Anterior prefrontal cortex: Insights into function from anatomy and neuroimaging

Nature Reviews Neuroscience

Volumn 5, Issue 3, 2004, Pages 184-194

  Ramnani, Narender ^a   Owen, Adrian M ^b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b MRC COGNITION AND BRAIN SCIENCES UNIT   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BEHAVIOR; BRAIN FUNCTION; BRAIN REGION; COGNITION; FUNCTIONAL ANATOMY; NEUROIMAGING; PREFRONTAL CORTEX; PRIMATE; PRIORITY JOURNAL; REVIEW; TASK PERFORMANCE;

PRIMATES;

EID: 1342289404     PISSN: 1471003X     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrn1343     Document Type: Review

References (106)

1. Brett, M., Johnsrude, I. S. & Owen, A. M. The problem of functional localization in the human brain. Nature Rev. Neurosci. 3, 243-249 (2002).
2. Goldman-Rakic, P. S. Working memory dysfunction in schizophrenia. J. Neuropsychiatry Clin. Neurosci. 6, 348-357 (1994).
3. Jonides, J. et al. Spatial working memory in humans as revealed by PET Nature 363, 623-625 (1993).
4. Courtney, S. M., Petit, L., Haxby, J. V. & Ungerleider, L. G. The role of prefrontal cortex in working memory: examining the contents of consciousness. Philos. Trans. R. Soc. Lond. B 353, 1819-1828 (1998).
5. Owen, A. M. The functional organization of working memory processes within human lateral frontal cortex: the contribution of functional neuroimaging. Eur. J. Neurosci. 9, 1329-1339 (1997).
6. Petrides, M. Frontal lobes and behaviour. Curr. Opin. Neurobiol. 4, 207-211 (1994).
7. Rowe, J. B., Toni, I., Josephs, O., Frackowiak, R. S. & Passingham, R. E. The prefrontal cortex: response selection or maintenance within working memory? Science 288, 1656-1660 (2000).
8. Bor, D., Duncan, J., Wiseman, R. J. & Owen, A. M. Encoding strategies dissociate prefrontal activity from working memory demand. Neuron 37, 361-367 (2003).
9. Fletcher, P. C., Shallice, T. & Dolan, R. J. The functional roles of prefrontal cortex in episodic memory. I. Encoding. Brain 121, 1239-1248 (1998).
10. Dobbins, I. G., Foley, H., Schacter, D. L. & Wagner, A. D. Executive control during episodic retrieval: multiple prefrontal processes subserve source memory. Neuron 35, 989-996 (2002).
11. Rugg, M. D. et al. Neural correlates of memory retrieval during recognition memory and cued recall. Neuroimage 8, 262-273 (1998).
12. Courtney, S. M., Ungedeider, L. G., Keil, K. & Haxby, J. V. Transient and sustained activity in a distributed neural system for human working memory. Nature 386, 608-611 (1997).
13. Dove, A., Pollmann, S., Schubert, T., Wiggins, C. J. & von Cramon, D. Y. Prefrontal cortex activation in task switching: an event-related fMRI study. Brain Res. Cogn. Brain Res. 9, 103-109 (2000).
14. Coois, R., Clark, L., Owen, A. M. & Robbins, T. W. Defining the neural mechanisms of probabilistic reversal learning using event-related functional magnetic resonance imaging. J. Neurosci. 22, 4563-4567 (2002).
15. Rushworth, M. F., Nixon, P. D., Eacott, M. J. & Passingham, R. E. Ventral prefrontal cortex is not essential for working memory. J. Neurosci. 17, 4829-4838 (1997).
16. Henson, R. N., Shallice, T. & Dolan, R. J. Right prefrontal cortex and episodic memory retrieval: a functional MRI test of the monitoring hypothesis. Brain 122, 1367-1381 (1999).
17. Wagner, A. D. et al. Building memories: remembering and forgetting of verbal experiences as predicted by brain activity. Science 281, 1188-1191 (1998).
