 1740-1756.
Benoit, R. G., Gilbert, S. J., Volle, E., & Burgess, P. W. (2010). When I think about me and
simulate you: medial rostral prefrontal cortex and self-referential processes. Neuroimage,
50 (3), 1340-1349.
Gilbert, S. J., Meuwese, J. D. I., Towgood, K. J., Frith, C. D., & Burgess, P. W. (2009).
Abnormal functional specialization within medial prefrontal cortex in high-functioning
autism: a multi-voxel similarity analysis. Brain, 132 (4), 869-878.
doi:10.1093/brain/awn365
Towgood, K. J., Meuwese, J. D., Gilbert, S. J., Turner, M. S., & Burgess, P. W. (2009).
Advantages of the multiple case series approach to the study of cognitive deficits in
autism spectrum disorder. Neuropsychologia, 47 (13), 2981-2988.
doi:10.1016/j.neuropsychologia.2009.06.028
John, J. P., Burgess, P. W., Yashavantha, B. S., Shakeel, M. K., Halahalli, H. N., & Jain, S.
(2009). Differential relationship of frontal pole and whole brain volumetric measures
with age in neuroleptic-naïve schizophrenia and healthy subjects. Schizophrenia Research,
109 (1-3), 148-158.
Dawson, D., R, A., N, D., Burgess, P., Cooper, E., Krpan, K., . . . D, T. (2009). Further
development of the Multiple Errands Test: standardized scoring, reliability, and
ecological validity for the Baycrest version. Archives of Physical Medicine and
Rehabilitation, 90 (11 Suppl 1), 41-51.
White, S., Burgess, P., & Hill, E. (2009). Impairments in 'open-ended' executive function
tests in autism. Autism Research, 2 (3), 138-147.
Mesulam’s
frontal lobe mystery re-examined. Restorative Neurology and Neuroscience, 27 (5), 493506.
Burgess, P. (2009). ROLE OF ROSTRAL PREFRONTAL CORTEX IN
DISCRIMINATING REAL FROM IMAGINARY EVENTS. JOURNAL OF
NEUROLOGY NEUROSURGERY AND PSYCHIATRY, 80 (7), 824.
Gilbert, S. J., Gollwitzer, P. M., Cohen, A. L., Oettingen, G., & Burgess, P. W. (2009).
Separable brain systems supporting cued versus self-initiated realization of delayed
intentions. Journal of Experimental Psychology: Learning, Memory and Cognition, 35 (4),
905-915.
Gilbert, S. J., Bird, G., Brindley, R., Frith, C. D., & Burgess, P. W. (2008). Atypical
recruitment of medial prefrontal cortex in autism spectrum disorders: An fMRI study of
two executive function tasks. Neuropsychologia, 46 (9), 2281-2291.
doi:10.1016/j.neuropsychologia.2008.03.025
Dumontheil, I., Burgess, P., & Blakemore, S. J. (2008). Development of rostral prefrontal
cortex and cognitive and behavioural disorders. Developmental Medicine and Child
Neurology, 50 (3), 168-181.
Turner, M. S., Simons, J. S., Gilbert, S. J., Frith, C. D., & Burgess, P. W. (2008). Distinct
roles for lateral and medial rostral prefrontal cortex in source monitoring of perceived
and imagined events. Neuropsychologia, 46 (5), 1442-1453.
doi:10.1016/j.neuropsychologia.2007.12.029
Christodoulou, T., Hadjulis, M., Frangou, S., & Burgess, P. W. (2008). Executive function
measures in healthy relatives of bipolar and schizophrenia probands. EUR PSYCHIAT,
23, S109.
Christodoulou, T., Hadjulis, M., Gilbert, S. J., Frangou, S., & Burgess, P. W. (2008).
Executive function measures in healthy relatives of bipolar and schizophrenia probands.
EUR PSYCHIAT, 23, S109.
Gilbert, S. J., & Burgess, P. W. (2008). Executive Function. Current Biology, 18, R110R114.
Burgess, P., Dumontheil, I., Gilbert, S. J., Okuda, J., Schölvinck, M. L., & Simons, J. S.
(2008). On the role of rostral prefrontal cortex (area 10) in prospective memory. In M.
Kliegel, M. A. McDaniel, G. O. Einstein (Eds.), Prospective memory: Cognitive,
neuroscience, developmental, and applied perspectives. Mahwah: Erlbaum (pp. 235-260).
Gilbert, S. J., & Burgess, P. W. (2008). Social and non-social functions of rostral
prefrontal cortex: Implications for education. Mind, Brain and Education, 2, 148-156.
Burgess, P. W., Gilbert, S. J., & Dumontheil, I. (2007). A gateway between mental life and
the external world: Role of the rostral prefrontal cortex (area 10). Japanese Journal of
Neuropsychology, 23 (1), 8-26.
Gilbert, S. J., Dumontheil, I., Simons, J. S., Frith, C. D., & Burgess, P. W. (2007). Comment
on "Wandering Minds: The Default Network and Stimulus-Independent Thought".
Science, 317 (5834), 43. doi:10.1126/science.1140801
Okuda, J., Fujii, T., Ohtake, H., Tsukiura, T., Yamadori, A., Frith, C. D., & Burgess, P. W.
(2007). Differential involvement of regions of rostral prefrontal cortex (Brodmann area
10) in time- and event-based prospective memory. International Journal of
Psychophysiology, 64 (3), 233-246. doi:10.1016/j.ijpsycho.2006.09.009
Gilbert, S. J., Williamson, I. D. M., Dumontheil, I., Simons, J. S., Frith, C. D., & Burgess, P.
W. (2007). Distinct regions of medial rostral prefrontal cortex supporting social and
nonsocial functions. Social Cognitive and Affective Neuroscience, 2 (3), 217-226.
doi:10.1093/scan/nsm014
Burgess, P. W., Gilbert, S. J., & Dumontheil, I. (2007). Function and localization within
rostral prefrontal cortex (area 10). Philosophical Transactions of the Royal Society B:
Biological Sciences, 362 (1481), 887-899. doi:10.1098/rstb.2007.2095
Burgess, P. W., Gilbert, S. J., & Dumontheil, I. (2007). The gateway hypothesis of rostral
PFC (area 10) function. Trends in Cognitive Sciences, 11, 290-298.
Burgess, P. W., Dumontheil, I., & Gilbert, S. J. (2007). The gateway hypothesis of rostral
prefrontal cortex (area 10) function. Trends Cogn Sci, 11 (7), 290-298.
doi:10.1016/j.tics.2007.05.004
Simons, J. S., Schölvinck, M., Gilbert, S. J., Frith, C. D., & Burgess, P. W. (2006).
Differential components of prospective memory? Evidence from fMRI. Neuropsychologia,
44 (8), 1388-1397.
Gilbert, S. J., Spengler, S., Simons, J. S., Frith, C. D., & Burgess, P. W. (2006). Differential
functions of lateral and medial rostral prefrontal cortex (area 10) revealed by brainbehavior associations. Cerebral Cortex, 16 (12), 1783-1789. doi:10.1093/cercor/bhj113
Gilbert, S. J., Spengler, S., Simons, J. S., Frith, C. D., & Burgess, P. W. (2006). Differential
functions of lateral and medial rostral prefrontal cortex (area 10) revealed by brainbehaviour correlations. Cerebral Cortex, 16 (12), 1783-1789. doi:10.1093/cercor/bhj113
Simons, J. S., Davis, S. W., Gilbert, S. J., Frith, C. D., & Burgess, P. W. (2006).
Discriminating imagined from perceived information engages brain areas implicated in
schizophrenia. NeuroImage, 32 (2), 696-703. doi:10.1016/j.neuroimage.2006.04.209
Gilbert, S. J., Spengler, S., Simons, J. S., Steele, J. D., Lawrie, S. M., Frith, C. D., & Burgess,
P. W. (2006). Functional specialization within rostral prefrontal cortex (Area 10): a
meta-analysis. Journal of Cognitive Neuroscience, 18 (6), 932-948.
doi:10.1162/jocn.2006.18.6.932
Gilbert, S. J., Simons, J. S., Frith, C. D., & Burgess, P. W. (2006). Performance-related
activity in medial rostral PFC (Area 10) during low demand tasks. Journal of
Experimental Psychology: Human Perception and Performance, 32 (1), pp.45-58.
doi:10.1037/0096-1523.32.1.000
Gilbert, S. J., Simons, J. S., Frith, C. D., & Burgess, P. W. (2006). Performance-related
activity in medial rostral prefrontal cortex (Area 10) during low-demand tasks. Journal
of Experimental Psychology: Human Perception and Performance, 32 (1), pp.45-58.
Gilbert, S. J., Simons, J. S., Frith, C. D., & Burgess, P. W. (2006). Performance-related
activity in medial rostral prefrontal cortex (area 10) during low-demand tasks. J Exp
Psychol Hum Percept Perform, 32 (1), 45-58. doi:10.1037/0096-1523.32.1.45
Burgess, P. W., Gilbert, S. J., Okuda, J., & Simons, J. S. (2006). Rostral prefrontal brain
regions (area 10): A gateway between inner thought and the external world?. In W. Prinz,
N. Sebanz (Eds.), Disorders of Volition (pp. 373-396). Cambridge,MA: MIT Press.
Burgess, P. W., Alderman, N., Forbes, C., Costello, A., Coates, L., Dawson, D. R., . . .
Channon, S. (2006). The case for the development and use of "ecologically valid"
measures of executive function in experimental and clinical neuropsychology. Journal of
the International Neuropsychological Society, 12 (2), 1-16.
Burgess, P. W., Alderman, N., Forbes, C., Costello, A., Coates, L. M. A., Dawson, D. R., . . .
Channon, S. (2006). The case for the development and use of "ecologically valid"
measures of executive function in experimental and clinical neuropsychology. J INT
NEUROPSYCH SOC, 12 (2), 194-209. doi:10.1017/S135561770606310
Burgess, P. W., Alderman, N., Forbes, C., Costello, A., Coates, L. M., Dawson, D. R., . . .
Channon, S. (2006). The case for the development and use of "ecologically valid"
measures of executive function in experimental and clinical neuropsychology. J Int
Neuropsychol Soc, 12 (2), 194-209. doi:10.1017/S1355617706060310
Simons, J. S., Owen, A. M., Fletcher, P. C., & Burgess, P. W. (2005). Anterior prefrontal
cortex and the recollection of contextual information. Neuropsychologia, 43 (12), pp.17741783.
Simons, J. S., Owen, A. M., Fletcher, P. C., & Burgess, P. W. (2005). Anterior prefrontal
cortex and the recollection of contextual information. Neuropsychologia, 43 (12), 17741783. doi:10.1016/j.neuropsychologia.2005.02.004
Simons, J. S., Gilbert, S. J., Owen, A. M., Fletcher, P. C., & Burgess, P. W. (2005). Distinct
roles for lateral and medial anterior prefrontal cortex in contextual recollection. Journal
of Neurophysiology, 94 (1), pp.813-820.
Simons, J. S., Gilbert, S. J., Owen, A. M., Fletcher, P. C., & Burgess, P. W. (2005). Distinct
roles for lateral and medial anterior prefrontal cortex in contextual recollection. J
Neurophysiol, 94 (1), 813-820. doi:10.1152/jn.01200.2004
Zlotowitz, S., Channon, S., Gilbert, S. J., & Burgess, P. J. (2005). Independence of executive
control processes involved in prospective memory and task switching. Proceedings of
British Psychological Society, 13, 220-?.
Gilbert, S. J., Frith, C. D., & Burgess, P. W. (2005). Involvement of rostral prefrontal
cortex in selection between stimulus-oriented and stimulus-independent thought.
European Journal of Neuroscience, 21 (5), 1423-1431. doi:10.1111/j.14609568.2005.03981.x
Sukantarat, K. T., Burgess, P. W., Williamson, R. C. N., & Brett, S. J. (2005). Prolonged
cognitive dysfunction in survivors of critical illness. Anaesthesia, 60 (9), pp.847-853.
Sukantarat, K. T., Burgess, P. W., Williamson, R. C. N., & Brett, S. J. (2005). Prolonged
cognitive dysfunction in survivors of critical illness. ANAESTHESIA, 60 (9), 847-853.
doi:10.1111/j.1365-2044.2005.04148.x
Burgess, P. W., Gilbert, S. J., Okuda, J., & Simons, J. S. (2005). Rostral Prefrontal Brain
Regions (Area 10): A Gateway between Inner Thought and the External World?. In N.
Sebanz, W. Prinz (Eds.), Disorders of Volition. Cambridge, MA: MIT Press.
Burgess, P. W., Simons, J. S., Dumontheil, I., & Gilbert, S. J. (2005). The gateway
hypothesis of rostral prefrontal cortex (area 10) function. In J. Duncan, L. Phillips, P.
McLeod (Eds.), Measuring the Mind: Speed, Control, and Age (pp. 215-246). Oxford:
University Press.
Gilbert, S., Simons, J., Frith, C., & Burgess, P. (2005). The role of medial rostral prefrontal
cortex in low-demand baseline conditions. JOURNAL OF COGNITIVE NEUROSCIENCE,
88. M I T PRESS.
Burgess, P. W., Simons, J. S., Coates, L. M. -. A., & Channon, S. (2005). The search for
specific planning processes. In G. Ward, R. Morris (Eds.), The Cognitive Psychology of
Planning (pp. 199-227). Hove, UK: Psychology Press.
Burgess, P. W., & Simons, J. S. (2005). Theories of frontal lobe executive function: clinical
applications. In P. W. Halligan, D. T. Wade (Eds.), Effectiveness of Rehabilitation for
Cognitive Deficits (pp. 211-232). Oxford: Oxford University Press.
Burgess, P. (2004). A specialised role for Rostral prefrontal cortex (area 10) in
prospective memory. INTERNATIONAL JOURNAL OF PSYCHOLOGY, 39 (5-6), 36.
Okuda, J., Frith, C. D., & Burgess, P. W. (2004). Organisation of time-and-event-based
intentions in rostral prefrontal cortex. NeuroImage, 22, S1-S53.
Zlotowitz, S., Channon, S., & Burgess, P. W. (2004). Real-life outcomes and performance
on an advanced planning test. Cognitive Neuroscience Society Abstracts, 130-?.
Burgess, P. W., Simons, J. S., Dumontheil, I., & Gilbert, S. J. (2004). The gateway
hypothesis of rostral PFC function. In J. Duncan, L. Phillips, P. McLeod (Eds.), Speed,
Control and Ageing: In Honour of Patrick Rabbit. OPU.
Burgess, P. W., & Simons, J. S. (2004). Theories of frontal lobe executive function:
Clinical applications. In P. W. Halligan, D. T. Wade (Eds.), Effectiveness of Rehabilitation
for Cognitive Deficits. Oxford: OUP.
Alderman, N., & Burgess, P. W. (2003). Assessment and Rehabilitation of the
Dysexecutive Syndrome. In R. Greenwood, T. M. McMillan, M. P. Barnes, C. D. Ward
(Eds.), Handbook of Neurological Rehabilitation (pp. 387-402). Hove: Psychology Press.
Burgess, P. W. (2003). Assessment of executive function. In P. W. Halligan, U. Kischka, J.
Marshall (Eds.), Handbook of Clinical Neuropsychology (pp. 302-321). Oxford: Oxford
University Press.
Alderman, N., & Burgess, P. (2003). Chapter 9. Executive Dysfunction. In L. Goldstein, J.
McNeil (Eds.), Clinical Neuropsychology: A Practical Guide to Assessment and Management
for Clinicians. Chichester, UK: Wiley.
Alderman, N., Burgess, P. W., Knight, C., & Henman, C. (2003). Ecological validity of a
simplified version of the Multiple Errands Test. Journal of the International
Neuropsychological Society, 9, 31-44.
Burgess, P. W., & Alderman, N. (2003). Executive dysfunction. In L. H. Goldstein, J. E.
McNeil (Eds.), Clinical Neurospychology: A Practical Guide to Assessment and Management
for Clinicians (pp. 185-210). Chichester: John Wiley.
Burgess, P. W., Scott, S. K., & Frith, C. D. (2003). The role of the rostral frontal cortex
(area 10) in prospective memory: a lateral versus medial dissociation. Neuropsychologia,
41 (8), 906-918. doi:10.1016/S0028-3932(02)00327-5
Burgess, P. W. (2002). Assessment of executive function. In P. W. Halligan, J. Marshall
(Eds.), Oxford Handbook of Neurological Assessment. Oxford University Press.
Knight, C., Alderman, N., & Burgess, P. (2002). Development of a simplified version of the
multiple errands test for use in hospital settings. Neuropsychological Rehabilitation, 12 (3),
pp.231-255.
Knight, C., Alderman, N., & Burgess, P. W. (2002). Development of a simplified version of
the multiple errands test for use in hospital settings. NEUROPSYCHOL REHABIL, 12 (3),
231-255. doi:10.1080/09602010244000039
Burgess, P. W., & Robertson, I. H. (2002). Principles of the rehabilitation of frontal lobe
function. In D. T. Stuss, R. T. Knight (Eds.), Principles of Frontal Lobe Function (pp. 557572). New York: Oxford University Press.
McNeil, J., & Burgess, P. (2002). The selective impairment of arithmetical procedures.
Cortex, 38 (4), pp.569-587.
McNeil, J. E., & Burgess, P. W. (2002). The selective impairment of arithmetical
procedures. CORTEX, 38 (4), 569-587.
Alderman, N., & Burgess, P. W. (2001). Assessment and Rehabilitation of the
Dysexecutive Syndrome. In R. Greenwood, T. M. McMillan, M. P. Barnes, C. D. Ward
(Eds.), Handbook of Neurological Rehabilitation. Hove: Psychology Press.
Burgess, P. W., Quayle, A., & Frith, C. (2001). Brain regions involved in prospective
memory as determined by positron emission tomography. Neuropsychologia, 39 (6), 545555. doi:10.1016/S0028-3932(00)00149-4
Burgess, P. W. (2001). Rehabilitation of multitasking deficits. BRAIN COGNITION, 47 (12), 7-8.
Burgess, P. W. (2000). Real-world multitasking from a cognitive neuroscience
perspective. In S. Monsell, J. Driver (Eds.), Control of Cognitive Processes: Attention and
Performance VVIII (pp. 465-472). Cambridge, MA: MIT Press.
Burgess, P. (2000). Strategy application disorder: the role of the frontal lobes in human
multitasking. Psychological Research, 63 (3-4), pp.279-288. doi:10.1007/s004269900006
Burgess, P. W. (2000). Strategy application disorder: the role of the frontal lobes in
human multitasking. Psychol Res, 63 (3-4), 279-288.
Burgess, P. W., Costello, A. D. L., Frith, C., Quayle, A., Scott, S., & Veitch, E. (2000). The
brain regions involved in creating and realizing a delayed intention. INT J PSYCHOL, 35
(3-4), 184.
Burgess, P., Veitch, E., Costello, A., & Shallice, T. (2000). The cognitive and
neuroanatomical correlates of multitasking. Neuropsychologia, 38 (6), 848-863.
doi:10.1016/S0028-3932(99)00134-7
Burgess, P., & McNeil, J. (1999). Content-specific confabulation. Cortex, 35 (2), 163-182.
doi:10.1016/S0010-9452(08)70792-5
Burgess, P., & McNeil, J. (1998). Content-specific confabulation. Cortex (34), 1-18.
Wilson, B., Evans, J., Emslie, H., Alderman, N., & Burgess, P. (1998). The development of
an ecologically valid test for assessing patients with a dysexecutive syndrome.
Neuropsychological Rehabilitation, 8 (3), 213-228. doi:10.1080/713755570
Wilson, B. A., Evans, J. J., Emslie, H., Alderman, N., & Burgess, P. (1998). The
development of an ecologically valid test for assessing patients with a dysexecutive
syndrome. NEUROPSYCHOL REHABIL, 8 (3), 213-228.
Shallice, T., & Burgess, P. (1998). The domain of supervisory processes and the temporal
organisation of behaviour. In A. Roberts, T. Robbins, L. Weiskrantz (Eds.), The Prefrontal
Cortex:Executive and Cognitive Functions (pp. pp.22-35). Oxford, UK: Oxford University
Press.
Burgess, P., Alderman, N., Evans, J., Emslie, H., & Wilson, B. (1998). The ecological
validity of tests of executive function. Journal of the International Neuropsychological
Society, 4 (6), pp.547-558.
Burgess, P. W., Alderman, N., Evans, J., Emslie, H., & Wilson, B. A. (1998). The ecological
validity of tests of executive function. J Int Neuropsychol Soc, 4 (6), 547-558.
Wilson, B., Evans, J., Alderman, N., Burgess, P., & Emslie, H. (1997). Behavioural
assessment of the dysexecutive syndrome. In P. Rabbitt (Ed.), Theory and Methodology of
Frontal and Executive Function (pp. pp.239-250). East Sussex, UK: Psychology Press.
Burgess, P. W., & Shallice, T. (1997). The Hayling and Brixton Tests.
Burgess, P., & Shallice, T. (1997). The relationship between prospective memory and
retrospective memory: neuropsychological evidence. In S. Gathercole, M. Conway (Eds.),
Cognitive Models of Memory. London, UK: Psychology Press.
Burgess, P. (1997). Theory and methodology in executive function research. In P. Rabbitt
(Ed.), Theory and Methodology of Frontal and Executive Function (pp. pp.81-116). East
Sussex, UK: Psychology Press.
Burgess, P., & Shallice, T. (1996). Bizarre responses, rule detection and frontal lobe
lesions. Cortex, 32, 241-260.
Burgess, P., & Shallice, T. (1996). Confabulation and the control of recollection. Memory,
4 (4), 359-412.
Burgess, P. W., Baxter, D., Rose, M., & Alderman, N. (1996). Delusional paramnesic
misidentification. In P. W. Halligan, J. C. Marshall (Eds.), Method in Madness: Case Studies
in Neuropsychiatry (pp. 51-78). Hove, U.K.: Psychology Press..
Burgess, P., & Shallice, T. (1996). Response suppression, initiation and strategy following
frontal lobe lesions. Neuropsychologia, 34, 263-273.
Burgess, P. W., & Cooper, R. (1996). The control of thought and action. In D. W. Green
(Ed.), Cognitive Science. London: Blackwell.
Shallice, T., & Burgess, P. (1996). The domain of supervisory processes and temporal
organization of behaviour. Philos Trans R Soc Lond B Biol Sci, 351 (1346), 1405-1411.
doi:10.1098/rstb.1996.0124
Duncan, J., Burgess, P. W., & Emslie, H. (1995). Fluid intelligence after frontal lobe
lesions. Neuropsychologia, 33 (3), 261-268.
BURGESS, P. W. (1995). THE NEUROPSYCHOLOGY OF SCHIZOPHRENIA DAVID,AS, CUTTING,JC. J PSYCHOPHYSIOL, 9 (2), 159-161.
Alderman, P. W., & Burgess, P. W. (1994). A comparison of treatment methods for
behaviour disorder following herpes simplex encephalitis. Neuropsychological
Rehabilitation, 4 (31), 48-?.
BURGESS, P. W., & SHALLICE, T. (1994). FRACTIONATION OF THE FRONTALLOBE SYNDROME. REV NEUROPSYCHOL, 4 (3), 345-370.
Burgess, P. W., & Shallice, T. (1994). Fractionnement du syndrome frontal. Revue de
Neuropsychologie (4), 345-370.
Shallice, T., & Burgess, P. W. (1993). Supervisory control of action and thought selection.
In A. Baddeley, L. Weiskrantz (Eds.), Attention: Selection, Awareness and Control: A Tribute
to Donald Broadbent (pp. 171-187). Oxford: Clarendon Press.
Goldstein, L. H., Bernard, S., Fenwick, P. B. C., Burgess, P. W., & McNeil, J. (1993).
Unilateral frontal lobectomy can produce strategy application disorder. Journal of
Neurology, Neurosurgery and Psychiatry, 56 (3), 274-276.
Shallice, T., & Burgess, P. W. (1991). Deficits in strategy application following frontal
lobe damage in man. Brain, 114 (2), 727-741.
Shallice, T., & Burgess, P. W. (1991). Higher-order cognitive impairments and frontal
lobe lesions in man. In H. S. Levin, H. M. Eisenberg, A. L. Benton (Eds.), Frontal Lobe
Function and Dysfunction (pp. 125-138). New York: Oxford University Press.
Alderman, N., & Burgess, P. W. (1990). Integrating cognition and behaviour: A
pragmatic approach to brain injury rehabilitation. In R. L. Wood, I. ussey (Eds.),
Cognitive Rehabilitation in Perspective (pp. 204-228). London, U.K.: Taylor and Francis.
Burgess, P. W., & Alderman, N. (1990). Rehabilitation of dyscontrol syndromes following
frontal lobe damage: A cognitive neuropsychological approach. In R. L. Wood (Ed.),
Neurobehavioural Sequelae of Traumatic Brain Injury (pp. 110-132). London, U.K.: Taylor
and Francis.
Shallice, T., Burgess, P. W., Schon, F., & Baxter, D. M. (1989). The origins of utilisation
behaviour. Brain, 112, 1587-1598.
Davies, W., & Burgess, P. W. (1988). Prison officers' experience as a predictor of risk of
attack: An analysis within the British prison system. Medicine, Science and the Law, 28
(2), 135-138.
Giles, G. M., Fussey, I., & Burgess, P. W. (1988). The behavioural treatment of verbal
interaction skills following severe head injury: A single case study. Brain Injury, 2 (1), 7579.
Davies, W., & Burgess, P. W. (1988). The effect of management regime on disruptive
behaviour: An. Medicine, Science and the Law, 28 (3), 243-247.
Wood, R. L., & Burgess, P. W. (1988). The psychological management of behaviour
disorders following brain injury. In I. Fussey, G. M. Giles (Eds.), Rehabilitation of the
Severely Brain Injured Adult: A Practical Approach. London, U.K.: Croom Helm.
Burgess, P. W., Mitchelmore, S., & Giles, G. M. (1987). Behavioral treatment of attention
deficits in mentally impaired subjects. American Journal of Occupational Therapy, 41 (8),
505-509.
Scott, S. K., Clegg, F., Rudge, P., & Burgess, P. W. (n.d.). Foreign accent syndrome, speech
rhythm and the functional neuronatomy of speech production. Journal of
Neurolinguistics.
Volle, E., Gilbert, S. J., Benoit, R. G., & Burgess, P. W. (n.d.). Specialization of the rostral
prefrontal cortex for distinct analogy processes. Cerebral Cortex.
Benoit, R. G., Gilbert, S. J., Volle, E., & Burgess, P. W. (n.d.). When I think about me and
simulate you: Medial rostral prefrontal cortex and self-referential processes.
NeuroImage.
31
ROSTRAL PREFRONTAL CORTEX (BRODMANN AREA 1 0 )
M ETACOGNITION IN THE BRAIN
Paul W. Burgess and Hsuan-Chen Wu zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJ
Burgess, P. W. & Wu, H-C. (2013) Rostral prefrontal cortex (Brodmann area 10):
metacognition in the brain. Chapter 31 in: Principles of Frontal Lobe Function, 2 edition
(Editors: Donald T. Stuss & Robert T. Knight) pp. 524-534. New York: OUP
nd
INTRODUCTION zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA
size (Semendeferi, Armstrong, Schleicher, Zilless, & Van
Hoesen, 1998).
The study of rostral prefrontal cortex (PFC) must count
now as perhaps the fastest-growing new area of cognitive
IT HAS AN U N U S U ALLY LOW N E U R O N AL
D E N S ITY
neuroscience. Until approximately 10 years ago, virtually
( P O IN T 2 )
nothing was known about this huge brain region (actually
the largest architectonic subregion of the PFC). Now we Rostral PFC is not only unusual in terms of its size, but also in
have evidence that stretches across neuroanatomy, anthro- terms of neuronal density. I n humans, its density is particupology, brain development, cognitive neuroscience, neu- larly low (Semendeferi et al., 2001). However, the number of
ropsychology, neuropsychiatry (adults and children), and, dendritic spines per cell and the spine density are higher than
most recently, even behavioral neuroscience (Tsujimoto, those of comparable areas (Jacobs et al., 2001). These differGenovesio, & Wise, 2011). The purpose of this chapter is to ences may be of anthropological significance. Semendeferi
lay out, in as straightforward a way as possible, the current et al. (2011) compared the horizontal spacing distance of
state of our knowledge about this fascinating brain region. neurons in different regions of the cortex across primates
We will conclude by suggesting that perhaps the best (including humans). They found that it is only after the split
description for the overall function of this brain region in from our last common ancestor that BA 10 neuronal spacing
humans would be that it is a hub forzyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA
metacognition.
became the largest in humans compared with the other apes.
So, what do we currently know about rostral PFC, especially as it relates to cognition? zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA
TH E R E
AR E D IF F E R E N T
S U B R E G IO N S
R O S TR A L
P F C IS A VE R Y
E S P E C IA L L Y
IN HUM AN S
B IG B R AIN
( P O IN T
R E G IO N ,
1)
Confusingly, in the literature, rostral PFC (approximating Brodmann area [BA] 10) is referred to by many
names. These include "frontopolar cortex," "frontal pole,"
"anterior prefrontal cortex," and so forth. All these terms
are used to refer to a large part of the cortex that sits at
the very front of the brain, and given our current state of
knowledge, these terms are all virtually interchangeable.
Rostral PFC is conspicuously large in humans, comprising approximately 500 million neurons spread over an
area of roughly 28,000 mm (Semendeferi, Armstrong,
Schleicher, Zilles, & Van Hoesen, 2001). Indeed, it is larger
in humans, both relatively and absolutely, than in any other
animal. This is especially noteworthy since this is not the
case for all subregions of PFC. For instance, BA 13 is actually smaller than would be expected given overall brain
3
524
W ITHIN
C Y T 0 A R C H IT E C T U R A L
BA 1 0 ( P O IN T 3 )
Rostral PFC is a complex structure from a cytoarchitectural viewpoint. There appear to be at least three different
subregions in humans (with only two in, e.g., the macaque;
Carmichael & Price, 1994). According to Ongiir, Ferry, and
Price (2003), there is a large and highly differentiated region
in humans that covers the frontal pole itself (i.e., the most
anterior section), extending across both medial and lateral
aspects. This region has a thick, highly granular cortex with
a well-developed sublaminated layer I I I . Ongur et al. term
this region " lOp." The other two subregions of BA 10 occupy
the medial surface only. Ongiir et al. describe how the first
of these regions lies directly behind (i.e., caudally) lOp and
is termed "lOr." This has granular layers I I and IV, with a
moderately developed layer I I I . The most caudal subregion
of BA 10 lies behind lOr and is termed "10m." This is granular, but with a thinner layer I V and radial and horizontal
striations. I t is located ventral to BA 24 and ventral and
anterior to BA 32 but superior to BA 11 and 13, extending the brain, does not in fact stop in the early 20s, as has been
anteriorly to the level of the genu of the corpus callosum.
assumed, and the later stages of this process might afford
What are we to make of this, as researchers interested some kind of protection against undesirable cognitive
in determining the cognitive functions supported by this phenomena.
intriguing brain region? Should we take this information
as relevant for constraining theories about the functional
AC TIVATIO N S OF R O S TR A L P F C CAN B E FO UN D
organization of rostral PFC (i.e., mapping between strucD UR IN G ALM O S T ANY K IN D OF C O G N ITIV E TAS K
tural and functional levels of explanation)? I t is unwise to
( P O IN T 5 )
expect a straightforward relation between structure and
function, at least using the forms of data currently avail- As Burgess, Simons, Dumontheil, and G ilbert (2005)
able to us. Nevertheless, perhaps the fact that there are pointed out, local hemodynamic (e.g., blood flow, blood
distinct cytoarchitectonic subregions within rostral PFC oxygenation) changes occur in BA 10 during the performight be taken to be congruent with a general notion that mance of a very wide variety of cognitive tasks, from the
there may be differences between these regions in the way simplest (e.g., conditioning paradigms; Blaxton et al.,
they operate, the contributions they make to cognition, or 1996) to highly complex tests involving memory and judgthe behaviors or mental abilities afforded by them. I n fact, ment (e.g., Burgess, Quayle, & Frith, 2001; Burgess, Scott,
as we shall see later, these anatomical subdivisions appear & Frith, 2003; Frith & Frith, 2003; K oechlin, Basso,
to be remarkably well reflected in the different functional Pietrini, Panzer, & Grafman, 1999) or problem solving
specializations of these subregions. It is also the case that a (e.g., Christoff et al., 2001). Indeed, one can find activanumber of these abilities, while not perhaps entirely unique tion of the rostral PFC in just about any kind of task—for
to humans, nevertheless would be among those that we example, verbal episodic retrieval (Rugg, Fletcher, Frith,
might think of as strongly typifying what is more charac- Frackowiak, & Dolan, 1996; Tulving, Markowitsch,
teristic of them than of other primates. zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA
Criak, Habib, & Houle, 1996), nonverbal episodic retrieval
(Haxbyet al. 1996; Roland & Gulyas, 1995), semantic memory (Jennings, Mcintosh, Kapur, Tulving, & Houle, 1997;
R O S TR A L P F C ( B A 10)
D E V E L O P S LATE
Martin, Haxby, Lalonde,Wiggs, & Ungerleider 1995),
IN L IF E ( P O IN T 4 )
language (B ottini et al., 1994; K lein, Milner, Zatorre,
I f this is true, then perhaps it would not be surprising if Meyer, & Evans, 1995), motor learning (Jenkins, Brooks,
the development of rostral PFC showed a particularly pro- Nixon, Frackowiak, & Passingham, 1994), rule learning
tracted course. After all, the most subtle faculties of the (Strange, Henson,Friston,&Dolan, 2001), shock/tone conhuman mind are generally thought to be acquired after ditioning (Hugdahl et al., 1995), nonverbal working memchildhood. And rostral PFC obliges (see Dumontheil, ory (Gold, Berman, Randolph, Goldberg, & Weinberger,
Burgess, & Blakemore, 2008, for review): I t is a cortical 1996; Haxby, Ungerleider, Horwitz, Rapoport, & Grady,
region that displays an unusually large degree of brain 1995), verbal working memory (Petrides, Alivisatos,
growth between the ages of 5 and 11 years (Sowell et al., Meyer, & Evans, 1993), spatial memory (Burgess, Maguire,
2004) . But the changes do not stop there. There are large Spiers, & O'Keefe, 2001), auditory perception (Zatorre,
decreases in gray matter density in this region between Halpern, Perry, Meyer, & Evans, 1996), object processadolescence (12-16 years old) and young adulthood ing (Kosslyn et al., 1994; Kosslyn, Alpert, & Thompson,
1995), the Tower of London Test (Baker et al., 1996),
(23-30 years old; Sowell, Thompson, Holmes, Jernigan, zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCB
& c Toga, 1999), with maturation of dendritic systems con- the Wisconsin Card Sorting Test (Berman et al., 1995),
tinuing into late adolescence (e.g., Travis, Ford, & Jacobs, reasoning tasks (Goel, G old, Kapur, & Houle, 1997), and
2005) . The developmental changes in gray matter volume intelligence tests such as Raven's Progressive Matrices
might be consequent upon an increase in cortical myelina- (Christoff et al., 2001; Prabhakaran, Smith, Desmond,
tion (Paus, 2005), which for many years has been thought Glover, & Gabrieli, 1997).
Indeed, it might be more of a challenge to find a task
to be particularly late in this region (Bonin, 1950). Then
there appear to be sharp changes in early adulthood as well: that does not activate some subregion of rostral PFC at least
John et al. (2009) compared the volume of rostral PFC as some of the time. This means that the scientific emphasis, in
a proportion of total brain volume in healthy people 20 to the struggle to determine the functions of the brain region,
40 years old. They found a sharp decrease in relative vol- turns to (1) those paradigms where there is an usually freume over this period. Moreover, this normally occurring quent finding of rostral PFC activation and (2) those where
decrease was absent in people with schizophrenia. So, it is performance on the paradigm is directly related to these
tempting to speculate that the "sculpting" of rostral PFC activations. Fortunately, there are some, which will be outthat we see throughout childhood and into early adult- lined in the section dealing with the specific functions of roshood, which is part of the normal developmental course of tral PFC.
31.
R O S TR AL PR EFR O N TAL
C O R TEX
525
L E S IO N S
TO
R O S TR A L
zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA
NOT C A U S E
rostral PFC damage are not typically impaired across a
P FC DO
wide range of tasks, and their performance on IQtests can
remain unimpaired. Many single cases have been reported
THE LIM ITS OF THE F U N C TIO N S THAT W E
in which patients have scored in the superior range on I Q
C U R R E N TLY T E S T ) ( P O IN T 6 ) zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA
tests, despite extensive rostral PFC involvement (e.g., Goel
& Grafman, 2000; Goldstein, Bernard, Fenwick, Burgess,
A natural expectation from the finding of activity in ros& McNeil, 1993; Shallice & Burgess, 1991; see Burgess
tral PFC duringjust about any class of cognitive task might
et al., 2009, for review). I n fact, Uretzky and Gilboa's
be that damage to rostral PFC in humans should cause a
(2010) patient, ZP (WAI S-I I I V I Q 121, PI Q 104, FSIQ
very wide range of deficits. However, this does not seem to
113), who has circumscribed right frontopolar atrophy folbe the case, as revealed by both single-case and group studlowing a road traffic accident, gained degrees in civil engiies in humans.
neering and business administration after his injury, which
Probably the first group human lesion study of this type
would seem unlikely if rostral PFC dysfunction causes a
was carried out by Asenath Petrie in 1952. Petrie was a clinmarked decrement in general intellectual capabilities.
ical psychologist who had initially studied at University
Group studies have largely supported these observaCollege London and subsequently received clinical traintions. For instance, Dreher et al. (2008) compared patients
ing at the Maudsley Hospital in London. I n her groundwith rostral PFC lesions (N= 7; called " frontopolar lesions"
breaking book, written while she was at Pennsylvania
by Dreher et al.) and patients whose lesions affected the
State University (and surely deserves greater recognition),
frontal lobes but not the rostral aspects of it (A^= 5). There
she reported a study of the effects of leucotomy upon her
was no significant difference in the performance of the two
patients at St. George's Hospital in London. More specifigroups in terms of WAI S-I I I FSIQ scores (rostral patients'
cally, she compared the effects of two different leucotomy
mean 110.43, SD 20.4; nonrostral patients 103.20, SD
procedures upon cognition in participants with "neurotic"
8.35). Moreover, the largest study of its kind (to our knowlsymptoms. The standard procedure at that time was to
edge) also supports this contention. Warrington, James,
make an incision at a rostral-caudal plane that, if extended
and Maciejewski (1986) examined 656 patients with unito the outer surface of the brain, would have bisected BA
lateral cerebral lesions on a shortened version of perhaps the
45,47,46,9, and 8. Petrie compared the effects of this intermost widely used neuropsychological test of intelligence,
vention with the effects of a more rostral incision, where
the WAIS. They found that V I Q was impaired following
the cut was made just behind BA 10.
left hemisphere lesions, regardless of where the lesion was
The results were, prima facie, surprising. This rostral located within the hemisphere. Performance I Q was only
operation actually led tozyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA
improvements in a range of tasks, impaired following lesions affecting the right parietal lobe.
notably manual dexterity, less perseveration, greater con- I n an analysis by individual subtest, only a relationship
centration, and better performance on the Wechsler Adult between Block Design and Picture Arrangement decrement
Intelligence Scale (WAIS) D igit Symbol and Similarities and right parietal involvement was found. There was no spesubtests. I t is tempting to ascribe these improvements to cific deficit for lesions in the frontal lobe. Glascher et al.
the effects of alleviation of many of the neurotic symp- (2009) carried out a similar study, using the more sophistoms that Petrie reports (1952, p. 98). However, this must ticated lesion imaging methods now available and examinremain conjecture since the sample was not large enough ing 241 patients with focal brain damage on the WAI S-I I I .
for formal analysis of this type. Nevertheless, one might They found a statistically significant lesion-deficit relaperhaps conclude that this pattern would be very unlikely tionship in left inferior frontal cortex for verbal compreto occur if rostral PFC supports to a very substantial degree hension scores, with an association between lesions in left
the mental faculties tapped by these tests. O n other tests, lateral frontal and parietal cortex for the working memory
relative to preoperative ability, there was no change. These index and in right parietal cortex for perceptual organizaincluded the Porteus Mazes, WAIS verbal I Q (VI Q ), per- tion. Again, there was no evidence for a link between rosformance I Q (PI Q ), full-scale I Q (F SI Q ), Cattell fluency, tral PFC lesions and a generalized cognitive impairment,
and proverb interpretation tests.
as one might perhaps have expected from a simple-minded
Indeed, out of the substantial battery that Petrie extrapolation from the neuroimaging findings of activaadministered, postoperative decrements were detected on tions across a wide range of tasks.
only two tests. First, there was a varied response to distracIndeed, those who have specifically addressed this
tion. Second, the patients seemed to experience the sense matter reinforce the idea that whatever role it is that prothat time passed more quickly, as measured by unfilled esti- cesses supported by rostral PFC play in cognition, it is not
mation of the passage of 60 s.
strongly linked to notions of "general intelligence." Roca
Since the publication of Petrie's study, a substantial et al. (2010) studied the relationship between measures of
body of further evidence from human lesion studies has "fluid intelligence" (e.g., Cattell's Culture Fair Test) and
accumulated that also demonstrates that patients with performance on a range of measures of executive functions.
D E F IC IT S
S EEM
526
IN
A W ID E
R E LA TIV E LY
R AN G E
OF TA S K S
C IR C U M S C R IB E D
B UT
( W ITH IN
P R IN C IP LE S
OF FRON TAL
LO B E
FUN CTIO N
I n their first experiment, the sample was 44 patients with assessing the overall impact of lesions within the PFC on a
chronic lesions affecting the frontal lobes. For two of the range of cognitive domains.
The question Burgess et al. (2012) were trying to
most commonly used executive function tasks (Wisconsin
Card Sorting Test [WCST], Nelson version, and Verbal address in their meta-analysis was whether lesions affectFluency), they found that although the patients were sig- ing rostral PFC cause a breadth of deficits comparable to
nificantly poorer than a group of matched healthy controls that of lesions elsewhere within the frontal cortex. This is
in terms of raw performance on all three tests, once the an important issue for knowing where to start about thevariance attributable to "fluid intelligence" was accounted orizing about functional specialization of the region (see
Burgess et al,. 2012, for further explanation).
for by covariance, this difference disappeared.
Broadly, Stuss and Alexander tested patients whose
However, in their second experiment, Roca et al. (2010)
administered a wider range of executive and social function lesions involved the frontal lobes, and collected sets of data
tasks to 21 patients. Most of these were performed more from nonpatient control subjects matched as closely as pospoorly by the patient group. This time, however, Roca et al. sible to the patients for sex, age, and education. The lesions
found that for some of the executive tasks, adjusting for were acute, andincluded infarction, hemorrhage (including
fluid intelligence didnot remove the group difference. These ruptured aneurysms), trauma, and tumors. Most patients
tests were Go-no go (Dubois, Slachevsky, Litvan, & Pillon, with tumors had resection of meningiomas or low-grade
2000; Luria, 1966), proverb interpretation (Hodges, gliomas and had not been treated with radiation. Stuss and
1994), the Hayling Sentence Completion Task (Burgess Alexander avoided patients in the very acute phase of their
& Shallice 1996,1997), the Hotel Task (Manly, Hawkins, illness (e.g., less than two months' onset) and also excluded
Evans, Woldt, & Robertson, 2002), aversion of Shallice and patients with significant aphasia, visual neglect, apraxia, or
Burgess's Six Element Task (Shallice & Burgess, 1991), and any other significant neurological or psychiatric disorders.
the Faux Pas Test (Stone, Baron-Cohen, & K night, 1998). Further, the patients tended to have I Q scores within the
Roca et al. (2010) then devised a score that represented the normal range. Incidentally, it should be mentioned that in
mean residual from these tests (i.e., a score that represented these studies, and in comparable ones where rigorous neuthe degree of impairment on the tests that could not be ropsychological screening is used to remove potential conexplained by fluid intelligence). When they examined the founds (e.g., Burgess, Veitch, de Lacy Costello, & Shallice,
lesion overlaps for the six patients who showed the greatest 2000), no simple link between etiology and cognitive
negative value, they found that the location of the overlap results is found: it is the location of the lesion that is the
was in rostral PFC, especially in the right hemisphere. I n principal determining factor.
Burgess et al. (2012) presented an analysis of the
summary, then, Roca et al. showed that rostral PFC lesions
caused an impairment that showed up on a number of exec- results from a range of the published papers by the Stuss/
utive tasks but that could not be explained by changes in Alexander team over roughly a 10-year period, using this
fluid intelligence. zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA
population. This analysis looked at how many variables
showed impairment following lesions to different parts of
the frontal lobes out of 44 under consideration (see Burgess
On the Spe cificity o f the De ficit Fo llo wing Ro s tral
et al., 2012, for a list of them). The 44 variables were scores
PFC Le s io ns
from a range of tests and paradigms, including the WCST,
various verbal fluency measures, humor measurement, the
Roca et al.'s (2010) study moves the argument about the Stroop Test, simple and choice reaction time tests under
specificity of functions supported by rostral PFC away various conditions, inhibition, and various measures of
from notions of "intelligence" (i.e., a construct involved in attentional performance.
the performance of virtually all tasks). Yet their study still
The meta-analysis shows two clear results. The first is
showed that rostral PFC lesions caused deficits larger than that rostral PFC lesions did not cause deficits on more of
range of tasks. So, the measurements than lesions elsewhere within the froncan be explained by intelligence across azyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA
perhaps rostral PFC lesions in humans still cause wide- tal lobes. For both left and right hemispheres, lateral and
spread cognitive problems of some sort, but these problems medial surfaces, deficits were noted on the range ofvariables
are just not well measured by IQtests.
examined by Stuss and Alexander less frequently than for
An analysis that speaks to this issue is presented by some other frontal lobe regions; indeed, with the possible
Burgess, Gonen-Yaacovi, and Voile (2012). They carried exception of some aspects of ventral PFC, cognitive deficits
out a meta-analysis of the set of group human lesion stud- associated with BA 10 lesions, regardless of hemisphere or
ies carried out over many years by Donald T . Stuss and surface, were consistently among the leastfrequent findings
Michael Alexander and their colleagues in Toronto. They in this series of studies stretching over 10 years.
The second finding from the Stuss/Alexander
applied similar methods to the analysis of their data over a
long period of time, and some of the cases were shared across meta-analysis is that the deficits that can be exclusively
studies, which made this dataset particularly valuable for attributed to rostral PFC lesions seem to relate to quite zyxwvutsr
31.
R O S TR AL PR EFR O N TAL
C O R TEX
527
specific situations. I f one considers just those variables only partly complete one task and move to another task
where rostral PFC (BA 10) lesions caused an impair- before returning to the first one.