18. Tataranni, P. A. et al. Neuroanatomical correlates of hunger and satiation in humans using positron emission tomography. Proc. Natl Acad. Sci. USA 96, 4569-4574 (1999).
19. Gottfried, J. A., O'Doherty, J. & Dolan, R. J. Appetitive and aversive olfactory learning in humans studied using event-related functional magnetic resonance imaging. J. Neurosci. 22, 10829-10837 (2002).
20. Rolls, E. T. The orbitofrontal cortex and reward. Cereb. Cortex 10, 284-294 (2000).
21. Rolls, E. T., Critchley, H. D., Browning, A. & Hernadi, I. The neurophysiology of taste and olfaction in primates, and umami flavor. Ann. NY Acad. Sci. 855, 426-437 (1998).
22. Tremblay, L. & Schultz, W. Relative reward preference in primate orbitofrontal cortex. Nature 398, 704-708 (1999).
23. Roberts, A. C. & Wallis, J. D. Inhibitory control and affective processing in the prefrontal cortex: neuropsychological studies in the common marmoset. Cereb. Cortex 10, 252-262 (2000).
24. Montague, P. R. & Bems, G. S. Neural economics and the biological substrates of valuation. Neuron 36, 265-284 (2002).
25. Elliott, R., Friston, K. J. & Dolan, R. J. Dissociable neural responses in human reward systems. J. Neurosci. 20, 6159-6165 (2000).
26. Dias, R., Robbins, T. W. & Roberts, A. C. Dissociation in prefrontal cortex of affective and attentional shifts. Nature 380, 69-72 (1996).
27. Duncan, J. & Owen, A. M. Common regions of the human frontal lobe recruited by diverse cognitive demands. Trends Neurosci. 23, 475-483 (2000).
28. Ongur, D., Ferry, A. T. & Price, J. L. Architectonic subdivision of the human orbital and medial prefrontal cortex. J. Comp. Neurol. 460, 425-449 (2003). This paper describes the cytoarchitecture of the medial and orbital PFC. The results are particularly striking because they indicate that BA 10 is larger than all other prefrontal areas in the human brain.
29. Semendeferi, K., Armstrong, E., Schleicher, A., Zilles, K. & van Hoesen, G. W. Prefrontal cortex in humans and apes: a comparative study of area 10. Am. J. Phys. Anthropol. 114, 224-241 (2001). This is the only anatomical study to comprehensively examine the comparative cytoarchitecture of BA 10 in the brains of several primate species, including humans.
30. Brodmann, K. Vergleichende Lokalisationlehre der Grosshimrinde in Ihren Prinzipien Dargestellt auf Grund des Zellenbaues (Barth, Leipzig, Germany, 1909).
31. Petrides, M. & Pandya, D. N. Comparative cytoarchitectonic analysis of the human and the macaque ventrolateral prefrontal cortex and corticocortical connection patterns in the monkey. Eur. J. Neurosci. 16, 291-310 (2002).
32. Jacobs, B. et al. Regionad dendritic and spine variation in human cerebral cortex: a quantitative golgi study. Cereb. Cortex 11, 558-571 (2001).
33. Passingham, R. E. The Frontal Lobes and Voluntary Action (Oxford Univ. Press, Oxford, 1995).
34. Petrides, M. & Pandya, D. N. Dorsolateral prefrontal cortex: comparative cytoarchitectonic analysis in the human and the macaque brain and corticocortical connection patterns. Eur. J. Neurosci. 11, 1011-1036 (1999).
35. McGuire, P. K., Bates, J. F. & Goldman-Rakic, P. S. Interhemispheric integration: I. Symmetry and convergence of the corticocortical connections of the left and the right principal sulcus (PS) and the left and the right supplementary motor area (SMA) in the rhesus monkey. Cereb. Cortex 1, 390-407 (1991).
36. Barbas, H. & Pandya, D. N. Architecture and intrinsic connections of the prefrontal cortex in the rhesus monkey. J. Comp. Neurol. 286, 353-375 (1989).