Much of the complex behavior in work and family situament that was significantly worse than the impairments
in patients with lesions elsewhere, the result is a very tions is of this form. For instance, one might start preparing
restricted subset of the 44 variables indeed. Patients with a meal until such time as a phone call has to be made, then
rostral PFC lesions showed impairments in humor judg- break off to make the call and return to preparing the meal.
ment in two (only) of the 10 WCST variables considered by Often each day will be composed of many of these routines
Stuss and Alexander, and in maintaining performance in and subroutines, which have to be dovetailed if one is to
time-keeping tasks, and were worst during slow conditions use one's time effectively. This type of scheduling is called
of sustained attention tasks. With this latter finding, there "multitasking." It is distinguished from "multiple-task peris an interesting concordance with the findings of Petrie formance" (e.g., trying to type something while holding
(1952), more than 50 years earlier (described above), which a conversation) by the characteristic that only one task is
suggested that rostral PFC lesions can lead to a variable trying to be accomplished at any one time. (The relations
response to distraction, and the sense that time passes more between the processes and brain regions involved in these
two behaviors are, however, not well established.) I n other
quickly, but leaves other cognitive abilities intact.
This helps a great deal in the search to discover the cog- words, multitasking is the ability to sequence the perfornitive functions supported by rostral PFC. Rostral PFC mance of a series of subtasks, which in practice means
lesions do not usually cause serious deficits in primary performing one task with the intention of switching to
sensory functions, or in the "routinized" learned skills another in the future or rehearsing information relevant to
such as basic aspects of language processing, motor or one task while performing another.
visuo-perceptual abilities, reading, writing, simple aspects
This type of behavior—multitasking—was probably
of memory (e.g., knowledge; episodic recognition mem- the first for which a case was made for a link with rostral
ory), and so forth, since virtually all the studies reviewed PFC structures. How this came about is documented
here describe patients who have rostral PFC damage but by Burgess et al. (2009). The first historical stage was the
whose abilities in these domains are unaffected. Nor do demonstration that some patients with frontal lobe damrostral PFC lesions cause widespread cognitive decline. age showed multitasking impairments in the context of
Instead, they seem to cause deficits on quite a restricted set normal performance on most, if not all, of the traditional
of tasks.
tests of neuropsychological function used at the time (e.g.,
Putting these findings from human neuropsychology memory, language, perception, executive function). The
together with those from neuroimaging, it seems likely second stage was the demonstration that this pattern was
caused most frequently by lesions to rostral PFC.
that whatever the functions of rostral PFC are, they (1) are zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGF
critical to the actual performance of only a restricted range
Regarding the first stage, the pattern of relatively isoof tasks and (2) are nevertheless operational during a much lated behavioral disorganization in everyday life had been
wider range of tasks. So, what kind of processing could ful- observed clinically for many years. For instance, Penfield
fill these criteria? We will argue later that this kind of pro- and Evans (1935) described the symptoms that Penfield's
cessing can best be described as "metacognition." zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIH
sister was experiencing after the removal of a right frontal
glioma: "She had planned to get a simple supper for one
guest and four members of her family. She looked forward
R O S TR A L P FC IS IN VO LVED
IN THE
to it with pleasure and had the whole day for preparation.
M E TAO R G AN IZ ATIO N OF B E H AVIO R
When the appointed hour arrived she was in the kitchen,
( M U LTITA S K IN G
AND P R O S P E C T IV E M E M O R Y )
the food was all there, one or two things were on the stove,
( P O IN T 7 ) zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA
but the salad was not ready, the meat had not been started
and she was distressed and confused by her long continued
M ultitas king
effort alone" (p. 131).
This impairment was not caused by problems with
Virtually all meaningful behavior has a structure to it,
and so could be said to be organized at some level. This is memory, language, or perception, or by gross intellectual
true of even relatively simple goal-directed behaviors such decline, but instead seemed to be more specifically related
as reaching for a cup of tea. However, at the heart of most to prefrontal lobe function— although none of the theorists
influential models of the role of frontal lobe processes in at the time attempted either to characterize the problem in
human cognition is the notion of a division between behav- information processing terms or describe the characterisioral routines that have become automated through repeti- tics of the situation in which the disability was shown. This
tion (like the ability to reach for an object and grasp it) and situation changed in the mid-1980s. Eslinger and Damasio
those one-time sequences of behavior that are created to (1985) described the case of E VR, who had undergone
deal with novel situations. One of the most common forms surgical removal of a large bilateral frontal meningioma.
of the latter behavioral sequences is where one wishes to At the time of his operation, E VR was a financial officer
528
P R IN C IP LE S
OF FRON TAL
LO B E FUN CTION
with a small company and a respected member of his community. He was married and the father of two children;
his brothers and sisters considered him a role model and a
natural leader. After the operation, however, E VR lost his
job, went bankrupt, was divorced by his wife, and moved in
with his parents. He subsequently married a prostitute and
was divorced again within two years. Extensive psychological evaluations found no deficit; in fact, he was superior or
above average on most tests (e.g., V I Q o f 125; PI Q of 124;
no difficulty on the WCST ). He was also able to discuss
intelligently matters such as the economy, foreign affairs,
financial matters, and moral dilemmas. Despite these
normal findings, E VR was often unable to make simple
everyday decisions, such as which toothpaste to buy, what
restaurant to go to, or what to wear. He would instead make
endless comparisons and contrasts, often being completely
unable to come to a decision at all. Further, Eslinger and
Damasio report prospective memory problems:" it was as if
he forgot to remember short- and intermediate-term goals"
(p. 1737).
Eslinger and Damasio's (1985) studywas the first empirical demonstration that this level of behavioral disorganization could occur in the context of intact intellect and
intact performance on some tests traditionally thought to
be sensitive to deficits in "frontal lobe" executive functions;
previously, there had only been observational reports.
However, although Eslinger and Damasio quantified the
degree of specificity of the impairment (i.e., by showing
normal performance on many neuropsychological tests),
they did not quantify the actual impairment itself.
Shallice and Burgess (1991) addressed this lacuna. They
presented the cases of three patients who had all suffered
frontal lobe damage following traumatic brain injury. All
three had no significant impairment on formal tests of perception, language, and intelligence, and two performed
well on a variety of traditional tests of executive function.
Indeed, one of these patients (AP) was probably the best
example of the syndrome so far reported (this patient was
later called " N M" by Metzler & Parkin, 2000). AP had sustained an open head injury in a road traffic accident when
he was in his early 20s. The injury caused a virtually complete removal of the rostral PFC bilaterally plus damage
to surrounding regions. O n standard neuropsychological
measures of intellectual functioning, memory, perception,
and even traditional tests of executive function, AP performed within the superior range.
However, AP did show cognitive impairment in other
situations (Metzler & Parkin, 2000; Shallice & Burgess,
1991). The most noticeable of these in everyday life was a
marked multitasking and prospective memory problem.
This manifested itself as tardiness and disorganization,
the severity of which ensured that despite his excellent
intellect and social skills, he never managed to return to
work at the level he had enjoyed premorbidly. Shallice and
Burgess (1991) invented two new tests of multitasking to
31
R O S TR AL P R EFR O N TAL C O R TEX
assess these problems. The first of these tests, called the
"Multiple Errands Test" (ME T ), was a real-life multitasking test carried out in a shopping precinct. Participants
have to complete a number of tasks, principally involving
shopping in an unfamiliar shopping precinct while following a set of rules (e.g., no shop should be entered other
than to buy something). The tasks vary in complexity (e.g.,
buy a small brown loaf of bread vs. discover the exchange
rate of the euro yesterday), and there are a number of " hidden" problems in the tasks that have to be appreciated and
the possible course of action evaluated (e.g., on one task,
participants must write and send a postcard, yet they are
given no pen, and although they cannot use anything they
haven't brought during the test to help them, they are also
told that they need to spend as little money as possible). I n
this way, the task is quite open-ended or ill-structured (i.e.,
there are many possible courses of action, and it is up to the
individual to determine which one he or she will choose).
The second task that Shallice and Burgess invented
was a more controlled experimental task (the "Six Element
Test" [SE T]). This required subjects to shift efficiently
between three simple subtasks, each divided into two sections, within 15 mins, while following some arbitrary rules
(e.g., "You cannot do part A of a subtask followed immediately by part B of the same subtask"). There are no cues as
to when to switch tasks, and although a clock is present, it
is covered, so that checking it has to be a deliberate action.
Thus, this paradigm has a strong component of voluntary
time-based task switching, that is, one form of prospective
memory.
Despite their excellent general cognitive skills, AP and
the other cases reported by Shallice and Burgess all performed these tasks below the 5% level compared with ageand IQ-matched controls. O n the ME T the subjects made
a wide range of errors. Many of these could be interpreted
as problems with prospective memory. For instance, they
had to go into the same shop more than once to buy items
that could all have been bought at one visit; they forgot to
carry out tasks that they had previously learned that they
needed to do, and they forgot to follow task rules. They also
made a range of social behavior errors (e.g., leaving a shop
without paying; offering sexual favors in lieu of payment).
Shallice and Burgess (1991) rather inelegantly termed this
kind of behavioral disorganization in the context of preserved intellect and other cognitive functions the "Strategy
Application Disorder."
It was not possible, on the basis of Shallice and Burgess's
data, to speculate on the anatomical localization of the
lesion critical for this pattern of deficit, since the patients
had large traumatic lesions that invaded many subregions.
Two years later, however, Goldstein et al. (1993) described
a case that began to suggest a possible locus. A 51-year-old
right-handed man (G N) had undergone a left frontal lobectomy 2.5 years earlier following the discovery of a frontal
lobe tumor (mixed astrocytoma-oligodendroglioma). zyxwvuts
529
A 5 cm resection of the left frontal lobe from the frontal
pole was undertaken. This surgery made little difference to
his general cognitive abilities (e.g., WAIS-R V I Q 129, PI Q
111; story recall immediate 75th-90th percentile, delayed
50th-70th percentile; Rey Osterreith delayed figure recall
80th-90th percentile; Trail-making 70th-75th percentile). However, it was clear from his everyday behavior
that something was seriously wrong. He had held a senior
management position in an international company, but
two years after surgery he had to take medical retirement
because of increasing lethargy. He worked from home as
a free-lance management consultant, but had difficulty
making decisions, culminating in his taking two weeks to
decide which slides to use for a work presentation but never
actually reaching a decision. He also experienced anger
control difficulties.
Goldstein et al. (1993) administered Shallice and
Burgess's (1991) ME T . G N made significantly more errors
than controls, being less efficient (e.g., havingto return to a
shop), breaking tasks rules (e.g., using a stamp that another
customer gave him), and misinterpreting tasks (e.g., sticking the stamp on the wrong card), as well as failing to complete some tasks altogether, reporting that he knew he had
to do them but somehow "forgot" them. He also showed
some "social rule" breaks. For instance, he had omitted to
find out the price of tomatoes earlier in the fruit and vegetable shop, and realizing that he should not go back there
unless he wanted to buy something, he very conspicuously
climbed onto the fruit display outside the shop and peered
in the window.
It was not until the study of Burgess et al. (2000), however, that the link between multitasking deficits and rostral
PFC damage was formally demonstrated by the principal
localizingmethod in neuropsychology: agroup lesion study.
Sixty patients with acute neurological damage from an
unselected series of referrals (approximately three-quarters
ofwhom were suffering from brain tumors) and 60 age- and
IQ-matched healthy controls were administered a multitasking test called the "Greenwich Test." This test follows
the principles of the SET but, in contrast, the majority of
the variance in test performance comes from rule infractions rather than task-switchingproblems. Participants are
presented with three different simple tasks and told that
they have to attempt at least part of each of the tasks within
10 min while following a set of rules. One of these rules
relates to all subtests ("In all three tasks, completing a red
item will gain you more points than completing an item of
any other color"), and there are four task-specific rules (e.g.,
" I n the tangled lines test you must not mark the paper other
than to write your answers down"). The test was administered in a form that allowed consideration of the relative
contributions of task rule learning and remembering, planning, plan following, and remembering one's actions in
relation to overall multitasking performance. Specifically,
before participants began the test, their ability to learn
530
the task rules (by both spontaneous and cued recall) was
measured. They were then asked how they intended to do
the test, and a measure of the complexity and appropriateness of their plans was calculated. This enabled us to look at
whether their failures could be due to poor planning. The
participants then performed the task itself, and by comparing what they did with what they had planned to do, a measure of plan following could be determined. Multitasking
performance was measured as the number of task switches
minus the number of rule breaks. After these stages were
finished, subjects were asked to recollect their own actions
by describing in detail what they had done. Finally, delayed
memory for the task rules was examined.
Burgess et al. (2000) found that lesions in different
brain regions were associated with impairment at different stages in the multitasking procedure. For instance,
lesions to a large region of superior posterior medial cortex
including the left posterior cingulate and forceps major led
to deficits on all measures except planning. Remembering
task contingencies after a delay was also affected by lesions
in the region of the anterior cingulate. Critically, however,
Burgess et al. found that patients with rostral PFC lesions
in the left hemisphere, when compared with patients with
lesions elsewhere, showed asignificant multitaskingimpairment despite no significant impairment in planning, or in
rememberingwhat they had done, or the task rules. Indeed,
the left rostral prefrontal patients showed no significant
impairment on any variable except the one reflecting multitasking performance. I n other words, despite being able
to learn the task rules, form a plan, remember their actions,
and say what they should have done, they nevertheless did
not do what they said that they intended to do.
The Burgess etal. (2001) result—an association between
rostral PFC lesions and multitasking impairments—has
now been replicated several times (e.g., Dreher et al., 2008;
Roca et al., 2010,2011) and thus seems secure. These studies have also opened up an entirely new area of inquiry (the
cognitive [neuro] science of multitasking) that did not exist
just a few years ago.
But what is the nature of the critical processing impairment shown by these patients? The multitasking situations
presented to a participant by the two experimental paradigms developed by Burgess and Shallice (ME T and SE T)
share a number of similarities. These are:
1. A number of discrete and different tasks have to be
completed.
2. Performance on these tasks needs to be dovetailed in
order to be time effective.
3. Due to either cognitive or physical constraints, only one
task can be performed at any one time.
4. The times for returns to task are not signaled directly
by the situation. zyxwvutsrqponmlkjihgfedcbaZYXW
P R IN C IP LE S
OF FRON TAL
LO B E
FUN CTIO N
5. There is no moment-by-moment performance feedback
of the sort that participants in many laboratory
experiments receive. Typically, failures are not signaled
at the time they occur.
with activation in lateral aspects of rostral PFC (Burgess,
Quayle, & Frith, 2001; Burgess, Scott, & Frith, 2003; den
Ouden, Frith, Frith, & Blakemore, 2005; G ilbert et al.,
2009; Okuda et al., 2011; Reynolds, West, & Braver, 2009;
Simons, Schoivinck, G ilbert, Frith, & Burgess, 2006. By
6. Unforeseen interruptions, sometimes of high priority,
contrast, ongoing tasks tend to activate medial rostral PFC
will occasionally occur, and things will not always go as
structures more than during the PM conditions (Burgess
planned.
et al., 2001, 2003; Hashimoto, Umeda, & K ojima, 2011;
7. Tasks usually differ in terms of priority, difficulty, and
Okuda et al., 2007; Simons, Schoivinck, G ilbert, Frith,
the length of time they will occupy.
& Burgess, 2006). Many of these rostral PFC activations
(either medial or lateral) seem surprisingly insensitive to
8. People decide for themselves what constitutes adequate
the
form of stimulus material presented, the nature of the
performance.
ongoing task, how easy or hard the PM cue is to detect, or
A key component of dealing with situations that have these how easy or hard the intended action is to recall (Burgess
characteristics (and that, incidentally, are very common et al, 2001; 2003; Simons, Schoivinck, G ilbert, Frith, &
in everyday life) is that they make demands upon prospec- Burgess,).
tive memory. "Prospective memory" (PM) is the ability to
Second, there does seem to be functional specializaenact delayed intentions, that is, to remember to carry out tion for different components, forms, and types of PM
an intended act in the future, while engaged in another for some regions within rostral PFC (Gilbert et al., 2009;
task (referred to as the "ongoing task"). zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA
Hashimoto, Umeda, & K ojima, 2011; Haynes et al., 2007;
Okuda et al., 2007; Simons, Schoivinck, G ilbert, Frith, &
Burgess,
2006). For instance, it appears that there might
Pro s pe ctive M e m o ry
be activation pattern differences during event-based verThere are three main forms of the PM situation: event-based, sus time-based paradigms. I t is too early in the course of
time-based, and activity-based. I n event-based PM situa- investigations in this field to be certain, but it is possible,
tions, one intends to carry out the action (or thought) in on the basis of current evidence, that the rostral PFC actiresponse to an event, typically a prospective memory "tar- vations that occur during time-based PM conditions tend
get" or "cue". I n time-based PM conditions, the intention to be more medial than those occurring during eventis to carry out the act at a particular time (e.g., at 3 p.m. or based conditions. Other factors that seem to affect rostral
30 min from now), regardless of what else is occurring. These PFC activations during PM paradigms include variation
are by far the most commonly studied forms. The third, and in implicit cues (Hashimoto et al., 2010), the nature of
less well understood PM situation, activity-based PM, is where the intention itself (Haynes et al., 2007), the form of the
the intention is to do something when one is engaged in a par- instruction given (Gilbert et al., 2009), and the characterticular activity (e.g., "The next time I go surfing (regardless of istics of intention retrieval (Simons, Schoivinck, G ilbert,
when or where), I will do X " ), or at the start or cessation of it. F rith, & Burgess, 2006). I n general, the patterns of rosThe link between PM and rostral PFC was first high- tral PFC activation seem less affected by differences in the
lighted by Burgess and colleagues (e.g., Burgess, Quayle, particular stimuli used (e.g., words, pictures) than they do
& Frith, 2001; Burgess, Scott, & Frith, 2003) using func- by other aspects of the paradigm, such as those that affect
tional neuroimaging. Subsequent studies by this group higher-level aspects of cognition. This may be the reason
and others have shown this to be a remarkably consistent why apparently small changes in task instruction can have
association. Indeed, all currently published neuroimaging a marked effect upon the patterns of activation in rostral
studies in which a straightforward comparison has been PFC (Gilbert et al., 2009) and why broader environmental
made between a condition requiring the maintenance of a aspects that might affect strategic behavior may also have
delayed intention and ongoing task performance only have an effect (e.g., whether a clock is present or not during timeshown activation within rostral PFC (see Burgess et al., based PM tasks; Okuda et al., 2007). But perhaps the biggest clue to the nature of the cognition that at least some of
2011, for review).
A full review of what we have learned so far from this these rostral PFC activations are indexing is given by the
technique about the role of rostral PFC in PM is given in fact that they can be seen during PM tasks even when no
Burgess et al. (2011). Some of the most consistent or prom- targets are encountered (Burgess et al., 2001); it is enough
that participants merelyzyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQ
expect a target to occur. However,
ising findings are outlined in Table 31-1.
A key finding is that PM performance does not acti- these patterns of activation can be so specific that one
vate all subregions within rostral PFC equally. As shown can use them to predict which intentions a participant is
in Figure 31-1, during event-based tasks, maintenance considering (Haynes et al., 2007). Moreover, this appears
of the intention over the delay period while the partici- not to be reducible to the notion of "working memory" in
pant is occupied with another task tends to be associated one of its many guises. There are regions of lateral rostral zyxwvutsr
31.
R O S TR AL PR EFR O N TAL
C O R TEX
531
TAB LE 3 1 - 1
zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA
PRIN CIPLES OF ROS TRAL PFC ACTIVATION IN PROS PECTIVE MEMORY TAS KS ACCORDING
GONEN-YAACOVI, AND
TO
B URG ES S ,
VOLLE (2 0 1 1 )
Se e m ingly S e cure Findings
1.
Pe rfo rm a nc e o f p ro s p e c tive m e m o ry p a ra d igm s , re la tive to th e o ngo ing ta s k a lo ne , is typ ic a lly a c c o m p a nie d by a c tiva tio ns within ro s tra l
PFC (a ppro xim a te ly, BA 1 0 ; Burge s s e t a l., 2 0 0 1 , 2 0 0 3 ; d e n Oude n e t a l., 2 0 0 5 ; Gilb e rt e t a l., 2 0 0 9 ; Ha s him o to e t a l. , 2 0 1 0 ; Hayne s e t a l.,
2 0 0 7 ; Okuda e t a l., 1 9 9 8 , 2 0 0 7 ; Po ppe nk e t a l. , 2 0 1 0 ; Re yno lds e t a l., 2 0 0 9 ; S im o ns , Sc ho ivinc k e t a l., 2 0 0 6 ).
2.
Ac tiva tio ns d uring o ngo ing o r (m o s t) c o ntro l ta s ks in m e d ia l ro s tra l PFC s truc ture s te nd to be highe r tha n d uring PM c o nd itio ns (Burge s s
e t a l., 2 0 0 1 , 2 0 0 3 ; Ha s him o to e t a l., 2 0 1 0 ; Okuda e t a l., 2 0 0 7 ; S im o ns , Sc ho ivinc k e t a l., 2 0 0 6 ) .
3.
Ma inte na nc e o f an inte ntio n o ve r a de lay pe rio d d uring whic h the p a rtic ip a nt is fully o c c up ie d with a no the r ta s k te nd s to be a s s o c ia te d with
a c tiva tio n in la te ra l a s p e c ts o f ro s tra l PFC (Burge s s e t a l. , 2 0 0 1 , 2 0 0 3 ; d e n Oude n e t a l. , 2 0 0 5 ; Gilb e rt e t a l. , 2 0 0 9 ; Okuda e t a l. , 2 0 1 1 ;
Re yno lds e t a l., 2 0 0 9 ; S im o ns , Sc ho ivinc k e t a l., 2 0 0 6 ) .
4.
So m e o f the s e ro s tra l PFC a c tiva tio ns (e ithe r m e d ia l o r la te ra l) s e e m re m a rka b ly ins e ns itive (at le a s t with e ve nt-b a s e d ta s ks ) to the fo rm
o f s tim ulus m a te ria l p re s e nte d , the na ture o f the o ngo ing ta s k, ho w e a s y o r hard th e PM c ue is to d e te c t, o r ho w e a s y o r hard th e inte nd e d
a c tio n is to re c a ll (Burge s s e t a l., 2 0 0 1 , 2 0 0 3 ; Sim o ns , Sc hdlvinc k e t a l., 2 0 0 6 ) .
5.
Ho we ve r, fo r o the r re gio ns within ro s tra l PFC, the re d o e s s e e m to be func tio na l s p e c ia liza tio n fo r d iffe re nt c o m p o ne nts , fo rm s , a nd typ e s
o f PM. For ins ta nc e , a c tiva tio n in s ub s e c tio ns o f th is re gio n c a n be s e ns itive to c ha nge s in the na ture o f wha t is inte nd e d (Hayne s e t a l.,
2 0 0 7 ); in ta rg e t re c o gnitio n ve rs us inte ntio n re trie va l d e m a nd s (Sim o ns , Sc ho ivinc k e t a l., 2 0 0 6 ) ; whe the r the ta s k is tim e -b a s e d o r
e ve nt-b a s e d (Okuda e t a l., 2 0 0 7 ); a nd th e na ture o f th e PM c ue ing pro c e d ure (s p o nta ne o us vs . c ue d ; Gilb e rt e t a l., 2 0 0 9 ) .
6.
The re is fre q ue nt a c tiva tio n o f th e p re c une us , p a rie ta l lo b e (BA 7 a nd 4 0 ) a nd o fte n a ls o o f th e a nte rio r c ingula te (BA 3 2 ) d uring th e
p e rfo rm a nc e o f PM ta s ks (Burge s s e t a l., 2 0 0 1 ; de n Oude n e t a l., 2 0 0 5 ; Es c he n e t a l., 2 0 0 7 ; Gilb e rt e t a l., 2 0 0 9 ; Ha s him o to e t a l. , 2 0 1 0 ;
Okuda e t a l., 1 9 9 8 , 2 0 0 7 , 2 0 1 1 ; Po ppe nk e t a l., 2 0 1 0 ; Re yno lds e t a l., 2 0 0 9 ; Sim o ns , Sc ho ivinc k e t a l„ 2 0 0 6 ) . So m e o f the s e re gio ns are
o fte n c o a c tiva te d with ro s tra l PFC d uring many typ e s o f c o gnitive ta s ks , no t ju s t PM o ne s (Gilb e rt e t a l., 2 0 1 0 ). But th e s ignific a nc e o f the s e
c o a c tiva tio ns re m a ins to b e d is c o ve re d .
Prom is ing Findings That Could Be ne fit from Re plication
7.
In e ve nt-b a s e d PM ta s ks , a p p a re ntly s m a ll c ha nge s in ta s k ins truc tio n c an have a m a rke d e ffe c t upo n the p a tte rns o f a c tiva tio n in ro s tra l
PFC (Gilb e rt e t a l., 2 0 0 9 ).
8.
(Re la te d to [5 ] ab o ve .) The re is a d iffe re nc e in a c tiva tio ns in ro s tra l PFC a c c o rd ing to whe the r the PM ta s k is tim e - o r e ve nt-b a s e d (Okuda
e t a l. , 2 0 0 7 ) .
9.
(Re la te d to [5 ] ab o ve .) In tim e -b a s e d ta s ks , a c tiva tio n p a tte rns in ro s tra l PFC may c hange a c c o rd ing to whe the r a c lo c k is a va ila b le fo r th e
p a rtic ip a nt to us e (Okuda e t a l. , 2 0 0 7 ). This may be due to d iffe re nc e s in c lo c k m o nito ring o r tim e e s tim a tio n c a us e d by s uc h m a nip ula tio n.
10.
Ro s tra l PFC a c tiva tio ns c an b e s e e n d uring PM ta s ks e ve n whe n no ta rg e ts are e nc o unte re d (Burge s s , Quayle & Frith, 2 0 0 1 ); it is e no ugh
th a t p a rtic ip a nts m e re ly e xpe c t ta rg e ts (s e e a ls o Ma rtin e t a l., 2 0 0 7 ).
11.
The re are re gio ns o f la te ra l ro s tra l PFC (BA 1 0 ) tha t are a c tiva te d d uring e ve nt-b a s e d PM ta s ks th a t are
zyxwvutsrqponmlkjihgfedcbaZYXWVUTS
not a ls o a c tiva te d d uring wo rking
m e m o ry d e m a nd s (Re yno lds e t a l., 2 0 0 9 ) .
12.
So m e a c tiva tio n p a tte rns within PFC (inc lud ing re gio ns o f m e d ia l a nd ro s tro la te ra l PFC) are s o ta s k-s p e c ific tha t o ne c a n us e th e m to p re d ic t
whic h inte ntio ns a p a rtic ip a nt is c o ns id e ring (Hayne s e t a l., 2 0 0 7 ). Ho we ve r, a c tiva tio n in o the r ro s tra l re gio ns (with p o s s ib ly a m o re a nte rio r
la te ra l lo c a tio n) is unre la te d to th e s p e c ific s o f th e inte ntio n; ins te a d , th e s e a re a s are c o a c tiva te d with m o re p o s te rio r re gio ns within th e
b ra in tha t are re la te d to the inte ntio n (Gilb e rt, 2 0 1 1 ).
13.
Ro s tra l PFC a c tiva tio ns are no t ne c e s s a rily s yno nym o us with "c o ns c io us th o u g h t" (Okuda e t a l., 2 0 1 1 ; Ha s him o to e t a l. , 2 0 1 0 ) s inc e the y
c a n o c c ur a lo ngs id e b e ha vio ra l (and pre s um a b ly the re fo re m e nta l) c ha nge s (e .g., re a c tio n tim e ) o f whic h th e p a rtic ip a nt is una wa re .
14.
So m e inve s tiga to rs have fo und la te ra l BA 1 0 s us ta ine d re s p o ns e s d uring PM c o nd itio ns (Burge s s , Quayle & Frith, 2 0 0 1 ; Re yno lds e t a l.,
2 0 0 9 , Table 1 , p. 1 2 1 5 ). Ho we ve r, o the rs have fo und la te ra l BA 1 0 to be tra ns ie ntly a s s o c ia te d with d e te c tio n o f PM ta rg e ts (Gilb e rt
e t a l., 2 0 0 9 , in Table 2 , p. 9 1 1 , e xp lic itly d is c us s e d o n p. 9 1 2 ). The re is th u s e vid e nc e fo r b o th s us ta ine d a nd tra n s ie n t e ffe c ts in la te ra l
BA 1 0 d uring PM ta s ks . The re a s o n fo r th e s e d iffe re nc e s b e twe e n s us ta ine d o r tra n s ie n t a c tiva tio ns a c ro s s s tud ie s is no t c urre ntly we ll
und e rs to o d b ut s e e m s a p ro m is ing ave nue fo r future s tud y.
zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCB
PFC (BA 10) that are activated during event-based PM remember to hand back to the examiner, at the end of testtasks that arezyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA
not also activated during working memory ing, a card given to them at the beginning. They examined
demands (Reynolds et al., 2009). Furthermore, the activa- the relation between performance on this task and damage
tions that occur during PM tasks are not necessarily syn- to 12 different brain regions previously identified by neuonymous with "conscious thought": Okuda et al. (2011) roimaging studies as involved in PM. Using discriminant
have shown that changes in target frequency can provoke function analysis, Umeda et al. reported that damage to
both activation of some subregions of rostral PFC and three brain regions was particularly associated with PM
significant behavior changes, yet the participant may be failure: right dorsolateral PFC, involving sections of BA 9
completely unaware (in the sense of being able to verbally and the superior sections of BA 10 and 46; right ventromereport) of the effect of these contingency changes upon his dial PFC, involving B A 11 and 47 and inferior parts ofB A
or her behavior or mental life.
10 and 46; and left dorsomedial PFC, involving BA 9 and
Very recently, human group lesion studies have con- superior parts of BA 10. Interestingly, as predicted by both
firmed that rostral PFC damage is not only involved in the single-case studies (e.g., Shallice & Burgess, 1991) and
PM performance but is necessaryforit. Umeda et al. (2011) the group lesion studies (e.g., Burgess et al., 2000), Umeda
asked a group of 74 patients with traumatic brain injury to et al. also found no difference between those who failed the
532
P R IN C IP LE S
OF
FRON TAL LO B E
FUN CTIO N
PM task and those who passed on a range of neuropsycho- And there is a meeting point between studies of these cognitive phenomenon and prospective memory not only in
logical tests not involving PM.
The degree of specificity of this cognitive deficit is amply a conceptual sense, but also in the prominent findings of
demonstrated in another recent group lesion study (Voile, rostral PFC activation when people are imagining future
Gonen-Yaacovi, de Lacy Costello, G ilbert, & Burgess, scenarios (e.g., Addis, Wong, & Schacter, 2007).
2011). We assessed both time-based and event-based PM
Burgess et al. (2011) present a meta-analysis of
using two types of material, words and pictures, for each. neuroimaging studies involving future thinking (see
I n addition, we administered tests of time estimation, sus- Figure 31-1). A considerable caveat needs to be applied
tained attending, target detection, inhibition, and ability to this analysis: the field of "future thinking" or, perhaps
to deal with multiple instructions. These tests were given to more elegantly, "prospection" (also sometimes called "men45 patients with focal brain lesions and 107 healthy control tal time travel"), is in its infancy, so it would be premature
subjects. We found that lesions in the right rostral (polar) to draw strong conclusions from the patterns of activation
prefrontal region (in BA 10) were specifically associated demonstrated so far. However, as Figure 31-1 shows, roswith a deficit in time-based PM tasks for both words and tral PFC activations appear to be extremely common in
pictures. This deficit could not be explained by impair- studies of prospection; this frequency may be higher than
ments in attending, target detection abilities, inhibition, for perhaps any other function examined so far in this conor ability to deal with multiple instructions, and there was text, except perhaps prospective memory. But as there are
also no significant deficit in event-based PM conditions. currently few if any comprehensive information processing
(This may be particularly noteworthy in reference to the models of the demands made by prospection, it is difficult
predominantly right lateralized finding of Umeda et al. to ascertain the significance of this finding for understand[2011] with their activity-based PM task.)
ing either prospection or the role of rostral PFC structures
I n addition to their PM difficulties, the patients with in supporting it. However, the consistency of the findings
right rostral frontal lobe lesions were significantly impaired is striking, and this bodes well for future discoveries.
in time estimation ability compared to other patients.
Thus, Voile et al.'s (2011) findings suggest that time-based
R O S TR A L P FC IS IN VO LVED IN M E TA M E M 0 R Y :
and event-based PM might be supported at least in part by
S O U R C E AND C O N TE X T M EM O R Y AND
R E A LITY
distinct brain regions, and that the same cognitive mechaM O N ITO R IN G ( P O IN T 9 )
nisms that are required for estimating the unfilled passage
of time (especially when changes of timing are involved) The term "metamemory" refers to a range of cognitive
might also be involved in time-based PM (although the operations during which a person deliberates over their
design did not, of course, enable us to exclude the possibil- own memory processes or traces, searching, editing, reconfiguring, and recombining traces or representations to
ity that this finding is an epiphenomenon).
More generally, the cognitive neuroscience of PM, and form new insights. This is often prompted by a failure of
especially the role of rostral PFC in it, is an area of inquiry more automatic recognition and recall processes. Many
that is moving extremely rapidly, and where there is good examples of this kind of processing in everyday life recolconcordance between the indications from neuroimaging lection are given in Burgess and Shallice (1996a). This kind
and those from lesion studies. This seems very promising of processing is typically measured experimentally using
for future discoveries (see Burgess et al., 2011, for further paradigms tapping constructs such as "source memory,"
"context memory," or "reality monitoring." All of these pardiscussion). zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA
adigms provoke high-level memory control/metamemory
processing because they ask for information that was not
R O S TR A L P FC IS IN VO LVED IN IM AG IN IN G THE
central to the representation (indeed, was often incidental)
F U TU R E ( P R O S P E C T IO N ) ( P O IN T 8 )
when it was encoded. A fairly typical example is given by
Aside from the (largely) rather experimentally constrained Simons, G ilbert, Owen, Fletcher, and Burgess (2005), a
paradigms from the cognitive neuroscience literature study in which two temporally distinct lists of items were
(see, e.g., the large body of work relating to Shallice and presented. I n each list, participants were cued to make one
McCarthy's Tower of London test; Shallice, 1982; see of two different kinds of semantic judgments about people
Burgess, Simons, Coates, & Channon, 2005, for review), identified either by their face or by their name. Then the
relatively little attention has been given, until recently, to participants were asked either whether a particular stimuinvestigation of how people plan for and envisage future lus had appeared in the first or second list of stimuli (i.e., to
situations. However, in the last few years there have been test temporal source memory) or which of the two semanexciting developments on this front (Addis, Pan, Vu, tic judgments they had made in response to it (context
Laiser, & Schacter, 2009; Schacter, Addis, & Buckner, recollection).
2007, 2008; Szpunar, Watson, McD ermott, 2007;
By contrast, in a reality monitoring paradigm, the key
Weiler, Suchan, & Daum, 2010a,b; Williams et al., 1996). component is that the participant is required to distinguish
31.
R O S TR AL PR EFR O N TAL
C O R TEX
533
(A)
• S u m m e rf ie ld e t a l. 2 0 1 0
zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA
• D'Arge m b e a u e t a l. 2 0 1 0
i
i
>
T
R
i
!
™ *™
"K !
Ai, . \. i
i
D'Arge m b e a u e t a l. 2 0 1 0
x D'Arge m b e a u e t a l. 2 0 0 8
+ Po p p e nk e t a l. 2 0 1 0
•
H
Ab ra h a m e t a l. 2 0 0 8
zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA
a S p re n g a nd Gra d y 2 0 0 9
o Ad d is e t a l. 2 0 0 9
f\
u_i L_
*
Ad d is a nd S c ha c te r 2 0 0 8
A Ad d is e t a l . 2 0 0 7
0
B o tz u n g e ta l. 2 0 0 8
- S z p u n a re t a l. 2 0 0 7
• Okud a e t a l. 2 0 0 3
• Okud a e t a l. 2 0 0 7
a Okud a e t a l. 2 0 0 7
• Burge s s e t a l. 2 0 0 1
• S im o n s e t a l. 2 0 0 6
• Gilb e rt e t a l. 2 0 0 9
o d e n Oud e n e t a l . 2 0 0 5
A Be no it e t a l., in p re p ,
o Re yno ld s e t a l. 2 0 0 9
% Okud a e t a l. 1 9 9 8
• Ha s h im o to e t a l . 2 0 1 0
0 Okud a e t a l. s u b m itte d
• Burge s s e t a l. 2 0 0 3
• S im o ns e t a l. 2 0 0 6
• Be no it e t a l., in p re p .
Tim e -b a s e d
zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDC
Eve nt-b a s e d
Ongo ing
zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQ
• Okud a e t a l. 2 0 0 7
zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA
Pane l C s ho ws the typ ic a l p a tte rn o f ro s tra l PFC a c tiva tio ns fo und d uring e ve nt-b a s e d p ro s p e c tive
Figure 31-1
m e m o ry ta s ks . The to p pa ne l s ho ws
a c tiva tio ns o c c urring while m a inta ining an inte ntio n; the b o tto m pane l s ho ws the highe r m e d ia l ro s tra l PFC a c tiva tio ns tha t o c c ur whe n p e rfo rm ing the
o ngo ing ta s k o nly (c o m pa re d with p e rfo rm ing the o ngo ing ta s k + m a inta ining an inte ntio n). Pane l A: m e ta -a na lys is fro m Burge s s e ta l. (2 0 1 1 ) s ho wing
c o ns is te nt ro s tra l PFC a c tiva tio ns fro m ne uro im a ging s tud ie s o f p ro s p e c tio n (e .g., future thinking ). Pane l B: m e ta -a na lys is fro m Burge s s e ta l. (2 0 1 1 )
o f a c tiva tio ns d uring b o th tim e -a n d e ve nt-b a s e d PM e xp e rim e nts in the lite ra ture , whe re s im p le c o ntra s ts b e twe e n PM c o nd itio ns and the o ngo ing ta s k
have b e e n m a d e .
zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA
between something that was witnessed and something recollection: recollection of whether stimuli had previthat was just imagined. An example is given in Simons, ously been perceived or imagined and recollection of which
Davis, G ilbert, Frith, & Burgess (2006). Participants first of two temporally distinct lists where the stimuli belonged.
studied either well-known word pairs or the first word of Lateral regions of rostral PFC were activated in both tasks.
a word pair accompanied by a question mark, which were However medial regions of rostral PFC were activated only
presented either on the left or right side of a monitor screen. when participants were required to recollect source inforThey were cued to view each word pair and either to look mation for self-generated, "imagined" stimuli (see also
at, or to imagine, the second word of each pair and to count Simons, Davis, G ilbert, Frith, & Burgess, 2006). I n addithe number of letters it contained. I n the subsequent test tion, reduced activity in a region of medial ventrocaudal
phase, the first word of each word pair was presented again, PFC/basal forebrain was associated with making "imagand participants were asked to say either whether the sec- ined-to-perceived" confabulation errors. Thus, it seems at
ond word in the word pair had been seen or imagined (real- present that lateral rostral PFC is involved in a very broad
ity monitoring) or, in a contrast condition, whether the way with performance of this whole class of metamemory
word pair had been presented on the left or right side of the tasks, and that there appears to be an additional more specific relation between medial rostral PFC (and adjoining
screen (i.e., testing position context memory).
The remarkable aspect of all these paradigms from medial PFC regions) and making perceived/imagined
the point of view of rostral PFC is that, despite varying judgments (i.e., "reality monitoring") (see Figure 31-2).
But if these lateral rostral PFC activations in particular
greatly in the nature of the stimuli presented, the questions asked of the participants, what they had to remember, are the signature of a cognitive process that is used across all
and how they gave their answer, every paradigm activates of these tasks, what might this process be? We will address
(when contrasted with a suitable baseline) very similar this further below. However, it might be noted at this point
parts of rostral PFC (e.g., Cansino, Maquet, Dolan, & that what participants report about their thought proRugg, 2002; Dobbins, Foley, Schacter, & Wagner, 2002; cesses when trying to answer these context-type questions
Fan, Snodgrass, & Bilder, 2003; Mitchell, Johnson, Raye, is similar to the processes that Burgess and Shallice (1996a)
& Greene, 2004; Nolde, Johnson, & D'E sposito, 1998; identified in their study of the control of recollection of
Ranganath, Johnson, & D'E sposito, 2000; Raye, Johnson, everyday life events. One participant described it as "walkMitchell, Nolde, & D'E sposito, 2000; Rugg, Fletcher, ing around the mind's eye," that is, a disengagement from
Chua, & Dolan, 1999). Turner etal. (2008) shows the typi- attending to the external world, and attempted generation
cal pattern. They used event-related functional magnetic of the desired representation in the imagination, with the
resonance imaging (fMRI ) to contrast two forms of source aim of seeing if this process might yield information to
534
P R INCIP LES
OF FRONTAL
LOBE
FUNCTION
(A)
Pe rce ive d/ Im a gine d &
(B)
Ta s k & Pos ition Me m ory >
Te m poral Orde r > New
(C)
Ba s e line
(E)
Lis t & Ta s k Me m ory :
Ba s e line
Activation in the m PFC (picture d) s ignifica ntly corre la te d with
the like lihood of m is a ttributing im agine d ite m s a s pe rce ive d
(D)
Im a gine d a t s tudy >
Pe rce ive d a t s tudy
zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA
-.1 0
-. 0 5 -. 0 0 -. 0 5
-. 1 0 -. 1 5
-. 2 0 -. 2 5 -. 3 0
-. 3 5
Percent signal change in medial ante rio r pre tro ntal cortex
Figure 3 1 -2
zyxwvutsrqponmlkjihgfedcbaZYX
Typic al ro s tra l a c tiva tio ns d uring s o urc e a nd c o nte xt m e m o ry e xp e rim e nts . Pane l B s ho ws a c o ntra s t fro m Sim o ns , Owe n, e ta l. (2 0 0 5 ) whe re
m e m o ry fo r the ta s k s o m e o ne had p e rfo rm e d with a s tim ulus wa s c o ntra s te d with re c a lling whe re o n the s c re e n the s tim ulus ha d a p p e a re d . Pane l C
s ho ws a c tiva tio ns fro m Sim o ns , Gilb e rt, e ta l. (2 0 0 5 ) whe re lis t a nd ta s k m e m o ry we re c o ntra s te d . Altho ugh the s e two s tud ie s te s te d d iffe re nt s a m p le s
o f p a rtic ip a nts a nd m a de d iffe re nt s o urc e / c o nte xt m e m o ry c o n tra s ts , the la te ra l ro s tra l PFC a c tiva tio ns are ve ry s im ila r. Pane l A: re s ults fro m Turne r
e ta l. (2 0 0 8 ). La te ra l ro s tra l PFC is a ls o c o m m o nly a c tiva te d whe n m a king te m p o ra l o rd e r a nd p e rc e ive d / im a gine d ju d g m e n ts . But m e d ia l re gio ns o f
ro s tra l PFC a re a c tiva te d whe n p a rtic ip a nts a re re q uire d to re c o lle c t s o urc e info rm a tio n fo r s e lf-g e ne ra te d , "im a g in e d " s tim uli (Pane l D, Turne r e ta l. ,
2 0 0 8 ) . Finally, Pane l E s ho ws re s ults a d a p te d fro m Sim o ns Da vis , Gilb e rt, Frith, & Burge s s , (2 0 0 6 ): s ignific a nt c o rre la tio n a c ro s s p a rtic ip a nts b e twe e n
re d uc e d a c tiva tio n in m e d ia l a nte rio r PFC (p ic ture d ) a nd m is a ttrib utio ns o f im a gine d s tim uli a s ha ving b e e n p e rc e ive d , re info rc ing the ro le o f m e d ia l
ro s tra l PFC in this a b ility.
zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA
answer the question. But there are other strategies people
seem to use as well. Sometimes people will report, especially during reality monitoring paradigms, alternating
between attending intently to the stimuli and introspecting on the level of familiarity it provokes, with the aim of
getting a " feeling" for the answer.
R O S TR A L
AND
P FC IS
AW AR EN ES S
IN VO LVED
IN
IN TR O S P E C TIO N
OF C O M P E T E N C E ( P O IN T
10)
The argument, therefore, is that at least some of the activations seen during the paradigms mentioned above are due
to this introspective process of walking around the mind's
eye. This interpretation is given more plausibility by the
evidence of involvement of rostral PFC activation during
paradigms that aim directly to instigate a mental state of
introspection. An example of this latter mental state might
be a situation where you are asked to rate your confidence
that you are correct about something.
Fleming et al. (2010) designed a task of this kind.
They showed people perceptually similar displays, but
one of them had a distinct feature they had to detect (a
high-contrast Gabor patch). They varied the difficulty of
this task to ensure that for all participants, performance
remained about 71%. Each time after the participants had
given their answer, they were asked to rate how confident
31.
ROS TRAL PREFRONTAL CORTEX
they were that they were correct. Using the accuracy of
these judgments as a measure of introspection, Fleming
et al showed a correlation between this behavioral measure
and gray matter volume in rostral PFC (BA 10; peak voxel
coordinates: 24,65,18).
A similar principle was followed by Miele et al. (2011).
I n their task, participants used a trackball to move a cursor to touch certain objects scrolling down a screen
and avoid others. The program sometimes introduced
noise geared to the degree of precision with which the
cursor followed the inputs to the trackball so that the participant would feel out of control. D uring these phases,
Miele et al. found increased activity in the right temporoparietal junction and other nonfrontal regions. By contrast,
when participants were more in control, activitywas seen in
regions linked to self-initiated action (e.g., the pre-supplementary motor area, dorsal striatum, anterior cingulate).
However, importantly, when the activation that occurred
during participants' judgments about the extent to
which they were in control was contrasted with activation
during their judgments about their own performance,
Miele et al. found increased activity in rostral PFC (—20,
50, 20) during the former compared with the latter situation. So, at least in this context, this region seems to be
more involved in judgments of agency rather than of
performance.
535
R O S TR A L
AND
P FC IS
IN VO LVED
IN
M E N TALIZ IN G
yes," "unsure no," "sure no"). So, the correct response was
zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA
11)
"yes" only for old/same words but "no" for both old/differ-
S E L F - JU D G M E N T ( P O IN T
ent and new words, and participants would only respond
The intriguing differences between the locations of the
"old," if the word was previously seen in the specified task.
regions identified by Fleming et al. (2010) and Miele et al.
For example, they might have encountered the trait "edu(2011) perhaps create the possibility that different forms of
cated" during a Self Study phase and "modest" during an
introspection, metacognition, or self-judgment may actiOther Study phase before seeing both words again during a
vate different subregions of rostral PFC.
self test phase. I n this case, they would have had to respond
One can see local hemodynamic changes with very
"yes" to the old/same word "educated" but "no" to the old/
fine-grained differences in the type of judgment that is
different word "modest."
being made when one turns to the arena of "mentalizing"
We found that there was a positive correlation between
or "self-judgment." Schmitz et al. (2004) employed a parasignal change in medial rostral PFC for self versus friend
digm that requiredpeople to make decisions about howwell
judgments and subsequent memory for the reference
adjectives that were presented to them described themselves
of such judgments. So, these results link hemodynamic
or other people they knew (plus a purely semantic positive
changes in medial rostral PFC to both personality judgvalence judgment control condition). These adjectives comments about oneself and subsequent episodic memory
prised a wide selection of personality traits such as "daring"
retrieval of these judgments. But the hemodynamic effects
or "intelligent" as well as physical traits such as "weak."
showed even greater specificity. The degree to which blood
Comparing the self-evaluation with the semantic control
oxygen level-dependent (BO LD ) signal in this region was
condition, Schmitz et al. found significant activation in a
associated with thinking about others correlated with the
network that involved medial rostral PFCzyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA
(x,y, z of maxima
perceived similarity of the traits to oneself in both tasks.
= 6, 56, 4) and medial orbitofrontal cortex (-4, 18, -10),
Moreover, participants who perceived themselves as having
as well as retrosplenial cortex (2, -60, 16) and thalamus
traits similar to those of their friend tended to be poorer at
(2, -24, 2). A very similar pattern was found when people
remembering whether they had made trait judgments in
made judgments about other people (compared with the
reference to themselves or their friend. So, the behavioral
same control condition), with activation in rostral medial
effect was reflected in the B O LD signal in medial rosPFC (-4, 58, 4), retrosplenial cortex, and thalamus. But
tral PFC: there was a positive correlation between signal
direct comparison of judgments about oneself versus judgchange for self versus friend judgments and subsequent
ments about other people revealed activation bilaterally in
memory for the reference of such judgments. These results
dorsolateral PFC and parahippocampal gyrus, with higher
therefore suggest a link between medial rostral PFC activactivation for self-judgments. So, these results perhaps sugity and a "psychological similarity" effect in making pergest that (medial) rostral PFC is involved in personality
sonality judgments.
trait judgments in a fairly broad way.
However, Benoit et al. (2010) showed a more specific
relation. Their study built upon that of Schmitz et al.
(2004), also using f MR I . Functional MR I was used while
two factors were crossed: (1) engaging in personality trait
or episodic source memory judgments and (2) the source
memory for these judgments (i.e., oneself or a friend).
Participants alternated between study and test phases. I n
a "self" study condition, they judged how well a set of personality traits described them. I n a second, "other" study
condition, they made similar judgments in reference to
their best friend. There was also a control condition during which participants were asked to judge the number
of syllables of the trait words (i.e., two, three, four, or five
syllables). Test phases also consisted of self, other, and syllables conditions. For each condition of the test phase (i.e.,
self, other, syllables), words were presented that were either
previously encountered in the respective study condition
(old/same words) or in the other two study conditions (old/
different words) or were not shown before (new words).
Participants were asked to accept only old/same words
and reject both old/different and new words. Responses
were always given on a 4-point scale ("sure yes," "unsure
536
R O S TR A L
P FC
A N A LO G IC A L
IN TE G R ATIO N
IS
IN VO LVED
R E A S O N IN G
( P O IN T
IN
AND
M E TA LE A R N IN G :
R E LA TIO N A L
12)
How do we learn from our experience ? I f each lesson learned
resided as a unique experience, to be considered only when
exactly the same situation that had provoked it recurred,
then humans would be limited in their development purely
by time and experience, and imagination would count
for nothing. But this is not how we learn. Instead, we are
constantly detecting similarities between situations and
looking for parallels between them in order to applylessons
learned from one situation to another. This is the crux of
"analogical reasoning." I n this form of thought, a familiar
situation (referred to as the "source") is used to make inferences about a less familiar situation (called the "target"),
and out of this process can emerge a more abstract schema
that encompasses structural aspects of both. Thus, two of
the most influential theories, the "structure mapping
theory" of Gentner and colleagues (e.g., Gentner 1983;
Gentner & Holyoak, 1997; Gentner, Ratterman, & Forbus,
1993) and the "multiconstraint theory" of Holyoak and
P R IN C IP LE S
OF FRON TAL
LO B E
FUN CTIO N
colleagues (e.g., Holyoak & Thagard 1995,1997), mapping a more general role in cognition. So, what might this more
between source and target, involves seeking commonalities general role be? zyxwvutsrqponmlkjihgfedcbaZYXWVUTS
not only in elements between the two situations, but also
between relations that link those elements. I n this sense,
R O S TR A L P FC IS IN VO LVE D IN
D IR E C TIN G
analogical reasoning shares considerable overlap with
ATTE N D IN G E ITH E R TO THE E X TE R N A L W O R LD
"relational integration" (see Voile et al., 2010, for further
OR TO OUR OW N IN N ER M EN TAL L IF E ( TH E
detail).
R O S TR A L P FC A TTE N TI0 N A L G ATEW AY)
There is good evidence for the involvement of rostral
( P O IN T 1 3 )
PFC in both analogical reasoning and relational integration. As Voile et al. (2010) point out, although there have Burgess and colleagues (e.g., Burgess, Simons, Dumontheil,
been relatively few studies of analogical reasoning and rela- & G ilbert, 2005; Burgess, Dumontheil, & G ilbert, 2007;
tional integration, those that have been performed have Burgess, G ilbert, & Dumontheil, 2007; Burgess, G ilbert,
consistently suggested that rostral PFC structures support Okuda, & Simons, 2006) sought to try to discover whether
some aspect of the processing that is involved (e.g., Bunge, the involvement of rostral PFC in all of the cognitive abiliHelskog, & Wendelken, 2009; Bunge, Wendelken, Badre, ties outlined above (e.g., multitasking, prospective mem& Wagner, 2005; Christoff et al., 2001; Green, Fugelsang, ory, metamemory, competence judgments, mentalizing,
Kraemer, Shamosh, & Dunbar, 2006; Kroger et al., 2002; self-judgment, analogical reasoning, relational integraPrabhakaran et al., 1997; Wendelken, Nakhabenko, tion) might reflect the operation of a cognitive system that
Donohue, Carter, & Bunge, 2008). Furthermore, devel- is common to dealingwith all these situations.
opment of these abilities throughout childhood has been
Burgess and colleagues hypothesized that this comassociated with the maturation of this region (Crone et al., mon cognitive system might be one involved in control2009; D umontheil et al., 2008).
ling the direction of attending, allowing us to engage
However, a recent study has cast doubt upon some of novel amounts of either "stimulus-oriented" (S) or
the more straightforward interpretations of findings of "stimulus-independent" (SI) attending. I n SO attendhemodynamic change during analogical reasoning, espe- ing, our attentional focus is directed toward the external
cially where it is assumed that those changes that are con- environment; we are simply paying attention to the things
comitant with performance of the task reflect the process we can see, hear, and so on. By contrast, in SI attending,
of target-source mapping. Voile et al. (2010) designed an we are caught up with the "thoughts in our head," that is,
analogical reasoning paradigm that separated in time the self-generated and/or maintained representations. Burgess
presentation of the source and the presentation of the tar- and colleagues called the notion that at least some parts of
get, thus allowing examination of the similarities and dif- rostral PFC support a system that exerts control over the
ferences in activation patterns (compared to the control) degree of SO or SI attending the "gateway hypothesis" of
during these phases. I f rostral PFC is involved in analogical rostral PFC.
reasoning per se, it should not be seen before the target is
I n the first of a series of experiments (Gilbert, Frith, &
presented, since prior to this stage no analogy can be drawn. Burgess, 2005), Burgess and colleagues tested this hypothI n fact, a lateral rostral PFC (BA 10) region was found to esis. We designed a range of tasks contrasting the activadur'mganyphase of analogical reasoning (com- tions that occur in the brain while people are attending
be activatedzyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA
pared with a control task that involved attribute matching to external stimuli with those that occur while people
only). Unlike other rostral prefrontal regions, this region are doing exactly the same tasks but have to imagine the
was activated right from the initial time of the presenta- stimuli in their heads. We used a "conjunction-type"
tion of the source. Thus, while it may be the case that this design using a series of tasks that measure the construct
activation indexes a process that is important to analogical of interest (SI/SO attending control or, as we have rather
reasoning, it is not specific to the phase where an analogy is inelegantly called it, the "supervisory attentional gateway";
drawn, but it may play a much more general (perhaps funda- Burgess, Dumontheil, & G ilbert, 2007) but that differ in
mental) role.
as many other ways as possible (e.g., in terms of the stimuli
By contrast, a more dorsomedial region of BA 10 was encountered, the question that has to be answered). Then,
specifically activated when the target was presented, and by looking at the activations that were common across the
not during the source period. This may suggest that this tasks, we could determine the pattern that is true for this
region is associated with comparison or mapping pro- whole class of tasks rather than being true of only one (see
cesses. Overall, the study of Voile et al. (2010) confirms Figure 31-3).
that there seems to be an interesting relation between perThe results from G ilbert et al. (2005) confirmed the
formance of analogical reasoning and activation of rostral hypothesis. Lateral aspects of rostral PFC (BA 10) were
PFC. However, it also suggests that different subregions activated when people switched from either SO to SI or
may play distinct roles, with some perhaps more broadly from SI to SO modes of attending (i.e., switching between
involved not only in analogical reasoning, but also playing attending to external stimuli or doing the task " in one's
31.
R O S TR AL
PR EFR O N TAL
CO R TEX
537
Stim ulus -Orie nte d
S tim ulus -Ind e p e nd e nt
Atte nd ing (SO)
Atte nd ing (SI)
(A)
o
zyxwvutsrqponmlkjihgfedcbaZYXWVUTSR
(B)
1
B B M B B B B zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA
Task 1
Task 2
zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA
1 5 zyxwvutsrqponmlkjihgfedcbaZYXW
zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQP
zyxwvutsrqponmlkjihgfe
zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPON
WBM
Figure 3 1 -3
\I B
LO
•5
P I G
zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA
Si block s
I I 111
B
Task 3
RSB
Sal
•
^
Bit
B
zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQ
'6
4
0
|
zyxwvutsrqponmlkjihgfe
zyxwvutsrqponmlkjihgfedcbaZYXWVU
Ro s tral PFC s truc ture s play a ro le in the c o ntro l o f SO ve rs us SI a tte nd ing. Pane l A s ho ws the thre e d iffe re nt ta s ks us e d by Gilb e rt e ta l. (2 0 0 5 )
to m e a s ure the s e c o n s tru c ts . Task 1 re q uire d p a rtic ip a nts to a ntic ip a te whe n a c lo c k hand wo uld re ac h a c e rta in p o int; the y we re e ithe r a b le to s e e th e
c lo c k (SO pha s e s ) o r the y we re d is tra c te d by irre le va nt info rm a tio n (SI p ha s e s ). Task 2 invo lve d na viga ting a ro und a figure th a t the p a rtic ip a nt c o uld
e ithe r s e e (SO) o r no t (SI). Tas k 3 re q uire d m a king ju d g m e n ts a b o ut the s ha p e o f le tte rs o f th e a lp ha b e t, whic h we re e ithe r d is p la ye d o r ha d to be
im a gine d by th e p a rtic ip a nt. Pane l B s ho ws the typ ic a l a c tiva tio ns in ro s tra l PFC d uring SO ve rs us SI p ha s e s ; re s ults fro m Gilb e rt, Willia m s o n, e ta l.
(2 0 0 7 ).
head only, or vice versa). An anterior region of medial BA
10 was active specifically in the SO conditions (i.e., when
attending to external stimuli rather than doing the same
task in one's head). This basic pattern has recently been
confirmed by a separate research group in a clever study by
Henseler, Kriiger, Dechent, and Gruber (2011). We have
now conducted a series of experiments that have examined
the dynamics of the hemodynamic changes that occur
while variously stressing the supervisory attentional gateway. The three main conclusions so far, very briefly, are:
1. Lateral aspects of rostral PFC are activated not only
at the SO/SI attending switch points, but also during
longer phases of SI attending (Gilbert, Williamson,
Dumontheil, Simons, Frith & Burgess, 2007).
2. The rostral PFC activations seem remarkably invariant
to the stimulus you are attending to or what you
are thinking about (Dumontheil, Gilbert, Frith, &
Burgess, 2010).
3. The medial anterior rostral activation increases seen
with these types of tasks are associated with faster
reaction times.
4. The same regions involved in this form of attentional
control are also involved in prospective memory.
The last point (4) will be covered in the next section. Point
2 deserves a caveat: So far we have only examined tasks
that present stimuli visually. It is possible that auditory or
tactile presentations, for example, may reveal a different
pattern (this would be a very interesting finding in terms
538
of understanding the functional organization of rostral
PFC).
Point 3 is an important finding because of the debate
surrounding the role of medial PFC structures in supporting mind wandering or other off-task processing. It would
appear, prima facie, that the findings presented here are
in conflict with those of authors who maintain that this
medial PFC region is part of a "default mode network,"
which typically shows decreased activation during the performance of demanding cognitive tasks. A full appraisal of
the vigorous debate surrounding this apparent conflict is
beyond the scope of this chapter, and the reader is referred
to Mason et al. (2007), G ilbert, D umontheil, Simons,
Frith, and Burgess (2007), and G ilbert, Bird, Frith, and
Burgess (2012). However, not only have we shown in previous studies that the anterior medial PFC activation during our reaction time tasks is performance-related, but we
have also examined the possibility of a relation with task
difficulty. I n a very recent study (Gilbert, Bird, Frith, and
Burgess, 2012), we used f MR I to study 18 participants
performing two "stimulus-oriented" (SO) tasks where
responses were directly cued by visual stimuli, as well as an
"stimulus-independent" (SI) task with greater reliance on
internally generated information. The SI task was intermediate in difficulty, as measured by response time and
error rate, relative to the two SO tasks. The B O LD signal in
medial rostral PFC, despite claims that this region is part of
the default mode network, was reduced in the SI condition
in comparison with both the more difficult and less difficult SO conditions. This result suggests that task difficulty zyxwvu
P R INCIP LES OF FRONTAL LOBE FUNCTION
(as measured by response time and error rate) does not pro- jointly recruited during (1) mere ongoing task activity
vide a comprehensive account of signal change in medial versus additional engagement in a PM task and (2) SO
PFC; instead, it is the relative demand made upon SI and versus SI processing. This is congruent with the notion that
5 0 attendingsystems that is thebetter predictor. This latter some of the processes mediating PM performance can be
study is important because it is possible to argue from the characterized by relative differences in these attentional
evidence from our earlier simple reaction time tasks that modes, as proposed by the gateway hypothesis (Burgess,
good performance indicates that the task is well within the G ilbert, and Dumontheil, 2007; Burgess et al., 2009).
capabilities of the participant, and so would also provide At the same time, the PM contrast was consistently
the opportunity for mind wandering (i.e., that mind wan- associated with more dorsal peak activation than the
dering and fast reaction times might be correlated in some stimulus contrast, perhaps reflecting engagement of
circumstances). But it is much more difficult to square the additional processes. I t would be interesting, and theoevidence from this latter study on task difficulty with the retically noteworthy, to see similar methods applied to the
default mode hypothesis. zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA
mapping of rostral PFC activations during prospection
versus PM. zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA
S OM E
IN
R E G IO N S
M O R E THAN
OF R O S TR A L
P F C A R E IN VO LVED
O N E C O G N ITIV E
D O M AIN
( P O IN T 1 4 )
A natural question emerging from the finding of rostral
PFC involvement in supporting a broad function like
an attentional gateway is whether these same regions are
involved in the other functions identified as associated with
this brain region. One might suppose, perhaps on information processing grounds, that an ability such as maintaining an intention in the face of demands associated with
competing external stimuli might require a high degree of
control over SO versus SI attending. Thus, the hypothesis
that there might be a corresponding overlap in the brain
regions involved is an obvious one.
Ideally perhaps, distinguishing between the foci of
activation involved during performance of these kinds
of cognitive activities would be tested using a direct
within-subjects comparison. This is exactly the kind of
design that Benoit et al. (2012) have attempted with prospective memory.
Their study aimed to discover whether functional
imaging data are consistent with the idea that the rostral
PFC attentional gateway is involved in performance of
prospective memory paradigms. As mentioned above,
the supervisory (or rostral PFC) attentional gateway is a
hypothetical cognitive mechanism proposed by the gateway hypothesis of rostral PFC function (Burgess, Simons,
D umontheil, & G ilbert, 2005; Burgess, D umontheil, &
G ilbert, 2007; Burgess, G ilbert, & D umontheil, 2007;
Burgess et al., 2006). This asserts that aprincipal purpose of
rostral PFC is to control differences in attending between
51 thought (i.e., inner mental life) and SO thought (i.e.,
attending to the external world). Benoit et al. (2012) used
a factorial design, crossing prospective memory (PM vs.
no-PM) with mode of attending (stimulus-oriented [SO]
vs. stimulus-independent [SI]; e.g., G ilbert et al., 2005; see
Figure 31-3). The purpose of the experiment was to determine whether the foci of activations in PM were the same
as those activated by SI/SO attention changes. Benoit
et al. (2012) found that parts of medial rostral PFC were
31.
R O S TR AL PR EFR O N TAL
C O R TEX
CONCLUSION: IS ROSTRAL PFC A HUB
FOR METACOGNITION?
Stuss and Alexander (2007) have characterized the functions supported by rostral PFC as being involved in "metacognitive" processing. This label has considerable appeal
given the foregoing review. There is, however, no agreed
set of abilities or behaviors that this label might encompass. For instance, Shammi and Stuss (1999) showed that
humor appreciation is affected by lesions involving the
right rostral PFC region. Should this cognitive ability be
considered to have a strong metacognitive component?
We know of no comprehensive information processing
model for humor appreciation, or for many of the other
cognitive abilities reviewed above, which might allow a
firm decision on this point.
For this reason, it may be better to start with an account
of metacognition developed without knowledge of the
cognitive neuroscience of rostral PFC and judge retrospectively whether the functions outlined above (i.e., for which
there is strong reason to believe that supporting structures
are located in rostral PFC) fit within the framework. I f
there is a remarkable coincidence between the functions
we have recently found to be supported at least in part by
rostral PFC structures and the functions that have been
described as requiring metacognition from another field,
then this may give the label more credence for its application in cognitive neuroscience.
Such a prior framework does exist, although perhaps
not always with the form of specification that might be ideal
for cognitive neuroscience purposes. "Metacognition" is
commonly defined as " thinking about thinking," that is,
reflecting or introspecting upon one's own thoughts. But
while most theorists would indeed count such a mental
experience as metacognition, the person widely credited
with the introduction of the term to the psychological
literature (J. H . Flavell) provided a much broader and
more practical definition. For instance, his widely cited 1979
paper, titled "Metacognition and Cognitive Monitoring: A
539
New Area of Cognitive Developmental Inquiry," opens
thus:
Preschool and elementary school children were
asked to study a set of items until they were sure they
could recall them perfectly (Flavell, Friedrichs, &
Hoyt, 1970). The older subjects studied for a while,
said they were ready, and usually were, that is, they
showed perfect recall. The younger children studied
for a while, said theywere ready, and usuallywere not.
I n another study, elementary school children were
asked to help the experimenter evaluate the communicative adequacy of verbal instructions, indicating
any omissions and obscurities (Markman, 1977).
Although the instructions were riddled with blatant
omissions and obscurities, the younger subjects were
surprisingly poor at detecting them. They incorrectly
thought they had understood and could follow the
instructions, much as their counterparts in the study
by Flavell et al. (1970) incorrectly thought they had
memorized and could recall the items, (p. 906)
From these examples, it is clear that it is not thinking
about thinking that is the immediate focus for Flavell,
but issues such as awareness of competence, knowledge
about one's tendency to err, and knowing when you know
something—or do not. Indeed, Flavell goes on to define
metacognition very broadly, indeed, as "knowledge and
cognition about cognitive phenomena" (1979, p. 906). He
gives as examples of situations where metacognition plays
an important role "oral communication... [and] persuasion, oral comprehension, reading comprehension, writing, language acquisition, attention, memory, problem
solving, social cognition and various types of self-control
and self-instruction" (ibid.). It would seem, therefore, that
the principal source of the term "metacognition" refers to a
far wider range of cognition than introspection upon one's
thoughts.
Indeed, Flavell described four broad classes of mental phenomenon which together might be thought of as
an operational definition. The first was "metacognitive
knowledge," referring to knowledge about individuals
as cognate agents, and their diverse and individual goals,
actions, and experiences, including, for example, how good
or bad people are at things. The second class of mental phenomenon was "metacognitive experiences," which were
thoughts provoked by, or accompanying, any kind of intellectual operation, such as the "sudden feeling that you do
not understand something another person has said" (1979,
p. 906). I t is noteworthy here that the example involves a
spontaneous realization rather than something that one
has had to work toward: similar effects accompany many
behavioral phenomena associated with the realization of
delayed intentions (e.g., Okuda et al., 2011). Flavell's the
third component of metacognition was "goals," referring
540
to the intended outcome of one's actions. The fourth was
"actions and strategies," referring to the behaviors and cognitive operations required in order to achieve one's goals.
Flavell (1979) describes the situations in which such
cognitions are most likely to occur. He says, "my present
guess is that metacognitive experiences are especially likely
to occur in situations that stimulate a lot of careful, highly
conscious thinking: in a job or school task that expressly
demands that kind of thinking; in novel roles or situations, where every major step you take requires planning
beforehand and evaluation afterwards; where decisions
and actions are at once weighty and risky; where high affective arousal or other inhibitors of reflective thinking are
absent
Such situations provide many opportunities for
thoughts and feelings about your own thinking to arise
and, in many cases, call for the kind of quality control that
metacognitive experiences can help supply" (p. 908).
Given that a key aspect of Flavell's characterization of
metacognitive processes was that they are used in a very
wide range of situations (e.g., oral communication and
comprehension, language acquisition, attention, memory, problem solving, social cognition, self-control, and
self-instruction), i f rostral PFC structures were part of a
system that supported these forms of cognition, then we
would expect activations in this region to occur in a wide
range of situations. And this is, of course, what point 5
above outlines. But how would this then be squared with
the apparently contradictory finding that lesions to rostral
PFC do not cause deficits in a correspondingly large (or
often even similar) range of tasks (point 6) ?
One explanatory hypothesis might be that some processing carried out by rostral PFC may not necessarily be
reflected in task performance. Many metacognitive experiences may bear only a passing relation to behavior seen
on a moment-by-moment basis. This is because much of it
may relate to consideration of future, rather than present,
actions (see points 7 and 8) or consideration of many possibilities for immediate action that are then not enacted
(see point 12). Further, judgments arising from reflections
upon one's own performance are known to be not necessarily closely related to "objective" (e.g., normative) estimates,
so they are not necessarily helpful to test scores (although
in some circumstances they might be more so to future
performance perhaps, which may be their utility). There is
also the possibility sometimes of mind wandering, as highlighted above.
I n this way, the possibility that rostral PFC (BA 10)
structures support metacognition may help to explain
perhapszyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPON
the principal puzzle of current rostral PFC findings (i.e., that rostral PFC activation occurs during a very
wide range of tasks, but lesions to the region may not
cause impairments in many of those tasks). Further, there
are obvious parallels between the core components of
Flavell's metacognitive knowledge and more recent conceptions of theory of mind and mentalizing (see point 11). zyxwv
P R IN C IP LE S
OF FRON TAL
LO B E
FUN CTION
offigurativeaspects of language: A positron emission tomography
And metacognitive experiences, (goals, actions, and strateactivation study. Brain, 117(pt 6), 1241-1253.
gies) all sound like descriptions of processes that could be
Bunge, S. A., Helskog, E . H . , & Wendelken, C . (2009). Left, but not
impaired in the patients we have reviewed who have sufright, rostrolateral prefrontal cortex meets a stringent test of the
fered rostral PFC damage, or processes that are the focus of
relational integration hypothesis. N euroimage, 46(1), 338-342.
neuroimaging experiments attempting to characterize the Bunge, S. A., Wendelken, C , Badre, D., & Wagner, A. D. (2005).
Analogical reasoning and prefrontal cortex: E vidence for sepafunctions of rostral PFC (see points 7 and 12 in particular).
rable retrieval and integration mechanisms. Cerebral Cortex, 15(3),
The emphasis on controlled processing and reflecting upon
239-249.
one's performance is not only reminiscent of most concep- Burgess, N ., Maguire, E . A., Spiers, H . J., & O'Keefe, J. (2001). A temporoparietal and prefrontal network for retrieving the spatial contualizations of prefrontally supported cognitive systems,
text of lifelike events. N euroimage, 14(2), 439-453.
but is also more specifically echoed in the tasks described
Burgess, P. W, Alderman, N ., Voile, E „ Benoit, R. G., & Gilbert, S.
in points 10 and 11 here. There are many other parallels
J. (2009). Mesulam's frontal lobe mystery re-examined. Restorative
also. Altogether, these are probably enough to postulate (in
N eurology and N euroscience, 27(5), 493-506.
agreement with Stuss & Alexander, 2007) that a substan- Burgess, P. W, Dumontheil, I., & Gilbert, S. J . (2007). The gateway
hypothesis of rostral prefrontal cortex (area 10) function. Trends in
tial amount of the processing supported by rostral PFC
Cognitive Sciences, 11(7), 290-298.
structures is highly relevant to Flavell's notions of metaBurgess, P. W., Gilbert, S. J., & Dumontheil, I. (2007). Function and
cognition. These notions were advanced long before techlocalization within rostral prefrontal cortex (area 10). Philosophical
niques like functional imaging were generally available.
Transactions of the Royal Society of L ondon, Series B, Biological
Sciences, 362(1481), 887-899.
I t may be that cognitive neuroscience is finally starting to
discover their full significance for understanding brain Burgess, P. W, Gilbert, S. J., Okuda, J., & Simons, J. S. (2006). Rostral
prefrontal brain regions (Area 10): A gateway between inner thought
function— and indeed, perhaps vice versa. zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA
and the external world? In W. Prinz & N . Sebanz (E ds.), Disorders of
volition (pp. 373-396). Cambridge, MA: MI T Press.
Burgess, P. W, Gonen-Yaacovi, G., & Voile, E . (2011). Functional neuroimaging studies of prospective memory: What have we learnt so
DISCLOSURE STATEMENT
far? N europsychologia, 49(8), 2246-2257.
Burgess, P. W, Gonen-Yaacovi, G., & Voile, E . (2012) Rostral preP.W.B. and H.-C.W. have no conflicts of interest to
frontal cortex: What neuroimaging can learn from human neuropsychology. In B. Levine & F . I. M. Craik (E ds.), Mind and the
disclose.
frontal lobes: Cognition, behavior, and brain imaging (pp. 47-92).
New York: Oxford University Press.
Burgess, P. W, Quayle, A., & F rith, C D . (2001). Brain regions involved
REFERENCES zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA
in prospective memory as determined by positron emission tomography. N europsychologia, 39(6), 545-555.
Burgess, P. W, Scott, S. K., & F rith, C. D. (2003). The role of the rosAddis, D. R„ Pan, L„ Vu, M.-A., Laiser, N ., & Schacter, D. L . (2009).
tral frontal cortex (area 10) in prospective memory: A lateral versus
Constructive episodic simulation of the future and the past:
medial dissociation. N europsychologia, 41(8), 906-918.
Distinct subsystems of a core brain network mediate imagining and
Burgess, P. W, & Shallice, T . (1996a). Confabulation and the control of
N europsychologia, 47(11), 2222-2238.
remembering. zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA
recollection. Memory (Hove, E ngland), 4(4), 359-411.
Addis, D. R., Wong, A. T ., & Schacter, D. L . (2007). Remembering the
Burgess, P. W, & Shallice, T . (1996b). Response suppression, initiation
past and imagining the future: Common and distinct neural suband strategy use following frontal lobe lesions. N europsychologia,
strates during event construction and elaboration. N europsychologia,
34(4), 263-272.
45(7), 1363-1377.
Baker, S. C , Rogers, R. D., Owen, A.M., Frith, C D . , Dolan, R.J., Frackowiak, Burgess, P. W, & Shallice, T . (1997). The Hayling and Brixton tests.
R. S., et al. (1996). Neural systems engaged by planning: A PE T study of
Bury St. E dmunds, U K: Thames Valley Test Co.
the Tower ofLondon task. N europsychologia, 34(6), 515-526.
Burgess, P. W, Simons, J . S., Coates, L . M., & Channon, S. (2005).
The search for specific planning processes. In G. Ward & R. Morris
Benoit, R. G„ Gilbert, S. J. , F rith, C . D., & Burgess, P. W. (2012).
(E ds.), The cognitive psychology of planning (pp. 199-227). Hove,
Rostral prefrontal cortex and the focus of attention in prospective
U K: Psychology Press.
memory. Cerebral Cortex, 22(8), 1876-86.
Burgess, P. W., Simons, J. S., Dumontheil, I., & Gilbert, S. J. (2005).
Benoit, R. G., Gilbert, S.J., Voile, E„ & Burgess, P. W. (2010). When I
The gateway hypothesis of rostral P F C function. In J. Duncan, L .
think about me and simulate you: Medial rostral prefrontal cortex
and self-referential processes. N euroimage, 50(3), 1340-1349.
Phillips, & P. McLeod (E ds.), Measuring the mind: Speed, control
Berman, K. F ., Ostrem, J. L ., Randolph, C , Gold, J., Goldberg, T . E . ,
and age (pp. 215-246). Oxford: Oxford University Press.
Coppola, R., et al. (1995). Physiological activation of a cortical
Burgess, P. W, Veitch, E ., de Lacy Costello, A., & Shallice, T . (2000).
network during performance of the Wisconsin Card Sorting Test:
The cognitive and neuroanatomical correlates of multitasking.
A positron emission tomography study. N europsychologia, 33,
N europsychologia, 38(6), 848-863.
1027-1046.
Cansino, S., Maquet, P., Dolan, R.J., & Rugg, M. D. (2002). Brain activity underlying encoding and retrieval of source memory. Cerebral
Blaxton, T . A., Zeffiro, T . A, Gabrieli, J . D., Bookheimer, S. Y.,
Cortex, / 2(10), 1048-1056.
Carrillo, M. C , Theodore, W. H ., et al. (1996). Functional mapping
Carmichael, S. T , & Price, J . L . (1994). Architectonic subdivision of
of human learning: A positron emission tomography activation
study of eyeblink conditioning. TheJournal of N euroscience, 16(12),
the orbital and medial prefrontal cortex in the macaque monkey.
4032-4040.
TheJournal of Comparative N eurology, 346(3), 366-402.
Bonin, G. von. (1950). E ssay on the cerebral cortex. Springfield, I L :
ChristofF, K., Prabhakaran, V., Dorfman, J., Zhao, Z ., Kroger, J . K.,
Charles C. Thomas.
Holyoak, K. J., et al. (2001). Rostrolateral prefrontal cortex involveBottini, G., Corcoran, R., Sterzi, R., Paulesu, E ., Schenone, P., Scarpa, P.,
ment in relational integration during reasoning. N euroimage, 14(5),
et al. (1994). The role of the right hemisphere in the interpretation
1136-1149. zyxwvutsrqponmlkjihgfedcbaZYXW
31.
R O S TR AL
PR EFR O N TAL
CO R TEX
541
Crone, E . A., Wendelken, C , van Leijenhorst, L . , Honomichl, R. D.,
versus medial rostral prefrontal cortex: A meta-analysis. N euroimage,
ChristofF, K„ & Bunge, S. A. (2009). Neurocognitive development
53(4), 1359-1367.
of relational reasoning.zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA
Developmental Science, 12(1), 55-66.
Gilbert, S. J., Williamson, I. D. M., Dumontheil, I., Simons, J. S., F rith,
den Ouden, H . E . M., F rith, U., F rith, C , & Blakemore, S.-J. (2005).
C. D., & Burgess, P. W. (2007). Distinct regions of medial rostral
Thinking about intentions. N euroimage, 28(4), 787-796.
prefrontal cortex supporting social and nonsocial functions. Social
Dobbins, I. G., Foley, K , Schacter, D. L ., & Wagner, A. D. (2002).
Cognitive and A ffective N euroscience, 2(3), 217-226.
E xecutive control during episodic retrieval: Multiple prefrontal proGlascher, J., Tranel, D., Paul, L . K., Rudrauf, D., Rorden, C , Hornaday,
cesses subserve source memory. N euron, 35(5), 989-996.
A., et al. (2009). Lesion mapping of cognitive abilities linked to
Dreher, J . - C , Koechlin, E . , Tierney, M., & Grafman,J. (2008). Damage
intelligence. N euron, 61(5), 681-691.
to the fronto-polar cortex is associated with impaired multitasking. Goel, V., Gold, B„ Kapur, S., & Houle, S. (1997). The seats ofreason? An
PloS One, 3(9), c3227.
imaging study of deductive and inductive reasoning. N euroreport,
Dubois, B., Slachevsky, A., Litvan, I., & Pillon, B. (2000). The F AB:
8(5), 1305-1310.
A Frontal Assessment Battery at bedside. N eurology, 55(11)
Goel, V., & Grafman, J . (2000). Role of the right prefrontal cor1621-1626.
tex in ill-structured planning. Cognitive N europsychology, 17(5),
415-436.
Dumontheil, I., Burgess, P. W., & Blakemore, S.-J. (2008). Development
of rostral prefrontal cortex and cognitive and behavioural disorders.
Gold, J . M., Berman, K. F ., Randolph, C , Goldberg, T . E . , &
Developmental Medicine and Child N eurology, 50(3), 168-181.
Weinberger, D. R. (1996). P E T validation of a novel prefrontal task:
Dumontheil, I., Gilbert, S. J., F rith, C . D., & Burgess, P. W. (2010).
Delayed response alternation. N europsychology, 10,3-10
Recruitment of lateral rostral prefrontal cortex in spontaneous and
Goldstein, L . H . , Bernard, S., Fenwick, P. B., Burgess, P. W, &
task-related thoughts. QuarterlyJournal of E xperimental Psychology,
McNeil, J. (1993). Unilateral frontal lobectomy can produce strat63(9), 1740-1756.
egy application disorder. Journal of N eurology, N eurosurgery, and
Psychiatry, 56(3), 274-276.
E slinger P. J., & Damasio A. R. (1985). Severe disturbance ofhigher cognition after bilateral frontal lobe ablation: Patient E VR . N eurology, Green, A. E . , Fugelsang, J. A., Kraemer, D. J. M., Shamosh, N . A., &
35,1731-1741.
Dunbar, K. N . (2006). Frontopolar cortex mediates abstract integration in analogy. Brain Research, 1096(1), 125-137.
Fan, J., Gay Snodgrass, J., & Bilder, R. M. (2003). Functional magnetic
resonance imaging of source versus item memory. N euroreport,
Hashimoto, T ., Umeda, S„ & Kojima, S. (2010). Neural substrates of
14(17), 2275-2281.
implicit cueing effect on prospective memory. N euroimage, 54(1),
Flavell, J. H . (1979). Metacognition and cognitive monitoring: A new
645-652.
area of cognitive developmental inquiry. A merican Psychologist,
Haxby, J . V, Ungerleider, L . G., Horwitz, B., Maisog, J. M., Rapoport,
S. I., & Grady, C. L . (1996). Face encoding and recognition in
34(10), 906-911.
the human brain. Proceedings of the N ational A cademy of Sciences
Flavell, J. H . , Friedrichs, A. G., & Hoyt, J. D. (1970). Developmental
of the United States of A merica, 93(2), 922-927. Haxby, J . V.,
changes in memorization processes. Cognitive Psychology, 1(4),
Ungerleider, L . G., Horwitz, B., Rapoport, S. I., & Grady, C. L .
324-340.
(1995). Hemispheric differences in neural systems for face working
Fleming, S. M., Weil, R. S., Nagy, Z., Dolan, R. J., & Rees, G. (2010).
memory: A PE T -rCB F study. Human Brain Mapping, 3(2), 68-82.
Relating introspective accuracy to individual differences in brain
structure. Science, 329(5998), 1541-1543.
Haynes, J.-D., Sakai, K., Rees, G., Gilbert, S., F rith, C , & Passingham,
F rith, U., & Frith, C. D. (2003). Development and neurophysiology
R. E . (2007). Reading hidden intentions in the human brain.
Current Biology, 17(4), 323-328.
of mentalizing. Philosophical Transactions of the Royal Societyof
L ondon, Series B, Biological Sciences, 355(1431).
Henseler, I., Kriiger, S., Dechent, P., & Gruber, O. (2011). A gateway
system in rostral PF C? E vidence from biasing attention to percepGentner, D. (1983). Structure-mapping: A theoretical framework for
tual information and internal representations. N euroimage, 56(3),
analogy. Cognitive Science, 7, 155-170.
1666-1676.
Gentner, D., & Holyoak, K. J. (1997). Reasoning and learning by analogy. A merican Psychology, 52(1), 32-34.
Hodges, J . R. (1994). Cognitive assessment for clinicians: A practical
Gentner, D., Rattermann, M. J., & Forbus, K. D. (1993). The roles of
guide. Oxford: Oxford University Press.
similarity in transfer: Separating retrievability from inferential
Holyoak, K. J. & Thagard, P. (1995). Mental leaps: A nalogy in creative
thought. Cambridge, MA: MI T Press.
soundness. Cognitive Psychology, 25, 524-575.
Gilbert, S. J. (2011). Decoding the content of delayed intentions. The Holyoak, K. J., & Thagard, P. 1997. The analogical mind. A merican
Psychology, 52(1), 35-44.
Journal of N euroscience, 31(8), 2888-2894.
Gilbert, S.J., Armbruster, D.J. N ., & Panagiotidi, M. (2012). Similarity
Hugdahl, K., Berardi, A., Thompson, W. L ., Kosslyn, S. M., Macy, R.,
Baker, D. P., et al. (1995). Brain mechanisms in human classical conbetween brain activity at encoding and retrieval predicts successful
ditioning: A P E T blood flow study. N euroreport, 6(13), 1723-8.
realization of delayed intentions. Journal of Cognitive N euroscience,
Jacobs, B., Schall, M., Prather, M., Kapler, E . , Driscoll, L ., Baca, S„
24(1), 93-105.
et al. (2001). Regional dendritic and spine variation in human
Gilbert, S. J., Bird, G., Frith, C. D., & Burgess, P. W. (2012). Does
cerebral cortex: A quantitative Golgi study. Cerebral Cortex, 11(6),
" task difficulty" explain " task-induced deactivation" ? Frontiers in
558-571.
Psychology, 12(3), 125.
Gilbert, S. J., Dumontheil, I., Simons, J. S., F rith, C. D., & Burgess, P. W. Jenkins, I. H . , Brooks, D. J., Nixon, P. D., Frackowiak, R. S. J., &
(2007). Comment on " Wandering Minds: Stimulus-Independent
Passingham, F . E . (1994). Motor sequence learning: A study with
Thought." Science, 317,4-5.
positron emission tomography. Journal of N euroscience, 14(6),
3775-3790.
Gilbert, S. J., F rith, C. D., & Burgess, P. W. (2005). Involvement of rostral prefrontal cortex in selection between stimulus-oriented and Jennings, J. M., Mcintosh, A. R., Kapur, S., Tulving, E ., & Houle, S.
stimulus-independent thought. E uropean Journal of N euroscience,
(1997). Cognitive subtractions may not add up: The interaction
21(5), 1423-1431.
between semantic processing and response mode. N euroimage, 5(3),
Gilbert, S. J. , Gollwitzer, P. M., Cohen, A.-L ., Burgess, P. W, &
229-239.
Oettingen, G. (2009). Separable brain systems supporting cued versus John, J . P., Burgess, P. W, Yashavantha, B. S., Shakeel, M. K.,
self-initiated realization ofdelayed intentions.Journal of E xperimental
Halahalli, H . N . , & Jain, S. (2009). Differential relationship of
Psychology: L earning, Memory, and Cognition, 35(4), 905-915.
frontal pole and whole brain volumetric measures with age in
neuroleptic-naive schizophrenia and healthy subjects. Schizophrenia
Gilbert, S. J., Gonen-Yaacovi, G., Benoit, R. G., Voile, E ., & Burgess, P. W.
Research, 109,148-158. zyxwvutsrqponmlkjihgfedcb
(2010). Distinct functional connectivity associated with lateral
542
P R IN C IP LE S
OF FRON TAL
LO B E
FUN CTIO N
Klein, D., Milner, B., Zatorre, R. J., Meyer, E ., & E vans, A. C. (1995).
Paus, T . (2005). Mapping brain maturation and cognitive development
The neural substrates underlying word generation: A bilingual
during adolescence. Trends in Cognitive Sciences, 9(2), 60-68.
functional-imaging study. zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA
Proceedings of the N ational A cademyof Penfield, W, & E vans, J. (1935). The frontal lobe in man: A clinical
Sciences of the United States of A merica, 92(7), 2899-903.
study of maximum removals. Brain, 58, 115-133.
Koechlin, E . , Basso, G., Pietrini, P., Panzer, S., & Grafman, J. (1999).
Petrides, M., Alivisatos, B., Meyer, E . , & E vans, A. C. (1993). Functional
The role of the anterior prefrontal cortex in human cognition.
activation of the human frontal cortex during the performance of
N ature, 399(6732), 148-151.
verbal working memory tasks. Proceedings of the N ational A cademy
of Sciences ofthe United States of A merica, 90(3), 878-882.
Kosslyn, S. M., Alpert, N . M., and Thompson, W. L . (1995). Identifying
objects at different levels ofhierarchy: A positron emission tomograPetrie, A. (1952). Personality and the frontal lobes. London: Routledge
phy study. Human Brain Mapping, 3, 107-132.
& Kegan Paul.
Kosslyn, S. M., Alpert, N . M., Thompson, W. L„ Chabris, C. F„ Rauch,
Poppenk, J., Moscovitch, M., Mcintosh, A. R., Ozcelik, E ., & Craik, F. I. M.
S. L .,& Anderson, A. K. (1994). Identifying objects seen from differ(2010). E ncoding the future: Successful processing of intentions
ent viewpoints: A P E T investigation. Brain, 117(pt 5), 1055-1071.
engages predictive brain networks. N euroimage, 49(1), 905-913.
Kosslyn, S. M., Thompson, W. L ., Kim, I. J., & Alpert, N . M. (1995).
Prabhakaran, V., Smith, J . A., Desmond, J . E ., Glover, G. H . , &
Topographical representations of mental images in primary visual
Gabrieli, J. D. (1997). Neural substrates offluid reasoning: An fMRI
study of neocortical activation during performance of the Raven's
cortex. N ature, 378, 496 -498.
Progressive Matrices Test. Cognitive Psychology, 33(1), 43-63.
Kroger, J. K., Sabb, F. W., Fales, C. L ., Bookheimer, S. Y„ Cohen, M. S.,
& Holyoak, K. J. (2002). Recruitment of anterior dorsolateral preRanganath, C.Johnson, M. K., & D'E sposito, M. (2000). Left anterior
frontal cortex in human reasoning: A parametric study of relational
prefrontal activation increases with demands to recall specific percomplexity. Cerebral Cortex, 72(5), 477-485.
ceptual information. TheJournal of N euroscience, 20(22), RC108.
Luria, A. R. (1966). Higher corticalfunctions in man. New York: Basic
Raye, C. L.Johnson, M. K., Mitchell, K.J., Nolde, S. F ., & D'E sposito,
Books.
M. (2000). fMRI investigations of left and right P F C contributions
to episodic remembering. Psychobiology, 28, 197-206.
Manly, T , Hawkins, K., E vans, J. , Woldt, K., & Robertson, I. H .
(2002). Rehabilitation of executive function: Facilitation of effecReynolds J . R., West, R., & Braver, T . (2009). Distinct neural circuits
tive goal management on complex tasks using periodic auditory
support transient and sustained processes in prospective memory
alerts. N europsychologia, 40(3), 271-281.
and working memory. Cerebral Cortex, 19(5), 1208-1221.
Markman, E . M. (1977). Realizing that you don't understand: A preRoca, M., Parr, A., Thompson, R., Woolgar, A., Torralva, T , Antoun,
liminary investigation. Child Development, 48(3), 986.
N ., et al. (2010). E xecutive function andfluidintelligence after fronMartin, A., Haxby, J. V., Lalonde, F. M., Wiggs, C. L . . & Ungerleider, L . G.
tal lobe lesions. Brain, 133(pt 1), 234-247.
(1995). Discrete cortical regions associated with knowledge of color Roca, M., Torralva, T , Gleichgerrcht, E ., Woolgar, A., Thompson, R.,
and knowledge of action. Science, 270(5233), 102-105.
DuncanJ., et al. (2011). The role of Area 10 (BA10) in human multitasking and in social cognition: A lesion study. N europsychologia,
Martin, T , McDaniel, M. A., Guynn, M. J., Houck, J. M., Woodruff,
49, 3525-3531.
C. C , Bish, J. P., et al. (2007). Brain regions and their dynamics in
prospective memory retrieval: A ME G study. InternationalJournal
Roland, P. E ., & Gulyas, B. (1995). Visual memory, visual imagery,
ofPsychophysiology, 64(3), 247-258.
and visual recognition of large field patterns by the human brain:
Mason, M. F., Norton, M. I., Van Horn, J. D., Wegner, D. M., Grafton,
Functional anatomy by positron emission tomography. Cerebral
S. T , & Macrae, C. N . (2007). Wandering minds: The default
Cortex, 5(1), 79-93.
network and stimulus-independent thought. Science, 3/ 5(5810),
Rugg, M. D., Fletcher, P. C , Chua, P. M., & Dolan, R . J. (1999). The
393-395.
role of the prefrontal cortex in recognition memory and memory for
source: An fMRI study. N euroimage, 10(5), 520-529.
Metzler, C , & Parkin, A. J. (2000). Reversed negative ptiming following frontal lobe lesions. N europsychologia, 38(4), 363-379.
Rugg, M. D., Fletcher, P. C , F rith, C. D., Frackowiak, R. S., &
Dolan, R. J. (1996). Differential activation of the prefrontal cortex
Miele, D. B., Wager, T . D., Mitchell, J . P., & Metcalfe, J . (2011).
in successful and unsuccessful memory retrieval. Brain, I19(pt 6),
Dissociating neural correlates of action monitoring and meta2073-2083.
cognition of agency. Journal of Cognitive N euroscience, 23(11),
3620-3636.
Schacter, D. L ., Addis, D. R., & Buckner, R. L . (2007). Remembering
Mitchell, K. J., Johnson, M. K., Raye, C. L ., & Greene, E . J . (2004).
the past to imagine the future: The prospective brain. N ature
Prefrontal cortex activity associated with source monitoring in a
Reviews N euroscience, 8(9), 657-661.
working memory task. Journal of Cognitive N euroscience, 16(6),
Schacter, D. L ., Addis, D. R., & Buckner, R. L . (2008). E pisodic simula921-934.
tion of future events: Concepts, data, and applications. A nnals of the
New York A cade?ny oj Sciences, 1124, 39-60.
Nolde, S. F .Johnson, M. K., & D'E sposito, M. (1998). Left prefrontal
activation during episodic remembering: An event-related fMRI
Schmitz, T . W, Kawahara-Baccus, T . N ., & Johnson, S. C. (2004).
study. N euroreport, 9, 3509-3514.
Metacognitive evaluation, self-relevance, and the right prefrontal
Okuda, J., Fujii, T„ Ohtake, H . , Tsukiura, T„ Yamadori, A., F rith, C.
cortex. N euroimage, 22(2), 941-947.