37. Bachevalier, J., Meunier, M., Lu, M. X. & Ungerleider, L. G. Thalamic and temporal cortex input to medial prefrontal cortex in rhesus monkeys. Exp. Brain Res. 115, 430-444 (1997).
38. Andersen, R. A., Asanuma, C. & Cowan, W. M. Callosal and prefrontal associational projecting cell populations in area 7A of the macaque monkey: a study using retrogradely transported fluorescent dyes. J. Comp. Neurol. 232, 443-455 (1985).
39. Moran, M. A., Mufson, E. J. & Mesulam, M. M. Neural inputs into the temporopolar cortex of the rhesus monkey. J. Comp. Neurol. 256, 88-103 (1987).
40. Amarai, D. G. & Price, J. L. Amygdalo-cortical projections in the monkey (Macaca fascicularis). J. Comp. Neurol. 230, 465-496 (1984).
41. Morecraft, R. J. & Van Hoesen, G. W. Frontal granular cortex input to the cingulate (M3), supplementary (M2) and primary (M1) motor cortices in the rhesus monkey. J. Comp. Neurol. 337, 669-689 (1993).
42. Arikuni, T., Sako, H. & Murata, A. Ipsilateral connections of the anterior cingulate cortex with the frontal and medial temporal cortices in the macaque monkey. Neurosci. Res. 21, 19-39 (1994).
43. Passingham, R. E., Stephan, K. E. & Kotter, R. The anatomical basis of functional localization in the cortex. Nature Rev. Neurosci. 3, 606-616 (2002).
44. Christoff, K. & Gabrieli, J. D. E. The frontopolar cortex and human cognition: evidence for a rostrocaudal heirarchical organisation within the human prefrontal cortex. Psychobiology 28, 168-186 (2000). In this comprehensive review of functional neuroimaging studies of reasoning and episodic memory, Christoff and Gabrieli set out their arguments that BA 10 might be specialized for the explicit processing of internal states.
45. Buckner, R. L., Raichle, M. E., Miezin, F. M. & Petersen, S. E. Functional anatomic studies of memory retrieval for auditory words and visual pictures. J. Neurosci. 16, 6219-6235 (1996).
46. Shallice, T. Specific impairments of planning. Philos. Trans. R Soc. Lond. B 298, 199-209 (1982).
47. Baker, S. C. et al. Neural systems engaged by planning: a PET study of the Tower of London task. Neuropsychologia 34, 515-526 (1996).
48. Owen, A. M., Downes, J. J., Sahakian, B. J., Polkey, C. E. & Robbins, T. W. Planning and spatial working memory following frontal lobe lesions in man. Neuropsychologia 28, 1021-1034 (1990).
49. Owen, A. M., Sahakian, B. J., Semple, J., Polkey, C. E. & Robbins, T. W. Visuo-spatial short-term recognition memory and learning after temporal lobe excisions, frontal lobe excisions or amygdalo-hippocampectomy in man. Neuropsychologia 33, 1-24 (1995).
50. Lee, A. C., Robbins, T. W. & Owen, A. M. Episodic memory meets working memory in the frontal lobe: functional neuroimaging studies of encoding and retrieval. Crit. Rev. Neurobiol. 14, 165-197 (2000).
51. Tulving, E. Elements of Episodic Memory (Clarendon, Oxford, 1983).
52. Cabeza, R. et al. Age-related differences in neural activity during memory encoding and retrieval a positron emission tomography study. J. Neurosci. 17, 391-400 (1997).
53. Duzel, E. et al. Task-related and item-related brain processes of memory retrieval. Proc. Natl Acad. Sci. USA 96, 1794-1799 (1999).
54. Kapur, S. et al. Functional role of the prefrontal cortex in retrieval of memories: a PET study. Neuroreport 6, 1880-1884 (1995).
55. Nyberg, L. et al. Functional brain maps of retrieval mode and recovery of episodic information. Neuroreport 7, 249-252 (1995).