D, et al. (2007). Differential involvement of regions of rostral preSemendeferi, K., Armstrong, E ., Schleicher, A., Zilles, K., & Van
Hoesen, G. W. (1998). Limbic frontal cortex in hominoids: A comfrontal cortex (Brodmann area 10) in time- and event-based proparative study of area 13. A mericanJournal of PhysicalA nthropology,
spective memory. International Journal oj Psychophysiology, 64(3),
233-246.
106(2), 129-155.
Okuda, J., F ujii, T , Yamadori, A., Kawashima, R., Tsukiura, T , Fukatsu, Semendeferi, K., Armstrong, E . , Schleicher, A., Zilles, K., & Van
R., et al. (1998). Participation of the prefrontal cortices in prospecHoesen, G. W. (2001). Prefrontal cortex in humans and apes: A comtive memory: E vidence from a P E T study in humans. N euroscience
parative study of area 10. A mericanJournal of PhysicalA nthropology,
L etters, 253(2), 127-130.
114(3), 224-241.
Okuda, J., Gilbert, S. J., Burgess, P. W, F rith, C . D., & Simons, J. S. Semendeferi, K., TefFer, K., Buxhoeveden, D. P., Park, M. S., Bludau, S.,
(2011). Looking to the future: Automatic regulation of attention
Amunts, K., et al. (2011). Spatial organization of neurons in the
between current performance and future plans. N europsychologia,
frontal pole sets humans apart from great apes. Cerebral Cortex,
49(8), 2258-2271.
21(7), 1485-1497.
Ongiir, D., Ferry, A. T„ & Price, J. L . (2003). Architectonic subdivision Shallice, T . (1982). Specific impairments of planning. Philosophical
of the human orbital and medial prefrontal cortex. Tf;e Journal of
Transactions of the Royal Society B: Biological Sciences, 295(1089),
Comparative N eurology, 460(3), 425-449.
199-209. zyxwvutsrqponmlkjihgfedcbaZYXWVU
31.
R O S TR AL
PR EFR O N TAL
C O R TEX
543
Shallice, T., & Burgess, P. W. (1991). Deficits in strategy application fol- Tulving, E . , Markowitsch, H . J., Craik, F. E . , Habib, R., & Houle, S.
lowing frontal lobe damage in man.zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA
Brain, 114(pt 2), 727-741.
(1996). Novelty and familiarity activations in P E T studies of memShammi, P., & Stuss, D. T . (1999). Humour appreciation: A role of the
ory encoding and retrieval. Cerebral Cortex, 6(1), 71-79.
right frontal lobe. Brain, 122(pt 4), 657-666.
Turner, M. S., Simons, J. S., Gilbert, S. J., F rith, C. D., & Burgess, P.
W. (2008). Distinct roles for lateral and medial rostral prefronSimons, J. S., Davis, S. W, Gilbert, S. J., Frith, C. D., & Burgess, P. W.
tal cortex in source monitoring of perceived and imagined events.
(2006). Discriminating imagined from perceived information engages
brain areas implicated in schizophrenia. N euroimage, 32(2), 696-703.
N europsychologia, 46(5), 1442-1453.
Simons, J. S., Gilbert, S. J., Owen, A. M., Fletcher, P. C., & Burgess, P. W. Umeda, S., Kurosaki, Y., Terasawa, Y , Kato, M., & Miyahara, Y. (2011).
(2005). Distinct roles for lateral and medial anterior prefrontal corDeficits in prospective memory following damage to the prefrontal
tex in contextual recollection. Journal of N europhysiology, 94(1),
cortex. N europsychologia, 49(8), 2178-2184.
813-820.
Uretzky, S., & Gilboa, A. (2010). Knowing your lines but missing your
Simons, J. S., Owen, A. M„ Fletcher, P. C., & Burgess, P. W. (2005).
cue: Rostral prefrontal lesions impair prospective memory cue
Anterior prefrontal cortex and the recollection of contextual infordetection, but not action-intention superiority. Journal of Cognitive
mation. N europsychologia, 43,1774-1783.
N euroscience, 22(12), 2745-2757.
Simons, J . S., Schoivinck, M. L . , Gilbert, S. J. , F rith, C. D., &
Voile, E ., Gilbert, S. J. , Benoit, R. G., & Burgess, P. W. (2010).
Burgess, P. W. (2006). Differential components ofprospective memSpecialization of the rostral prefrontal cortex for distinct analogy
ory? E vidence from fMRI. N europsychologia, 44(8), 1388-1397.
processes. Cerebral Cortex, 20(11), 2647-2659.
Sowell, E . R., Thompson, P. M., Holmes, C. J., Jernigan, T . L . , & Voile, E ., Gonen-Yaacovi, G., de Lacy Costello, A., Gilbert, S. J., &
Toga, A. W. (1999). In vivo evidence for post-adolescent brain matBurgess, P. W. (2011). The role of rostral prefrontal cortex in prouration in frontal and striatal regions. N ature N euroscience, 2(10),
spective memory: A voxel-based lesion study. N europsychologia,
859-861.
49(8), 2185-2198.
Sowell, E . R., Thompson, P. M., Leonard, C. M., Welcome, S. E .,
Warrington, E . K.James, M., & Maciejewski, C. (1986). The WAIS as
Kan, E . , & Toga, A. W. (2004). Longitudinal mapping of cortia lateralizing and localizing diagnostic instrument: A study of 656
cal thickness and brain growth in normal children. The Journal of
patients with unilateral cerebral lesions. N europsychologia, 24(2),
N euroscience, 24(38), 8223-8231.
223-239.
Stone, V. E . , Baron-Cohen, S„ & Knight, R. T . (1998). Frontal lobe
Weiler, J. A., Suchan, B., & Daum, I. (2010a). Foreseeing the future:
contributions to theory of mind. Journal of Cognitive N euroscience,
Occurrence probability of imagined future events modulates hip10(5), 640-656.
pocampal activation. H ippocampus, 20(6), 685-690.
Strange, B. A., Henson, R. N ., Friston, K. J., & Dolan, R. J . (2001).
WeilerJ . A., Suchan, B.,&Daum, I. (2010b). When the future becomes
Anterior prefrontal cortex mediates rule learning in humans.
the past: Differences in brain activation patterns for episodic
Cerebral Cortex, 11(11), 1040-1046.
memory and episodic future thinking. Behavioural Brain Research,
212(2), 196-203.
Stuss, D. T , & Alexander, M. P. (2007). Is there a dysexecutive syndrome? Philosophical Transactions of the Royal Society of L ondon,
Wendelken, C , Nakhabenko, D., Donohue, S. E ., Carter, C. S., &
Series B, Biological Sciences, 362(1481), 901-915.
Bunge, S. A. (2008). " Brain is to thought as stomach is to??" :
Szpunar, K. K., Watson, J. M.,&McDermott, K. B. (2007). Neural subInvestigating the role of rostrolateral prefrontal cortex in relational
strates ofenvisioning the future. Proceedingsof theN ational'A cademy
reasoning. Journal of Cognitive N euroscience, 20(4), 682-693.
of Sciences of the United States of A merica, 104(2), 642-647.
Williams J . M., E llis, N . C , Tyers, C , Healy, H ., Rose, G.,&MacLeod,
Travis, K., Ford, K., & Jacobs, B. (2005). Regional dendritic variation in
A. K. (1996). The specificity ofautobiographical memory and imageneonatal human cortex: A quantitative Golgi study. Developmental
ability of the future. Memory and Cognition, 24,116-125.
N euroscience, 27(5), 277-287.
Zatorre, R.J., Halpern, A. R., Perry, D. W, Meyer, E . , & E vans, A. C .
Tsujimoto, S., Genovesio, A., & Wise, S. P. (2011). Frontal pole cor(1996). Hearing in the mind's ear: A P E T investigation of musical
tex: E ncoding ends at the end of the endbrain. Trends in Cognitive
imagery and perception. Journal of Cognitive N euroscience, 8(1),
Sciences, 15(4), 169-176.
29-46. zyxwvutsrqponmlkjihgfedcbaZYXWVUT
544
P R IN C IP LE S
OF FRON TAL
LO B E FUN CTIO N
NeuroImage 56 (2011) 1666–1676
Contents lists available at ScienceDirect
NeuroImage
j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / y n i m g
A gateway system in rostral PFC? Evidence from biasing attention to perceptual
information and internal representations
Ilona Henseler a,b,⁎, Sebastian Krüger b, Peter Dechent c, Oliver Gruber b
a
b
c
Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
Centre for Translational Research in Systems Neuroscience and Clinical Psychiatry, Department of Psychiatry and Psychotherapy, Georg August University, Göttingen, Germany
MR-Research in Neurology and Psychiatry, Georg August University, Göttingen, Germany
a r t i c l e
i n f o
Article history:
Received 20 September 2010
Revised 13 January 2011
Accepted 17 February 2011
Available online 23 February 2011
Keywords:
Gateway hypothesis
Rostral prefrontal cortex
Regional specialization
Attentional control
Functional connectivity
a b s t r a c t
Some situations require us to be highly sensitive to information in the environment, whereas in other
situations, our attention is mainly focused on internally represented information. It has been hypothesized
that a control system located in the rostral prefrontal cortex (PFC) acts as gateway between these two forms of
attention. Here, we examined the neural underpinnings of this ‘gateway system’ using fMRI and functional
connectivity analysis. We designed different tasks, in which the demands for attending to external or internal
information were manipulated, and tested 1) whether there is a functional specialization within the rostral
PFC along a medial–lateral dimension, and 2) whether these subregions can influence attentional weighting
processes by specifically interacting with other parts of the brain. Our results show that lateral aspects of the
rostral PFC are preferentially activated when attention is directed to internal representations, whereas
anterior medial aspects are activated when attention is directed to sensory events. Furthermore, the
rostrolateral subregion was preferentially connected to regions in the prefrontal and parietal cortex during
internal attending, whereas the rostromedial subregion was connected to the basal ganglia, thalamus, and
sensory association cortices during external attending. Finally, both subregions interacted with another
important prefrontal region involved in cognitive control, the inferior frontal junction, in a task-specific
manner, depending on the current attentional demands. These findings suggest that the rostrolateral and
rostromedial part of the anterior PFC have dissociable roles in attentional control, and that they might, as part
of larger networks, be involved in dynamically adjusting the contribution of internal and external information
to current cognition.
© 2011 Elsevier Inc. All rights reserved.
Introduction
A key aspect of higher cognition is the ability to voluntarily direct
attention to the information that is currently most relevant. This
information can either be something present in the sensory
environment (i.e. external information) or something that exists
without a direct correlate in the environment (i.e. internal information). In different situations, the relevance of these two types of
information differs, requiring a control system that flexibly biases the
allocation of attentional resources to external or internal information,
depending on the current goals. In order to enable adaptive behavior,
this system should further allow individuals to rapidly switch
between the different sources of information and to integrate the
information coming from these sources. These operations have
recently been suggested to be carried out by a control system located
in the rostral prefrontal cortex (PFC), the ‘supervisory attentional
⁎ Corresponding author at: Max Planck Institute for Human Cognitive and Brain
Sciences, Stephanstraβe 1A, D-04103 Leipzig, Germany. Fax: +49 341 9940 2335.
E-mail address: [email protected] (I. Henseler).
1053-8119/$ – see front matter © 2011 Elsevier Inc. All rights reserved.
doi:10.1016/j.neuroimage.2011.02.056
gateway system’ (Burgess et al., 2007a,b). According to this theory,
the system plays a key role in the attentional selection between
‘stimulus-oriented (SO) cognition’ (i.e. attention toward stimuli
external to the body) and ‘stimulus-independent (SI) cognition’ (i.e.
attention toward internally represented information) and thus
operates as a ‘gateway’ between the internal mental life and the
mental life that is associated with interaction with the outside world.
This model is noteworthy since the rostral PFC is one of the brain
regions currently most discussed and least understood. There are a
large number of different findings and competing theoretical accounts
of its functions. Some models suggest that the region is involved in the
“coordination of information processing and information transfer
between multiple cognitive operations” (Ramnani and Owen 2004,
p. 193), others in the “processing of internally generated information”
(Christoff and Gabrieli 2000, p.169), and again others in processes like
“branching”, “updating”, or “planning” (Koechlin et al., 1999; Collette
et al., 2007; Soon et al., 2008), to name but a few. During the last 10
years, an almost equal number of neuroimaging studies have been
published supporting the one or the other account, meaning that the
function of the rostral PFC remains a matter of current debate.
I. Henseler et al. / NeuroImage 56 (2011) 1666–1676
The situation is aggravated by confusion in the nomenclature
regarding this most frontal region of the brain. Some authors speak of
the ‘rostral PFC’, others of the ‘anterior frontal cortex’, the ‘frontopolar
cortex’, ‘rostrolateral PFC’, or just ‘Brodmann area 10’.1 Furthermore,
the fact that structurally and functionally different subregions might
exist within the rostral PFC is often not taken into account. The
existence of such subregions, however, is suggested by a number of
studies on the microarchitectonic, structural, and functional level.
Ongur and colleagues (2003), for instance, identified three dissociable
regions within the rostral PFC with different cytoarchitectonic
properties, and a recent meta-analysis of 104 imaging studies
provided further evidence of a functional specialization of at least
two distinct subregions within the rostral PFC (Gilbert et al., 2006c). In
the light of these findings, the conflicting results and competing
models of rostral PFC function may not be mutually exclusive but may
rather describe the function of different anatomical regions within
rostral PFC.
However, to date, few imaging studies have been conducted that
explicitly examine the question whether there is a functional
dissociation of subregions within the rostral PFC. These studies
provided first experimental evidence of a functional specialization of
the rostral PFC along a medial–lateral dimension, with rostrolateral
aspects being specifically involved in orienting attention to internal
representations and anterior medial aspects in directing attention to
information that is present in the sensory environment (Gilbert et al.,
2005, 2006a,b). Based on these findings, Burgess et al. (2007a)
formulated the ‘gateway hypothesis of rostral PFC function’, according
to which a ‘supervisory system’ is located in the rostral PFC, which
exerts control over the coordination of stimulus-independent and
stimulus-oriented cognition. Within this system, the anterior rostromedial PFC is supposed to be involved in generating an attentional
bias towards incoming perceptual information and the rostrolateral
PFC in maintaining attention to internal representations.
Importantly, however, according to the model, both rostral PFC
subregions are not sites of information processing per se but
accomplish their function by “altering the flow of information
between other parts of the cognitive system” (Burgess et al., 2007a,
p. 292). Thus, the system is supposed to act as a routing system that
modulates the flow of information. This description is reminiscent of
the ideas of ‘gating models’, which assume that frontal regions
interact with other cortical and subcortical regions in order to bias
information processing. In particular, it has been suggested that
interactions of the frontal cortex with the basal ganglia and the
thalamus are the basis for controlling the access of incoming information to higher processing areas (Frank et al., 2001; Hazy et al.,
2007; LaBerge 2002). In addition, accumulating evidence suggests
that the PFC can modulate information processing in sensory
association cortices depending on the current attentional demands
(Hopfinger et al., 2000; Kastner et al., 1999; Giesbrecht et al., 2006).
Similar interactions can also be assumed to be essential for the
proposed functions of the gateway system, especially as the SOsystem is supposed to be able to afford an “amplification of input” and
the SI-system to “ensure that the activation of representations is less
determined by sensory input” (Burgess et al., 2007a, p. 292). However,
the gateway hypothesis remains relatively vague on this point and, in
particular, the neurofunctional interactions which may underlie the
described attentional weighting processes are not specified. In the
current study, we addressed this issue using functional magnetic
resonance imaging (fMRI) and functional connectivity analysis. In the
first step, we sought to investigate whether we could find additional
support for the notion of a functional subdivision of the rostral PFC
1
We will use the term “rostral PFC,” as well as “rostrolateral” and “rostromedial”
PFC. With respect to the literature, “rostrolateral PFC” is used for the part of rostral PFC
with an x-coordinate N 20 (see Christoff and Gabrieli 2000; Smith et al., 2007; Gilbert
et al., 2006c) and “rostromedial PFC” for the part with an x-coordinate b20.
1667
into a rostrolateral and an anterior medial part, and if so, in the second
step, we aimed to assess whether these subregions bias attentional
orienting towards external or internal information by specifically
interacting with other parts of the brain.
In addressing these issues, we designed an experimental paradigm
that imposes different demands on external or internal attending.
Taking into account that most natural situations do not involve the
processing of either solely internal or solely sensory information, we
decided to vary the relative degree to which attention had to be
directed to the different sources of information. Using these tasks, we
hypothesized that if the gateway hypothesis is correct, 1) the degree
to which attention is directed to external or internal information
should be reflected in the differential activation pattern of a
rostromedial and rostrolateral PFC subregion, and 2) these subregions
should functionally interact with other brain regions in order to
prioritize the processing of internal or external information depending on the current attentional demands.
Materials and methods
Subjects
Participants were 27 right-handed native speakers of German (14
females, 13 males; mean age: 24.56 ± 2.53 years). All participants
were recruited from an academic environment and had normal or
corrected to normal vision. Ethical approval from the local ethics
committee and written informed consent were obtained prior to the
experiments. Subjects were paid for their participation.
Experimental design
The experiment comprised three experimental tasks imposing
different demands on attending to externally presented or internally
represented information, respectively. In designing these tasks, we
considered the prerequisites named by the authors of the gateway
hypothesis for tasks stressing external or internal attending. According to Burgess et al. (2007b), an external attention task requires 1)
that the information to be processed is currently available (i.e. present
in the sensory environment), 2) that the attention is directed to
external stimuli or stimulus features, and 3) that the operations
involved prior to responding are relatively automatic or well-learnt.
In contrast, a task stressing internal attending requires 1) that
the information attended to is not currently being presented (i.e.
not available in the sensory environment), 2) that this information is
self-generated or comes from a previously witnessed episode, and
3) that the responses to be made are triggered by these internal
representations.
In accordance with these characteristics, we designed three tasks
engaging internal and external attending to a different degree.
Importantly, we decided to vary the relative degree to which attention
is directed to either type of information, instead of using the most
extreme task variants (e.g. an internal task with no external
stimulation at all). This was done for two reasons. Firstly, most
natural situations do not exclusively involve the processing of either
internal or external information but involve both types of information,
just differing in the relative degree to which attention is directed to
each of them. Secondly, we wanted to ensure greatest possible
comparability between the internal and external tasks in all aspects,
with the exception of the directing of attention to sensory or
internally represented information. This requires the tasks to be
closely matched with respect to the visual stimulation and the
responses to be made (which is hardly accomplishable when
comparing a task involving a reaction to sensory stimuli with a task
that is performed entirely “in the head” of the participants).
All tasks had the same stimulation design and timing and were
performed in short blocks. At the beginning of each block, subjects
1668
I. Henseler et al. / NeuroImage 56 (2011) 1666–1676
received a cue (geometric shape) that informed them about which
task they had to perform during the upcoming five response trials (see
Fig. 1). The task cue was presented for 1500 ms, followed by a variable
time interval of 1000–2000 ms (varied in steps of 500 ms) and a
display showing two colored squares for 1500 ms (serving as the
memory set in the internally oriented [IO] task and being irrelevant in
the other two tasks). This presentation was followed by a second
variable time interval of 1000–2000 ms (varied in steps of 500 ms,
depending on the length of the first delay). Both variable time
intervals served as jitter, allowing the separate analysis of the activity
related to the cue, the memory set, and the activity related to the time
period comprising the response trials. After the second jitter, five
successive response trials of the same type were presented, during
each of which a display showing three squares in a horizontal row was
presented for 500 ms, followed by a blank screen for 2300 ms. In each
of these trials, one of the squares was colored and the other two
squares were gray and subjects had to make a response (button press
with the index finger of the left or right hand) according to the current
task instruction.
In the first task, which was designed to engage external attending
to the relatively highest degree, the colored square occurred either on
the left or on the right position on the screen (i.e. it was located either
to the left or the right of the two gray squares) and subjects were
instructed to attend to its spatial location and to press a button with
the left or right index finger accordingly (externally oriented position
task, EOposition). This task is highly stimulus-oriented as it requires
subjects to focus on externally presented (sensory) information,
involves little task set information, and requires almost automatic,
stimulus-triggered responses.
The second task was designed to impose high demands on
stimulus-oriented attending as well, but it was also intended to
involve internally represented information to a slightly higher degree
than the first task. In this task, the colored square was presented
between the two gray squares and subjects had to decide whether this
central stimulus matched a predefined target (red square) or not and
to press a button accordingly (externally oriented target task,
EOtarget). This task again mainly engages stimulus-oriented attending
but additionally requires the maintenance of the target representation
and the response mapping.
In the third task, which was designed to involve attending to
stimulus-independent information to the relatively highest degree,
subjects had to focus their attention on internally represented
information with no direct correlate in the sensory environment
and to base their responses on this information. Specifically, two
colored squares (presented at the beginning of the block) had to be
maintained internally, and during the subsequent response trials,
subjects had to decide whether the current stimulus (again a colored
square presented in the center between two gray squares) matched
one of the internally represented items or not (internally oriented
task, IO). This task was considered to fulfill the above-mentioned
requirements for a task engaging internally oriented attention, as
stimulus-independent information is in the focus of attention and
determines the responses to be made.
Thus, importantly, all three task variants involve attending to both
external and internal information; however, the relative degree to
which attention is directed to either type of information was varied:
The EOposition task engages external attending to the relatively highest
degree, the IO task involves attending to internal representations
to the relatively highest degree, and the EOtarget task takes an
intermediate position between them.
The tasks were presented in pseudorandom order (with no more
than 3 blocks of the same task in direct succession). The whole
experiment comprised 3 runs of 24 blocks (8 blocks per task per
session, 24 blocks per task for the whole experiment, 72 blocks in
total) with short pauses between runs and fixation periods between
blocks. The transitions between task variants were counterbalanced.
There were a total of 36 task repeats and 36 task switches, with each
task variant having the same number of repeat and switch blocks. We
additionally controlled for the number of the different delays in each
task variant. Furthermore, the different trial types (match/non-match,
target/non-target, left/right position) occurred equally often over the
experiment and the transition probabilities of the trial types within a
task variant were counterbalanced. A total of nine different colors
(plus gray) with equal luminance were used for the experiment. The
target color from Task 2 did not occur in the two other tasks in order
to avoid interference, and the colors representing the memory set in
the IO task were chosen randomly out of the remaining eight colors.
The cues were geometric forms. All stimuli were created using
Presentation software (Version 11.1, Neurobehavioral Systems,
Albany, NY, USA).
During scanning, participants viewed the stimuli on a black
background using a goggle system (Resonance Technology, Northridge, CA, USA). Button presses were made with the index finger
of the left or right hand via a response system (Current Designs,
Fig. 1. Experimental design with example stimuli and timing (for details, see text). Left: EOposition task, middle: EOtarget task, right: IO task. For simplicity, only three of the five
consecutive trials in each block are shown.
I. Henseler et al. / NeuroImage 56 (2011) 1666–1676
Philadelphia, PA, USA). The total scanning time was 40 min (including
positioning and anatomic scanning) and one run lasted about 10 min.
Subjects were trained on the tasks for about 30 min outside the
scanner before the experiment.
fMRI data acquisition
Imaging was performed on a 3 T Magnetom Tim Trio system
(Siemens Healthcare, Erlangen, Germany) equipped with a 12
channel head coil. Thirty-three axial slices parallel to the anterior
commissure–posterior commissure (AC-PC) line were obtained in
ascending acquisition order using a gradient-echo echo planar
imaging (EPI) sequence (voxel size: 3 × 3 × 3 mm; echo time 30 ms;
flip angle 70°; field-of-view 192 mm; 64 × 64 matrix; interscan
repetition time = 2000 ms). A total of 873 volumes were acquired
(291 per run). Additionally, anatomical (T1-weighted) scans were
acquired for each subject (voxel size: 1 × 1 × 1 mm). The head was
stabilized with small cushions to avoid head movements and
triggering of the stimulation by the scanner pulses was conducted
using Presentation Software.
Data analysis
Behavioral data
Behavioral and demographic data were analyzed using SPSS
software (version 16, SPSS Inc., Chicago, IL, USA). Firstly, normal
distribution of the behavioral data was tested using the Kolmogorov–
Smirnov test. As this test did not reach statistical significance, the
application of parametric tests was justified. Accuracy data and
reaction times (RTs) were aggregated and means were submitted to a
repeated-measures ANOVA with the within-subject factor TASK
(EOposition, EOtarget, IO). Subsequently, specific effects were tested
with two-sided post-hoc t-tests and results are reported assuming
significance at a criterion of p b 0.05. Error and omission trials were
excluded from the reaction time analysis. The behavioral data from
one subject was not recorded and could not be analyzed.
Identification of task-related activity
The fMRI data were preprocessed and statistically analyzed using
SPM2 (Wellcome Department of Cognitive Neurology, London, UK).
Preprocessing comprised realignment and unwarping, correction for
slicetime acquisition differences and low-frequency fluctuations
(highpass filter with 128-s cutoff), coregistration of the functional
and anatomical volumes, and spatial normalization to standard
stereotactic space (using the Montreal Neurological Institute (MNI)
template provided by SPM2; normalized voxel size: 3 × 3 × 3 mm).
For group analysis, data were additionally smoothed using a 9 mm
full-width half-maximum (FWHM) Gaussian kernel.
Statistical analyses were conducted using the general linear model
(GLM) in SPM, creating a design matrix that allowed testing for brain
activity changes associated with the different experimental tasks. The
design matrix comprised four regressors, one for each task variant
(EOposition, EOtarget, IO) and one for the fixation period between task
blocks. As we were interested in brain regions showing sustained
activity during periods of external or internal attending, we modeled
the sustained activity over the whole blocks (i.e. the activity that was
time-locked to the beginning of the first response trial and lasted until
the end of the last response trial; the activity related to the processing
of the cue and the set were not included). These time periods had a
length of 14 s. The corresponding vectors were convolved with a
canonical hemodynamic response function (HRF) using a boxcar
function in order to produce the predicted hemodynamic response for
each experimental condition.
Next, linear t-contrasts were performed on this data in order to test
for effects at the single-subject level. Subsequently, these singlesubject contrast images were taken to a second-level group analysis, in
1669
which inter-subject variability was treated as random factor (random
effects analysis). Results of this second-level analyses are reported at a
statistical threshold of p b 0.05, corrected for multiple comparisons at
the cluster level using the family-wise error (FWE) approach. In
addition to the whole-brain analyses, we extracted the beta values
from a set of regions of interest (ROI) using the MarsBar toolbox for
SPM (http://marsbar.sourceforge.org). These ROIs were defined
creating a 5-mm sphere around the maxima of activation located in
rostrolateral and rostromedial PFC (i.e. in those regions that have
previously been reported to be sites of functional activation during
internal and external attending; see Gilbert et al., 2005, 2006a,b,
2007; Burgess et al., 2003, 2007a,b), yielding one parameter estimate
per subject, per region and per contrast. In a further step, the beta
values were correlated with behavioral performance measures using
SPSS.
Functional connectivity analysis
For the functional connectivity analysis, we used the psychophysiological interactions (PPI) approach proposed by Friston et al. (1997).
This approach allows the detailed examination of task-related
functional interactions between brain regions. It requires one
regressor representing the signal time course in a given volume of
interest (VOI) and one regressor representing the psychological
variable of interest. In the present study, the VOI regressors were
created by extracting the BOLD signal from 5-mm spheres around the
local maxima of task-related brain activation in subregions of the
rostral PFC showing differential activation during external versus
internal attending.
Accordingly, the time series of the local activations in rostromedial
PFC specifically associated with external attending (MNI coordinates x
y z: −3 60 0 and 3 60 15, see Table 1) and in rostrolateral PFC
specifically associated with internal attending (MNI coordinates x y z:
30 48 9 and − 33 48 18, see Table 1) were extracted. The time series of
all voxels in a VOI were averaged and the resulting (deconvolved)
activation time course served as the physiological vector Y. The
second vector was the psychological vector P of the time t, which was
set to 1 if t was the onset of an epoch requiring external attending and
to −1 if it was the onset of an epoch requiring internal attending (this
accounts for the VOI in rostromedial PFC and was the reverse for the
VOI in rostrolateral PFC). The product of the physiological and the
psychological vector determined the PPI term. After reconvolution
with the hemodynamic response function, whole-brain correlation
analyses were carried out in a voxel-wise manner for each seed region
in each subject in order to determine brain regions showing taskrelated modulation of connectivity with the seed region. The singlesubject data were then entered into a random effects model and group
results were thresholded at p b 0.005, uncorrected.
Results
Behavioral data
All participants performed well. During the EOposition task, subjects
had a mean of 99.5% correct responses (SD 0.97), during the EOtarget
task 97.7% (SD 2.12), and during the IO task 92.2% (SD 4.85). The mean
reaction times were 413.83 ms (SD 49.56) for the EOposition task,
478.26 ms (SD 68.82) for the EOtarget task, and 569.39 (SD 93.28)
for the IO task. The repeated-measures ANOVA for accuracy and
reaction times showed a significant main effect of TASK (accuracy:
F2,50 = 63.56; p b .001; RT: F2,50 = 114.69; p b .001, Greenhouse–Geisser corrected) and the post-hoc t-tests revealed that accuracy
measures differed significantly between all three task variants
(accuracy: EOposition vs. EOtarget: t(25) = 4.71, p b .001; EOposition vs. IO:
t(25) = 8.05, p b .001; EOtarget vs. IO: t(25) = 8.75, p b .001; RT: EOposition
vs. EOtarget: t(25) = −9.42, p b .001; EOposition vs. IO: t(25) = −11.32,
p b .001; EOtarget vs. IO: t(25) = −9.94, p b .001).
1670
I. Henseler et al. / NeuroImage 56 (2011) 1666–1676
Brain activation
Table 1
Significant task-related brain activation during external and internal attending, and
direct task comparisons.
Contrast
Brain region
MNI coordinates
(x y z)
External attending to positions (EOposition N baseline)
R
Anterior rostromedial PFC
3 60 15
L
Anterior rostromedial PFC
−3 60 0
R
Inferior frontal gyrus
54 36 −6
M
Orbitofrontal cortex
0 45 −18
L
Posterior cingulate cortex
−6 −54 30
R
Temporo-parietal junction
69 −27 18
L
Middle temporal gyrus
−63 −12 −18
R
Parieto-occipital cortex
60 −63 27
L
Parieto-occipital cortex
−51 −75 30
R
Amygdala
24 −9 −18
L
Amygdala
−24 −12 −21
R
Putamen
33 −6 3
External attending to targets (EOtarget N baseline)
R
Rostromedial PFC
9 57 27
L
Rostromedial PFC
−9 45 27
R
Inferior frontal gyrus
45 42 −3
R
Temporo-parietal junction
66 −36 39
L
Middle temporal gyrus
−63 −21 −18
R
Parieto-occipital cortex
57 −63 36
L
Parieto-occipital cortex
−57 −63 36
Internal attending (IO N baseline)
R
Rostrolateral PFC
24 51 −9
L
Rostrolateral PFC
−27 51 −3
R
Superior frontal gyrus
21 15 63
R
Middle frontal gyrus
42 39 24
R
Deep frontal operculum
36 21 −9
L
Deep frontal operculum
-30 18 −12
R
Pre-SMA
6 30 48
R
Intraparietal cortex
54 −57 51
External N internal attending (EOposition N IO)
R
Anterior rostromedial PFC
3 60 15
L
Anterior rostromedial PFC
−3 60 0
R
Inferior frontal gyrus
54 36 3
M
Orbitofrontal cortex
0 39 −18
L
Posterior cingulate cortex
−6 −51 30
R
Posterior insula
45 −18 18
R
Temporo-parietal junction
69 −24 15
R
Middle temporal gyrus
63 −6 −21
L
Middle temporal gyrus
−57 0 −21
R
Temporo-occipital cortex
57 −66 3
R
Parieto-occipital cortex
54 −72 27
L
Parieto-occipital cortex
−48 −75 30
R
Occipital cortex
39 −87 24
L
Occipital cortex
−33 −87 33
R
Hippocampus
24 −15 −21
L
Hippocampus
−24 −21 −18
L
Parahippocampal gyrus
−27 −36 −15
R
Amygdala
30 3 −21
L
Amygdala
−27 0 −27
R
Putamen
39 −9 −3
Internal N external attending (IO N EOposition)
R
Rostrolateral PFC
30 48 9
L
Rostrolateral PFC
−33 48 18
R
Superior frontal cortex
33 −3 54
R
Middle frontal gyrus
45 33 27
L
Middle frontal gyrus
−42 27 30
R
IFJ
48 15 33
L
IFJ
−39 9 27
R
Deep frontal operculum
36 24 −6
L
Deep frontal operculum
−30 18 3
R
Middle cingulate cortex
9 18 42
M
Pre-SMA
0 12 54
R
Intraparietal cortex
36 −54 42
L
Intraparietal cortex
−36 −54 48
R
Caudate
12 9 6
R
Pallidum
15 −3 3
Statistical effect
(T-value)
7.38
5.53
6.57
8.75
6.74
4.90*
7.12
9.18
9.12
4.49*
5.13*
3.51*
7.38
7.56
6.31
3.60*
3.74*
7.17
8.50
5.65
3.67*
6.84
5.92
5.65
6.05
7.13
6.99
11.32
10.88
4.70*
11.93
12.14
8.10
6.92
7.95
8.79
9.36
6.09
11.00
9.34
10.29
9.01
8.98
12.70
7.60
7.17
6.77
6.52
8.24
6.33
10.62
8.27
6.39
8.32
11.53
11.24
10.11
12.36
10.97
9.11
4.61
5.18
All activations are significant at p b 0.05 (FWE-corrected on cluster level), if not
indicated otherwise (*p b 0.001 uncorrected).
Task-related activation
Attending to external spatial information (positions) activated the
bilateral anterior rostromedial PFC, the right inferior frontal gyrus
(IFG), the medial orbitofrontal cortex (OFC), the posterior cingulate
cortex (PCC), the right temporo-parietal junction (TPJ), the left middle
temporal gyrus (MTG), the bilateral parieto-occipital cortex, the
bilateral amygdala, and the right putamen (EOposition N baseline,
Table 1). External attending to targets elicited activity in the bilateral
medial superior frontal cortex, the right IFG, the right TPJ, the left
MTG, and in the bilateral parieto-occipital cortex (EOtarget N baseline,
Table 1). Orienting attention to internal representations activated the
bilateral rostrolateral PFC, the right superior and right middle frontal
cortex, the bilateral deep frontal opercular cortex (FOC), the presupplementary motor area (pre-SMA), and the right intraparietal
cortex (IPC) (IO N baseline, Table 1).
Increased activation during external versus internal attending
The direct comparison between orienting attention to external
versus internal information revealed that the anterior rostromedial
PFC was significantly more strongly activated when attention was
directed to external information (Fig. 2). In addition, there was increased activation during external as compared to internal attending
in the right IFG, the medial OFC, the PCC, the posterior insula, the
right TPJ, the bilateral MTG, bilateral parieto-occipital and occipital
cortices, the bilateral amygdala–hippocampal complex, and in the
right putamen (EOposition N IO, Fig. 3A, Table 1, see also EOtarget N IO,
Supplementary Table). The contrast of orienting attention to the
spatial occurrence of a stimulus versus detecting a predefined target
(also reflecting relatively stronger external attending) also yielded
significantly increased activity in the bilateral anterior rostromedial
PFC, as well as in the left superior frontal cortex, the PCC, the bilateral
temporal and occipital cortices, and in the right parahippocampal
cortex (EOposition N EOtarget, Supplementary Table).
Increased activation during internal versus external attending
The reverse contrast comparing internal versus external attending
showed increased activity during internal attending in the bilateral
rostrolateral PFC, the bilateral superior and middle frontal cortices,
the bilateral inferior frontal junction area (IFJ), the bilateral FOC, the
middle cingulate cortex, the pre-SMA, the bilateral IPC, the caudate,
and the pallidum (IO N EOposition, Figs. 2 and 3B, Table 1, see also IO N
EOtarget, Supplementary Table). The bilateral rostrolateral PFC was also
significantly more strongly activated while performing the target task
as compared to the position task (this contrast also reflects relatively
stronger internal attending), as was the right IFJ, the bilateral middle
frontal cortex, the bilateral deep FOC, the right pre-SMA, and the right
IPC (EOtarget N EOposition, Supplementary Table).
Functional connectivity
Task-related connectivity modulation
During attending to external positions, the rostromedial PFC
showed increased functional connectivity to the left IFJ, the bilateral
superior frontal cortices, the medial OFC, the PCC, the right MTG,
bilateral parieto-occipital and occipital cortices, the bilateral amygdala, the bilateral caudate, bilateral putamen, and the thalamus, as
compared to baseline (EOposition N baseline, Table 2, Fig. 4A). During
target detection (compared to baseline), the rostromedial PFC was
significantly more strongly connected to the left IFJ, the left superior
frontal cortex, the left parieto-occipital and occipital cortex, the
precuneus, and the thalamus (EOtarget N baseline, Table 2). During
attending to internal representations, the rostrolateral PFC was
significantly more strongly connected to the bilateral IFJ, bilateral
superior and middle frontal cortices, the bilateral FOC, the pre-SMA,
I. Henseler et al. / NeuroImage 56 (2011) 1666–1676
1671
Fig. 2. Differential activation of the rostromedial and rostrolateral PFC during attentional orientation to external and internal information, respectively. Center: Brain activation map
showing significantly stronger activation of the anterior rostromedial PFC during the orientation of attention to external as compared to internal information (blue), and significantly
stronger activation of the rostrolateral PFC during the orientation of attention to internal as compared to external information (red). The scale below shows the color-coding of
the displayed T-values. Periphery: Parameter estimates extracted from the rostromedial PFC (left side) and rostrolateral PFC (right side) color coded for the different tasks
(blue: EOposition task; purple: EOtarget task; red: IO task). Images are shown at p b 0.05 (FWE-corrected). T-values and stereotactic coordinates are given in Table 1.
the right lateral OFC, the bilateral temporo-occipital cortex, and the
bilateral superior and intraparietal cortices, as compared to baseline
(IO N baseline, Table 2, Fig. 4B).
Increased connectivity during external versus internal attending
The contrast between external and internal attending revealed
that the anterior rostromedial PFC was significantly more strongly
connected to the left IFJ (see Fig. 5), the left superior frontal cortex, the
bilateral medial OFC, the PCC, the right MTG, the bilateral parietooccipital cortex, and the bilateral caudate during external attending
(EOposition N IO, Table 2). Additionally, the same region in the anterior
rostromedial PFC was significantly more strongly connected to the
left IFJ during target detection as compared to internal attending
(EOtarget N IO, Table 2).
Increased connectivity during internal versus external attending
During internal compared to external attending, the rostrolateral
PFC was significantly more strongly connected to the left IFJ (see
Fig. 5), the bilateral superior and middle frontal cortex, the middle
cingulate cortex, and the pre-SMA (IO N EOposition, Table 2). The
rostrolateral PFC was also significantly more strongly connected to
the left IFJ during internal attending than during target detection
(IO N EOtarget, Table 2).
Correlations
The intensity of the activation in rostromedial PFC while performing the external position task (as compared to the internal task)
correlated significantly with the subjects’ accuracy during this task
(r = .37, p = 0.031). This means that the more the rostromedial PFC
Fig. 3. (A) Brain regions showing significantly stronger activation together with the rostromedial PFC during external compared to internal attending (EOposition N IO, pb0.05, FWEcorrected). (B) Brain regions showing significantly stronger activation together with the rostrolateral PFC during internal compared to external attending (IO N EOposition,
p b 0.05, FWE-corrected). T-values and stereotactic coordinates are given in Table 1. R: right; L: left; A: anterior; P: posterior.
1672
I. Henseler et al. / NeuroImage 56 (2011) 1666–1676
Table 2
Functional connectivity of the anterior rostromedial PFC and the rostrolateral PFC
during attentional orienting to external and internal information.
Contrast
Brain region
MNI coordinates
(x y z)
Statistical effect
(T-value)
Increased connectivity of anterior rostromedial PFC during external attending
(EOposition N baseline)
L
IFJ
-33 6 42
3.84
R
Superior frontal cortex
21 36 54
4.50
L
Superior frontal cortex
−12 39 51
5.70
R
Medial superior frontal gyrus
6 48 27
5.67
L
Medial superior frontal gyrus
−6 57 27
4.75
R
Medial orbitofrontal cortex
3 42–18
4.18
M
Posterior cingulate cortex
0 −60 27
6.16
R
Middle temporal gyrus
63 −12 −21
4.41
R
Parieto-occipital cortex
51 −63 39
3.57
L
Parieto-occipital cortex
−45 −72 42
4.47
R
Occipital cortex
21 −72 −9
3.31
L
Occipital cortex
−6 −84 −9
3.82
R
Caudate
12 6 21
4.35
L
Caudate
−12 9 21
4.09
R
Putamen
15 3 −9
3.47
L
Putamen
−27 9 −6
3.07
R
Amygdala
15 −6 −15
2.95
L
Amygdala
−18 −9 −18
3.40
R
Thalamus
6 −6 0
4.07
Increased connectivity of anterior rostromedial PFC during external attending
(EOtarget N baseline)
L
IFJ
−48 18 30
4.10
L
Superior frontal cortex
−33 3 66
3.10
L
Parieto-occipital cortex
−33 −78 48
2.87
M
Occipital cortex
0 −87 42
3.32
R
Precuneus
3 −75 42
3.06
R
Thalamus
6 −6 6
3.79
Increased connectivity of rostrolateral PFC during internal attending (IO N baseline)
L
IFJ
−51 9 30
3.11
R
IFJ
45 15 42
4.78
R
Superior frontal sulcus
27 18 63
3.29
L
Superior frontal sulcus
−27 21 51
3.63
R
Anterior middle frontal gyrus
36 57 −3
3.81
L
Anterior middle frontal gyrus
−36 54 0
4.95
R
Deep frontal operculum
39 27 3
3.68
L
Deep frontal operculum
−51 18 3
3.92
R
Lateral orbitofrontal cortex
30 42 −18
4.17
L
Pre-SMA
−3 36 36
4.03
R
Intraparietal cortex
45 −48 57
2.95
L
Intraparietal cortex
−27 −54 33
3.22
R
Superior parietal lobule
27 −60 69
3.57
L
Superior parietal lobule
−24 −51 72
3.43
R
Temporo-occipital cortex
57 −45 −6
3.80
L
Temporo-occipital cortex
−60 −48 18
4.88
L
Occipital cortex
−21 −72 30
3.85
Stronger connectivity of anterior rostromedial PFC during external N internal
attending (EOposition N IO)
L
IFJ
−30 15 27
2.73*
L
Superior frontal cortex
−15 33 54
3.07
R
Medial orbitofrontal cortex
9 54 −12
3.91
L
Medial orbitofrontal cortex
−9 30 −15
3.37
M
Posterior cingulate cortex
0 −57 33
3.70
R
Middle temporal gyrus
63 −3 −24
4.11
R
Parieto-occipital cortex
54 −66 42
3.27
L
Parieto-occipital cortex
−45 −75 45
3.04
R
Caudate
18 18 12
3.38
L
Caudate
−9 18 −6
2.84
Stronger connectivity of rostrolateral PFC during internal N external attending
(IO N EOposition)
L
IFJ
−45 15 27
4.16
R
Superior frontal cortex
33 −12 69
2.87
L
Middle frontal gyrus
−45 15 27
4.16
R
Middle cingulate cortex
3 6 30
3.65
R
Pre-SMA
3 −3 60
2.90
Stronger connectivity of anterior rostromedial PFC during external N internal
attending (EOtarget N IO)
L
IFJ
−45 18 30
3.16
Stronger connectivity of rostrolateral PFC during internal N external attending
(IO N EOtarget)
L
IFJ
−54 18 33
3.01
All results are significant at pb 0.005 (uncorrected), if not indicated otherwise (*pb 0.01,
uncorrected).
was activated during the external task, the better the behavioral
performance was. The same was true for the parieto-occipital cortex,
whose activity also correlated significantly with better task performance during the external task (r = .36; p = 0.037). Furthermore, the
strength of the functional connectivity between the rostromedial PFC
and the parieto-occipital cortex showed a trend towards a positive
correlation with accuracy in the external task (r = .29; p = 0.081).
Therefore, there is evidence that the signal change in the rostromedial
PFC and in the parieto-occipital cortex, as well as the strength of
coupling between these two regions is related to better performance
in the externally oriented attention task.
In addition, we investigated whether the signal change in the
rostromedial and rostrolateral PFC related to the contrast of external
versus internal attending is correlated with between-subject differences in the behavioral data (i.e. whether the behavioral effect of “task
difficulty” as reflected by differences in RTs and error rates between
both task variants correlates with the signal differences between
these tasks). This analysis revealed that the signal change in the
rostromedial PFC for the contrast of external versus internal attending
was not correlated with either the difference in RTs or error rates
between these conditions (RT: r = 0.19, p N 0.3; accuracy: r = 0.19,
p N 0.3). Similarly, the signal change in the rostrolateral PFC related to
the internal–external contrast was unrelated to behavioral measures
of “task difficulty” (RT: r = 0.05, p N 0.8; accuracy: r = 0.02, p N 0.9).
Thus, it is unlikely that differences in “task difficulty” between the
conditions are responsible for the detected signal changes in the
rostromedial and rostrolateral PFC.
Discussion
The present study aimed to test two core proposals of the ‘gateway
hypothesis of rostral prefrontal cortex function’ as proposed by
Burgess et al. (2007a,b) and Gilbert et al. (2005, 2006a,b). The first is
that there is a functional subdivision of the rostral PFC into a medial
and a lateral part, with these regions being differentially sensitive to
the demands on externally and internally oriented cognition. The
second is that these subregions can actively modulate attentional
orienting towards external or internal information by specifically
interacting with other parts of the brain.
As predicted by the gateway hypothesis, we found differential
activation in the rostral PFC depending on the current attentional
demands, demonstrating segregation between a rostromedial and a
rostrolateral subregion. In particular, we observed recruitment of the
rostromedial PFC during conditions requiring high degrees of
attention to the external environment and of the rostrolateral PFC
when attention had to be mainly directed to internally represented
information. These observed activation differences cannot be attributed to differences in “task difficulty” (as indexed by RTs and error
rates) as the observed signal changes were unrelated to behavioral
differences between the internal and external tasks. Thus, the current
findings are congruent with the gateway hypothesis in suggesting
that the rostromedial PFC may play a role in supporting stimulusoriented attending and the rostrolateral PFC in supporting attentional
orientation to internally represented information.
Together with the rostromedial PFC, the TPJ, IFG, insular cortex,
OFC, PCC, amygdala, striatum, and the bilateral visual association
cortices were significantly more strongly activated when external
information was in the focus of attention. These coactivated areas
have repeatedly been shown to be involved in attending to behaviorally
relevant sensory stimuli (Downar et al., 2000, 2001, 2002; Kiehl et al.,
2005; Sridharan et al., 2007; Williams et al., 2007; Hahn et al., 2006;
Mesulam et al., 2001; Gruber et al., 2010; Diekhof et al., 2009), and the
observed activation pattern is thus compatible with the suggestion
that the rostromedial PFC may be part of a ‘stimulus-oriented attending
system’ supporting the processing of external information (Burgess
et al., 2007a,b).
I. Henseler et al. / NeuroImage 56 (2011) 1666–1676
1673
Fig. 4. Functional connectivity of the rostromedial and rostrolateral PFC during external and internal orientation of attention. (A) Functional connectivity of the rostromedial
PFC during external attending. (B) Functional connectivity of the rostrolateral PFC during internal attending. T-values and stereotactic coordinates are given in Table 2. R: right;
L: left; A: anterior; P: posterior.
It has further been reported that the activity in the TPJ, IFG, and
PCC predicts performance in upcoming trials (Weissman et al., 2006;
Mesulam et al., 2001; Small et al., 2003). For instance, PCC activation
was found to be correlated with the speed of detecting a lateralized
visual target in a task where targets were preceded by a predictive
cue (Mesulam et al., 2001), and increased IFG and TPJ activity reliably
predicted better performance in the next trial in a visual attention task
Fig. 5. Differential connectivity of the rostromedial and rostrolateral PFC to the IFJ
depending on the current attentional demands. The rostromedial PFC is significantly
more strongly connected to the left IFJ during external attending (upper row) and the
rostrolateral PFC is significantly more strongly connected to the left IFJ during internal
attending (lower row). T-values and stereotactic coordinates are given in Table 2.
(Weissman et al., 2006). Other studies have shown that higher-order
regions can modulate the activity of the TPJ (Shulman et al., 2003;
Kincade et al., 2005), suggesting the influence of a top–down
attentional bias. Following the ideas of the gateway hypothesis, the
anterior rostromedial PFC might be one of the higher-order control
regions generating this bias. A first finding indeed supporting this
notion is our observation of a significant relationship between higher
rostromedial PFC activation and better performance during the
externally oriented attention task. Similar activation–performance
relationships have been described previously (Small et al., 2003;
Gilbert et al., 2006a,b) and have been interpreted as reflecting an
internally generated attentional bias to information in the environment that has particular relevance for ongoing behavior. These results
indicate a functional relevance of the rostromedial PFC, TPJ, IFG, and
PCC in the performance of external attention tasks and suggest an
involvement of these regions in a system that generates an attentional
bias towards the preferential processing of sensory information.
At the same time, the observed relationship between higher
rostromedial PFC activity and better cognitive task performance
speaks against the interpretation that the activation reflects daydreaming or mentalizing. The latter might be suggested with regard to
the ‘default mode hypothesis’, according to which the medial PFC is
part of a network that is especially activated during conscious rest (i.e.
“when there are no external demands on our attention,” see Fransson,
2006, p. 2836). The default mode activity is thought to reflect selfreferential processing (D'Argembeau et al., 2005; Fransson, 2006;
Raichle et al., 2001; Mason et al., 2007) and since this sort of
processing is assumed to disturb cognitive operations, the default
mode regions are expected to be deactivated during cognitive task
performance. In clear contrast to this hypothesis, the region in the
rostromedial PFC that we identified was found to be activated during
cognitive task performance and the intensity of this activation
predicted better task performance during an attention-demanding
cognitive task. Thus, the region we describe is engaged, rather than
shut down, during cognitive task performance.
1674
I. Henseler et al. / NeuroImage 56 (2011) 1666–1676
The most probable explanation for this discrepancy between our
finding and the default mode account is that the different models of
rostral PFC function may apply for different subregions. Brain
activations associated with the ‘default mode function’ are typically
located in the caudal part of the medial prefrontal cortex adjacent to
the anterior cingulate cortex (Fransson, 2006; Mantini et al., 2007;
Greicius et al., 2003; Jafri et al., 2008; D'Argembeau et al., 2005). This
brain region has also been reported to be activated during the
evaluating of one's own feelings, self-referential decision-making,
mentalizing, and perspective-taking (Gusnard et al., 2001; Frith and
Frith, 2003; Johnson et al., 2005). In contrast, the activation clusters
observed in the context of external attention are localized in the most
anterior part of the medial rostral PFC at the convexity to the lateral
PFC (Small et al., 2003; Gilbert et al., 2005, 2006a,b,c; Burgess et al.,
2003). These data indicate that the regions associated with external
attending are neuroanatomically distinct from those associated with
the default mode function, and, indeed, evidence of such an anterior–
posterior dissociation within the rostromedial PFC has been reported
(Gilbert et al., 2006c, 2007; Simons et al., 2008). The findings of the
present study are in line with these findings in suggesting that the
most anterior part of the rostromedial PFC is involved in generating an
attentional bias toward the processing of incoming sensory information.
In order to generate this bias, it has been proposed that the
rostromedial PFC specifically interacts with other parts of the brain
(Burgess et al., 2007a). A first (descriptive) finding of the present
study indeed suggesting such coordinated activity of the rostromedial
PFC with other brain regions was that of striking similarities between
the activation profiles obtained for the rostromedial PFC and those
obtained for the OFC, PCC, TPJ, amygdala, putamen, and the parietooccipital cortex. All profiles were characterized by high activation
during task periods imposing high demands on stimulus-oriented
attending and lower activation/deactivation during periods of internal
attending, and are thus congruent with the expected pattern for
regions engaged in stimulus-oriented processing (see Hahn et al.,
2006).
In order to directly test for functional interactions, we conducted
functional connectivity analysis and evaluated whether the identified
region in the anterior rostromedial PFC specifically interacts with
other brain regions to prioritize the flow of incoming sensory
information. These analyses revealed that the rostromedial PFC is
functionally connected to the OFC, PCC, thalamus, striatum, the
amygdala, and bilateral visual processing areas during phases of
external attending. Functional top–down connections between the
rostromedial PFC and more ‘downstream’ regions like the amygdala
and visual association cortices have been reported previously
(Summerfield et al., 2006), and a recent meta-analysis found
conclusive evidence that the rostromedial PFC is connected to the
PCC and temporo-parietal regions (Gilbert et al., 2010). Furthermore,
some of the regions that we found to be connected to the rostromedial
PFC show an overlap with the ‘saliency network’ described by Seeley
et al. (2007)—a network that has been suggested to magnify the drive
for transmission of salient signals. In particular, the interaction of the
rostromedial PFC with the striatum and the thalamus is important to
notice, as these connections might be directly involved in regulating
the flow of incoming sensory information to the PFC (see for instance
Frank et al., 2001; O'Reilly and Frank, 2006).
It is known that the rostral PFC has strong anatomical connections
to the basal ganglia (Leh et al., 2007, 2008; Thottakara et al., 2006) and
it has been hypothesized that it can modulate other cortical regions
through these connections. According to functional 'gating models' an
open gate (i.e. access of sensory input to higher processing areas) is
associated with coordinated activity of the PFC, striatum, and
thalamus (O'Reilly and Frank, 2006; Frank et al., 2001; Hazy et al.,
2007; LaBerge 2002; Haber and McFarland 2001), which is an
excellent fit with the connectivity pattern we observed while subjects
focused their attention on externally presented stimulus information.
This pattern might be a correlate of a thalamo-cortical loop which
provides incoming sensory information with access to higher
processing areas. Our observation also fits well to the findings of
Soto and colleagues (2007), who observed increased coupling
between the rostral PFC and the thalamus during a visual attention
task. This connectivity pattern was interpreted as reflecting a
'frontothalamic attention system' and is consistent with the notion
that the rostromedial PFC is involved in attentional weighting
processes that prioritize the processing of task-relevant sensory
information. In line with this assumption, we additionally found
strong functional coupling between the rostromedial PFC and bilateral
visual association cortices during external attending, and, in addition,
higher activity in these regions correlated with better task performance. These findings are in good agreement with the idea that the
anterior rostromedial PFC may be involved in a 'fast route of
attending' accomplishing an amplification of input, as proposed by
Burgess et al. (2007a) in the gateway hypothesis.
In contrast to the rostromedial PFC, the rostrolateral PFC was
preferentially activated when attention had to be directed to internal
representations that have no direct correlate in the sensory
environment. This finding is in line with studies indicating that the
rostrolateral PFC plays a key role in the evaluation, monitoring and
manipulation of mental representations and, thus, in situations which
require a high degree of internally oriented cognition (Dumontheil et
al., 2010; Koechlin et al., 1999; Collette et al., 2007; Soon et al., 2008;
Christoff and Gabrieli 2000, Diekhof and Gruber, 2010). In the present
study, the rostrolateral PFC was activated together with the
dorsolateral and ventrolateral prefrontal cortex, the cingulate and
the intraparietal cortex during internal attending. These regions are
all well-known to be involved in working with internal representations and have repeatedly been implicated in neural networks
underlying the maintenance of mentally represented information
(Cole and Schneider 2007; Dosenbach et al., 2008; Gruber 2001;
Gruber and von Cramon 2001, 2003; Li et al., 2004). We consistently
found strong functional connectivity between the rostrolateral PFC
and the ventro-/dorsolateral prefrontal cortex, as well as cingulate
and parietal cortex regions during internal orienting, revealing a
functional network that is preferentially involved when internal
representations are the focus of attention. This connectivity pattern is
highly congruent with the coactivation pattern described for the
rostrolateral PFC in the recent meta-analysis by Gilbert et al. (2010)
and fits well with theoretical accounts implicating prefronto-parietal
networks in the processing of internally generated and internally
maintained information (Christoff and Gabrieli 2000; Cole and
Schneider 2007; Gruber and von Cramon 2003).
In addition, the pallidum was found to be more strongly activated
during phases of internal than external attending, together with the
rostrolateral PFC. This finding is in line with the notion that the
pallidum might be involved in restricting the access of sensory
information to higher processing areas. Recently, it has been
demonstrated that higher pallidum activity is associated with better
filtering of incoming sensory information and with more efficient
working memory processing (McNab and Klingberg 2008). Thus, the
pallidum activity we observed during task periods requiring high
attention to internal representations might reflect the fact that these
internal representations are “shielded” against disturbing sensory
information. This is especially plausible, as the internally maintained
information in our experiment had to be preserved over several trials
in which competing stimulus information was present. Taken
together, these findings are in good agreement with the suggestion
that, together with other brain regions, the rostrolateral PFC is part of
an attending system which is involved in focusing on internally
represented information in the face of potentially competing stimuli
as proposed in the gateway hypothesis (Burgess et al., 2007b).
Interestingly, the rostromedial and rostrolateral PFC further
cooperated with another important prefrontal region involved in
I. Henseler et al. / NeuroImage 56 (2011) 1666–1676
cognitive control, the inferior frontal junction area (IFJ), in a taskspecific manner. The IFJ has been related to processes of attentional
orienting to mental or external information, as well as to gating and
selection processes (Nobre et al., 2004; Lepsien and Nobre, 2006,
2007; Knott et al., 2009; Li et al., 2004). In good agreement with these
results, we found the rostromedial PFC subregion to be more strongly
connected to the IFJ when attention had to be directed to sensory
information, while the rostrolateral PFC region was more strongly
connected to the IFJ when information had to be oriented to internal
representations. This task-specific coupling of the two rostral PFC
subregions to the IFJ may be a key aspect in dynamically setting the
gains towards the preferential processing of external or internal
information.
Taken together, the present results support the notion that the
rostral PFC may play a key role in balancing attentional orienting to
external and internal information. In particular, the data are in line
with the previously proposed functional specialization within the
rostral PFC along a medial–lateral dimension, with anterior rostromedial areas being preferentially involved in directing attention to
external stimuli, and rostrolateral areas in maintaining high degrees
of attention upon internal representations. In addition, the connectivity analyses revealed that the anterior rostromedial PFC, together
with the striatum, thalamus, OFC, PCC, and sensory association
cortices constitutes a functional network that gives sensory information high priority, whereas the rostrolateral PFC, together with regions
in the dorsolateral and ventrolateral prefrontal cortex, as well as the
parietal and cingulate cortex, constitutes a network that supports the
maintenance of internally represented information. Moreover, both
rostral PFC subregions interacted in a task-specific manner with
another key region involved in setting attentional gains, the IFJ,
depending on the current attentional demands.
In summary, the current findings add evidence indicating the
existence of an attentional control system in the rostral PFC which is
involved in attentional weighting processes by constituting functional
networks that give the currently most relevant information highest
priority. This system may also be important for the goal-directed
coordination of external and internal information, as the rostral PFC has
been found to be part of a network that is especially sensitive to sensory
information that is congruent with current goals (Soto et al., 2007). This
is in line with theories assuming that the rostral PFC plays an important
role in the integration of internally and externally oriented cognition
(Burgess et al., 2007a; Ramnani and Owen, 2004) and suggests that the
two adjacent subregions in the rostromedial and rostrolateral PFC are
not only involved in balancing attentional orientation to internal or
external information but also in integrating the information coming
from these different sources. Disturbances in this system might be
important in the context of disorders involving deficits in reality
monitoring and in determining whether information comes from an
internal or external source, like it is the case in schizophrenia. It has
already been reported that schizophrenic patients show deficits in
rostral PFC activation (Vinogradov et al., 2008), and it has been
suggested that this might be related to patients’ deficits in reality
monitoring. This is an important question for future research.
Supplementary materials related to this article can be found online
at doi:10.1016/j.neuroimage.2011.02.056.
References
Burgess, P.W., Scott, S.K., Frith, C.D., 2003. The role of the rostral frontal cortex (area 10)
in prospective memory: a lateral versus medial dissociation. Neuropsychologia 41
(8), 906–918.
Burgess, P.W., Dumontheil, I., Gilbert, S.J., 2007a. The gateway hypothesis of rostral
prefrontal cortex (area 10) function. Trends Cogn. Sci. 11 (7), 290–298.
Burgess, P.W., Gilbert, S.J., Dumontheil, I., 2007b. Function and localization within
rostral prefrontal cortex (area 10). Philos. Trans. R. Soc. B 362 (1481), 887–899.
Christoff, K., Gabrieli, J.D.E., 2000. The frontopolar cortex and human cognition:
evidence for a rostrocaudal hierarchical organization within the human prefrontal
cortex. Psychobiology 28 (2), 168–186.
1675
Cole, M.W., Schneider, W., 2007. The cognitive control network: integrated cortical
regions with dissociable functions. Neuroimage 37 (1), 343–360.
Collette, F., Van der Linden, M., Laureys, S., Arigoni, F., Delfiore, G., Degueldre, C., Luxen,
A., Salmon, E., 2007. Mapping the updating process: common and specific brain
activations across different versions of the running span task. Cortex 43 (1),
146–158.
D'Argembeau, A., Collette, F., Van der Linden, M., Laureys, S., Del Fiore, G., Degueldre, C.,
Luxen, A., Salmon, E., 2005. Self-referential reflective activity and its relationship
with rest: a PET study. Neuroimage 25 (2), 616–624.
Diekhof, E.K., Gruber, O., 2010. When desire collides with reason: functional interactions
between anteroventral prefrontal cortex and nucleus accumbens underlie the human
ability to resist impulsive desires. J. Neurosci. 30 (4), 1488–1493 2010 27.
Diekhof, E.K., Falkai, P., Gruber, O., 2009. Functional interactions guiding adaptive
processing of behavioral significance. Hum. Brain Mapp. 30 (10), 3325–3331.
Dosenbach, N.U.F., Fair, D.A., Cohen, A.L., Schlaggar, B.L., Petersen, S., 2008. A dualnetworks architecture of top–down control. Trends Cogn. Sci. 12 (3), 99–105.
Downar, J., Crawley, A.P., Mikulis, D.J., Davis, K.D., 2000. A multimodal cortical network
for the detection of changes in the sensory environment. Nat. Neurosci. 3 (3),
277–283.
Downar, J., Crawley, A.P., Mikulis, D.J., Davis, K.D., 2001. The effect of task relevance on
the cortical response to changes in visual and auditory stimuli: an event-related
fMRI study. Neuroimage 14 (6), 1256–1267.
Downar, J., Crawley, A.P., Mikulis, D.J., Davis, K.D., 2002. A cortical network sensitive to
stimulus salience in a neutral behavioral context across multiple sensory
modalities. J. Neurophysiol. 87 (1), 615–620.
Dumontheil, I., Gilbert, S.J., Frith, C.D., Burgess, P.W., 2010. Recruitment of lateral rostral
prefrontal cortex in spontaneous and task-related thoughts. Q. J. Exp. Psychol.
(Colchester) 63 (9), 1740–1756.
Frank, M.J., Loughry, B., O'Reilly, R., 2001. Interactions between frontal cortex and basal
ganglia in working memory: a computational model. Cogn. Affect. Behav. Neurosci.
1 (2), 137–160.
Fransson, P., 2006. How default is the default mode of brain function? Further
evidence from intrinsic BOLD signal fluctuations. Neuropsychologia 44 (14),
2836–2845.
Friston, K.J., Buechel, C., Fink, G.R., Morris, J., Rolls, E., Dolan, R.J., 1997. Psychophysiological and modulatory interactions in neuroimaging. Neuroimage 6 (3),
218–229.
Frith, U., Frith, C.D., 2003. Development and neurophysiology of mentalizing. Philos.
Trans. R. Soc. B Biol. Sci. 358 (1431), 459–473.
Gilbert, S.J., Frith, C.D., Burgess, P.W., 2005. Involvement of rostral prefrontal cortex in
selection between stimulus-oriented and stimulus-independent thought. Eur. J.
Neurosci. 21 (5), 1423–1431.
Gilbert, S.J., Simons, J.S., Frith, C.D., Burgess, P.W., 2006a. Performance-related activity in
medial rostral prefrontal cortex (Area 10) during low-demand tasks. J. Exp. Psychol.
Hum. Percept. Perform. 32 (1), 45–58.
Gilbert, S.J., Spengler, S., Simons, J.S., Frith, C.D., Burgess, P.W., 2006b. Differential
functions of lateral and medial rostral prefrontal cortex (area 10) revealed by
brain-behavior associations. Cereb. Cortex 16 (12), 1783–1789.
Gilbert, S.J., Spengler, S., Simons, J.S., Steele, J.D., Lawrie, S.M., Frith, C.D., Burgess, P.W.,
2006c. Functional specialization within rostral prefrontal cortex (Area 10): a metaanalysis. J. Cogn. Neurosci. 18 (6), 932–948.
Gilbert, S.J., Williamson, I.D.M., Dumontheil, I., Simons, J.S., Frith, C.D., Burgess, P.W.,
2007. Distinct regions of medial rostral prefrontal cortex supporting social and
nonsocial functions. Scan 2, 217–226.
Gilbert, S.J., Gonen-Yaacovi, G., Benoit, R.G., Volle, E., Burgess, P.W., 2010. Distinct
functional connectivity associated with lateral versus medial rostral prefrontal
cortex: a meta-analysis. Neuroimage 53 (4), 1359–1367. Epub 2010 Jul 21.
Greicius, M.D., Krasnow, B., Reiss, A.L., Menon, V., 2003. Functional connectivity in the
resting brain: a network analysis of the default mode hypothesis. Proc. Natl Acad.
Sci. USA 100 (1), 253–258.
Giesbrecht, B., Weissman, D.H., Woldorff, M.G., Mangun, G.R., 2006. Pre-target activity
in visual cortex predicts behavioral performance on spatial and feature attention
tasks. Brain Res. 1080, 63–72.
Gruber, O., 2001. Effects of domain-specific interference on brain activation associated with verbal working memory task performance. Cereb. Cortex 11 (11),
1047–1055.
Gruber, O., von Cramon, D.Y., 2001. Domain-specific distribution of working memory
processes along human prefrontal and parietal cortices: a functional magnetic
resonance imaging study. Neurosci. Lett. 297 (1), 29–32.
Gruber, O., von Cramon, D.Y., 2003. The functional neuroanatomy of human working
memory revisited—evidence from 3-T fMRl studies using classical domain-specific
interference tasks. Neuroimage 19 (3), 797–809.
Gruber, O., Diekhof, E.K., Kirchenbauer, L., Goschke, T., 2010. A neural system for
evaluating the behavioural relevance of salient events outside the current focus of
attention. Brain Res. 1351, 212–221.
Gusnard, D.A., Akbudak, E., Shulman, G.L., Raichle, M.E., 2001. Medial prefrontal cortex
and self-referential mental activity: relation to a default mode of brain function.
Proc. Natl Acad. Sci. USA 98 (7), 4259–4264.
Haber, S., McFarland, N.R., 2001. The place of the thalamus in frontal cortical–basal
ganglia circuits. Neuroscientist 7 (4), 315–324.
Hahn, B., Ross, T.J., Stein, E.A., 2006. Neuroanatomical dissociation between bottom–up
and top–down processes of visuospatial selective attention. Neuroimage 32 (2),
842–853.
Hazy, T.E., Frank, M.J., O'Reilly, R.C., 2007. Towards an executive without a homunculus:
computational models of the prefrontal cortex/basal ganglia system. Philos. Trans.
R. Soc. B Biol. Sci. 362 (1485), 1601–1613.
1676
I. Henseler et al. / NeuroImage 56 (2011) 1666–1676
Hopfinger, J.B., Buonocore, M.H., Mangun, G.R., 2000. The neural mechanisms of top–
down attentional control. Nat. Neurosci. 3 (3), 284–291.
Jafri, M.J., Pearlson, G.D., Stevens, M., Calhoun, V.D., 2008. A method for functional
network connectivity among spatially independent resting-state components in
schizophrenia. Neuroimage 39 (4), 1666–1681.
Johnson, S.C., Schmitz, T.W., Kawahara-Baccus, T.N., Rowley, H.A., Alexander, A.L., Lee, J.H.,
Davidson, R.J., 2005. The cerebral response during subjective choice with and without
self-reference. J. Cogn. Neurosci. 17 (12), 1897–1906.
Kastner, S., Pinsk, M.A., De Weerd, P., Desimone, R., Ungerleider, L., 1999. Increased
activity in human visual cortex during directed attention in the absence of visual
stimulation. Neuron 22 (4), 751–761.
Kiehl, K.A., Stevens, M.C., Laurens, K.R., Pearlson, G., Calhoun, V.D., Liddle, P.F., 2005. An
adaptive reflexive processing model of neurocognitive function: supporting
evidence from a large scale (n = 100) MRI study of an auditory oddball task.
Neuroimage 25 (3), 899–915.
Kincade, J.M., Abrams, R.A., Astafiev, S.V., Shulman, G.L., Corbetta, M., 2005. An eventrelated functional magnetic resonance imaging study of voluntary and stimulusdriven orienting of attention. J. Neurosci. 25 (18), 4593–4604.
Knott, V., Millar, A., Fisher, D., 2009. Sensory gating and source analysis of the auditory
P50 in low and high suppressors. Neuroimage 44 (3), 992–1000.
Koechlin, E., Basso, G., Pietrini, P., Panzer, S., Grafman, J., 1999. The role of the anterior
prefrontal cortex in human cognition. Nature 399 (6732), 148–151.
LaBerge, D., 2002. Attentional control: brief and prolonged. Psychol. Res. 66, 220–233.
Leh, S.E., Ptito, A., Chakravarty, M.M., Strafella, A.P., 2007. Fronto–striatal connections in
the human brain: a probabilistic diffusion tractography study. Neurosci. Lett. 419
(2), 113–118.
Leh, S.E., Chakravarty, M.M., Ptito, A., 2008. The connectivity of the human pulvinar:
a diffusion tensor imaging tractography study. Int. J. Biomed. Imaging 2008,
1–5.
Lepsien, J., Nobre, A.C., 2006. Cognitive control of attention in the human brain: insights
from orienting attention to mental representations. Brain Res. 1105, 20–31.
Lepsien, J., Nobre, A.C., 2007. Attentional modulation of object representations in
working memory. Cereb. Cortex 17 (9), 2072–2083.
Li, Z.H., Sun, X.W., Wang, Z.X., Zhang, X.C., Zhang, D.R., He, S., Hu, X.P., 2004. Behavioral
and functional MRI study of attention shift in human verbal working memory.
Neuroimage 21 (1), 181–191.
Mantini, D., Perrucci, M.G., Del Gratta, C., Romani, G.L., Corbetta, M., 2007. Electrophysiological signatures of resting state networks in the human brain. Proc. Natl
Acad. Sci. USA 104 (32), 13170–13175.
Mason, M.F., Norton, M.I., Van Horn, J.D., Wegner, D.M., Grafton, S.T., Macrae, C.N., 2007.
Wandering minds: the default network and stimulus-independent thought.
Science 315 (5810), 393–395.
Mcnab, F., Klingberg, T., 2008. Prefrontal cortex and basal ganglia control access to
working memory. Nat. Neurosci. 11 (1), 103–107.
Mesulam, M.M., Nobre, A.C., Kim, Y.H., Parrish, T.B., Gitelman, D.R., 2001. Heterogeneity
of cingulate contributions to spatial attention. Neuroimage 13 (6), 1065–1072.
Nobre, A.C., Coull, J.T., Maquet, P., Frith, C.D., Vandenberghe, R., Mesulam, M.M., 2004.
Orienting attention to locations in perceptual versus mental representations.
J. Cogn. Neurosci. 16 (3), 363–373.
Ongur, D., Ferry, A.T., Price, J.L., 2003. Architectonic subdivision of the human orbital
and medial prefrontal cortex. J. Comp. Neurol. 460 (3), 425–449.
O'Reilly, R.C., Frank, M.J., 2006. Making working memory work: a computational model
of learning in the prefrontal cortex and basal ganglia. Neural Comput. 18 (2),
283–328.
Raichle, M.E., MacLeod, A.M., Snyder, A.Z., Powers, W.J., Gusnard, D.A., Shulman, G.L.,
2001. A default mode of brain function. Proc. Natl Acad. Sci. USA 98 (2), 676–682.
Ramnani, N., Owen, A.M., 2004. Anterior prefrontal cortex: insights into function from
anatomy and neuroimaging. Nat. Rev. Neurosci. 5 (3), 184–194.
Seeley, W.W., Menon, V., Schatzberg, A.F., Keller, J., Glover, G.H., Kenna, H., Reiss, A.L.,
Greicius, M.D., 2007. Dissociable intrinsic connectivity networks for salience
processing and executive control. J. Neurosci. 27 (9), 2349–2356.
Shulman, G.L., McAvoy, M.P., Cowan, M.C., Astafiev, S.V., Tansy, A.P., G, d'Avossa,
Corbetta, M., 2003. Quantitative analysis of attention and detection signals during
visual search. J. Neurophysiol. 90 (5), 3384–3397.
Simons, J.S., Henson, R.N.A., Gilbert, S.J., et al., 2008. Separable forms of reality monitoring
supported by anterior prefrontal cortex. J. Cog. Neurosci. 20 (3), 447–457.
Small, D.M., Gitelman, D.R., Gregory, M.D., Nobre, A.C., Parrish, T.B., Mesulam, M.M.,
2003. The posterior cingulate and medial prefrontal cortex mediate the
anticipatory allocation of spatial attention. Neuroimage 18 (3), 633–641.
Smith, R., Keramatian, K., Christoff, K., 2007. Localizing the rostrolateral prefrontal
cortex at the individual level. Neuroimage 36, 1387–1396.
Soon, C.S., Brass, M., Heinze, H.J., Haynes, J.D., 2008. Unconscious determinants of free
decisions in the human brain. Nat. Neurosci. 11 (5), 543–545.
Soto, D., Humphreys, G.W., Rotshtein, P., 2007. Dissociating the neural mechanisms of
memory-based guidance of visual selection. Proc. Natl Acad. Sci. USA 104 (43),
17186–17191.
Sridharan, D., Levitin, D.J., Chafe, C.H., Berger, J., Menon, V., 2007. Neural dynamics of
event segmentation in music: converging evidence for dissociable ventral and
dorsal networks. Neuron 55 (3), 521–532.
Summerfield, C., Egner, T., Greene, M., et al., 2006. Predictive codes for forthcoming
perception in the frontal cortex. Science 314 (5803), 1311–1314.
Thottakara, P., Lazar, M., Johnson, S.C., Alexander, A.L., 2006. Application of Brodmann's
area templates for ROI selection in white matter tractography studies. Neuroimage
29 (3), 868–878.
Vinogradov, S., Luks, T.L., Schulman, B.J., Simpson, G.V., 2008. Deficit in a neural
correlate of reality monitoring in schizophrenia patients. Cereb. Cortex 18 (11),
2532–2539.
Weissman, D.H., Roberts, K.C., Visscher, K.M., Woldorff, M.G., 2006. The neural bases of
momentary lapses in attention. Nat. Neurosci. 9 (7), 971–978.
Williams, L.M., Felmingham, K., Kemp, A.H., Rennie, C., Brown, K.J., Bryant, R.A., Gordon,
E., 2007. Mapping frontal-limbic correlates of orienting to change detection.
NeuroReport 18 (3), 197–202.
173
Psychologica Belgica
2012, 52/2-3, 173-204
PROSPECTIVE MEMORY: THE FUTURE FOR FUTURE
INTENTIONS
Gil Gonen-Yaacovi, & Paul W. Burgess*
University College London, UK
Prospective memory is the ability to remember to execute future intentions and
thoughts. It is probably the newest established field of memory research. We
provide a selective review of work conducted in the last two decades with
respect to the following issues: (1) the different types and characteristics of
prospective tasks, (2) the theoretical models of the cognitive processes supporting prospective memory, (3) prospective memory performance in younger and
older adults and (4) the findings from neuropsychological and neuroimaging
studies. The findings indicate an extraordinarily fast progress in our understanding of the behaviour and the brain regions that are involved in this important ability, and suggest at least two possible emerging areas of enquiry for
future research: a link with the closely related field of prospection (i.e., thinking about the future), and “expectation prospective memory” (triggering of
behaviour in the absence of awareness depending on contingencies learnt from
the environment).
Prospective memory (PM) is commonly defined as the set of abilities that are
used when remembering to perform an intended action, or thought, at some
future point (Brandimonte, Einstein, & McDaniel, 1996). This type of memory is in constant use in everyday life in order to fulfil intentions ranging from
the simple, such as remembering to take out the garbage when leaving home,
to the more complex, such as remembering to organise a surprise party for a
friend’s birthday. This ability is critical to competent human functioning, so
much so that previous studies have suggested that PM problems are the most
frequent memory failures in everyday life (Kliegel & Martin, 2003). Relatively little experimental and theoretical investigation was conducted on this
topic until the last 15 years. However, since then there has been a remarkable
increase in number of research studies that have considered PM.
The nature of typical prospective memory paradigms
The majority of studies of the psychology of memory have focused on the
phenomena related to learning and the reproduction of information or content,
broadly referred to (mainly by prospective memory theorists) as retrospective
*
Gil Gonen-Yaacovi, PhD and Paul W. Burgess, Professor, Institute of Cognitive Neuroscience, University College London, UK.
Correspondence concerning this article should be addressed to Paul W. Burgess, UCL Institute of Cognitive Neuroscience, 17 Queen Square, London UK, WC1N 3AR. E-mail: [email protected]
174
PROSPECTIVE MEMORY: THE FUTURE FOR FUTURE INTENTIONS
memory (RM; Baddeley & Wilkins, 1984). In a typical retrospective memory
experiment, the participant is asked to learn and remember certain material,
such as a list of words. In the next stage either the experimenter or the presentation of an instruction, serves as an external cue, which encourages the
participant to remember the material at the appropriate time. Since this type
of remembering is always triggered by an external cue, it has been termed
“cued remembering” (Levy & Loftus, 1984; Wilkins & Baddeley, 1978). By
comparison, in a typical PM paradigm one is required to remember to perform
intentions to be carried in the future without any obvious requirement from
the environment regarding the appropriate execution time of these intentions.
For this reason, remembering intentions is sometimes called ‘uncued’ (Levy
& Loftus, 1984) or ‘self cued’ (Wilkins & Baddeley, 1978) remembering.
Different types of PM intentions, which vary along many dimensions,
have been studied over the past twenty years (Kvavilashvili & Ellis, 1996).
However, the most cited distinction between them contrasts event-based with
time-based PM (e.g., Einstein & McDaniel, 1990; Park, Hertzog, Kidder,
Morrell, & Mayhorn, 1997), both of which have been well studied. In eventbased PM the environment can serve as an external cue to prompt the intention that was formed. For example, the sight of a convenience store might
bring to mind the intention to replenish the milk. In time-based PM, an intention is formed to be executed either at a predetermined time, such as calling
the dentist at 5pm, or after a specific period of time has elapsed, such as taking
the cookies out of the oven before they get overcooked. One way to view the
distinction between these two types of tasks is that time-based PM is more
self-initiated whereas event-based PM is more environmentally cued (Block
& Zakay, 2006). However, others claim that this distinction is not useful since
in some naturalistic time-based situations one has access to external chronometers, which may serve as event-based cues (Graf & Grondin, 2006).
Most published work has concerned itself with the cognitive processes associated with storing and realising event-based intentions (Cook, Marsh, &
Hicks, 2005). As a result, the theories concerning event-based memory are
more developed, as are the various laboratory techniques used in its study.
Less studied forms of PM (in addition to time-based PM) are habitual PM
(Meacham & Leiman, 1975), and activity-based PM (Kvavilashvili & Ellis,
1996). Habitual PM tasks are those where the action is performed repeatedly
and in a routine manner. For example, remembering to take vitamins every
day at 8pm. Activity-based PM, on the other hand, requires the intention to be
retrieved and executed upon completing some other task. For example,
remembering to call a friend after dinner.
For experimental purposes the characteristics of tasks involving PM have
been simplified and are summarised below (adapted from Burgess, Scott, &
Frith, 2003).
GIL GONEN-YAACOVI, & PAUL W. BURGESS
175
1. There is an intention, or multiple intentions (Kliegel, McDaniel, &
Einstein, 2000), upon which to act.
2. The intended act cannot be performed immediately after the intention has been formed.
3. The intention is to be performed in a particular circumstance, called
the “retrieval context” (Ellis, Kvavilashvili, & Milne, 1999). This
can be marked by an external cue, in event-based paradigms, or a
particular time, or certain duration, in time-based paradigms.
4. The delay period between creating the intention and the appropriate
time to act (i.e., the “retention interval”) is filled with an activity
called the ongoing activity (Ellis et al., 1999).
5. Performance of the ongoing task prevents continuous, conscious
rehearsal of the intention over the entire delay period. This is typically because the ongoing activity places a heavy demand on competing cognitive resources or the delay is too long.
6. The PM cue does not interfere with, or directly interrupt, performance of the ongoing task. Intention enactment is therefore self-initiated (Graf & Uttl, 2001) and, thus participants are required to recognise the PM cues or retrieval context themselves.
7. In most situations involving PM no immediate feedback is given in
response to the participants’ errors or other aspect of performance.
In 1990, Einstein and McDaniel developed a typical experimental paradigm
for controlled laboratory-based studies on PM. In order to parallel a ‘real life’
situation as far as possible, participants are first engaged in an ongoing activity (e.g., indicate which of the 2 numbers presented on the screen is numerically bigger). In the second stage, while they are fully engaged with the ongoing activity, the PM instructions are introduced and participants are asked to
try to remember to perform an unrelated action at some pre-specified point in
the experiment (e.g., respond differently when both numbers are even). This
paradigm allows one to measure performance by the proportion of trials in
which participants correctly remembered to execute the PM task and the
ongoing activity. Many variations of this paradigm were carried out in order
to look at the different cognitive processes that form the basis of PM, including, for example, the length of the retention interval, the importance of the PM
task, and the cognitive load of the ongoing activity.
Cognitive processes underlying prospective memory retrieval
In the last 15 years several theories have been proposed to account for the
cognitive processes that support event-based PM retrieval in an attempt to
discover how the cognitive system enables one to execute intended actions at
the appropriate time. The main approaches are as follows:
176
PROSPECTIVE MEMORY: THE FUTURE FOR FUTURE INTENTIONS
Spontaneous retrieval theory
When Einstein and McDaniel (1990) started using the experimental design
they had developed, they noticed that many participants were reporting that
the PM intention “popped” into their mind while they were performing the
ongoing task. In an attempt to explain how the environment can trigger the
retrieval of associated memories, McDaniel, Robinson-Riegler, and Einstein
(1998) described an ‘automatic-associative’ memory system. Their mechanism was directly linked to Moscovitch’s (1994) automatic-associative subsystem mechanism. During the formation of an intention, an associative link
is formed between the intention and the associated action related to this intention. This cue-action pairing exists with a certain level of activation. Unless
rehearsal, or some other activity aimed to raise the activation level, occurs,
the level of activation will gradually decay. However, if the cue produces
enough interaction with the memory trace, then the system will deliver the
information associated with the cue to a person’s awareness. In other words,
the aim of this mechanism is to mediate PM retrieval if the cue interacts sufficiently with the representation of the associated action in such a way that the
associated action is transferred to awareness (McDaniel et al., 1998). Illustrating this model in an everyday life situation, one might consider when someone forms the intention of giving their flatmate a message. When forming the
intention, an initial association is made between the flatmate, who serve as the
PM cue, and the message, which is the intended action that is linked to the PM
cue. If the association between the flatmate and the message is strong enough,
when encountering the flatmate the cognitive system will reflexively deliver
the intended message into the person’s awareness.
To test this idea, McDaniel, Guynn, Einstein, and Breneiser (2004)
manipulated the strength of the association between PM cue words. Some of
the words were strongly associated, such as spaghetti/sauce, while others
were weakly associated, such as spaghetti/church. They found that PM performance was better when the cue was strongly associated with the intentions
(accuracy of 85%) compared with when the cue-response association was
weak (accuracy of 56%). Similar findings were reported when the semantic
context of the PM cue changed from encoding to retrieval, e.g., the PM cue
word ‘bat’ was encoded in a specific context (‘a baseball player will use a bat
several times in a game’) but retrieved in either the same (‘a hard swing of the
bat could lead to a home run’) or different (‘a bat is commonly classified as a
bird because it flies’) contexts (McDaniel et al., 1998, experiment 1). In addition, superior PM performance was found when the ongoing task involved
deep semantic processing (e.g., generating adjectives) compared with shallower processing (e.g., generating rhymes, McDaniel et al., 1998, experiment
3). These findings suggest that under certain encoding conditions one can
increase the likelihood of forming a strong cue-action association that, in turn,
GIL GONEN-YAACOVI, & PAUL W. BURGESS
177
will increase the chances of the cue to interact with the memory trace and the
intention to be retrieved at the appropriate time. A last set of findings comes
from self reports of participants while performing the PM task (e.g., Hicks,
Marsh, & Russell, 2000). In one study, participants were tested in a PM
experiment and were asked to indicate at various time points during the
experiment what they were thinking about. Most often (around 69% of the
time) participants reported thinking about the ongoing task, and less than 5%
of the time reported thinking about the PM task (Reese & Cherry, 2002). This
suggests that after the PM intention has been formed and the link between the
PM cue and the intended action was made, participants were relying on
appearance of the PM cue to activate the cue-action association in order to
trigger the execution of the PM intention.
Preparatory attentional and memory processes theory
An alternative model was suggested by Smith (2003; Smith & Bayen, 2004)
who proposed that PM retrieval occurs through the capacity-demanding
attentional process of monitoring the environment. According to the preparatory attentional and memory processes (PAM) theory (Smith, 2003), successful event-based PM requires capacity-consuming preparatory processes. The
preparatory processes are engaged in maintaining a state of readiness to perform a task, which involves some degree of monitoring of the environment
for the occurrence of PM target events. More specifically, the preparatory
processes are not automatic and therefore require the allocation of some of the
limited cognitive resources away from the ongoing activity and towards preparation for the PM task. In addition to the preparatory processes, according to
the PAM theory, RM processes are also involved in PM performance. RM
processes are needed for discrimination between PM target and non target
events, as well as for recollection of the intended action, processes that are
likely to absorb attentional resources when the target is present. This suggestion follows previous findings showing that increasing the cognitive load of
the ongoing activity influences the performance on PM tasks (e.g., Kvavilashvili, 1987). However, the most striking evidence supporting the attentional
monitoring theory comes from studies comparing performance in an ongoing
activity before any PM involvement with performance in the same ongoing
activity after adding the PM requirement. According to this theory, preparatory attentional processes include nonautomatic monitoring of the environment for the PM cue, therefore, when a PM task is embedded in an ongoing
task, a reduction in the resources available for the ongoing task is expected,
even when the PM cue is not present. To test this idea, Smith (2003) asked
participants to perform a lexical decision task as the ongoing activity. In this
task a string of letters was presented and participants were asked to indicate
178
PROSPECTIVE MEMORY: THE FUTURE FOR FUTURE INTENTIONS
whether or not the string represents a word. In the second part, the PM instructions were added and, in addition to performing the ongoing activity task, participants were instructed to respond differently to several PM cues. It was
found that speed in making the lexical decision in the ongoing activity trials
was significantly slower in the second part, when the PM task was embedded,
compared with similar trials in the first part, before the PM task was added.
This decrement in performance of the ongoing task whilst maintaining an
intention has variously been termed ‘attentional cost’, ‘task interference’ or
(our favoured term) ‘intention cost’, and was to our knowledge first demonstrated by Burgess, Quayle, and Frith, 2001. Other studies using a variety of
ongoing tasks and PM cues on different populations have yielded similar
findings, providing further support for the role of preparatory attention in PM
(e.g., Cook, Marsh, Clark-Foos, & Meeks, 2007; Einstein, McDaniel, Thomas, Mayfield, Shank, Morrisette et al., 2005; Gilbert, Gollwitzer, Cohen,
Burgess, & Oettingen, 2009; Guynn, 2003; Loft & Yeo, 2007; Marsh, Hicks,
& Cook, 2005; Marsh, Hicks, & Cook, 2006; Marsh, Hicks, Cook, Hansen,
& Pallos, 2003; McCauley & Levine, 2004; Smith, Bayen, & Martin, 2010;
Smith, Hunt, McVay, & McConnell, 2007; West, Bowry, & Krompinger,
2006; see Smith, 2008, p. 42-46 for review). Furthermore, the intention cost
upon the ongoing activity has been found to positively correlate with PM performance (Smith, 2003; Smith & Bayen, 2004), and has also been found on
trials preceding PM hits compared with trials preceding PM misses (West,
Krompinger, & Bowry, 2005).
Critics of this theory claim that constant use of attentional resources
directed towards the PM task would be too costly to allow competent functioning in everyday life activities (McDaniel & Einstein, 2007). Accordingly,
they argue that this theory might relate to PM in specific situations where the
predictability of the appearance of the PM cue is low (Marsh, Hicks et al.,
2006) or where retention intervals are relatively short (Einstein et al., 2005).
The multiprocess theory
The contradictory findings supporting both attentional monitoring and spontaneous retrieval processes led McDaniel and Einstein (2000) to change their
initial single-process model. According to their updated multiprocess model,
PM retrieval can be supported by both attention-demanding monitoring and
also by more automatic processes. Whether one will rely on a monitoring or
spontaneous retrieval process depends on several factors such as the characteristics of the PM task, the ongoing task, and also the individual. In other
words, they argue that the system that accomplishes PM retrieval is flexible
and dependent on several mechanisms. The task conditions that are likely to
favour each process are detailed below and summarised in Table 1 (p. 182).
GIL GONEN-YAACOVI, & PAUL W. BURGESS
179
1. The extent of attention directed from the ongoing activity to the PM cues
McDaniel and Einstein (2007) argue that spontaneous retrieval is more likely
to occur when there is a large overlap between the information that is
extracted from the PM cues at retrieval and the information that is considered
about this cue during the encoding. This idea was taken from the transferappropriate processing explanation of RM effects (e.g., Morris, Bransford, &
Franks, 1977) suggesting that memory performance is determined by the relationship between how information is initially encoded and how it is later
retrieved. In 2005, Einstein et al. (experiment 2) asked college students to
complete a category verification task and also to form an intention to make a
PM response each time they encountered a specific word (e.g., the word “dormitory”). In another condition, they asked participants to make a PM response
each time they encountered a word containing a specific syllable (e.g., the syllable “tor”) while performing the category verification task. Accuracy for cue
detection was dramatically different with greater accuracy in the condition
where a specific word was used as the PM cue (93%) compared to the condition where a syllable was used as the PM cue (61%). In addition, task interference to the ongoing activity was found when a syllable was used as the PM
cues but not when a specific word was used as the PM cues. The findings led
them to distinguish between focal cues and nonfocal cues. Focal cues were
defined as “PM cues that overlap with the information constellation relevant
to performing the ongoing task” and nonfocal cues as “cues that are present
in the environment but not part of the information being considered by the
person” (McDaniel, Einstein, & Rendell 2008, pp. 141-160). Further support
for the suggestion that the “focality” of the ongoing activity can influence the
retrieval processes in PM tasks has been given by subsequent studies
(Brewer, Knight, Marsh, & Unsworth, 2010; Scullin, McDaniel, & Einstein,
2010; Scullin, McDaniel, Shelton, & Lee, 2010). Importantly, a potential
problem has been highlighted in applying the distinction between focal versus
nonfocal a priori, which results in confusion in the classification of some task
conditions (e.g., Smith, 2010).
2. Cognitive load of the ongoing activity
According to the multiprocess theory (McDaniel & Einstein, 2000), the
demand on resources required by the ongoing activity is another essential factor that influences the dominance of either monitoring or spontaneous
retrieval processes. More specifically, it states that a decrease in resources
available for monitoring should interfere with PM performance mainly on
tasks involving nonfocal PM cues. For example, Marsh, Hancock, and Hicks
(2002) manipulated the demand of the ongoing activity task and found that
participants who were asked to switch randomly between two ongoing tasks
180
PROSPECTIVE MEMORY: THE FUTURE FOR FUTURE INTENTIONS
showed poorer PM performance when the PM cue was nonfocal, than those
performing a single task. Similar results were found when using PM cues that
were focal to the ongoing activity task (Einstein, Smith, McDaniel, & Shaw,
1997).
3. Saliency of the PM cue
Distinctive PM cues should produce a higher level of PM performance compared with nondistinctive cues (McDaniel & Einstein, 2000). Support for this
is found when using uppercase letters as PM cues, as opposed to lower case
letters in the ongoing activity task (Brandimonte & Passolunghi, 1994, experiment 2) and when using unfamiliar distinct cue words (e.g., the word “bole”)
than familiar non distinct cue words (e.g., the word “belt”; Einstein &
McDaniel, 1990, experiment 2; McDaniel & Einstein, 1993). However,
Smith et al. (2007, experiments 1 and 2) showed that using perceptually or
semantically salient PM cues resulted in task interference to the ongoing
activity, contradicting the predictions of the multiprocess account.
4. Association between the PM cue and the intended action
A further factor that affects cognitive processing during retrieval of PM is the
strength of the association between the cue and the associated action. More
specifically, spontaneous retrieval is likely to be dominant when the cue and
the action are highly associated. However, when the relationship between the
cue and the action is not very strong, processing of the cue is less likely to
result in reflexive retrieval of the intended action and therefore monitoring of
the environment for the cue is more likely to be dominant (McDaniel et al.,
2004). Loft and Yeo (2007) looked at the relationship between the ongoing
task performance and PM performance under conditions of low and high cueresponse association and found response cost on ongoing trials preceding PM
hits compared with PM misses under the low association condition but not
under the high association condition. Other studies showed improved performance when manipulating pre-exposure to PM cues between participants
(Guynn & McDaniel, 2007) or within participants (Mantyla, 1993), suggesting that pre-exposure to the PM cues benefited from high cue-action association promoting reflexive retrieval processes.