56. Rugg, M. D., Schloerscheidt, A. M., Doyle, M. C., Cox, C. J. & Patching, G. R. Event-related potentials and the recollection of associative information. Brain Res. Cogn. Brain Res. 4, 297-304 (1996).
57. Wagner, A. D., Desmond, J. E., Glover, G. H. & Gabrieli, J. D. Prefrontal cortex and recognition memory. Functional-MRI evidence for context-dependent retrieval processes. Brain 121, 1985-2002 (1998).
58. Velanova, K. et al. Functional-anatomic correlates of sustained and transient processing components engaged during controlled retrieval. J. Neurosci. 23, 8460-8470 (2003).
59. Lepage, M., Ghaffar, O., Nyberg, L. & Tulving, E. Prefrontal cortex and episodic memory retrieval mode. Proc. Natl Acad. Sci. USA 97, 506-511 (2000).
60. MacLeod, A. K., Buckner, R. L., Miezin, F. M., Petersen, S. E. & Raichle, M. E. Right anterior prefrontal cortex activation during semantic monitoring and working memory. Neuroimage 7, 41-48 (1998).
61. Ranganath, C., Johnson, M. K. & D'Esposito, M. Left anterior prefrontal activation increases with demands to recall specific perceptual information. J. Neurosci. 20, RC108 (2000).
62. Ranganath, C. & Paller, K. A. Neural correlates of memory retrieval and evaluation. Brain Res. Cogn. Brain Res. 9, 209-222 (2000).
63. Raye, C. L., Johnson, M. K., Mitchell, K. J., Nolde, S. F. & D'Esposito, M. fMRI investigations of left and right prefrontal contributions to episodic remembering. Psychobiology 28, 197-206 (2000).
64. Ranganath, C. & Paller, K. A. Frontal brain activity during episodic and semantic retrieval: insights from event-related potentials. J. Cogn. Neurosci. 11, 598-609 (1999).
65. Ranganath, C. & Paller, K. A. Frontal brain potentials during recognition are modulated by requirements to retrieve perceptual detail. Neuron 22, 605-613 (1999).
66. Nolde, S. F., Johnson, M. K. & D'Esposito, M. Left prefrontal activation during episodic remembering: an event-related fMRI study Neuroreport 9, 3509-3514 (1998).
67. Nyberg, L. et al. General and specific brain regions involved in encoding and retrieval of events: what, where, and when. Proc. Natl Acad. Sci. USA 93, 11280-11285 (1996).
68. Janowsky, J. S., Shimamura, A. P. & Squire, L. R. Source memory impairment in patients with frontal lobe lesions. Neuropsychologia 27, 1043-1056 (1989).
69. Thaiss, L. & Petrides, M. Source versus content memory in patients with a unilateral frontal cortex or a temporal lobe excision. Brain 126, 1112-1126 (2003).
70. Burgess, P. W., Quayle, A. & Frith, C. D. Brain regions involved in prospective memory as determined by positron emission tomography Neuropsychologia 39, 545-555 (2001).
71. Burgess, P. W., Veitch, E., de Lacy Costello, A. & Shallice, T. The cognitive and neuroanatomical correlates of multitasking. Neuropsychologia 36, 848-863 (2000).
72. Okuda, J. et al. Participation of the prefrontal cortices in prospective memory: evidence from a PET study in humans. Neurosci. Lett. 253, 127-130 (1998).
73. Coull, J. T., Frith, C. D., Frackowiak, R. S. & Grasby, P. M. A fronto-parietal network for rapid visual information processing: a PET study of sustained attention and working memory. Neuropsychologia 34, 1085-1095 (1996).
74. Koechlin, E., Basso, G., Pietrini, P., Panzer, S. & Grafman, J. The role of the anterior prefrontal cortex in human cognition. Nature 399, 148-151 (1999). We have suggested that the aPFC is required for integrating the outcomes of two or more separate cognitive processes. It is necessary to test for super-additive effects in functional neuroimaging studies to demonstrate a relationship between such a process and brain activity. Reference 74 elegantly demonstrates a highly specific super-additive effect in the aPFC when subjects held in mind goals while at the same time they processed secondary goals.