5. Importance of the prospective memory intention
The multiprocess account states that PM intentions of high importance, especially nonfocal ones, will produce better PM performance (McDaniel & Einstein, 2000). This suggestion follows previous findings showing higher PM
performance under conditions in which successful performance of the PM
GIL GONEN-YAACOVI, & PAUL W. BURGESS
181
task has been emphasised (e.g., Ellis, 1998; Kvavilashvili, 1987, experiment
2; Meacham & Singer, 1977). Kliegel, Martin, McDaniel, and Einstein (2001)
extended this prediction, claiming that task importance is relevant only in
event-based tasks and not in time-based ones. However in a later study
Kliegel, Martin, McDaniel, and Einstein (2004) demonstrated that task
importance can impact performance on some event-based PM tasks, especially when the task required strategic allocation of attentional monitoring
resources (see Einstein et al., 2005, experiment 1, for similar results).
6. Length of prospective memory retention interval
In the retrospective memory literature, longer retention intervals quite predictably lead to a higher forgetting level (Linton, 1978). For PM, however,
the dynamics determining forgetting seem less straightforward. Loftus (1971)
reported poorer performance after longer, compared with shorter, delays.
Similarly, Meacham and Leiman (1982) reported greater decline in performance after a 5-to 8-day delay compared with a 1-to 4-day delay, in the absence
of external memory aids. Finally, Brandimonte and Passolunghi (1994,
experiment 1) showed a decreased in PM performance when the retention
interval increased from 0 (i.e., no delay condition) to 3 minutes and proposed
that forgetting in PM task occurs primarily within the first 3 minutes after
encoding. According to the multiprocess account, when the PM cues are nonfocal, a decline in PM performance is expected when the retention intervals
are increased (McDaniel & Einstein, 2007). The results of some studies supported this prediction (e.g., Einstein et al., 2005, experiment 2). However,
other studies did not find any difference between short and long retention
intervals (e.g., Einstein, Holland, McDaniel, & Guynn, 1992; Guynn,
McDaniel, & Einstein, 1998), or found the opposite pattern of results such
that a longer retention interval produces better PM performance (Hicks et al.,
2000, experiments 1A, 1B and 3).
7. Planning
Burgess and colleagues (e.g., Burgess, Veitch, Costello, & Shallice, 2000; see
Burgess et al., 2008 for review) have demonstrated that what one does during
encoding, or planning, can affect the performance of retrieval of PM. In other
words, planning during encoding has an important consequence for the successful retrieval of PM intentions. The multiprocess theory predicts that good
planning at encoding will prompt spontaneous retrieval processes during PM
performance (McDaniel & Einstein, 2000). In one form of planning, the
instructions provide specific information about the context in which the PM
cues will appear (Marsh, Hicks et al., 2006). A different aspect of planning
was tested by Kliegel et al. (2000), who asked young and old participants to
182
PROSPECTIVE MEMORY: THE FUTURE FOR FUTURE INTENTIONS
remember to perform a single PM task while engaged in a range of processes
that included executing a series of multiple intentions (Six Element Test,
SET; Burgess, Alderman, Emslie, Evans, Wilson, & Shallice, 1996; Shallice
& Burgess, 1991). Even though participants were specifically asked to plan
aloud how they would perform the task, only 54.1% of the participants
remembered to execute the PM task on time and only 50% of the steps indicated in the plans were subsequently followed. This suggest that despite having a formulated plan concerning the different components involved in the
PM intention, execution of the intention did not necessary followed the
intended plan.
Table 1
A summary of the task conditions which according to the multiprocess theory
(McDaniel & Einstein, 2007) favour spontaneous retrieval or monitoring processes.
Factors
Task conditions related
to the ongoing activity
Task conditions related
to the PM cue
Others
Task conditions
favouring spontaneous
retrieval approach
Task conditions
favouring monitoring
approach
The extent of attention
directed from the ongoing activity to the PM
cues
Focal cues
Nonfocal cues
The cognitive load of the
ongoing activity
Lower cognitive load of
the ongoing activity task
Higher cognitive load of
the ongoing activity task
The salient of the PM
cue
Distinctive cues
Non-distinctive cues
The association between
the PM cue and the
intended action
Strong cue-action associ- Weak cue-action associaation
tion
Importance of the PM
task
Low importance of the
PM task
High importance of the
PM task
Length of PM retention
interval
Long retrieval intervals
Short retrieval intervals
Planning
Extensive planning
Poor planning
Prospective memory and aging
Craik (1986) suggested that performance in memory tasks in general is influenced by an interaction between external factors, such as environmental support and the type of operation required, such as self-initiated activity. Specifically, Craik hypothesised that age-related differences should increase with
the amount of self-initiated activity necessary to accomplish a memory task
and should decrease with the amount of environmental support provided. In
Craik’s view, PM is characterised by the greatest need for self-initiated activity and the lowest degree of environmental support when compared with RM
tasks such as free recall or recognition. Thus, larger age-related impairments
are expected in PM than in RM. However, findings from extensive work that
GIL GONEN-YAACOVI, & PAUL W. BURGESS
183
was done on how age effects PM within the older population indicate that the
picture is more complex than one might think at first (see Henry, MacLeod,
Phillips, & Crawford, 2004, for a meta-analytic review).
Age-related effects were initially investigated in laboratory studies that
used time- and event-based PM tasks, (e.g., Einstein, McDaniel, Richardson,
Guynn, & Cunfer, 1995), where no age-related effect was found in the eventbased task; however, older participants performed significantly worse in the
time-based task, a finding which was in accordance with Craik’s prediction.
Subsequent studies supported this finding (e.g., Cherry & LeCompte, 1999;
Cherry, Martin, Simmons-D’Gerolamo, Pinkston, Griffing, & Gouvier, 2001;
Einstein & McDaniel, 1990; Marsh, Hicks, Cook, & Mayhorn, 2007; Reese
& Cherry; 2002). A good example is that of d’Ydewalle, Bouckaert, and
Brunfaut (2001), who tested 48 younger participants (aged 18-25 yrs) and 48
older participants (aged 60-86 yrs). The ongoing task was an arithmetic test,
which aimed to use more executive resources with increasing complexity of
the arithmetic operation. They found that time-based prospective memory
among older adults was much poorer when the complexity of the ongoing
task was increased. An age-related impairment was also obtained when the
pacing of the event-based prospective memory task was high, which they
interpret as being due to general slowing due to age.
However, some studies have reported age-related effects in event-based
PM tasks (e.g., Maylor, 1993; Maylor, 1996; Maylor, 1998; Maylor, Smith,
Della Sala, & Logie, 2002; Park et al., 1997; Smith & Bayen, 2006; West &
Craik, 1999; West & Craik, 2001; Zimmerman & Meier, 2006), so age effects
may not be restricted to time-based PM. One potential explanation for these
differences is related to the design of these experiments. An analysis of the
studies that failed to find an age-related effect shows that the majority of
researchers adjusted, that is, reduced, the difficulty of the ongoing task for
older participants (Kvavilashvili, Kornbrot, Mash, Cockburn, & Milne,
2009).
Another controversial aspect is related to the environmental context of
this experiment. Younger adults tend to outperform older adults in laboratorybased PM tasks (e.g., d’Ydewalle, Luwel, & Brunfaut, 1999; Maylor, 1993;
Maylor, 1996; Rendell & Craik, 2000; Vogels, Dekker, Brouwer, & de Jong,
2002). However, when using real-life conditions in naturalistic settings, a different pattern emerges. Some studies did not find any difference between
young and old adults (West, 1988) while others showed that older adults outperform younger adults in naturalistic tasks (e.g., Bailey, Henry, Rendell,
Phillips, & Kliegel, 2010; Devolder, Brigham, & Pressley, 1990; Moscovitch,
1982; Rendell & Thomson, 1993; Rendell & Thomson, 1999). Together, the
discrepancy in these findings has been referred to as the age PM paradox
(Rendell & Craik, 2000), remaining a puzzle for applied developmental
184
PROSPECTIVE MEMORY: THE FUTURE FOR FUTURE INTENTIONS
research (Rendell, McDaniel, Forbes, & Einstein, 2007). Trying to resolve
these contradictory findings, it has been argued that young and old adults may
differ in their motivation to complete PM tasks successfully outside the laboratory (Patton & Meit, 1993; Rendell & Craik, 2000). A recent support for this
was given when incentives were found to affect younger but not older adult
participants’ PM performance (Aberle, Rendell, Rose, McDaniel, & Kliegel,
2010, experiment 2), suggesting that young adults might not be sufficiently
motivated in naturalistic settings, but when highly motivated, younger but not
older adults outperform their normally motivated counterparts.
The cognitive neuroscience of prospective memory
Neuropsychological studies
Extensive work from the last decade has targeted possible impairments in
event- and time-based PM functioning across a range of different neuropsychological populations. Impairments have been found when, for example,
testing patients with Parkinson’s disease (Costa, Peppe, Caltagirone, & Carlesimo, 2008; Katai, Maruyama, Hashimoto, & Ikeda, 2003; Kliegel, Phillips,
Lemke, & Kopp, 2005; although see Altgassen, Zöllig, Kopp, Mackinlay, &
Kliegel, 2007 for different findings), high-functioning children and adolescents with ASD (Jones, Happé, Pickles, Marsden, Tregay, Baird et al., 2011;
Rajendran, Law, Logie, van der Meulen, Fraser, & Corley, 2010; Zinke, Altgassen, Mackinlay, Rizzo, Drechsler, & Kliegel, 2010; although see Brandimonte, Filippello, Coluccia, Altgassen, & Kliegel, 2011 for different results),
patients with bipolar disorder (Lee, Xiang, Man, Au, Shum, Tang et al.,
2010), patients with obsessive-compulsive disorder (Racsmany, Demeter,
Csigo, Harsanyi, & Nemeth, 2011), and patients with schizophrenia (Altgassen, Kliegel, Rendell, Henry, & Zöllig, 2008; Henry, Rendell, Kliegel, & Altgassen, 2007; Kondel, 2002; Kumar, Nizamie, & Jahan, 2005).
Several studies have shown impaired event- and time-based PM performance in adults with traumatic brain injury (TBI) (Carlesimo, Casadio, & Caltagirone, 2004; Fortin, Godbout, & Braun, 2002; Groot, Wilson, Evans, &
Watson, 2002; Kinsella, Murtagh, Landry, Homfray, Hammond, O’Beirne et
al., 1996; Kliegel, Eschen, & Thöne-Otto, 2004; Knight, Harnett, & Titov,
2005; Knight, Titov, & Crawford, 2006; Mathias & Mansfield, 2005; Potvin,
Rouleau, Audy, Charbonneau, & Giguère, 2011; Roche, Fleming, & Shum,
2002; Shum, Valentine, & Cutmore, 1999; Umeda, Kurosaki, Terasawa,
Kato, & Miyahara, 2011; for review see Shum, Levin, & Chan, 2011). PM
impairments have also been found in children with TBI (e.g., McCauley &
Levin, 2004; McCauley, Pedroza, Chapman, Cook, Hotz, Vásquez et al.,
2010b; McCauley, Pedroza, Chapman, Cook, Vásquez, & Levin, 2011;
GIL GONEN-YAACOVI, & PAUL W. BURGESS
185
McCauley, Wilde, Merkley, Schnelle, Bigler, Hunter et al., 2010a; Ward,
Shum, McKinlay, Baker, & Wallace, 2007). This is commonly attributed to
the fact that the retrieval of PM intentions appears to be subserved by prefrontal and temporal regions, brain structures which are particularly vulnerable to
a TBI. Some researchers have looked at ways to improve PM performance
and found that reminders (McCauley & Levin, 2004), monetary rewards
(McCauley, McDaniel, Pedroza, Chapman, & Levin, 2009) and compensatory training (Shum, Fleming, Gill, Gullo, & Strong, 2011) improve performance in event-based PM tasks in children with both mild and severe TBI.
Other studies have examined patients with other form of neurological
problem, e.g., stroke patients (Brooks, Ross, Potter, Jayawardena, & Morling,
2004), and people with frontal lesions from a variety of causes (e.g., Cockburn, 1995). In general, they tend to demonstrate impaired performances on
both time- and event-based PM tasks compared with the matched control
group. However there are more specific findings in patients with particularly
circumscribed lesions. Volle, Gonen-Yaacovi, de Lacy Costello, Gilbert, and
Burgess (2011) compared the performance of 45 patients with focal brain
lesions with 107 control participants in event- and time-based PM tasks,
accompanied by a series of secondary tasks that examined the basic aspects
of attention and speed, response inhibition, problems remembering multiple
instructions, and task switching. They found that lesions in the right polar prefrontal region, approximating Brodmann area (BA) 10, were specifically
associated with a deficit in the time-based PM task. This could not be attributed to impairments in performance of the secondary tasks, and therefore was
associated solely with PM performance. In addition, the fact that the impairment was seen only in the time-based task suggests that time- and event-based
PM might be supported, at least in part, by distinct brain regions.
Neuropsychological investigations have suggested that other brain
regions also support PM performance. For instance, the involvement of temporal lobe structures in PM was examined when 13 patients with lesions in
the left temporal lobe plus a matched control group were tested on time-based
PM tasks (Palmer & McDonald, 2000). Significant impairments were found
in the patients group compared with the controls participants in all of the
time-based tasks (e.g., “every 15 minutes tell the experimenter what you are
working on”, “at a pre-specified time tell the experimenter that the testing
should almost be finished”).
Event-related brain potentials
There are few studies that have explored the neural correlates of processes
associated with encoding of PM. In three studies, age-related differences
were explored using a similar paradigm in which the encoding of the PM
186
PROSPECTIVE MEMORY: THE FUTURE FOR FUTURE INTENTIONS
intentions was embedded in a continuous ongoing activity (West, Herndon,
& Covell, 2003; West & Ross-Munroe, 2002; Zöllig, Martin, & Kliegel,
2010) and in one study a paradigm was used in which individuals encoded
short action phrases that were not part of an ongoing activity (Leynes, Marsh,
Hicks, Allen, & Mayhorn, 2003). Findings from the former studies have consistently revealed three modulations of event-related potentials (ERPs) that
have been shown to differentiate ongoing activity trials from intention formation trials: a late positivity complex (LPC), fronto-polar slow waves (FPSW),
and temporo-parietal slow waves (TPSW). The LPC reflects positivity over
the parietal region of the scalp and negativity over the lateral frontal regions
with a peak around 600 ms. after stimulus onset and reflects a difference
between later-retrieved (i.e., PM hit responses) and later-unretrieved (i.e., PM
miss responses) intention trials. The FPSW reflects a sustained negativity
over the frontal-polar region of the scalp and lasts approximately from 500 to
1000 ms. after stimulus onset. This phenomenon was shown to exist in young
adults but not in old ones (West, Herndon et al., 2003; Zöllig et al., 2010).
Finally, the TPSW reflects greater positivity in later-retrieved intention trials
than in later-unretrieved intention trials, only in old adults, beginning at 800
ms. after stimulus onset and lasting for the remainder of the ERP.
Similar to findings from studies of the neural correlates of encoding of PM
intentions, researchers who looked at retrieval processes in PM have consistently reported three components of modulations of the ERPs associated with
PM (West, Herndon, & Crewdson, 2001; West & Krompinger, 2005; West &
Ross-Munroe, 2002). The first is N300, representing negativity over the
occipital-parietal region starting around 300 ms. after stimulus onset. This
modulation represents differences between PM and ongoing activity trials.
The second modulation is frontal positivity, reflecting positivity over the midline frontal region which, similarly to the N300, represents differences
between PM and ongoing activity trials. This ERP modulation starts at around
200 ms. after stimulus onset and lasts for several hundred milliseconds. The
N300 and frontal positivity are thought to reflect processes that are related to
the processing of event-based PM intentions that go beyond the specific characteristic of the PM intention or the demand of the ongoing activity (West,
2007; West et al., 2001; West & Krompinger, 2005; West & Ross-Munroe,
2002). The last modulation associated with retrieval of PM is parietal positivity, representing sustained positivity over the parietal region of the scalp
between 400 and 1200 ms. after stimulus onset; it distinguishes PM cue trials
from ongoing activity trials (West & Wymbs, 2004). It is assumed to reflect
3 functionally and temporally distinct components of the ERP associated with
the detection of low probability intentions (West, Herndon et al., 2003; West
& Wymbs, 2004; West, Wymbs, Jakubek, & Herndon, 2003), the recognition
of the PM cues (called parietal old-new effect; West, 2007; West, Carlson, &
GIL GONEN-YAACOVI, & PAUL W. BURGESS
187
Cohen, 2007a; West & Krompinger, 2005; West, McNerney, & Travers,
2007b) and the configuration of the PM task set (Bisiacchi, Schiff, Ciccola,
& Kliegel, 2009; West et al., 2001; West, Wymbs et al., 2003).
Positron emission tomography
Four studies have so far used positron emission tomography (PET) to explore
the neuroscience PM. (Burgess et al., 2001; Burgess et al., 2003; Okuda,
Fujii, Ohtake, Tsukiura, Yamadori, Frith, et al., 2007; Okuda, Toshikatsu,
Yamadori, Kawashima, Tsukiura, Fukatsu et al., 1998). These add weight to
the neuropsychological findings suggesting some kind of frontal lobe
involvement in PM. More specifically, the findings highlight a consistent
relation between the activation of the rostral prefrontal cortex (rPFC) and performance on a variety of PM tasks. For example, Burgess et al. (2003) showed
that two rostral prefrontal regions show activation during PM tasks. Medial
anterior PFC shows a decrease in cerebral blood flow when people are maintaining an intention, and relatively greater regional cerebral blood flow when
performing the ongoing task only, with no intention to maintain. On the other
hand, lateral rostral PFC shows an increase in cerebral blood flow during performance of PM tasks, but relatively less when performing the ongoing task
only. These findings have been found in other PET studies (Burgess et al.,
2001; Okuda et al., 2007; Okuda et al., 1998), and agree well with findings
from fMRI as well (see Burgess, Gonen-Yaacovi, & Volle, 2011 for review).
They seem to represent a “standard pattern” of activation within this region
for event-based PM tasks. The situation for time-based tasks however seems
on present evidence to be more complex (Okuda et al., 2007).
Functional magnetic resonance imaging
As mentioned above, further support for the role of rFPC in PM has been
obtained from fMRI studies. A meta-analysis of the overlapping regions of
activation from all the fMRI studies of PM tasks reveals that performance
during PM tasks, relative to the ongoing tasks, tends to be associated with
activations in rPFC (Burgess et al., 2011). This general finding is supported
by all studies where paradigms have been used where the performance in an
ongoing task was compared directly with that in a PM task (den Ouden, Frith,
Frith, & Blakemore, 2005; Gilbert, 2011; Gilbert et al., 2009; Hashimoto,
Umeda, & Kojima, 2010; Haynes, Sakai, Rees, Gilbert, Frith, & Passingham,
2007; Okuda et al., 2007; Okuda, Gilbert, Burgess, Frith, & Simons, 2011;
Poppenk, Moscovitch, McIntosh, Ozcelik, & Craik, 2010; Reynolds, West, &
Braver, 2009; Simons, Schölvinck, Gilbert, Frith, & Burgess, 2006).
188
PROSPECTIVE MEMORY: THE FUTURE FOR FUTURE INTENTIONS
More specifically, activations in lateral rPFC are most often associated
with maintaining a delayed intention (den Ouden et al., 2005; Gilbert, 2011;
Gilbert et al., 2009; Okuda et al., 2011; Reynolds et al., 2009; Simons et al.,
2006), a finding which is in agreement with other suggested theories regarding the role of lateral rPFC (e.g., Christoff & Gabrieli, 2000; Koechlin, Basso,
Pietrini, Panzer, & Grafman, 1999). In addition, activation in medial rPFC
during an ongoing or control task tends to be higher than during a PM task
(Hashimoto et al., 2010; Okuda et al., 2007; Simons et al., 2006).
When considering the findings for activations in either medial or lateral
rPFC in event-based tasks, some regions (but certainly not all, see below)
seem remarkably insensitive to task-related performance details such as the
form of stimulus material presented, the nature of the ongoing task, and the
level of difficult in detecting the PM cues (Burgess et al., 2001; Burgess et al.,
2003; see also Simons et al., 2006). This idea follows the use of “conjunctiontype” designs (Burgess et al., 2003) where several tasks are used that differ
along many dimensions (e.g., the type of ongoing task, the stimulus material,
the question being answered, the PM cues etc.) and then at the analysis stage
one looks for activations that are common across all the tasks. For other
regions within the rPFC there does seem to be functional specialisation for
different components, forms, and types of PM. For example, Gilbert et al.
(2009) contrasted brain activity that supports the retrieval of PM in 2 conditions that differed only in the pre-task instructions provided to participants. In
a “cued condition”, participants were asked to produce a specific response
whenever a PM cue appeared. The task instruction was “if the same letter is
on both sides, then I will press the middle button”, i.e., emphasising a close
link between the intended action and the PM cue. By contrast, in a “self-initiated condition”, the instruction took the form of: “if the same letter is on
both sides, then I can score 5 points”, emphasising the reward goal of the task
rather than the specific action to be made in response to the PM target. Even
though all other aspects of the paradigm were identical, differences in rPFC
were found during the PM task even just with these small changes in instruction format. Responding to PM intentions in the self-initiated condition was
associated with greater activation in lateral rPFC, whereas responding to PM
intentions in the cued condition was associated with greater activation in
medial rPFC. Other factors that may affect rPFC during PM are variations in
implicit cues (Hashimoto et al., 2010), the nature of the PM intention (Haynes
et al., 2007) and the characteristic of the intention retrieval (Simons et al.,
2006).
Other activations outside rPFC are also commonly associated with PM
performance. More specifically, there is frequent activation of BA7 and
BA40 during PM tasks. Activation within one or both of these regions is
almost as common as activation within rPFC (e.g., Burgess et al., 2001; den
GIL GONEN-YAACOVI, & PAUL W. BURGESS
189
Ouden et al., 2005; Eschen, Freeman, Dietrich, Martin, Ellis, Martin et al.,
2007; Gilbert et al., 2009; Hashimoto et al., 2010; Okuda et al., 2011; Poppenk et al., 2010, Reynolds et al., 2009; Simons et al., 2006). Evidence from
electrophysiological methods also suggests a possible link between PM performance and tempo-parietal regions (see West, 2011 for review). It is likely
that sub-regions within BA40 & 7 support different processes associated with
PM. For instance, Poppenk et al. (2010) found angular gyrus activations
(BA7) for one condition (hits > misses) but also superior parietal lobe (BA7)
for the opposite contrast (misses > hits). Another example is from Hashimoto
et al. (2010), who found activations in the inferior region of the inferior parietal lobe (BA40) when comparing performance in the control condition compared with the PM condition, but at the same time, activations in more superior regions on the inferior parietal lobe (BA40) were found during PM
blocks.
Another region often associated with PM performance is the anterior cingulate cortex (BA32; Hashimoto et al., 2010; Okuda et al., 2011; Reynolds et
al., 2009; Simons et al., 2006). It seems that, similarly to BA40 & 7, different
subregions support different components of PM; however, the findings so far
are not as strong and consistent as the findings related to rPFC or parietal
lobe. For example, Okuda et al. (2011) reported activations in the right anterior cingulate cortex during PM performance in one condition (expand > contract) and also activations in another section of this region in the opposite condition (contract > expand).
Putting the future into prospective memory
The neuroscience of prospective memory has been progressing especially
rapidly over the last ten years or so, but is still in its infancy. This review has
attempted to cover the main recent empirical findings in a field which is
becoming increasingly coherent. So the time is right to consider where within
PM the newest developments may occur. Two of these will be considered
here.
The first concerns “prospection”. While the growth of PM as an area of
enquiry this has been happening, there has been a parallel development of a
new and strongly related field: the cognitive neuroscience of “episodic future
thinking” or “mental time travel” (e.g., Atance & O’Neill, 2001; Boyer, 2008;
see Burgess et al., 2011 for review). There are many different terms for this
kind of mental phenomenon, which we will refer to as “prospection” (Burgess
et al., 2011) since that was a rather neater and previously existing term for it.
Prospection refers to the mental experience of imagining the future, especially in a goal-driven way. Curiously perhaps, given that prospective memory and prospection are so obviously related in that they deal with future
190
PROSPECTIVE MEMORY: THE FUTURE FOR FUTURE INTENTIONS
thoughts and actions rather than the traces of past ones, each of these fields
has developed almost completely independently, thus far. However, in the
last few years there have been exciting developments in understanding
prospection (e.g., Addis, Pan, Vu, Laiser, & Schacter, 2009; Schacter, Addis,
& Buckner, 2007; Schacter, Addis, & Buckner, 2008; Szpunar, Watson, &
McDermott, 2007; Weiler, Suchan, & Daum, 2010; Williams, Ellis, Tyers,
Healy, Rose, & MacLeod, 1996), and there is one point in particular that
might be made when thinking about the future of future thinking and how it
relates to prospective memory.
This point is that, as with studies of prospective memory, rostral PFC activations appear to be found very commonly in neuroimaging studies of
prospection. Indeed, Burgess et al. (2011) reviewed 13 studies of prospection,
and found that all but one reported activation in rostral PFC, which is a
roughly comparable level of consistency that one finds with studies of prospective memory. This common activation need not reflect a common
processing component to prospection and maintaining an intention (the assertion that common activations reflect common processing across tasks is
known in the field of neuroimaging as a “reverse inference”, and is generally
thought to be precarious). However, if it does, what might that be?
One possibility is raised by Benoit, Gilbert, Frith, and Burgess (2011).
Their study aimed to see whether functional imaging data is consistent with
the idea that the “rostral PFC attentional gateway” is involved in performance
of prospective memory paradigms. The rostral PFC attentional gateway is a
hypothetical cognitive mechanism proposed by the “gateway hypothesis” of
rostral PFC function (e.g., Burgess, Dumontheil, & Gilbert, 2007). This
asserts that a principal purpose of rostral PFC is to control differences in
attending between “stimulus-independent thought” (i.e., our inner mental
life) and that involved in preferential attending to the external world (“stimulus-oriented attending”). Benoit et al. (2011) used a factorial design, crossing
prospective memory (PM vs. no-PM) with mode of attending (stimulus-oriented (SO) vs. stimulus-independent (SI)), the latter of which has previously
been shown to activate rostral PFC (see Burgess et al., 2007 for review). The
purpose of the experiment was to determine whether the foci of activations in
PM were the same as those activated by SI/SO attention changes. They found
that parts of mrPFC were jointly recruited during (i) mere ongoing task activity versus additional engagement in a PM task, and (ii) stimulus-oriented versus stimulus-independent processing. This is congruent with the notion that
some of the processes mediating PM performance can be characterised by relative differences in these attentional modes as proposed by the gateway
hypothesis. At the same time, the PM contrast was consistently associated
with more dorsal peak activation than the stimulus contrast, perhaps reflecting engagement of additional processes. Burgess et al. (2011) argue that this
GIL GONEN-YAACOVI, & PAUL W. BURGESS
191
same “attentional gateway” might also be used in engaging prospection,
because it requires drawing one’s attention away from the current environment and creating an “inner mental world”. Currently, it seems possible that
the currently larger topic of prospective memory may in the future be viewed
as perhaps the most developed sub-class under the broader heading of
“prospection”. Key to this is the very special role that rostral PFC (and other
PFC structures) seem to play in enabling people to engage in imaginative
thought, aspects of which are critical to creating intentions for future acts
(prospective memory), and considering the potential consequences of them
(prospection).
A second possible future development point within the field of prospective memory concerns the role of awareness and “cognitive control” in the
maintenance and remembering of delayed intentions. As this review outlines,
it is clear that most theorists regard there as being both automatic- and controlled-type processing underpinning the maintenance and execution of a
delayed intention. However, it seems to be generally assumed (but rarely
examined) that the participant is broadly “aware” of the contingencies affecting their behaviour. But this assumption is challenged by a recent study by
Okuda et al. (2011), who developed a PM task where the intervals between
prospective memory targets were manipulated in a predictable alternating
cycle of expanding and contracting target intervals. “Expanding” means that
the number of ongoing trials between PM targets was increasing, and “contracting” means that the number of ongoing trials between targets was
decreasing. Okuda et al. (2011) found that the participants’ behaviour
changed in accordance with these changing target intervals. Prospective
memory performance (measured by responses to PM targets) was faster and
more accurate in the expanding target interval phase, at the cost of less accurate and slower performance on ongoing trials. But in the contracting phase
the opposite pattern was found: faster and better ongoing trial performance
but poorer PM performance.
Remarkably however, although the participants’ behaviour was affected,
the changes in target intervals, they were completely unaware of them – in the
sense that when asked none of them reported being aware of any pattern in
target interval, or of any change in their behaviour. Nevertheless, fMRI
detected a trade-off effect in activations in the anterior medial prefrontal cortices that mirrored the changes in participant behaviour. We found activation
increases in response to the PM targets that was accompanied by deactivation
to the ongoing trials in the expanding phase as compared with the contracting
phase. The opposite pattern was observed in the anterior cingulate cortex.
These patterns of behaviour and BOLD signal changes are not easy to
explain according to the “monitoring” or “spontaneous retrieval” frameworks. The medial rostral PFC activations are probably not indicators for
192
PROSPECTIVE MEMORY: THE FUTURE FOR FUTURE INTENTIONS
some form of deliberate, conscious “monitoring” or “working memory” operation, because participants were unable to report their behaviour changes or
the changes in target intervals. Similarly, the consistency of the relation
between the changes in target interval and PM performance is also difficult to
explain by a simple “spontaneous retrieval” account, since it is entirely predictable and seems to be cued by the experimental context and not just the PM
target. It seems possible instead that what has been detected here may be the
neural signature of a process which effects automatic (i.e., unconscious) coordination of attentional resources between ongoing task performance and a
delayed intention.
Moreover, this kind of effect may not be restricted just to PM situations.
Blais, Harris, Guerrero, & Bunge (2012) have shown a similar effect using a
Stroop task. They examined the size of the congruency (i.e., Stroop) effect
according to the proportion of congruent trials given. Their paradigm demonstrated the well-known phenomenon where the proportion of congruent trials
had a marked behavioural effect upon performance (where reaction times are
slower when incongruent trials are less frequent). But, critically, they asked
participants about the relative proportion of congruent/incongruent trials.
They found that the proportion by congruency interaction was unrelated to
participants’ awareness of the actual frequencies. So here again, we have a situation where behaviour is being governed by contingencies even though participants are unaware of them (in the sense of being able to report them). It
seems very likely on the evidence of these very recent papers therefore, that
there may be processing at work in PM situations which has only just been
started to be considered – perhaps one might think of it as “expectation prospective memory” – i.e., where regularities in the environment (e.g., temporal
or proportional) set up expectations akin perhaps to priming within the cognitive system at a level which is not routinely available for self-report.
Conclusion
The past 15 years have seen a huge increase in experimental research targeted
at understanding prospective memory. By 1996 there were only 45 published
experimental studies on PM (Kvavilashvili & Ellis, 1996). However, from
1996 until 2005, over 285 published papers appeared (McDaniel & Einstein,
2007). This rate of increase is in turn increasing. We have attempted to summarise the main conclusions from the theoretical and empirical work that has
been carried out in this emerging field. As contrasted with 20 years ago, we
now have some degree of agreement about what constitutes a PM paradigm.
Moreover, whereas in the early years it was not clear whether the term “prospective memory” described a variety of behaviours supported by a variety of
different processing resources, or the operation of a particular construct (or
GIL GONEN-YAACOVI, & PAUL W. BURGESS
193
limited set of them), these days most theorists would take the former position.
The prevalent current theories highlight the importance of different factors
upon behaviour and processing, such as the characteristics of the ongoing task
and the PM cue, on determining the types of processes that support retrieval
of PM and the likelihood of PM success. Remarkably however, given the
complexity and multiplicity of these findings, neuropsychological and neuroimaging investigations have suggested that there is a particular part of the
brain (rostral prefrontal cortex, approximating Brodmann area 10) that is
involved in a wide range of PM situations, presenting hope that there may be
a common processing resource that might provide a meeting point for understanding the processing underpinning PM. Finally, we suggest that two promising future developments for the field of prospective memory might be integration with the findings from prospection more broadly, and also the consideration of “expectation prospective memory” – the triggering of PM
responses without awareness in response to contingencies detected in the
environment.
References
Aberle, I., Rendell, P.G., Rose, N.S., McDaniel, M.A., & Kliegel, M. (2010). The age
prospective memory paradox: Young adults may not give their best outside of
the lab. Developmental Psychology, 46, 1444-1453.
Addis, D.R., Pan, L., Vu, M.A., Laiser, N., & Schacter, D.L. (2009). Constructive episodic simulation of the future and the past: Distinct subsystems of a core brain
network mediate imagining and remembering. Neuropsychologia, 47, 22222238.
Altgassen, M., Kliegel, M., Rendell, P., Henry, J.D., & Zöllig, J. (2008). Prospective
memory in schizophrenia: The impact of varying retrospective-memory load.
Journal of Clinical and Experimental Neuropsychology, 30, 777-788.
Altgassen, M., Zöllig, J., Kopp, U., Mackinlay, R., & Kliegel, M. (2007). Patients with
Parkinson’s disease can successfully remember to execute delayed intentions.
Journal of the International Neuropsychological Society, 13, 888-892.
Atance, C.M., & O’Neill, D.K. (2001). Episodic future thinking. Trends in Cognitive
Sciences, 5, 533-539.
Baddeley, A.D., & Wilkins, A.J. (1984). Taking memory out of the laboratory. In J.E.
Harris & P.E. Morris (Eds.), Everyday memory, actions and absent-mindedness
(pp. 1-17). London: Academic Press.
Bailey, P.E., Henry, J.D., Rendell, P.G., Phillips, L.H., & Kliegel, M. (2010). Dismantling the “age-prospective memory paradox”: The classic laboratory paradigm
simulated in a naturalistic setting. Quarterly Journal of Experimental Psychology, 63, 646-652.
Benoit, R.G., Gilbert, S.J., Frith, C.D., & Burgess, P.W. (2011). Rostral prefrontal cortex and the focus of attention in prospective memory. Cerebral Cortex. Oct 4.
[Epub ahead of print]
194
PROSPECTIVE MEMORY: THE FUTURE FOR FUTURE INTENTIONS
Bisiacchi, P.S., Schiff, S., Ciccola, A., & Kliegel, M. (2009). The role of dual-task and
task-switch in prospective memory: Behavioral data and neural correlates. Neuropsychologia, 47, 1362-1373.
Blais, C., Harris, M.B., Guerrero, J.V., & Bunge, S.A. (2012). Rethinking the role of
automaticity in cognitive control. Quarterly Journal of Experimental Psychology, 65, 268-276.
Block, R.A., & Zakay, D. (2006). Prospective remembering involves time estimation
and memory processes. In J. Glicksohn & M.S. Myslobodsky (Eds.), Timing the
future: The case for a time-based prospective memory (pp. 25-49). London:
World Scientific.
Boyer, P. (2008). Evolutionary economics of mental time travel? Trends in Cognitive
Sciences, 12, 219-224.
Brandimonte, M., Einstein, G.O., & McDaniel, M.A. (1996). Prospective memory:
Theory and applications, Mahwah, NJ: Lawrence Erlbaum Associates.
Brandimonte, M.A., Filippello, P., Coluccia, E., Altgassen, M., & Kliegel, M. (2011).
To do or not to do? Prospective memory versus response inhibition in autism
spectrum disorder and attention-deficit/hyperactivity disorder. Memory, 19, 5666.
Brandimonte, M.A., & Passolunghi, M.C. (1994). The effect of cue-familiarity, cue
distinctiveness and retention interval on prospective remembering. The Quarterly Journal of Experimental Psychology, 47A, 565-587.
Brewer, G.A., Knight, J.B., Marsh, R.L., & Unsworth, N. (2010). Individual differences in event-based prospective memory: Evidence for multiple processes supporting cue detection. Memory and Cognition, 38, 304-311.
Brooks, B.M., Ross, F.D., Potter, J., Jayawardena, S., & Morling, A. (2004). Assessing stroke patients’ prospective memory using virtual reality. Brain Injury, 18,
391-401.
Burgess, P.W., Alderman, N., Emslie, H., Evans, J.J., Wilson, B.A., & Shallice, T.
(1996). The simplified six element test. In B.A. Wilson, N. Alderman, P.W. Burgess, H. Emslie, & J.J. Evans (Eds.), Behavioural assessment of the dysexecutive
syndrome. Bury St. Edmunds, U.K.: Thames Valley Test Company.
Burgess, P.W., Dumontheil, I., & Gilbert, S.J. (2007). The gateway hypothesis of rostral prefrontal cortex (area 10) function. Trends in Cognitive Sciences, 11, 290298.
Burgess, P.W., Dumontheil, I., Gilbert, S.J., Okuda, J., Scholvinck, M.L., & Simons,
J.S. (2008). On the role of rostral prefrontal cortex (area 10) in prospective memory. In M. Kliegel, M.A. McDaniel, & G.O. Einstein (Eds.), Prospective memory: Cognitive, neuroscience, developmental and applied perspectives (pp. 233258). Mahwah: Erlbaum.
Burgess, P.W., Gonen-Yaacovi, G., & Volle, E. (2011). Functional neuroimaging
studies of prospective memory: What have we learnt so far? Neuropsychologia,
49, 2185-2198.
Burgess, P.W., Quayle, A., & Frith, C.D. (2001). Brain regions involved in prospective memory as determined by positron emission tomography. Neuropsychologia, 39, 545-555.
GIL GONEN-YAACOVI, & PAUL W. BURGESS
195
Burgess, P.W., Scott, S.K., & Frith, C.D. (2003). The role of the rostral frontal cortex
(area 10) in prospective memory: A lateral versus medial dissociation Neuropsychologia, 41, 906-918.
Burgess, P.W., Veitch, E., Costello, A., & Shallice, T. (2000). The cognitive and neuroanatomical correlates of multitasking. Neuropsychologia, 38, 848-863.
Carlesimo, G.A., Casadio, P., & Caltagirone, C. (2004). Prospective and retrospective
components in the memory for actions to be performed in patients with severe
closed head injury. Journal of the International Neuropsychological Society, 5,
679-688.
Cherry, K.E., & LeCompte, D.C. (1999). Age and individual differences influence
prospective memory. Psychology and Aging, 14, 60-76.
Cherry, K.E., Martin, R.C., Simmons-D’Gerolamo, S.S., Pinkston, J.B., Griffing, A.,
& Gouvier, W.D. (2001). Prospective remembering in younger and older adults:
Role of the prospective cue. Memory, 9, 177-193.
Christoff, K., & Gabrieli, J.D.E. (2000). The frontopolar cortex and human cognition:
Evidence for a rostrocaudal hierarchical organization within the human prefrontal cortex. Psychobiology, 28, 168-186.
Cockburn, J. (1995). Task interruption in prospective memory: A frontal lobe function? Cortex, 31, 87-97.
Cook, G.I., Marsh, R.L., Clark-Foos, A., & Meeks, J.T. (2007). Learning is impaired
by activated intentions. Psychonomic Bulletin and Review, 14, 101-106.
Cook, G.I., Marsh, R.L., & Hicks, J.L. (2005). Associating a time-based prospective
memory task with an expected context can improve or impair intention completion. Applied Cognitive Psychology, 19, 345-360.
Costa, A., Peppe, A., Caltagirone, C., & Carlesimo, G.A. (2008). Prospective memory
impairment in individuals with Parkinson’s disease. Neuropsychology, 22, 283292.
Craik, F.I.M. (1986). A functional account of age differences in memory. In F. Klix &
H. Hagendorf (Eds.), Human memory and cognitive capabilities: Mechanisms
and performances (pp. 409-422). Amsterdam: Elsevier.
den Ouden, H.E.M., Frith, U., Frith, C., & Blakemore, S.J. (2005). Thinking about
intentions. NeuroImage, 28, 787-796.
Devolder, P.A., Brigham, M.C., & Pressley, M. (1990). Memory performance awareness in younger and older adults. Psychology and Aging, 5, 291-303.
d’Ydewalle, G., Bouckaert, D., & Brunfaut, E. (2001). Age-related differences and
complexity of ongoing activities in time- and event-based prospective memory.
The American Journal of Psychology, 114, 411-423.
d’Ydewalle, G., Luwel, K., & Brunfaut, E. (1999). The importance of on-going concurrent activities as a function of age in time- and event-based prospective memory. European Journal of Cognitive Psychology, 11, 219-237.
Einstein, G.O., Holland, L.J., McDaniel, M.A., & Guynn, M.J. (1992). Age-related
deficits in prospective memory: The influence of task complexity. Psychology
and Aging, 7, 471-478.
Einstein, G.O., & McDaniel, M.A. (1990). Normal aging and prospective memory.
Journal of Experimental Psychology: General, 16, 717-726.
196
PROSPECTIVE MEMORY: THE FUTURE FOR FUTURE INTENTIONS
Einstein, G.O., McDaniel, M.A., Richardson, L., Guynn, M.J., & Cunfer, A.R. (1995).
Aging and prospective memory: Examining the influences of self-initiated
retrieval processes. Journal of Experimental Psychology: Learning, Memory
and Cognition, 21, 996-1007.
Einstein, G.O., McDaniel, M.A., Thomas, R., Mayfield, S., Shank, H., Morrisette, N.,
& Breneiser, J. (2005). Multiple processes in prospective memory retrieval: Factors determining monitoring versus spontaneous retrieval. Journal of Experimental Psychology: General, 134, 327-342.
Einstein, G.O., Smith, R.E., McDaniel, M.A., & Shaw, P. (1997). Aging and prospective memory: The influence of increased task demands at encoding and retrieval.
Psychology and Aging, 12, 479-488.
Ellis, J.A. (1998). Prospective memory and medicine-taking. In L.B. Myers & K.
Midence (Eds.), Adherence to treatment in medical conditions (pp. 113-131).
London: Harwood Academic.
Ellis, J.A., Kvavilashvili, L., & Milne, A. (1999). Experimental tests of prospective
remembering: the influence of cue-event frequency on performance. British
Journal of Psychology, 90, 9-23.
Eschen, A., Freeman, J., Dietrich, T., Martin. M., Ellis, J., Martin, E., & Kliegel, M.
(2007). Motor brain regions are involved in the encoding of delayed intentions:
A fMRI study. International Journal of Psychophysiology, 64, 259-268.
Fortin, S., Godbout, L., & Braun, C.M.J. (2002). Strategic sequence planning and prospective memory impairments in frontally lesioned head trauma patients performing activities of daily living. Brain and Cognition, 48, 361-365.
Gilbert, S.J. (2011). Decoding the content of delayed intentions. The Journal of Neuroscience, 31, 2888-2894.
Gilbert, S.J., Gollwitzer, P.M., Cohen, A.L., Burgess, P.W., & Oettingen, G. (2009).
Separable brain systems supporting cued versus self-initiated realization of
delayed intentions. Journal of Experimental Psychology: Learning Memory and
Cognition, 35, 905-915.
Graf, P., & Grondin, S. (2006). Time perception in time-based prospective memory.
In J. Glicksohn & M.S. Myslobodsky (Eds.), Timing the future: The case for a
time-based prospective memory (pp. 1-24). London: World Scientific.
Graf, P., & Uttl, B. (2001). Prospective Memory: A new focus for research. Consciousness and Cognition, 10, 437-450.
Groot, Y.C., Wilson, B., Evans, J., & Watson, P. (2002). Prospective memory functioning in people with and without brain injury. Journal of the International Neuropsychological Society, 8, 645-654.
Guynn, M.J. (2003). A two-process model of strategic monitoring in event-based prospective memory: Activation/retrieval mode and checking. International Journal of Psychology, 38, 245-256.
Guynn, M.J., & McDaniel, M.A. (2007). Target pre-exposure eliminates the effect of
distraction on event-based prospective memory. Psychonomic Bulletin and
Review, 14, 484-488.
Guynn, M.J., McDaniel, M.A., & Einstein, G.O. (1998). Prospective memory: When
reminders fail. Memory and Cognition, 26, 287-298.
GIL GONEN-YAACOVI, & PAUL W. BURGESS
197
Hashimoto, T., Umeda, S., & Kojima, S. (2010). Neural substrates of implicit cueing
effect on prospective memory. NeuroImage, 54, 645-652.
Haynes, J.D., Sakai, K., Rees, G., Gilbert, S., Frith, C., & Passingham, R.E. (2007).
Reading hidden intentions in the human brain. Current Biology, 17, 323-328.
Henry, J.D., MacLeod, M., Phillips, L.H., & Crawford, J.R. (2004). Meta-analytic
review of prospective memory and aging. Psychology and Aging, 19, 27-39.
Henry, J.D., Rendell, P.G., Kliegel, M., & Altgassen, M. (2007). Prospective memory
in schizophrenia: Primary or secondary impairment? Schizophrenia Research,
95, 179-185.
Hicks, J.L., Marsh, R.L., & Russell, E.J. (2000). The properties of retention intervals
and their affect on retaining prospective memories. Journal of Experimental Psychology: Learning, Memory and Cognition, 25, 1160-1169.
Jones, C.R., Happé, F., Pickles, A., Marsden, A.J., Tregay, J., Baird, G., Simonoff, E.,
& Charman, T. (2011). ‘Everyday memory’ impairments in autism spectrum disorders. Journal of Autism and Developmental Disorders, 41, 455-464.
Katai, S., Maruyama, T., Hashimoto, T., & Ikeda, S. (2003). Event based and time
based prospective memory in Parkinson’s disease. Journal of Neurology, Neurosurgery and Psychiatry, 74, 704-709.
Kinsella, G., Murtagh, D., Landry, A., Homfray, K., Hammond, M., O’Beirne, L.,
Dwyer, L., Lamont, M., & Ponsford, J. (1996). Everyday memory following
traumatic brain injury. Brain Injury, 10, 499-507.
Kliegel, M., Eschen, A., & Thöne-Otto, A.I. (2004). Planning and realization of complex intentions in traumatic brain injury and normal aging. Brain and Cognition,
56, 43-54.
Kliegel, M., & Martin, M. (2003). Prospective memory research: Why is it relevant?
International Journal of Psychology, 38, 193-194.
Kliegel, M., Martin, M., McDaniel, M.A., & Einstein, G.O. (2001). Varying the
importance of a prospective memory task: Differential effects across time- and
event-based prospective memory. Memory, 9, 1-11.
Kliegel, M., Martin, M., McDaniel, M.A., & Einstein, G.O. (2004). Importance effects
on performance in event-based prospective memory tasks. Memory, 12, 553561.
Kliegel, M., McDaniel, M.A., & Einstein, G.O. (2000). Plan formation, retention, and
execution in prospective memory: A new approach and age-related effects.
Memory and Cognition, 28, 1041-1049.
Kliegel, M., Phillips, L.H., Lemke, U., & Kopp, U.A. (2005). Planning and realisation
of complex intentions in patients with Parkinson’s disease. Journal of Neurology, Neurosurgery and Psychiatry, 76, 1501-1505.
Knight, R.G., Harnett, M., & Titov, N. (2005). The effects of traumatic brain injury on
predicted and actual performance on a test of prospective remembering. Brain
Injury, 19, 27-38.
Knight, R.G., Titov, N., & Crawford, M. (2006). The effects of distraction on prospective remembering following traumatic brain injury assessed in a simulated naturalistic environment. Journal of the International Neuropsychological Society,
12, 8-16.
198
PROSPECTIVE MEMORY: THE FUTURE FOR FUTURE INTENTIONS
Koechlin, E., Basso, G., Pietrini, P., Panzer, S., & Grafman, J. (1999). The role of the
anterior prefrontal cortex in human cognition. Nature, 399, 148-151.
Kondel, T.K. (2002). Prospective memory and executive function in schizophrenia.
Brain and Cognition, 48, 405-410.
Kumar, D., Nizamie, S.H., & Jahan, M. (2005). Event-based prospective memory in
schizophrenia. Journal of Clinical and Experimental Neuropsychology, 27, 867872.
Kvavilashvili, L. (1987). Remembering intention as a distinct form of memory. British
Journal of Psychology, 78, 507-518.
Kvavilashvili, L., & Ellis, J. (1996). Varieties of intentions: Some distinctions and
classifications. In M. Brandimonte, G.O. Einstein, & M.A. McDaniel (Eds.),
Prospective memory: Theory and applications. Mahwah, NJ: Erlbaum.
Kvavilashvili, L., Kornbrot, D.E., Mash, V., Cockburn, J., & Milne, A. (2009). Differential effects of age on prospective and retrospective memory tasks in young,
young-old, and old-old adults. Memory, 17, 180-196.
Lee, E., Xiang, Y.T., Man, D., Au, R.W., Shum, D., Tang, W.K., Chiu, H.F., Wong,
P., & Ungvari, G.S. (2010). Prospective memory deficits in patients with bipolar
disorder: A preliminary study. Archives of Clinical Neuropsychology, 25, 640647.
Levy, R.L., & Loftus, G.R. (1984). Compliance and memory. In J.E. Harris & P.E.
Morris (Eds.), Everyday memory, actions, and absent-mindedness (pp. 93-112).
New York: Academic Press.
Leynes, P.A., Marsh, R.L., Hicks, J.L., Allen, J.D., & Mayhorn, C.B. (2003). Investigating the encoding and retrieval of intentions with event-related potentials.
Consciousness and Cognition, 12, 1-18.
Linton, M. (1978). Real world memory after six years. In M. Gruneberg, P. Morris, &
R. Sykes (Eds.), Practical Aspects of Memory. London: Academic Press.
Loft, S., & Yeo, G. (2007). An investigation into the resource requirements of event
based prospective memory. Memory and Cognition, 35, 263-274.
Loftus, E.F. (1971). The effect of presence of a cue and interpolated activity. Psychonomic Science, 24, 315-316.
Mantyla, T. (1993). Priming effects in prospective memory. Memory, 1, 203-218.
Marsh, R.L., Hancock, T.W., & Hicks, J.L. (2002). The demands of an ongoing activity influence the success of event-based prospective memory. Psychonomic Bulletin and Review, 9, 604-610.
Marsh, R.L., Hicks, J.L., & Cook, G.I. (2005). On the relationship between effort
toward an ongoing task and cue detection in event-based prospective memory.
Journal of Experimental Psychology: Learning, Memory and Cognition, 31, 6875.
Marsh, R.L., Hicks, J.L., & Cook, G.I. (2006). Task interference from prospective
memories covaries with contextual associations of filling them. Memory and
cognition, 29, 861-870.
Marsh, R.L., Hicks, J.L., Cook, G.I., Hansen, J.S., & Pallos, A.L. (2003). Interference
to ongoing activities covaries with the characteristics of an event-based intention. Journal of Experimental Psychology: Learning, Memory and Cognition,
29, 861-870.
GIL GONEN-YAACOVI, & PAUL W. BURGESS
199
Marsh, R.L., Hicks, J.L., Cook, G.I., & Mayhorn, C.B. (2007). Comparing older and
younger adults in an event-based prospective memory paradigm containing an
output monitoring component. Aging, Neuropsychology and Cognition, 14, 168188.
Mathias, J.L., & Mansfield, K.M. (2005). Prospective and declarative memory problems following moderate and severe traumatic brain injury. Brain Injury, 19,
271-282.
Maylor, E.A. (1993). Minimized prospective memory loss in old age. In J. Cerella, W.
Hoyer, J. Rybash, & M.L. Commons (Eds.), Adult information processing: Limits on loss (pp. 529-551). San Diego, CA: Academic Press.
Maylor, E.A. (1996). Does prospective memory decline with age? In M. Brandimonte,
G.O. Einstein, & M.A. McDaniel (Eds.), Prospective memory: Theory and
applications (pp. 173-197). Hillsdale, NJ: Erlbaum.
Maylor, E.A. (1998). Changes in event-based prospective memory across adulthood.
Aging, Neuropsychology and Cognition, 5, 107-128.
Maylor, E.A., Smith, G., Della Sala, S., & Logie, R.H. (2002). Prospective and retrospective memory in normal aging and dementia: An experimental study. Memory and Cognition, 30, 871-884.
McCauley, S.R., & Levin, H.S. (2004). Prospective memory in pediatric traumatic
brain injury: A preliminary study. Developmental Neuropsychology, 25, 5-20.
McCauley, S.R., McDaniel, M.A., Pedroza, C., Chapman, S.B., & Levin, H.S. (2009).
Incentive effects on event-based prospective memory performance in children
and adolescents with traumatic brain injury. Neuropsychology, 23, 201-209.
McCauley, S.R., Pedroza, C., Chapman, S.B., Cook, L.G., Hotz, G., Vásquez, A.C.,
& Levin, H.S. (2010b). Event-based prospective memory performance during
subacute recovery following moderate to severe traumatic brain injury in children: Effects of monetary incentives. Journal of the International Neuropsychological Society, 16, 335-341.
McCauley, S.R., Pedroza, C., Chapman, S.B., Cook, L.G., Vásquez, A.C., & Levin,
H.S. (2011). Monetary incentive effects on event-based prospective memory
three months after traumatic brain injury in children. Journal of Clinical and
Experimental Neuropsychology [Epub ahead of print].
McCauley, S.R., Wilde, E.A., Merkley, T.L., Schnelle, K.P., Bigler, E.D., Hunter,
J.V., Chu, Z., Vásquez, A.C., & Levin, H.S. (2010a). Patterns of cortical thinning in relation to event-based prospective memory performance three months
after moderate to severe traumatic brain injury in children. Developmental Neuropsychology, 35, 318-332.
McDaniel, M.A., & Einstein, G.O. (1993). The importance of cue familiarity and cue
distinctiveness in prospective memory. Memory, 1, 23-41.
McDaniel, M.A., & Einstein, G.O. (2000). Strategic and automatic processes in prospective memory retrieval: A multiprocess framework. Applied Cognitive Psychology, 14, S127-S144.
McDaniel, M.A., & Einstein, G.O. (2007). Prospective memory: An overview and synthesis of an emerging field: Thousand Oaks, CA: Sage.
McDaniel, M.A., Einstein, G.O., & Rendell, P.G. (2008). The puzzle of inconsistent
age-related declines in prospective memory: A multiprocess explanation. In M.
200
PROSPECTIVE MEMORY: THE FUTURE FOR FUTURE INTENTIONS
Kliegel, M.A. McDaniel, & G.O. Einstein (Eds.), Prospective memory: Cognitive, neuroscience, developmental, and applied perspectives (pp. 141-160).
Mahwah, NJ: Erlbaum.
McDaniel, M.A., Guynn, M.J., Einstein, G.O., & Breneiser, J.E. (2004). Cue-focused
and reflexive-associative processes in prospective memory retrieval. Journal of
Experimental Psychology: Learning, Memory and Cognition, 30, 605-614.
McDaniel, M.A., Robinson-Riegler, B., & Einstein, G.O. (1998). Prospective remembering: Perceptually driven or conceptually driven processes? Memory and Cognition, 26, 121-134.
Meacham, J.A., & Leiman, B. (1975). Remembering to perform future actions. In U.
Neisser (Ed.), Memory observed: Remembering in natural contexts (pp. 327336). San Francisco: Freeman.
Meacham, J.A., & Leiman, B. (1982). Remembering to perform future actions. In R.C.
Atkinson, J. Freedman, G. Lindzey, & R.F. Thompson (Eds.), Memory
observed: Remembering in natural contexts (pp. 327-336). San Francisco, CA:
W.H. Freeman & Co.
Meacham, J.A., & Singer, J. (1977). Incentive effects in prospective remembering.
Journal of Psychology, 97, 191-197.
Morris, C.D., Bransford, J.D., & Franks, J.J. (1977). Levels of processing versus transfer appropriate processing. Journal of Verbal Learning and Verbal Behavior, 16,
519-533.
Moscovitch, M. (1982). A neuropsychological approach to memory and perception in
normal and pathological aging. In F.I.M. Craik & S. Trehub (Eds.), Aging and
cognitive processes (pp. 55-78). New York: Plenum Press.
Moscovitch, M. (1994). Memory and working with memory: Evaluation of a component process model and comparisons with other models. In D.L. Schacter & E.
Tulving (Eds.), Memory systems (pp. 269-310). Cambridge, MA: MIT Press.
Okuda, J., Fujii, T., Ohtake, H., Tsukiura, T., Yamadori, A., Frith, C.D., & Burgess,
P. (2007). Differential involvement of regions of rostral prefrontal cortex (Brodmann area 10) in time- and event-based prospective memory. International Journal of Psychophysiology, 64, 233-246.
Okuda, J., Gilbert, S.J., Burgess, P.W., Frith, C.D., & Simons, J.S. (2011). Looking to
the future: Automatic regulation of attention between current performance and
future plans. Neuropsychologia, 49, 2258-2271.
Okuda, J., Toshikatsu, F., Yamadori, A., Kawashima, R., Tsukiura, T., Fukatsu, R.,
Suzuki, K., Ito, M., & Fukuda, H. (1998). Participation of the prefrontal cortices
in prospective memory: Evidence from a PET study in humans. Neuroscience
Letters, 253, 127-130.
Palmer, H.M., & McDonald, S. (2000). The role of frontal and temporal lobe processes in prospective remembering. Brain and Cognition, 44, 103-107.
Park, D.C., Hertzog, C., Kidder, D.P., Morrell, R.W., & Mayhorn, C.B. (1997). Effect
of age on event-based and time-based prospective memory. Psychology and
Aging, 12, 314-327.
Patton, G.W.R., & Meit, M. (1993). Effect of aging on prospective and incidental
memory. Experimental Aging Research, 19, 165-176.
GIL GONEN-YAACOVI, & PAUL W. BURGESS
201
Poppenk, J., Moscovitch, M., McIntosh, A.R., Ozcelik, E., & Craik, F.I.M. (2010).
Encoding the future: Successful processing of intentions engages predictive
brain networks. NeuroImage, 49, 905-913.
Potvin, M.J., Rouleau, I., Audy, J., Charbonneau, S., & Giguère, J.F. (2011). Ecological prospective memory assessment in patients with traumatic brain injury.
Brain Injury, 25, 192-205.
Racsmany, M., Demeter, G., Csigo, K., Harsanyi, A., & Nemeth, A. (2011). An experimental study of prospective memory in obsessive-compulsive disorder. Journal
of Clinical and Experimental Neuropsychology, 33, 85-91.
Rajendran, G., Law, A.S., Logie, R.H., van der Meulen, M., Fraser, D., & Corley, M.
(2010). Investigating multitasking in high-functioning adolescents with autism
spectrum disorders using the virtual errands task. Journal of Autism and Developmental Disorders [Epub ahead of print].
Reese, C.M., & Cherry, K.E. (2002). The effects of age, ability, and memory monitoring on prospective memory task performance. Aging, Neuropsychology and
Cognition, 9, 98-113.
Rendell, P.G., & Craik, F.I.M. (2000). Virtual and actual week: Age-related differences in prospective memory. Applied Cognitive Psychology, 14, S43-S62.
Rendell, P.G., McDaniel, M.A., Forbes, R.D., & Einstein, G.O. (2007). Age-related
effects in prospective memory are modulated by ongoing task complexity and
relation to target cue. Aging, Neuropsychology and Cognition, 14, 236-256.
Rendell, P.G., & Thomson, D.M. (1993). The effect of ageing on remembering to
remember: An investigation of simulated medication regimens. Australian Journal of Ageing, 12, 11-18.
Rendell, P.G., & Thomson, D.M. (1999). Aging and prospective memory: Differences
between naturalistic and laboratory tasks. Journal of Gerontology: Psychological Sciences, 54B, P256-P269.
Reynolds, J.R., West, R., & Braver, T. (2009). Distinct neural circuits support transient and sustained processes in prospective memory and working memory. Cerebral Cortex, 19, 1208-1221.
Roche, N.L., Fleming, J.M., & Shum, D. (2002). Self-awareness of prospective memory failure in adults with traumatic brain injury. Brain Injury, 16, 931-945.
Schacter, D.L., Addis, D.R., & Buckner, R.L. (2007). Remembering the past to imagine the future: The prospective brain. Nature Review Neuroscience, 8, 657-661.
Schacter, D.L., Addis, D.R., & Buckner, R.L. (2008). Episodic simulation of future
events: Concepts, data, and applications. Annals of the New York Academy of
Sciences, 1124, 39-60.
Scullin, M.K., McDaniel, M.A., & Einstein, G.O. (2010). Control of cost in prospective memory: Evidence for spontaneous retrieval processes. Journal of Experimental Psychology: Learning, Memory and Cognition, 36, 190-203.
Scullin, M.K., McDaniel, M.A., Shelton, J.T., & Lee, J.H. (2010). Focal/nonfocal cue
effects in prospective memory: Monitoring difficulty or different retrieval processes. Journal of Experimental Psychology: Learning, Memory and Cognition,
36, 736-749.
Shallice, T., & Burgess, P.W. (1991). Deficits in strategy application following frontal
lobe damage in man. Brain, 114, 727-741.
202
PROSPECTIVE MEMORY: THE FUTURE FOR FUTURE INTENTIONS
Shum, D., Fleming, J., Gill, H., Gullo, M.J., & Strong, J. (2011). A randomized controlled trial of prospective memory rehabilitation in adults with traumatic brain
injury. Journal of Rehabilitation Medicine, 43, 216-223.
Shum, D., Levin, H., & Chan, R.C. (2011). Prospective memory in patients with
closed head injury: A review. Neuropsychologia, 49, 2156-2165.
Shum, D., Valentine, M., & Cutmore, T. (1999). Performance of individuals with
severe long-term traumatic brain injury on time-, event-, and activity-based prospective memory tasks. Journal of Clinical and Experimental Neuropsychology,
2, 49-58.
Simons, J.S., Schölvinck, M., Gilbert, S.J., Frith, C.D., & Burgess, P.W. (2006). Differential components of prospective memory? Evidence from fMRI. Neuropsychologia, 44, 1388-1397.
Smith, R.E. (2003). The cost of remembering to remember in event-based prospective
memory: Investigating the capacity demands of delayed intention performance.
Journal of Experimental Psychology: Learning, Memory and Cognition, 29,
347-361.
Smith, R.E. (2008). Connecting the past and future attention, memory and delay intentions. In M. Kliegel, M.A. McDaniel, & G.O. Einstein (Eds.), Prospective Memory: Cognitive, Neuroscience, Developmental and Applied Perspectives (pp. 4246). Mahwah, NJ: Erlbaum.
Smith, R.E. (2010). What costs do reveal and moving beyond the cost debate: Reply
to Einstein and McDaniel. Journal of Experimental Psychology: Learning Memory and Cognition, 36, 1089-1095.
Smith, R.E., & Bayen, U.J. (2004). A multinomial model of event based prospective
memory. Journal of Experimental Psychology: Learning, Memory and Cognition, 30, 756-777.
Smith, R.E., & Bayen, U.J. (2006). The source of age differences in event-based prospective memory: A multinomial modeling approach. Journal of Experimental
Psychology: Learning, Memory and Cognition, 32, 623-635.
Smith, R.E., Bayen, U.J., & Martin, C. (2010). The cognitive processes underlying
event-based prospective memory in school-age children and young adults: A formal model-based study. Developmental Psychology, 46, 230-244.
Smith, R.E., Hunt, R.R., McVay, J.C., & McConnell, M.D. (2007). The cost of eventbased prospective memory: Salient target events. Journal of Experimental Psychology: Learning, Memory and Cognition, 33, 734-746.
Szpunar, K.K., Watson, J.M., & McDermott, K.B. (2007). Neural substrates for envisioning the future. Proceeding of the National Academy of Science U.S.A., 104,
642-647.
Umeda, S., Kurosaki, Y., Terasawa, Y., Kato, M., & Miyahara, Y. (2011). Deficits in
prospective memory following damage to the prefrontal cortex. Neuropsychologia, 49, 2178-2184.
Vogels, W.A., Dekker, M.R., Brouwer, W.H., & de Jong, R. (2002). Age-related
changes in event-related prospective memory performance: A comparison of
four prospective memory tasks. Brain and Cognition, 49, 341-362.
GIL GONEN-YAACOVI, & PAUL W. BURGESS
203
Volle, E., Gonen-Yaacovi, G., de Lacy Costello, A., Gilbert, S.J., & Burgess, P.W.
(2011). The role of rostral prefrontal cortex in prospective memory: A voxelbased lesion study. Neuropsychologia, 49, 2185-2198.
Ward, H., Shum, D., McKinlay, L., Baker, S., & Wallace, G. (2007). Prospective
memory and pediatric traumatic brain injury: Effects of cognitive demands.
Child Neuropsychology, 13, 219-239.
Weiler, J.A., Suchan, B., & Daum, I (2010). When the future becomes the past: Differences in brain activation patterns for episodic memory and episodic future
thinking. Behavioural Brain Research, 212, 196-203.
West, R. (1988). Prospective memory and aging. In M.M. Gruneberg, P.E. Morris, &
R.N. Sykes (Eds.), Practical aspects of memory: Current research and issues
(Vol. 2, pp. 119-125). Chichester, U.K: Wiley.
West, R. (2007). The influence of strategic monitoring on the neural correlates of prospective memory. Memory and Cognition, 35, 1034-1046.
West, R. (2011). The temporal dynamics of prospective memory: a review of the ERP
and prospective memory literature. Neuropsychologia, 49, 2233-2245.
West, R., Bowry, R., & Krompinger, J. (2006). The effects of working memory
demands on the neural correlates of prospective memory. Neuropsychologia, 44,
197-207.
West, R., Carlson, L., & Cohen, A.L. (2007a). What the eyes can tell us about prospective memory. International Journal of Psychophysiology, 64, 269-277.
West, R., & Craik, F.I.M. (1999). Age-related decline in prospective memory: The
roles of cue accessibility and cue sensitivity. Psychology and Aging, 14, 264272.
West, R., & Craik, F.I.M. (2001). Influences on the efficiency of prospective memory
in younger and older adults. Psychology and Aging, 16, 682-696.
West, R., Herndon, R.W., & Covell, E. (2003). Neural correlates of age related
declines in the formation and realization of delayed intentions. Psychology and
Aging, 18, 461-473.
West, R., Herndon, R.W., & Crewdson, S.J. (2001). Neural activity associated with
the realization of a delayed intention. Cognitive Brain Research, 12, 1-10.
West, R., & Krompinger, J. (2005). Neural correlates of prospective and episodic
memory. Neuropsychologia, 43, 418-433.
West, R., Krompinger, J., & Bowry, R. (2005). Disruptions of preparatory attention
contribute to failures of prospective memory. Psychonomic Bulletin and Review,
12, 502-507.
West, R., McNerney, M.W., & Travers, S. (2007b). Gone but not forgotten: The
effects of cancelled intentions in the neural correlates of prospective memory.
International Journal of Psychophysiology, 64, 215-225.
West, R., & Ross-Munroe, K. (2002). Neural correlates of the formation and realization of delayed intentions. Cognitive, Affective and Behavioral Neuroscience, 2,
162-173.
West, R., & Wymbs, N. (2004). Is detecting prospective cues the same as selecting targets? An ERP study. Cognitive, Affective and Behavioral Neuroscience, 4, 354363.
204
PROSPECTIVE MEMORY: THE FUTURE FOR FUTURE INTENTIONS
West, R., Wymbs, N., Jakubek, K., & Herndon, R. (2003). Effects of intention load
and background context on prospective remembering: An event related brain
potential study. Psychophysiology, 40, 260-276.
Wilkins, A.J., & Baddeley, A.D. (1978). Remembering to recall in everyday life: An
approach to absentmindedness. In M. Gruneberg & R. Sykes (Eds.), Practical
aspects of memory (pp. 27-34). London: Academic Press.
Williams, J.M., Ellis, N.C., Tyers, C., Healy, H., Rose, G., & MacLeod, A.K. (1996).
The specificity of autobiographical memory and imageability of the future.
Memory and Cognition, 24, 116-125.
Zimmermann, T., & Meier, B. (2006). The rise and decline of prospective memory
across the lifespan. The Quarterly Journal of Experimental Psychology, 59,
2040-2046.
Zinke, K., Altgassen, M., Mackinlay, R., Rizzo, P., Drechsler, R., & Kliegel, M.
(2010). Time-based prospective memory performance and time-monitoring in
children with ADHD. Child Neuropsychology, 16, 338-349.
Zöllig, J., Martin, M., & Kliegel, M. (2010). Forming intentions successfully: Differential compensational mechanisms of adolescents and old adults. Cortex, 46,
575-589.
Received March 7, 2012
Revision received May 31, 2012
Accepted June 2, 2012
This article appeared in a journal published by Elsevier. The attached
copy is furnished to the author for internal non-commercial research
and education use, including for instruction at the authors institution
and sharing with colleagues.
Other uses, including reproduction and distribution, or selling or
licensing copies, or posting to personal, institutional or third party
websites are prohibited.
In most cases authors are permitted to post their version of the
article (e.g. in Word or Tex form) to their personal website or
institutional repository. Authors requiring further information
regarding Elsevier’s archiving and manuscript policies are
encouraged to visit:
http://www.elsevier.com/copyright
Author's personal copy
Neuropsychologia 49 (2011) 2246–2257
Contents lists available at ScienceDirect
Neuropsychologia
journal homepage: www.elsevier.com/locate/neuropsychologia
Functional neuroimaging studies of prospective memory:
What have we learnt so far?
Paul W. Burgess a,∗ , Gil Gonen-Yaacovi a , Emmanuelle Volle b
a
b
Institute of Cognitive Neuroscience - UCL (University College London), 17 Queen Square, London WC1N 3AR, UK
CR-ICM/UPMC/INSERM UMR-S 975, Pitié-Salpêtrière Hospital, 47 Boulevard de l’Hopital, 75013 Paris, France
a r t i c l e
i n f o
Article history:
Received 1 October 2010
Received in revised form 13 January 2011
Accepted 8 February 2011
Available online 15 February 2011
Keywords:
Prospective memory
Frontal lobes
Neuroimaging
Rostral prefrontal cortex
Brodmann Area 10
a b s t r a c t
The complexity of the behaviour described by the term “prospective memory” meant that it was not at all
clear, when the earliest studies were conducted, that this would prove a fruitful area for neuroimaging
study. However, a consistent relation rapidly emerged between activation in rostral prefrontal cortex
(approximating Brodmann Area 10) and performance of prospective memory paradigms. This consistency
has greatly increased the accumulation of findings, since each study has offered perspectives on the
previous ones. Considerable help too has come from broad agreement between functional neuroimaging
findings and those from other methods (e.g. human lesion studies, electrophysiology). The result has
been a quite startling degree of advance given the relatively few studies that have been conducted. These
findings are summarised, along with those from other brain regions, and new directions suggested. Key
points are that there is a medial–lateral dissociation within rostral PFC. Some (but not all) regions of
medial rostral PFC are typically more active during performance of the ongoing task only, and lateral
aspects are relatively more active during conditions involving delayed intentions. Some of these rostral
PFC activations seem remarkably insensitive to the form of stimulus material presented, the nature of
the ongoing task, the specifics of the intention, how easy or hard the PM cue is to detect, or the intended
action is to recall. However there are other regions within rostral PFC where haemodynamic changes
vary with alterations in these, and other, aspects of prospective memory paradigms. It is concluded
that rostral PFC most likely plays a super-ordinate role during many stages of creating, maintaining and
enacting delayed intentions, which in some cases may be linked to recent evidence showing that this
brain region is involved in the control of stimulus-oriented vs. stimulus-independent attending. Other key
brain regions activated during prospective memory paradigms appear to be the parietal lobe, especially
Brodmann Area (BA) 40 and precuneus (BA 7), and the anterior cingulate (BA 32). These regions are often
co-activated with lateral rostral PFC across a wide range of tasks, not just those involving prospective
memory.
© 2011 Published by Elsevier Ltd.
1. Introduction
Prospective memory is a very new field of enquiry, but one
in which there has been a startling increase of interest over the
last few years. As Sellen, Louie, Harris, and Wilkins (1997) point
out, a review approximately 20 years ago (Kvavilashvili, 1992)
cited only twenty-four experimental studies of prospective memory. Yet there are now several entire books devoted to the topic
(e.g. Brandimonte, Einstein, and McDaniel, 1996; Glicksohn &
Myslobodsky, 2006; Kliegel, McDaniel, & Einstein, 2007; McDaniel
& Einstein, 2007), and substantial international conferences occupied exclusively with research into prospective memory (the first
∗ Corresponding author.
E-mail addresses: [email protected], [email protected]
(P.W. Burgess).
0028-3932/$ – see front matter © 2011 Published by Elsevier Ltd.
doi:10.1016/j.neuropsychologia.2011.02.014
International Conference on Prospective Memory was held in Hertfordshire, UK, in July, 2000). This explosion of interest has been
accompanied by a change in the way that “prospective memory”
has been viewed.
The earliest studies, which were largely behavioural only,
tended to be concerned with the practical aspects of remembering intentions, often relating to everyday life situations, rather than
experimental paradigms (e.g. Wilkins & Baddeley, 1978). Accordingly, the emphasis was very much on the study of situational and
behavioural characteristics affecting delayed intentions. However
as the field became more experimental, and with the help of a few
key papers (e.g. Kvavilashvili, 1987) the notion grew that there
might be cognitive processes or constructs unique to this form of
memory (in the sense of not also being shared with memory for
past events). From the viewpoint of a scientist trying to discover
principles of behaviour, or of brain–behaviour relations, this would
be fortuitous, making discovery simpler. However from a biologi-
Author's personal copy
P.W. Burgess et al. / Neuropsychologia 49 (2011) 2246–2257
cal viewpoint, at the extreme at least, such an arrangement would
likely be exceptionally inefficient: prospective memory is a highly
complex and multi-componential behaviour so it is unlikely to have
representations and brain structures dedicated entirely to it. Such
a principle, carried across all cognitive functions would likely be
far too costly, so it is always more likely that at both an information processing and functional level that processes and structures
operate across psychological domains, or at least across our narrow
definitions of subject fields. In this way it was clear to many from
the outset that it would be implausible that the study of prospective memory would grow entirely independently from other fields
of conceptual relevance (for review see Ellis, 1996).
And so, in large part has it transpired. However, there has been a
particularly fortuitous finding for cognitive neuroscientists studying prospective memory: a consistent relation between activation
in rostral PFC during prospective memory paradigms. This has given
an invaluable inroad into a topic that at one time had little or
no precedent within cognitive neuroscience. Moreover, as more
information about this brain region from the study of other functions appears, the field is being encouraged to consider prospective
behaviour more broadly, with the potential to encompass not just
prospective memory, but many other forms of “prospection”.
2. Characteristics of typical prospective memory paradigms
There are a very wide variety of situations in everyday life that
require prospective memory. However, for experimental purposes
in cognitive neuroscience the essential features of these situations
have been simplified. The typical features of prospective memory paradigms are summarised by Burgess, Scott, and Frith (2003).
These are:
(a) There is an intention, or multiple intentions to carry out a mental or physical act. A variant might be that the intention is to
withhold an act that is performed routinely in a particular context.
(b) The intended act cannot be performed immediately after the
intention to do it has been created.
(c) The intended act (or thought) is to be performed in a particular circumstance. This is known as the “retrieval context”
(Ellis, Kvavilashvili, & Milne, 1999). In event-based studies, the
retrieval context is signalled by a cue (the “intention cue”, or
“PM target”). In time-based tasks this is either at a particular
time, or after a certain duration, and with activity-based PM
tasks this might be after or during a particular ongoing activity
or another task.
(d) The delay period between creating the intention and occurrence
of the appropriate time to act (the “retention interval”) is filled
with activity known as the “ongoing task”.
(e) Performance of the ongoing task prevents continuous, conscious rehearsal of the intention over the entire delay period.
Typically this is because the activity is too demanding of competing cognitive resources (e.g. attention), or the delay period
is too long. This is a feature which distinguishes a prospective memory paradigm from e.g. some “working memory” or
vigilance paradigms.
(f) The intention cue (or retrieval context) does not interfere with,
or directly interrupt, performance of the ongoing task. Intention
enactment is therefore self-initiated, and the participant has to
recognise the PM cue or retrieval context for themselves (e.g.
rather than receiving a clear interrupt or instruction from an
external source).
(g) In many situations involving prospective memory no immediate feedback is given to the participant regarding errors or other
aspects of their performance.
2247
This is not intended as an exhaustive characterisation. Variants
upon these general themes have been created by experimental psychologists, and many aspects are hotly debated. However, these
seven features, when occurring together in the same paradigm, are
likely to describe a task which most theorists would recognise as
engaging processes relevant to “prospective memory”.
2.1. Neuroimaging studies of prospective memory – a very brief
overview
There have not been a large number of neuroimaging prospective memory studies thus far. A determined reader could read them
all in a day although the assimilation of their implications and significance would likely take very much longer, even for someone
familiar with the behavioural literature. The first neuroimaging
study of prospective memory was published only a dozen or so
years ago (Okuda et al., 1998). So it is appropriate that we now ask
(a) what we have learnt from these early years of neuroimaging of
prospective memory, and (b) what the priorities might be for future
study.
Considering the first question, it is likely that historians of the
subject, perhaps turning their attentions to the growth of this field
many years hence, might conclude that we learnt much more from
the first dozen or so studies in the first dozen years than might ever
have seemed likely at the outset. This has been facilitated by the fortuitous scientific discovery mentioned above: a consistent relation,
first noted by Burgess, Quayle, and Frith, (2001) and Burgess et al.
(2003), between activation of rostral prefrontal cortices (approximating Brodmann Area 10) and the performance of prospective
memory tests. The reason why this finding has been so helpful is
that, at the time of the first three studies around the beginning of
this century (Burgess et al., 2001, 2003; Okuda et al., 1998), virtually
nothing was known about rostral PFC. This has probably managed
to throw the relation between PM and rostral PFC activations into
sharp relief.
Prior to the emergence of neuroimaging, this large brain region
(in fact the largest single cytoarchitectonic region of the prefrontal
cortex) was almost completely ignored by cognitive neuroscientists. Whilst even from the earliest days of neuroimaging, a relation
between retrospective memory and rostral PFC activations had been
noted (see Grady, 1999 for review), the translation of these findings
into an information processing account of the functions of rostral PFC had not been straightforward, resulting in broad post hoc
characterisations that were not easy to falsify. The central problem
was that whilst rostral PFC activations occurred consistently during episodic memory paradigms, they also occurred during many
other paradigms which appeared to have little or no episodic memory component. These could be simple conditioning paradigms, or
tasks involving semantic memory; language, visual perception, as
well as functions more often associated with the frontal lobes such
as attentional switching (see Burgess, Gilbert, & Dumontheil, 2007;
Burgess, Simons, Dumontheil, & Gilbert, 2005 for review). However,
other ideas about the contributions of rostral PFC to human cognition were just beginning to emerge (e.g. Christoff & Gabrieli, 2000;
Koechlin, Basso, Pietrini, Panzer, & Grafman, 1999). These experimental papers, which attempted to link rostral PFC activations
to particular cognitive operations (e.g. “branching”; the manipulation of self-generated information; see Burgess, Gilbert, et al., 2007
for review), provided some very useful information regarding the
type of paradigm that might provoke rostral PFC activations. The
findings (which have largely been replicated since) were also new
enough that the field was open to new possibilities (as indeed it very
much still is), and a small cadre of investigators worldwide began
looking more carefully at the range of tasks which were found to
have provoked haemodynamic changes in this large brain region.
Author's personal copy
2248
P.W. Burgess et al. / Neuropsychologia 49 (2011) 2246–2257
2.1.1. Where did the link between rostral PFC and prospective
memory originate?
Before the advent of functional neuroimaging as a technique,
Burgess and colleagues in London had been working on trying
to unravel a clinical mystery in neurology. This was that some
neurological patients who had suffered frontal lobe damage could
apparently present no abnormality of behaviour in the clinic
(including excellent performance on the range of tools favoured
by neuropsychologists at the time), yet suffer from some form
of severe behavioural disability in everyday life. This problem
manifested itself in many forms, one of which appeared to be a
problem with prospective memory: employers and family members would report tardiness, “absent-mindedness” and general
disorganisation (see Burgess, Alderman, Volle, Benoit, & Gilbert,
2009 for review). This phenomenon had been known for several
years (e.g. Mesulam, 1986) but the first formal quantification of
their problem was presented by Shallice and Burgess (1991). They
described three people, all of whom had suffered frontal lobe damage (including damage to rostral PFC) who showed this pattern of
normal or near-normal performance on traditional tests of neuropsychological function (including on tests of executive function
considered sensitive to frontal lobe lesions) but behavioural disorganisation in everyday life. There were also changes in social
behaviour. Other investigators had documented similar clinical
manifestations before (e.g. Eslinger & Damasio, 1985), however
what was different about the Shallice and Burgess (1991) study
was that new tests were developed to measure the scale of these
problems. These new measures required multitasking (i.e. switching tasks after a delay period; this distinguishes the activity from
dual- or multiple-task performance, where more than one task are
attempted simultaneously) and had a strong prospective memory component. Principally these PM components were what has
since become known as “activity-based” and “time-based” prospective memory (McDaniel & Einstein, 2007). Burgess and colleagues
noted the regular co-incidence of rostral PFC lesions and these
kinds of problems (e.g. Goldstein, Bernard, Fenwick, Burgess, &
McNeil, 1993; Burgess, Veitch, Costello, & Shallice, 2000; Burgess
& Shallice, 1997 for review). Evidence from these cases and others (e.g. Cockburn, 1995) supported the developing notion that (a)
the frontal lobes supported some form of processing critical for
prospective memory, and (b) at least some processing relevant to
remembering to do things in the future was not shared with systems involved in remembering things that have happened in the
past, or other potentially relevant functions such as dual- or taskswitching (e.g. Bisiacchi, Schiff, Ciccola, & Kliegel, 2009).
It was therefore in the context of these lesion studies that
Okuda’s et al. (1998) first neuroimaging study was viewed. Burgess
and colleagues had actually carried out a PET study of prospective
memory in 1996, and had found rostral PFC (BA 10) activations
in that study. Interpretation of the activations was however made
difficult by an aspect of the design (involving temporal order; see
below) and was not therefore submitted. But it meant that when
Okuda reported rostral PFC activations in his PM study, using a
quite different type of PM task, this finding, combined with the
evidence from lesion cases, made the possibility of a particularly
noteworthy link between rostral PFC and prospective memory
much more likely. It also made much more likely the possibility
that whatever the contribution made by rostral PFC structures to
the performance of prospective memory tasks, this contribution
was relatively insensitive to small changes in task format. In the history of the study of frontal lobe function, using whatever method,
it has been more usual to find that relatively small changes in task
format or instruction can have large effects upon the dependent
variable (see e.g. Gilbert, Gollwitzer, Cohen, Burgess, & Oettingen,
2009; Stuss et al., 2000). So the possibility that there might be some
“super-ordinate” processing supported by rostral PFC which was,
to varying degrees, involved in the performance of a wide class
of paradigms, was tantalizing. However, on the data available at
the time, it was at least as plausible that even if rostral PFC were
involved in PM in some way, there were many different sub-regions
which were involved in complex ways. In other words, different PM
paradigms may activate different regions within rostral PFC, with
no common “core” regions. This would have rendered the scientific
problem of linking structure and processing much less tractable.
For this reason, Burgess et al. (2001), inspired by the notion
of “cognitive conjunction” type designs used in other fields (Price
& Friston, 1997) used not one, but several PM tasks in the same
neuroimaging experiment, each with their own control. Four PM
tasks were used, all of which measured the cognitive components
of interest, but where other components were designed to differ
from task-to-task. The analysis then sought activations common
to all tasks, rather than those specific to any one, in an attempt to
discover activations that are true of the class of tasks.
This method produced quite a “clean” pattern of activation
results, presumably because task-specific activations tend not to
reach threshold in the analysis. For this reason, it has been used
many times since by the Burgess group in the investigation of rostral PFC function (e.g. Burgess et al., 2003; Dumontheil, Gilbert,
Frith, & Burgess, 2010; Gilbert, Frith, & Burgess, 2005; Simons,
Gilbert, Owen, Fletcher, & Burgess, 2005; Simons, Owen, Fletcher, &
Burgess, 2005; Simons, Schölvinck, Gilbert, Frith, & Burgess, 2006).
These results, which have since been broadly replicated, are shown
in Fig. 1 (see also Table 1). In event-based prospective memory
tasks, there tends to be increased activation of lateral aspects of
rostral PFC during periods where participants are maintaining an
intention, whether or not a PM cue or target is encountered, or
the intended action enacted. At the same time, compared with
performance of the ongoing tasks alone, there is a decrease in
haemodynamic signal (either BOLD or rCBF) in the most anterior
and medial aspects of rostral PFC. In other words, this region seems
more active when people are performing the ongoing task alone,
especially if they are doing so before any PM instruction has been
encountered.
This aspect of prospective memory paradigms is an important
one in determining the results of functional imaging paradigms:
participants find it difficult, once a PM instruction has been given,
to subsequently “forget” that instruction, even if they are explicitly told that it is no longer relevant. Therefore the most effective
contrast to reveal activations specific to maintaining a delayed
intention is between “uncontaminated” ongoing task performance
(i.e. performance of the ongoing task before any PM instruction has
ever been encountered) and the PM condition (e.g. Simons et al.,
2006). Unfortunately, such a design necessarily also introduces a
potential temporal order artefact which has to be accounted for
in some way in other aspects of the design. The issue of temporal
order effects is central to many aspects of the study of frontal lobe
“executive functions” (Burgess, 1997) and looks set to become a
substantial issue for the field both methodologically and theoretically (Okuda et al., 2011).
2.1.2. What have we learnt from neuroimaging studies of
prospective memory?
The basic findings concerning rostral PFC activations in prospective memory are given in Table 1. Those where replication has been
achieved have been given priority. No effort has been made to take
into account the quality of the individual studies; the classification
of “seemingly secure” or “promising” is made only on the number
of replications. Some of the findings are necessarily related to each
other. Let us consider these in turn.
The first general finding, that performance of prospective memory paradigms is accompanied by evidence of activation (by BOLD
signal changes or increases in regional cerebral blood flow (rCBF))
Author's personal copy
P.W. Burgess et al. / Neuropsychologia 49 (2011) 2246–2257
2249
Fig. 1. Relating findings from prospective memory to general patterns of rostral PFC haemodynamic changes in neuroimaging experiments. Panel 1 shows the standard
pattern of rostral PFC activation in neuroimaging studies of event-based prospective memory (see also Fig. 2). The left-hand brain slice shows lateral rostral PFC (BA 10) rCBF
increases when people are maintaining an intention (Burgess et al., 2001). The right-hand brain slice shows the medial rostral PFC region which typically shows concomitant
decreases, relative to ongoing task performance only (Burgess et al., 2003). Panel 2 shows the relation between activation patterns in rostral PFC and behavioural performance
across a wide range of quite different tasks (Gilbert, Spengler, Simons, Frith, & Burgess, 2006). Data is from 104 functional neuroimaging studies that reported activation
peaks in rostral prefrontal cortex (PFC), approximating Brodmann’s area 10, and also reported reaction times. The difference in RT between the condition that provoked
the rostral PFC activation and whatever contrast condition was used was related to the pattern of rostral PFC activation. Whatever the task, lateral activations tended to be
associated with contrasts where response times were slower in the experimental condition (red shaded regions). Medial activations were associated with contrasts where
RTs were, if anything, faster in experimental than control conditions (blue shaded regions). These show a resemblance to the patterns both of behaviour and activation shown
during prospective memory tasks (see panel 1). Panel 3. Regions of the brain that often co-activate with rostral PFC. This figure shows the results of a meta-analysis of 200
activation peaks within rostral PFC and 1712 co-activations outside rostral PFC drawn from 162 studies (Gilbert et al., 2010). The study investigated which parts of the brain
outside rostral PFC were activated concurrently with rostral PFC across a wide range of different cognitive tasks. Lateral rostral PFC coactivations (cool colours) were found
principally in dorsal anterior cingulate, dorsolateral PFC, anterior insula and lateral parietal cortex. Medial rostral PFC co-activations (warm colours) were found principally in
the posterior cingulate, posterior superior temporal sulcus and temporal pole. There are perhaps early suggestions in prospective memory functional neuroimaging studies
that the patterns of activation in this class of task may follow these broad principles.
in rostral PFC seems most secure. All studies of which we know
where the relevant comparison has been made in a straightforward manner (i.e. ongoing-only task performance vs. maintaining
an intention) have shown this result. An important caveat is that
only a small proportion of the possible types of PM paradigms have
been administered, and there is a predominance of event-based
tasks. However there is early evidence that time-based PM tasks
are also accompanied by rostral PFC activations (Okuda et al., 2007).
Author's personal copy
2250
P.W. Burgess et al. / Neuropsychologia 49 (2011) 2246–2257
Table 1
Principles of rostral PFC activation in prospective memory tasks: the story so far.
Seemingly secure findings
1. Performance of prospective memory paradigms, relative to the ongoing task alone, is typically accompanied by activations within rostral PFC (approximately, BA 10;
Burgess et al., 2001, 2003; den Ouden et al., 2005; Gilbert et al., 2009; Hashimoto et al., 2010; Haynes et al., 2007; Okuda et al., 1998, 2007; Poppenk et al., 2010;
Reynolds et al., 2009; Simons et al., 2006).
2. Activations during ongoing, or (most) control tasks in medial rostral PFC structures tend to be higher than during prospective memory conditions (Burgess et al., 2001,
2003; Hashimoto et al., 2010; Okuda et al., 2007; Simons et al., 2006).
3. Maintenance of an intention over a delay period where the participant is fully occupied with another task tends to be associated with activation in lateral aspects of
rostral PFC (Burgess et al., 2001, 2003; den Ouden et al., 2005; Gilbert et al., 2009; Okuda et al., 2011; Reynolds et al., 2009; Simons et al., 2006).
4. Some of these rostral PFC activations (either medial or lateral) seem remarkably insensitive (at least with event-based tasks) to the form of stimulus material
presented, the nature of the ongoing task, how easy or hard the PM cue is to detect, or the intended action is to recall (Burgess et al., 2001, 2003; Simons et al., 2006).
5. However for other regions within rostral PFC there does seem to be functional specialisation for different components, forms, and types of prospective memory. For
instance, activation in subsections of this region can be sensitive to changes in the nature of what is intended (Haynes et al., 2007); in target recognition vs. intention
retrieval demands (Simons et al., 2006); whether the task is time-based or event-based (Okuda et al., 2007); and the nature of the PM cueing procedure (spontaneous
vs. cued, Gilbert et al., 2009).
6. There is frequent activation of BA 7 & 40 (precuneus, parietal lobe), and often also the anterior cingulate (BA 32) during performance of PM tasks (Burgess et al., 2001;
den Ouden et al., 2005; Eschen et al., 2007; Gilbert et al., 2009; Hashimoto et al., 2010; Okuda et al., 1998, 2007, 2011; Poppenk et al., 2010; Reynolds et al., 2009;
Simons et al., 2006). Some of these regions are often co-activated with rostral PFC during many types of cognitive task, not just PM ones (Gilbert et al., 2010). But the
significance of these co-activations remains to be discovered.
Promising findings that could benefit from replication.
7. In event-based PM tasks, apparently small changes in task instruction can have a marked effect upon the patterns of activation in rostral PFC (Gilbert et al., 2009).
8. (Related to [5] above.) There is a difference in activations in rostral PFC according to whether the PM task is time- or event-based (Okuda et al., 2007).
9. (Related to [5] above.) In time-based tasks, activation patterns in rostral PFC may change according to whether a clock is available for the participant to use (Okuda
et al., 2007). This may be due to differences in clock-monitoring or time estimation caused by such manipulation.
10. Rostral PFC activations can be seen during PM tasks even when no targets are encountered (Burgess et al., 2001); it is enough that participants merely expect targets
(see also Martin et al., 2007).
11. There are regions of lateral rostral PFC (BA 10) which are activated during event-based PM tasks which are NOT also activated during working memory demands
(Reynolds et al., 2009).
12. Some activation patterns within PFC (including regions of medial and rostrolateral PFC) are so task-specific that one can use them to predict which intentions a
participant is considering (Haynes et al., 2007). However, activation in other rostral regions (with possibly a more anterior lateral location) is unrelated to the specifics
of the intention; instead, they are co-activated with more posterior regions within the brain which are (Gilbert, 2011).
13. Rostral PFC activations are not necessarily synonymous with “conscious thought” (Okuda et al., 2011; Hashimoto et al., 2010) since they can occur alongside
behavioural (and presumably therefore mental) changes (e.g. RT) of which the participant is unaware.
14. Some find lateral BA 10 sustained responses during PM conditions (Burgess et al., 2001; Reynolds et al., 2009, Table 1, p. 1215). However, others find lateral BA 10 to
be transiently associated with detection of PM targets (Gilbert et al., 2009, in Table 2, p. 911, explicitly discussed on p. 912). There is thus evidence for both sustained
and transient effects in lateral BA 10 during PM tasks. The reason for these differences between sustained or transient activations across studies is not currently well
understood, but seems a promising avenue for future study.
There is as yet, to our knowledge, no functional imaging study of
activity-based PM. This is an unfortunate lacuna given that so many
situations in everyday life involve this form of prospective memory.
Findings two and three might be considered together since there
is some evidence that at least in some prospective memory situations the medial and lateral aspects of rostral PFC may work
together as a system (Burgess et al., 2003). Considering first the
rostrolateral activations, the proposition that these are associated
in some way with maintaining a delayed intention seems most
congruent with other accounts of the role of lateral rostral PFC in
human cognition. For instance, Christoff and Gabrieli (2000) have
argued that this region is involved in “active processing, such as
evaluation, monitoring or manipulation, performed on internally
generated information” (p. 183). Koechlin et al. (1999) argue that
lateral rostral PFC “selectively maintains the human ability to hold
in mind goals while exploring and processing secondary goals” (p.
148). Most theorists would agree that many instances where someone is maintaining an intention over a delay period would require
these forms of processing.
A characterisation of the processing associated with the medial
rostral PFC haemodynamic change in PM paradigms is however
more controversial. Burgess, Dumontheil, et al. (2007), Burgess,
Gilbert, et al. (2007), Burgess et al. (2006) and Burgess, Simons,
et al. (2005) have argued that rostral PFC supports an attentional
system which biases the degree to which one either attends to
stimuli in the sensory environment (“stimulus-oriented attending”) or, by contrast, engages “stimulus-independent attending”,
i.e. “deep thought”, where one is momentarily disengaged from
interacting with the external world and involved with our own
thoughts. According to this “gateway hypothesis” of rostral PFC
function, activations in the most anterior medial aspects of rostral PFC are usually associated with “stimulus-oriented attending”,
which explains why activations in this region tend to be greater
during performance of the ongoing task (OG) only (compared with
a PM condition). A different characterisation of medial PFC activations is held by e.g. Mason et al. (2007) who maintain that they
may be indicative of mind-wandering (i.e. stimulus-independent
thought). However, both in PM studies and in studies of other functions, the most anterior medial rostral PFC activations that are
typically activated during the ongoing tasks of PM experiments
tend to be associated with quicker reaction times (see Fig. 1, panel
2), rather than slower ones as one might expect if participants were
engaging in mind-wandering. Further, it is not at all clear that the
default region which Mason et al. highlight is not a more caudal
medial one to the one implicated in OG task performance: the
caudal medial rostral PFC region appears to have different properties from the more anterior portion (Gilbert, Spengler, Simons,
Steele, et al., 2006). This issue requires further investigation (see
Gilbert, Dumontheil, Simons, Frith, & Burgess, 2007 for discussion).
However the findings from prospective memory paradigms, where
medial rostral PFC activations tend to occur in conditions where RTs
are generally faster (e.g. ongoing or baseline tasks) than in the PM
condition, is congruent with findings from other types of cognitive
task (Gilbert, Spengler, Simons, Frith, & Burgess, 2006). This is in
turn congruent with the findings from studies which directly compare stimulus-oriented with stimulus-independent attending (e.g.
Dumontheil et al., 2010; Gilbert et al., 2005; Gilbert, Simons, Frith,
& Burgess, 2006). So it is perhaps the easier possibility to accept.
More generally, these ways of thinking about the processing
demands of PM paradigms accept a “multiprocess”-type framework (McDaniel & Einstein, 2000). According to this view there
are at least two main routes to successful enacting of a delayed
intention. The first is, in everyday language, to “keep what you
have to do in the forefront of one’s mind”, in other words, to
Author's personal copy
P.W. Burgess et al. / Neuropsychologia 49 (2011) 2246–2257
rehearse the intention as much as feasible (given the ongoing task
demands), engaging in continual checking behaviours. This is often
described as “monitoring” (e.g. McDaniel & Einstein, 2007, p. 14)
or “preparatory processing” (Smith & Bayen, 2004) in the experimental psychology literature. Probably there are several different
forms of this preparatory attention or monitoring, and differences
in what is attended to (e.g. one’s thoughts or the environment, or
characteristics of the stimuli). This kind of cognition is quite effortful, so in typical experimental paradigms measuring event-based
PM (see e.g. Burgess et al., 2001), participants will sometimes try
to reduce or remove these demands of the task by strategically
reconfiguring the task demands. In other words, they decide at the
start of the task that what they are going to do is to ask themselves, of each new ongoing stimulus, first whether it is a PM target,
and then, if it is not, perform the ongoing task. This removes the
“wait” aspect from the typical “test-wait-test-exit” model of monitoring (Miller, Galanter, & Pribram, 1960), and perhaps instead most
closely relates of concepts of “strategy application” in the cognitive
neuroscience literature (e.g. Shallice & Burgess, 1991).
Second, there is the situation where a participant does not consciously and voluntarily rehearse the intention, and if asked, would
report that they had (momentarily at least) “forgotten” about the
PM requirement of the task, or “was not paying attention to” the
PM aspects of the task. In this situation participants can nevertheless respond accurately to at least some of the PM targets or
cues. They will typically report that somehow the target had “triggered” the PM instruction. This is often referred to as “spontaneous
retrieval” in the experimental psychology literature (e.g. Einstein
et al., 2005), although the degree to which these behaviours are
truly “spontaneous” is the focus of some debate. A related situation
is where people report spontaneously remembering, whilst performing the OG task, that “there was something else I had to do”,
thereby triggering a more vigilant attending state akin to the one
outlined above.
For those conducting neuroimaging experiments, the first situation raises the theoretical question of whether the construct
under question is different in any way from “working memory”
(see Marsh & Hicks, 1998 for discussion of working memory and
PM). For the second, there is the matter of whether the processes
involved are any different from those involved in retrospective
memory functions such as recognition (of the cue), and retrieval
(of the intended act). This matter particularly vexed theorists in
the early modern era of experimental psychology PM research,
as they struggled to decide whether “prospective memory” was
a construct or behaviour (Burgess, Gilbert, Okuda, & Simons, 2006).
However, most would now agree that if there were a prototype of
the situation and behaviour which constitutes “prospective memory”, it might be one which likely may contain different aspects of
all these behaviours, but that the construct validity of the paradigm
is most severely tested by the extreme form of strategy application
outlined, i.e. where a participant in effect reduces or removes the
retention interval by adopting the strategy of deliberately and consciously first checking if each ongoing stimulus is a PM target before
proceeding with the processing relevant to the ongoing task itself.
Instead, the most relevant data is that which indicates, through
matters such as errors, and/or changes in reaction times to the
ongoing tasks or “intention cost” that the (delayed) intended action
is, for some proportion of the time, not at the absolute forefront of
the participant’s mind – at least not consciously. It is a historical
curiosity that demonstrates the potential cross-talk between neuroimaging and experimental psychology studies that probably the
first published demonstration of the behavioural effect of maintaining an intention upon RT to ongoing trials (“intention cost”) was
reported as part of a functional neuroimaging study (Burgess et al.,
2001). Similar patterns have been reported in many behavioural
studies since (e.g. Marsh, Hicks, Cook, Hansen, & Pallos, 2003;
2251
Smith, 2003; see McDaniel & Einstein, 2007, pp. 21–24 for review)
as well as in neuroimaging ones (e.g. Simons et al., 2006). Within
time-based (compared with event-based) PM tasks, these aspects
relating to strategy use are probably easiest to investigate within a
paradigm where clock-checks can be utilised as additional evidence
(e.g. Einstein, McDaniel, Richardson, Guynn, & Cunfer, 1995; Okuda
et al., 2007). The issue of haemodynamic changes that accompany
the interaction between the demands of the ongoing task and the
monitoring and maintenance of intentions is one which might be
expected to be investigated soon.
2.1.3. Will neuroimaging studies ever provoke
information-processing theorizing about prospective memory?
It is doubtful that neuroimaging data can regularly contribute
much to the building of information processing-level models of
cognition. The role of neuroimaging data is principally to contribute
to the mapping of a priori information-processing models onto
brain systems and structures, or interpreting activation patterns in
terms of them. However, there may be occasions when that process
– relating activation patterns to cognitive models – may provoke
new ideas which might be later incorporated into models. This is
especially the case where behavioural data, rather than activation
patterns alone, are a critical part of the neuroimaging study.
A possible example of this comes from trying to understand
what it is that the medial rostral PFC activations in prospective memory indicate. Okuda et al. (2011) developed a PM task
where the intervals between prospective memory targets were
manipulated in a predictable alternating cycle of expanding and
contracting target intervals. “Expanding” means that the number of ongoing trials between PM targets was increasing, and
“contracting” means that the number of ongoing trials between
targets was decreasing. Okuda et al. found that the participants’
behaviour changed in accordance with these changing target intervals. Prospective memory performance (measured by responses to
PM targets) was faster and more accurate in the expanding target
interval phase, at the cost of less accurate and slower performance
on ongoing trials. But in the contracting phase the opposite pattern
was found: faster and better ongoing trial performance but poorer
PM performance.
A key aspect of Okuda et al.’s finding however was that although
the participants behaviour was significantly modulated by these
changing target intervals, they were completely unaware of them
– in the sense that when asked none of them reported being aware
of any pattern in target interval, or of any change in their behaviour.
Yet fMRI detected a trade-off effect in activations in the anterior
medial prefrontal cortices that mirrored the changes in participant behaviour. In other words, they found relative BOLD response
increases to the PM targets as well as deactivation to the ongoing trials in the expanding phase as compared with the contracting
phase. An opposite direction of trade-off was observed in the anterior cingulate cortex. These results show a clear case in which
attention between current task performance and future action
plans in prospective memory tasks is automatically regulated
without particular task instructions or strategic control processes
initiated by subjects.
These patterns of behaviour and BOLD signal changes are not
easy to explain according to a simple “monitoring or spontaneous retrieval” framework. The medial rostral PFC activations
are unlikely to reflect some form of deliberate, conscious “monitoring” or “working memory” operation, since participants were
unable to report their behaviour changes or the changes in target intervals. Similarly, the consistency of the relation between the
changes in target interval and PM performance argues against a
simple “spontaneous retrieval” account also, or at least, stretches
the credibility of the descriptor “spontaneous”, since it is entirely
predictable and seems to be cued by the experimental context and
Author's personal copy
2252
P.W. Burgess et al. / Neuropsychologia 49 (2011) 2246–2257
Fig. 2. Comparative MNI coordinates of previous published neuroimaging results of rostral prefrontal cortex activation during prospective memory paradigms. Maxima of
activation reported in these functional imaging studies are projected on a glass brain in the MNI space. For each study, all maxima falling within BA10 for each contrast using
prospective memory tasks are reported. For comparability, only those results relating to direct contrasts between the ongoing task and prospective memory conditions are
shown. In red: activation related to time-based prospective memory task, in blue: activation related to event-based prospective memory, in green: ongoing only tasks minus
prospective memory tasks.
not just the PM target. It seems possible instead that what has been
detected here may be the neural signature of a process which effects
automatic (i.e. unconscious) coordination of attentional resources
between ongoing task performance and a delayed intention. A natural question is whether this process is distinct from those involved
in conscious monitoring or (truly) “spontaneous” retrieval.
Those who take a very hard line on the utility of neuroimaging findings for theorizing at an information processing level may
argue that the information provided by Okuda et al. that relate to
BOLD signal changes add nothing to this theorizing. However, there
are two aspects of the Okuda et al. fMRI data that provide food for
thought. The first is the location of these activations in medial caudal rostral PFC that accompanied the behavioural changes. These
were probably not in the same section of medial PFC that often
yields relative activation increases during the ongoing task (e.g.
Burgess et al., 2003), being more caudal (there is a well-known
rostal-caudal functional and anatomical distinction in medial PFC,
see Gilbert, Spengler, Simons, Steele, et al., 2006). Second, there is
the opposite pattern of activation in the anterior cingulate. Both
these patterns invite speculation, and perhaps further behavioural
investigations, regarding the multicomponential nature of prospective memory.
2.1.4. Characterising the determinants of rostral PFC activations
Turning now to finding 4, this follows principally from the use
of “conjunction-type” designs by Burgess et al. (2001, 2003), and
is congruent with the current state of our knowledge about rostral PFC more generally (Burgess, Dumontheil, & Gilbert, 2007).
There seem to be some rostral PFC regions which support process-
ing which is at a level super-ordinate to the structural or semantic
characteristics of visually-presented stimuli. However, there may
be other rostral PFC sub-regions which are more sensitive to such
differences. This has not, to our knowledge, been systematically
investigated. The vast majority of PM neuroimaging studies have
used visually-presented material. A notable exception is Okuda
et al. (1998), and whilst this study did report rostral PFC involvement in similar regions to those reported in other studies that used
visually-presented material, without a within-subjects repeatedmeasures type design, the possibility must remain that there may
be functional specialisation within rostral PFC according to the sensory modality of input (visual, auditory, tactile, etc.). This is another
promising avenue for future study.
Finding 4 also emphasises that it seems, on current evidence,
that characteristics of tasks that substantially alter the difficulty of
the task are not those which appear most effective in provoking
changes in activation patterns in rostral PFC. However, as finding
5 emphasises, there are some characteristics of PM tasks where
the preliminary evidence might suggest a difference. One of these
relates to the time-event distinction (see Fig. 2), where at this early
stage of investigation one might wonder if the rostral PFC activations during PM conditions tend to be more medial than during
event-based conditions. There is certainly early evidence for a timeevent localisation distinction from human lesion evidence: Volle
et al. (2011) have recently demonstrated that lesions to the right
rostral PFC in humans can cause deficits in time-based PM tasks,
but not event-based ones. Clearly this may be a promising avenue
for future research. However there are many additional factors that
seem to affect rostral PFC activations during PM paradigms which
Author's personal copy
P.W. Burgess et al. / Neuropsychologia 49 (2011) 2246–2257
might also be investigated. Currently, these include: (a) variation in
implicit cues (e.g. whether they are matched to the target category
or matched to the action associated with the target, Hashimoto,
Umeda, & Kojima, 2010); (b) the nature of the intention itself (e.g.
Haynes et al., 2007 showed that it is possible to decode from activity
in medial and lateral prefrontal cortex which of two tasks participants had freely chosen to do); (c) the form of the instruction given:
Gilbert et al. (2009) found rostral PFC activation differences during
a PM task according to whether the task instruction was either ““if
the same letter is on both sides, then I can score 5 points” or “if
the same letter is on both sides, then I will press the middle button. These differences occurred even though all other aspects of
the paradigm were identical; (d) the characteristics of intention
retrieval: Simons et al. (2006) found the largest differences in rostral PFC activation patterns during a PM task occurred when the
action to be performed was more complex (e.g. “if the words appear
in the same case, count the total syllables, and press the left key if
≤4, and the right key if >4” vs. “press a different key if the words
are semantically related”).
Overall, the patterns of rostral PFC activations seem less closely
bound to the nature of the stimuli (e.g. whether they are words,
faces, shapes, numbers, what colour, size or other physical property they have, appear singly or in combination, etc.) than they
do to aspects which might affect the “stimulus-independent
thought” aspects of the paradigms, and/or attending behaviour
more broadly.
3. Findings in brain regions outside rostral PFC
Finding 6 concerns activations outside rostral PFC that are also
commonly found during PM tasks. A large proportion of them
seem to be (bearing in mind the current temporal limits of our
technology) co-activations with rostral PFC. In particular, there is
a strikingly consistent finding in current functional neuroimaging studies of activation within BA 7 & 40 (precuneus; parietal
lobe) in prospective memory studies. Activation within one, or
both of, these regions is almost as common as for activation
within rostral PFC (see e.g. Burgess et al., 2001; den Ouden, Frith,
Frith, & Blakemore, 2005; Eschen et al., 2007; Gilbert et al., 2009;
Hashimoto et al., 2010; Okuda, Gilbert, Burgess, Frith, & Simons,
2011; Poppenk, Moscovitch, McIntosh, Ozcelik, & Craik, 2010;
Reynolds, West, & Braver, 2009; Simons et al., 2006). Interestingly,
there may be agreement here with evidence from electrophysiological methods (e.g. West, Herndon, & Crewdson, 2001; for review see
McDaniel & Einstein, 2007, pp. 183–189). It is too early to speculate
upon the information processing significance of these activations.
But two related points can be made. First, activations in this broad
region can be seen at many stages of prospective memory tasks,
including e.g. encoding (Eschen et al., 2007) and during the maintenance/retrieval context phases. Second, it is likely that sub-regions
within BA 40 & 7 support different contributions to prospective
memory. For instance, Poppenk et al. (2010) found angular gyrus
(BA 7; MNI co-ordinates −39 69 48) activations for one condition
(hits > misses) but also BA 7 activations (superior parietal lobe, −3
−51 69 and −24 −63 60) in the opposite contrast (misses > hits).
Additionally, Hashimoto et al. (2010) found activations in the inferior parietal lobule (BA 40) that were higher in control conditions
than in those relating to the PM intentions. The foci of these activations were quite inferior (46 −28 22 (control > target); 53 −41 30
(control > action). But activation of a slightly more superior region
of BA 40 (inferior parietal lobule 55 −56 38) was found in a prospective memory block. Furthermore, Simons et al. (2006) found both
BA 40 inferior parietal lobe activations (45 −42 51) and a right
superior parietal focus (33 −57 51) in one of their contrasts (cue
identification > uncontaminated ongoing task) but bilateral pre-
2253
cuneus (BA 7); 3 −33 54; −3 −48 60) activation in the opposite
contrast. Indeed, they found activations in this broad region (BA
40/7) in a number of contrasts within the same experiment.
Another region often implicated in prospective memory experiments is the anterior cingulate cortex (ACC, BA 32; Hashimoto et al.,
2010; Okuda et al., 1998, 2007; Reynolds et al., 2009; Simons et al.,
2006). The relation here is less strong than for rostral PFC or parietal
regions, and as before, it is not yet possible to know the key aspects
of the PM situation which are associated with such activations. But
as with the rostro-parietal activations, it seems likely that in time
functional distinctions between different sub-regions within ACC
may be made. For instance, Okuda et al. (2011) report activations in
right ACC (BA 32; 18 39 −6) when participants made their response
to PM targets during phases when the interval between PM targets
was expanding (compared with when it was contracting), but activation within another section of ACC (BA 32; 15 9 39) in the opposite
contrast (contract > expand).
There is too little data on PM paradigms to be sure whether these
regions that are co-activated with rostral PFC during this class of
task obey the general principles we have established about functional co-activations. However, these results do suggest that they
might. Gilbert, Gonen-Yaacovi, Benoit, Volle, and Burgess (2010)
investigated whether distinct subregions within rostral prefrontal
cortex tend to co-activate with distinct sets of brain regions outside it, in a meta-analysis of 200 activation peaks within rostral PFC
and 1712 co-activations elsewhere. The data was taken from any
paradigm for which suitable data was available, so covered a very
wide range of types of cognitive paradigm, from the simplest to
the most complex. Gilbert et al. (2010) found that lateral rostral
PFC activations were especially frequently associated with coactivations in anterior cingulate, dorsolateral PFC, anterior insula
and lateral parietal cortex. Medial rostral PFC activations however
tended to be associated with co-activation in posterior cingulate,
posterior superior temporal sulcus and temporal pole. However, it
was an additional finding which is especially important in the current context: Gilbert et al. (2010) showed that associations between
brain regions inside and outside rostral PFC can be influenced by the
type of task being performed. The most striking example was that
whilst dorsolateral PFC, anterior cingulate and lateral parietal cortex tended to co-activate with lateral rostral PFC in most tasks, for
mentalizing tasks these regions tended to co-activate with medial
rostral PFC. As the PM neuroimaging literature grows, it will be
interesting to determine if PM tasks similarly provoke a distinguishing pattern of co-activations, or follow the broader principles
as apply for instance to retrospective memory paradigms.
4. Findings awaiting replication
Findings 7–14 (Table 1) relate either to single findings within
the field, or where there is substantial apparent difference in findings amongst studies, but where each finding seems nevertheless
secure. It is only on these grounds that the recommendation is made
that the findings should be replicated: this is not at all a comment
on the quality of the individual studies. In general, these demonstrations also might perhaps emphasise how it is that at least some
regions of rostral PFC seem to vary in their activity with demands
that change attending behaviour. This is especially important in
relation to the penultimate finding. As noted above, Okuda et al.
(2011) have shown that systematic changes in target frequency
can provoke both activation of some sub-regions of rostral PFC,
and significant behaviour changes. However the participant may
be completely unaware of the effect of these contingency changes
upon their behaviour or mental life (in the sense of being able to
provide any verbally report relating to them) (see also Hashimoto
et al., 2010). It might be quite wrong therefore to think of the rostral
Author's personal copy
2254
P.W. Burgess et al. / Neuropsychologia 49 (2011) 2246–2257
Fig. 3. Foci of activation within rostral PFC during studies of “prospection”, i.e. the act of considering or imagining future circumstances, incorporating “future thinking”.
Studies involving prospective memory are considered separately in Fig. 2 (see text for full inclusion and exclusion criteria).
PFC activations (especially the medial ones) always as signatures
of some conscious thought processes, as one might consider those
relating to e.g. “working memory”. Support, albeit tangential, is
given by Okuda et al. (1998), who noted that whilst several areas
activated during their prospective memory paradigm are also typically activated during working memory paradigms, the activations
they found in the left frontal pole (area 10) during PM conditions
are not typical of working memory paradigms (p. 130).
Martin et al.’s (2007) study is unique amongst the current
published studies since it is the first, and only, MEG study specifically addressing PM (note however that there are several previous
electrophysiological studies of PM, especially by Robert West and
colleagues). The authors found an early response (87 ms) within
posterior parietal cortex during PM conditions (compared with
retrospective memory or oddball conditions), plus hippocampal
activity of longer duration in the retrospective and prospective
memory conditions, relative to oddball. These findings are potentially very interesting, and the authors’ interpretations of them are
inviting. Naturally, however, since this is the only study of its kind,
replication would be of benefit.
The last point of Table 1 (finding 14), concerns the issue of
sustained and transient effects in rostral PFC. This is an important matter, and one which may aid greatly in linking activation
to information processing models of cognition. However there is
currently some discrepancy in the literature, which awaits explanation. Reynolds et al. (2009) find lateral BA 10 sustained responses
during PM conditions (Table 1, p. 1215), which is broadly congruent with previous lateral BA 10 patterns of activation (e.g. Burgess
et al., 2001). However, Gilbert et al. (2009) have clearly shown that
lateral BA 10 can also be transiently associated with detection of PM
targets (Table 2, p. 911, discussed on p. 912). There is thus evidence
for both sustained and transient effects in lateral BA 10 during PM
tasks. These findings, which seem secure in themselves yet invite
contrast, await explanation.
5. Conclusion: from prospective memory to future thinking
In recent years, investigators and theorists from various different disciplines (e.g. economics, cognitive neuroscience, psychology,
anthropology) have shown an interest in an emerging field. This
concerns itself with how people envisage future scenarios, and the
effect that doing so has upon behaviour both in the present and the
future. In general, it seems possible that the involvement of rostral PFC in prospective memory and also the many other forms of
behaviour which have to do with imagining the future will unite
this aspect of human behaviour into a new field, along the likes of
“prospection” or “future thinking” (Atance & O’Neill, 2001; Boyer,
2008). Apart from the (largely) rather experimentally constrained
paradigms from the cognitive neuroscience literature (see e.g. the
large body of work relating to Shallice and McCarthy’s Tower of London test (Shallice, 1982, see Burgess, Simons, Coates, & Channon,
2005 for review) there has been little attention given, until recently,
to investigation of how people plan for, and envisage future situations. However, in the last few years there have been exciting
developments on this front (Addis, Pan, Vu, Laiser, & Schacter, 2009;
Schacter, Addis, & Buckner, 2007, 2008; Spreng and Grady, 2010;
Szpunar, Watson, & McDermott, 2007; Weiler, Suchan, & Daum,
2010; Williams et al., 1996). And there is a meeting point between
studies of these cognitive phenomenon and prospective memory
not only in a conceptual sense, but also in the prominent findings of rostral PFC activation when people are imagining future
scenarios (e.g. Addis, Wong, & Schacter, 2007). Consider Fig. 3.
This shows the MNI coordinates of rostral PFC activation in published neuroimaging studies involving future thinking. The studies
Author's personal copy
P.W. Burgess et al. / Neuropsychologia 49 (2011) 2246–2257
were selected from a PubMed search as follows: the terms ((future
and intentions) OR “future intentions” OR (future and thinking) OR
(thinking and intentions) OR (thinking and intention) OR (prospective and thinking) OR “future events” OR “prospection”) AND (PET
OR fMRI OR neuroimaging) AND (“prefrontal” OR “PFC” OR “BA 10”
OR “frontal pole”) had to be cited in either the title or abstract.
The search was limited to studies of adults, published since 2000
in the English language. To this we added one paper identified in
the review by Schacter et al. (2008). Only those studies reporting
rostral prefrontal activation associated with future thinking were
included, and the prospective memory studies included in Fig. 2
were excluded.
The field of “future thinking” or, perhaps more elegantly,
“prospection” (also sometimes called “mental time travel”) is more
in its infancy than the study of prospective memory. In particular,
there have been far fewer behavioural studies, and relatively little theory development. So it would be premature to draw strong
conclusions from the patterns of activation shown in Fig. 3. Nevertheless, and with these caveats in mind, there are some tentative
suggestions that might be put forward.
The first is that rostral PFC activations appear to be extremely
common in studies of prospection. The search above yielded 20
studies. Seven of these were excluded: five of them did not involve
prospection, one study was not conducted on adults, and one was
already included in the analysis of prospective memory presented
here. Of the remaining thirteen studies, all but one reported activation in rostral PFC. So prima facie the link between activation in
rostral PFC and “prospection” (i.e. the act of considering or imagining future events) seems almost as secure as the link we find
with prospective memory. There is one exceptionally important
caveat, however. This is that, as mentioned above, rostral PFC activations can be found during a very wide variety of psychological
paradigm, from the very simplest (e.g. conditioning) to the very
most complicated (e.g. “fluid intelligence” problems”), and crossing
just about every cognitive domain, from vision, through language,
memory, executive functions and so forth (see Gilbert, Spengler,
Simons, Steele, et al., 2006). So whilst the apparent consistency
with which rostral PFC activations are seen in studies of prospection might seem impressive, before asserting a noteworthy link we
really need to demonstrate that this link is more secure than it is
for other mental phenomena not qualifying as “prospection”.
The second suggestion that might follow from the meta-analysis
of studies of prospection concerns the location of the foci of activation relative to those found in the prospective memory studies. At
casual glance, it would seem that a greater proportion of the activations during prospection paradigms are located towards the more
medial aspects of rostral PFC. However: (a) this is only a comparison
relative to the prospective memory studies; (b) there are also many
activations outside the regions that would generally be thought of
as medial rostral PFC (e.g. within approx. 20 mm of the midline); (c)
there are far too few studies currently available to draw any strong
conclusions about functional specialisation.
Ideally perhaps, distinguishing between the foci of activation
involved during performance of a particular cognitive capacity
would be tested using a direct within-subjects comparison. This
is exactly the kind of design that Benoit et al. (submitted for
publication) have attempted with prospective memory. Their study
aimed to see whether functional imaging data is consistent with
the idea that the “rostral PFC attentional gateway” is involved in
performance of prospective memory paradigms. The rostral PFC
attentional gateway is a hypothetical cognitive mechanism proposed by the “gateway hypothesis” of rostral PFC function (Burgess,
Dumontheil, et al., 2007; Burgess, Gilbert, et al., 2007; Burgess
et al., 2006; Burgess, Simons, et al., 2005). This asserts that a principal purpose of rostral PFC is to control differences in attending
between “stimulus-independent thought” (i.e. our inner mental
2255
life) and that involved in preferential attending to the external
world (“stimulus-oriented attending”). Benoit et al. (submitted for
publication) used a factorial design, crossing prospective memory
(PM vs. no-PM) with mode of attending (stimulus-oriented (SO) vs.
stimulus-independent (SI)), the latter of which has previously been
shown to activate rostral PFC (e.g. Gilbert et al., 2005). The purpose
of the experiment was to determine whether the foci of activations in PM were the same as those activated by SI/SO attention
changes. They found that parts of mrPFC were jointly recruited during (i) mere ongoing task activity versus additional engagement in
a PM task, and (ii) stimulus-oriented versus stimulus-independent
processing. This is congruent with the notion that some of the processes mediating PM performance can be characterised by relative
differences in these attentional modes as proposed by the gateway
hypothesis (Burgess et al., 2008, 2009). At the same time, the PM
contrast was consistently associated with more dorsal peak activation than the stimulus contrast, perhaps reflecting engagement
of additional processes. It would be interesting, and theoretically
noteworthy, to see similar methods applied to the mapping of rostral PFC activations during prospection vs. prospective memory.
More generally, at the present time it seems possible that the
currently larger topic of prospective memory may in the future
be viewed as a (very important) sub-class of the broader topic
of “prospection”. If this occurs, it will likely be driven to a substantial degree by this sort of interaction between theoretical and
functional neuroimaging investigations. Key to this is the very special role that rostral PFC (and other PFC structures) seem to play
in enabling people to engage in imaginative thought, aspects of
which are critical to creating intentions for future acts (prospective memory), and considering the potential consequences of them
(prospection).
References
Abraham, A., Schubotz, R. I., & von Cramon, D. Y. (2008). Thinking about the future
versus the past in personal and non-personal contexts. Brain Research, 1233,
106–119.
Addis, D. R., Pan, L., Vu, M. A., Laiser, N., & Schacter, D. L. (2009). Constructive episodic
simulation of the future and the past: Distinct subsystems of a core brain network mediate imagining and remembering. Neuropsychologia, 47, 2222–2238.
Addis, D. R., & Schacter, D. L. (2008). Constructive episodic simulation: Temporal distance and detail of past and future events modulate hippocampal engagement.
Hippocampus, 18, 227–237.
Addis, D. R., Wong, A. T., & Schacter, D. L. (2007). Remembering the past and imagining the future: Common and distinct neural substrates during event construction
and elaboration. Neuropsychologia, 45, 1363–1377.
Atance, C. M., & O’Neill, D. K. (2001). Episodic future thinking. Trends in Cognitive
Sciences, 5, 533–539.
Benoit, R. G., Gilbert, S. J., Frith, C.D. Burgess, P. W. Rostral prefrontal cortex and the
focus of attention in prospective memory, submitted for publication.
Bisiacchi, P. S., Schiff, S., Ciccola, A., & Kliegel, M. (2009). The role of dual-task and
task-switch in prospective memory: Behavioural data and neural correlates.
Neuropsychologia, 47(5), 1362–1373.
Botzung, A., Denkova, E., & Manning, L. (2008). Experiencing past and future personal
events: Functional neuroimaging evidence on the neural bases of mental time
travel. Brain and Cognition, 66, 202–212.
Boyer, P. (2008). Evolutionary economics of mental time travel? Trends in Cognitive
Sciences, 12, 219–224.
Brandimonte, M. A., Einstein, G. O., & McDaniel, M. A. (1996). Prospective memory:
Theory and applications. Hillsdale, NJ: Lawrence Erlbaum.
Burgess, P. W. (1997). Theory and methodology in executive function research. In
P. Rabbitt (Ed.), Theory and methodology of frontal and executive function (pp.
81–116). Hove, UK: Psychology Press.
Burgess, P. W., Alderman, N., Volle, E., Benoit, R. G., & Gilbert, S. J. (2009). Mesulam’s
frontal lobe mystery re-examined. Restorative Neurology and Neuroscience, 27,
493–506.
Burgess, P. W., Dumontheil, I., Gilbert, S. J., Okuda, J., Schölvinck, M. L., & Simons, J.
S. (2008). On the role of rostral prefrontal cortex (area 10) in prospective memory. In M. Kliegel, M. A. McDaniel, & G. O. Einstein (Eds.), Prospective memory:
Cognitive, neuroscience, developmental, and applied perspectives (pp. 235–260).
Mahwah: Erlbaum.
Burgess, P. W., Dumontheil, I., & Gilbert, S. J. (2007). The gateway hypothesis of
rostral prefrontal cortex (area 10) function. Trends in Cognitive Sciences, 11,
290–298.
Author's personal copy
2256
P.W. Burgess et al. / Neuropsychologia 49 (2011) 2246–2257
Burgess, P. W., Gilbert, S. J., & Dumontheil, I. (2007). Function and localization within
rostral prefrontal cortex (area 10). Philosophical Transactions of the Royal Society
of London B, 362, 887–899.
Burgess, P. W., Gilbert, S. J., Okuda, J., & Simons, J. S. (2006). Rostral prefrontal brain
regions (Area 10): A gateway between inner thought and the external world?
In W. Prinz, & N. Sebanz (Eds.), Disorders of volition (pp. 373–396). Cambridge,
MA: MIT Press.
Burgess, P. W., Simons, J. S., Dumontheil, I., & Gilbert, S. J. (2005). The gateway
hypothesis of rostral PFC Function. In J. Duncan, L. Phillips, & P. McLeod (Eds.),
Measuring the mind: Speed, control and age (pp. 215–246). Oxford University
Press.
Burgess, P. W., Simons, J. S., Coates, L. M., & Channon, S. (2005). The search for specific
planning processes. In G. Ward, & R. Morris (Eds.), The cognitive psychology of
planning (pp. 199–227). Hove, U.K: Psychology Press.
Burgess, P. W., Quayle, A., & Frith, C. D. (2001). Brain regions involved in prospective
memory as determined by positron emission tomography. Neuropsychologia, 39,
545–555.
Burgess, P. W., Scott, S. K., & Frith, C. D. (2003). The role of the rostral frontal cortex
(area 10) in prospective memory: A lateral versus medial dissociation. Neuropsychologia, 41, 906–918.
Burgess, P. W., & Shallice, T. (1997). The relationship between prospective and retrospective memory: Neuropsychological evidence. In M. A. Conway (Ed.), Cognitive
models of memory (pp. 247–272). Hove, UK: Taylor and Francis.
Burgess, P. W., Veitch, E., Costello, A., & Shallice, T. (2000). The cognitive and neuroanatomical correlates of multitasking. Neuropsychologia, 38,
848–863.
Christoff, K., & Gabrieli, J. D. E. (2000). The frontopolar cortex and human cognition: Evidence for a rostrocaudal hierarchical organization within the human
prefrontal cortex. Psychobiology, 28, 168–186.
Cockburn, J. (1995). Task interruption in prospective memory: A frontal lobe function? Cortex, 31(1), 87–97.
D’Argembeau, A., Stawarczyk, D., Majerus, S., Collette, F., Van der Linden, M., Feyers,
D., et al. (2010). The neural basis of personal goal processing when envisioning
future events. Journal of Cognitive Neuroscience, 22, 1701–1713.
D’Argembeau, A., Stawarczyk, D., Majerus, S., Collette, F., Van der Linden, M., &
Salmon, E. (2010). Modulation of medial prefrontal and inferior parietal cortices
when thinking about past, present, and future selves. Society for Neuroscience, 5,
187–200.
D’Argembeau, A., Xue, G., Lu, Z. L., Van der Linden, M., & Bechara, A. (2008). Neural
correlates of envisioning emotional events in the near and far future. Neuroimage, 40, 398–407.
Dumontheil, I., Gilbert, S. J., Frith, C. D., & Burgess, P. W. (2010). Recruitment of lateral
rostral prefrontal cortex in spontaneous and task-related thoughts. Quarterly
Journal of Experimental Psychology, 63, 1740–1756.
Einstein, G. O., McDaniel, M. A., Richardson, S. L., Guynn, M. J., & Cunfer, A. R. (1995).
Aging and prospective memory: Examining the influences of self-initiated
retrieval processes. Journal of Experimental Psychology, Learning, Memory, and
Cognition, 21, 996–1007.
Einstein, G. O., McDaniel, M. A., Thomas, R., Mayfeild, S., Shank, H., Morisette, N., et al.
(2005). Multiple processes in prospective memory retrieval: Factors determining monitoring versus spontaneous retrieval. Journal of Experimental Psychology:
General, 134(3), 327–342.
Ellis, J. (1996). Prospective memory or the realisation of delayed intentions: A conceptual framework for research. In M. A. Brandimonte, G. O. Einstein, & M.
A. McDaniel (Eds.), Prospective memory: Theory and applications. Hillsdale, NJ:
Lawrence Erlbaum.
Ellis, J., Kvavilashvili, L., & Milne, A. (1999). Experimental tests of prospective remembering: The influence of cue-event frequency on performance. British Journal of
Psychology, 90, 9–23.
Eschen, A., Freeman, J., Dietrich, T., Martin, M., Ellis, J., Martin, E., et al. (2007). Motor
brain regions are involved in the encoding of delayed intentions: A fMRI study.
International Journal of Psychophysiology, 64, 259–268.
Eslinger, P. J., & Damasio, A. R. (1985). Severe disturbance of higher cognition after
bilateral frontal lobe ablation: Patient E.V.R. Neurology, 35, 1731–1741.
Gilbert, S. J. (2011). Decoding the content of delayed intentions. Journal of Neuroscience, 31(8), 2888–2894.
Gilbert, S. J., Dumontheil, I., Simons, J. S., Frith, C. D., & Burgess, P. W. (2007). Comment on “Wandering minds: The default network and stimulus-independent
thought”. Science, 317(5834), 43.
Gilbert, S. J., Frith, C. D., & Burgess, P. W. (2005). Involvement of rostral prefrontal cortex in selection between stimulus-oriented and stimulus-independent thought.
European Journal of Neuroscience, 21, 1423–1431.
Gilbert, S. J., Gollwitzer, P. M., Cohen, A. L., Burgess, P. W., & Oettingen, G. (2009). Separable brain systems supporting cued versus self-initiated realization of delayed
intentions. Journal of Experimental Psychology Learning Memory and Cognition, 35,
905–915.
Gilbert, S. J., Gonen-Yaacovi, G., Benoit, R. G., Volle, E., & Burgess, P. W. (2010). Distinct
functional connectivity associated with lateral versus medial rostral prefrontal
cortex: A meta-analysis. NeuroImage, 53, 1359–1367.
Gilbert, S. J., Simons, J. S., Frith, C. D., & Burgess, P. W. (2006). Performance
related activity in medial rostral prefrontal cortex (Area 10) during low demand
tasks. Journal of Experimental Psychology: Human Perception and Performance, 32,
45–58.
Gilbert, S. J., Spengler, S., Simons, J. S., Frith, C. D., & Burgess, P. W. (2006). Differential
functions of lateral and medial rostral prefrontal cortex (area 10) revealed by
brain–behavior associations. Cerebral Cortex, 16, 1783–1789.
Gilbert, S. J., Spengler, S., Simons, J. S. S., Steele, J. D., Lawrie, S. M., Frith, C. D., et al.
(2006). Functional specialisation within rostral prefrontal cortex (area 10): A
meta-analysis. Journal of Cognitive Neuroscience, 18, 932–948.
Glicksohn, J., & Myslobodsky, M. S. (2006). Timing the future. The case for a time-based
prospective memory. NY: World Scientific Books.
Goldstein, L. H., Bernard, S., Fenwick, P., Burgess, P. W., & McNeil, J. E. (1993). Unilateral frontal lobotomy can produce strategy application disorder. Journal of
Neurology, Neurosurgery and Psychiatry, 56, 274–276.
Grady, C. L. (1999). Neuroimaging and activation of the frontal lobes. In B. L. Miller,
& J. L. Cummings (Eds.), The human frontal lobes: Function and disorders (pp.
196–230). New York: Guilford Press.
Hashimoto, T., Umeda, S., & Kojima, S. (2010). Neural substrates of implicit cueing
effect on prospective memory. NeuroImage [Epub ahead of print].
Haynes, J., Sakai, K., Rees, G., Gilbert, S., Frith, C., & Passingham, R. E. (2007). Reading
hidden intentions in the human brain. Current Biology, 17, 323–328.
Koechlin, E., Basso, G., Pietrini, P., Panzer, S., & Grafman, J. (1999). The role of the
anterior prefrontal cortex in human cognition. Nature, 399(6732), 148–151.
Kliegel, M., McDaniel, M. A., & Einstein, G. O. (2007). Prospective memory: Cognitive,
neuroscience, developmental and applied perspectives. Chichester, UK: Psychology
Press.
Kvavilashvili, L. (1987). Remembering intentions as a distinct form of memory.
British Journal of Psychology, 78, 507–518.
Kvavilashvili, L. (1992). Remembering intentions: A critical review of existing experimental paradigms. Applied Cognitive Psychology, 6, 507–524.
Marsh, R. L., & Hicks, J. L. (1998). Event-based prospective memory and executive control of working memory. Journal of Experimental Psychology: Learning,
Memory, and Cognition, 24(2), 336–349.
Marsh, R. L., Hicks, J. L., Cook, G. I., Hansen, J. S., & Pallos, A. L. (2003). Interference to ongoing activities covaries with the characteristics of an event-based
intention. Journal of Experimental Psychology: Learning, Memory and Cognition, 29,
861–870.
Martin, T., McDaniel, M. A., Guynn, M. J., Houck, J. M., Woodruff, C. C., Bish, J. P., et al.
(2007). Brain regions and their dynamics in prospective memory retrieval: A
MEG study. International Journal of Psychophysiology, 64, 247–258.
Mason, M. F., Norton, M. I., Van Horn, J. D., Wegner, D. M., Grafton, S. T., & Macrae,
C. N. (2007). Wandering minds: The default network and stimulus-independent
thought. Science, 315, 393–395.
McDaniel, M. A., & Einstein, G. O. (2000). Strategic and automatic processes in
prospective memory retrieval: A multiprocess framework. Applied Cognitive Psychology, 14, S127–S144.
McDaniel, M. A., & Einstein, G. O. (2007). Prospective memory: An overview and synthesis of an emerging field. London: Sage.
Mesulam, M. M. (1986). Frontal cortex and behavior. Annals of Neurology, 19,
320–325.
Miller, G. A., Galanter, E., & Pribram, K. H. (1960). Plans and the structure of behavior.
New York: Holt, Rinehart & Winston.
Okuda, J., Fujii, T., Ohtake, H., Tsukiura, T., Tanji, K., Suzuki, K., et al. (2003). Thinking
of the future and past: The roles of the frontal pole and the medial temporal
lobes. NeuroImage, 19, 1369–1380.
Okuda, J., Fujii, T., Ohtake, H., Tsukiura, T., Yamadori, A., Frith, C. D., et al. (2007).
Differential involvement of regions of rostral prefrontal cortex (Brodmann area
10) in time- and event-based prospective memory. International Journal of Psychophysiology, 64, 233–246.
Okuda, J., Fujii, T., Yamadori, A., Kawashima, R., Tsukiura, T., Fukatsu, R., et al. (1998).
Participation of the prefrontal cortices in prospective memory: Evidence from a
PET study in humans. Neuroscience Letters, 253, 127–130.
Okuda, J., Gilbert, S. J., Burgess, P. W., Frith, C. D., & Simons, J. S. (2011). Looking to
the future: Automatic regulation of attention between current performance and
future plans. Neuropsychologia, 49, 2258–2271.
den Ouden, H., Frith, U., Frith, C., & Blakemore, S. (2005). Thinking about intentions.
NeuroImage, 28, 787–796.
Poppenk, J., Moscovitch, M., McIntosh, A., Ozcelik, E., & Craik, F. (2010). Encoding the
future: Successful processing of intentions engages predictive brain networks.
NeuroImage, 49, 905–913.
Price, C. J., & Friston, K. J. (1997). Cognitive conjunction: A new approach to brain
activation experiments. NeuroImage, 5, 261–270.
Reynolds, J. R., West, R., & Braver, T. (2009). Distinct neural circuits support transient
and sustained processes in prospective memory and working memory. Cerebral
Cortex, 19, 1208–1221.
Schacter, D. L., Addis, D. R., & Buckner, R. L. (2007). Remembering the past to imagine
the future: The prospective brain. Nature Review Neuroscience, 8, 657–661.
Schacter, D. L., Addis, D. R., & Buckner, R. L. (2008). Episodic simulation of future
events: Concepts, data, and applications. Annals of the New York Academy of
Sciences, 1124, 39–60.
Sellen, A. J, Louie, G., Harris, J. E., & Wilkins, A. J. (1997). What brings intentions to
mind? An in situ study of prospective memory. Memory, 5, 483–507.
Shallice, T. (1982). Specific impairments in planning. Philosophical Transactions of the
Royal Society of London B, 298, 199–209.
Shallice, T., & Burgess, P. W. (1991). Deficits in strategy application following frontal
lobe damage in man. Brain, 114, 727–741.
Simons, J. S., Gilbert, S. J., Owen, A. M., Fletcher, P. C., & Burgess, P. W. (2005). Distinct
roles for lateral and medial anterior prefrontal cortex in contextual recollection.
Journal of Neurophysiology, 94, 813–820.
Simons, J. S., Owen, A. M., Fletcher, P. C., & Burgess, P. W. (2005). Anterior prefrontal cortex and the recollection of contextual information. Neuropsychologia,
43, 1774–1783.
Author's personal copy
P.W. Burgess et al. / Neuropsychologia 49 (2011) 2246–2257
Simons, J. S., Schölvinck, M., Gilbert, S. J., Frith, C. D., & Burgess, P. W. (2006). Differential components of prospective memory? Evidence from fMRI. Neuropsychologia,
44, 1388–1397.
Smith, R. E. (2003). The cost of remembering to remember in event-based
prospective memory: Investigating the capacity demands of delayed intention
performance. Journal of Experimental Psychology: Learning, Memory, and Cognition, 29, 347–361.
Smith, R. E., & Bayen, U. J. (2004). A multinomial model of event-based prospective
memory. Journal of Experimental Psychology: Learning, Memory, and Cognition,
30, 756–777.
Spreng, R. N., & Grady, C. L. (2010). Patterns of brain activity supporting autobiographical memory, prospection, and theory of mind, and their relationship to
the default mode network. Journal of Cognitive Neuroscience, 22, 1112–1123.
Stuss, D. T, Levine, B., Alexander, M. P., Hong, J., Palumbo, C., Hamer, L., et al. (2000).
Wisconsin card sorting test performance in patients with focal frontal and posterior brain damage: Effects of lesion location and test structure on separable
cognitive processes. Neuropsychologia, 38, 388–402.
Summerfield, J. J., Hassabis, D., & Maguire, E. A. (2010). Differential engagement of brain regions within a ‘core’ network during scene construction.
Neuropsychologia, 48, 1501–1509.
2257
Szpunar, K. K., Watson, J. M., & McDermott, K. B. (2007). Neural substrates for envisioning the future. Proceeding of the National Academy of Science of United States
of America, 104, 642–647.
Volle, E., Gonen-Yaacovi, G., Costello, A., De, L., Gilbert, S. J., & Burgess, P. W. (2011).
The role of rostral prefrontal cortex in prospective memory: A voxel-based lesion
study. Neuropsychologia, 49, 2185–2198.
Weiler, J. A., Suchan, B., & Daum, I. (2010). When the future becomes the past: Differences in brain activation patterns for episodic memory and episodic future
thinking. Behavioural Brain Research, 212, 196–203.
West, R., Herndon, R. W., & Crewdson, S. J. (2001). Neural activity associated with
the realisation of a delayed intention. Brain Research: Cognitive Brain Research,
12(1), 1–9.
Wilkins, A. J., & Baddeley, A. D. (1978). Remembering to recall in everyday life: An
approach to absentmindedness. In M. M. Gruneberg, P. E. Morris, & R. N. Sykes
(Eds.), Practical aspects of memory. London: Academic Press.
Williams, J. M., Ellis, N. C., Tyers, C., Healy, H., Rose, G., & MacLeod, A. K. (1996). The
specificity of autobiographical memory and imageability of the future. Memory
and Cognition, 24, 116–125.