75. Koechlin, E., Corrado, G., Pietrini, P. & Grafman, J. Dissociating the role of the medial and lateral anterior prefrontal cortex in human planning. Proc. Natl Acad. Sci. USA 97, 7651-7656 (2000).
76. Braver, T. S. & Bongiolatti, S. R. The role of frontopolar cortex in subgoal processing during working memory. Neuroimage 15, 523-536 (2002).
77. Owen, A. M., Doyon, J., Petrides, M. & Evans, A. C. Planning and spatial working memory: a positron emission tomography study in humans. Eur. J. Neurosci. 8, 353-364 (1996).
78. Pollmann, S., Weidner, R., Muller, H. J. & von Cramon, D. Y. A fronto-posterior network involved in visual dimension changes. J. Cogn. Neurosci. 12, 480-494 (2000).
79. Pollmann, S. Switching between dimensions, locations, and responses: the role of the left frontopolar cortex. Neuroimage 14, S118-124 (2001).
80. Owen, A. M., Roberts, A. C., Polkey, C. E., Sahakian, B. J. & Robbins, T. W. Extradimensional versus intradimensional set shifting performance following frontal lobe excisions, temporal lobe excisions or amygdalohippocampectomy in man. Neuropsychologia 29, 993-1006 (1991).
81. Owen, A. M. et al. Contrasting mechanisms of impaired attentional set-shifting in patients with frontal lobe damage or Parkinson's disease. Brain 116, 1159-1175 (1993).
82. Kroger, J. K. et al. Recruitment of anterior dorsolateral prefrontal cortex in human reasoning: a parametric study of relational complexity. Cereb. Cortex 12, 477-485 (2002).
83. Christoff, K. et al. Rostrolateral prefrontal cortex involvement in relational integration during reasoning. Neuroimage 14, 1136-1149 (2001).
84. Robin, N. & Holyoak, K. J. in The Cognitive Neurosciences (ed. Gazzaniga, M. S.) 987-997 (MIT Press, Cambridge, Massachusetts, 1995).
85. Raven, J. C. Standardization of progressive matrices. Br. J. Med. Psychol. 19, 137-170 (1938, 1941).
86. Carpenter, P. A., Just, M. A. & Shell, P. What one intelligence test measures: a theoretical account of the processing in the Raven Progressive Matrices Test. Psychol. Rev. 97, 404-431 (1990).
87. Waltz, J. A. et al. A system for relational reasoning in human prefrontal cortex. Psychol. Sci. 10, 119-125 (1999).
88. Duncan, J., Burgess, P. & Emslie, H. Ruid intelligence after frontal lobe lesions. Neuropsychologia 33, 261-288 (1995).
89. Ramnani, N. & Passingham, R.-E. Changes in the human brain during rhythm learning. J. Cogn. Neurosci. 13, 1-15 (2001).
90. Sakai, K., Ramnani, N. & Passingham, R. E. Learning of sequences of finger movements and timing: frontal lobe and action-oriented representation. J. Neurophysiol. 88, 2035-2046 (2002).
91. Rogers, R. D. et al. Choosing between small, likely rewards and large, unlikely rewards activates inferior and orbital prefrontal cortex. J. Neurosci. 19, 9029-9038 (1999).
92. Ramnani, N. & Miall, C. Instructed delay activity in the human prefrontal cortex is modulated by monetary reward expectation. Cereb. Cortex 13, 318-327 (2003).
93. Braver, T. S., Reynolds, J. R. & Donaldson, D. I. Neural mechanisms of transient and sustained cognitive control during task switching. Neuron 39, 713-726 (2003).
94. Ramnani, N. & Passingham, R. E. Changes in the human brain during rhythm learning. J. Cogn. Neurosci. 13, 952-966 (2001).
95. Zeki, S. & Shipp, S. The functional logic of cortical connections. Nature 335, 311-317 (1988).
96. Ungerleider, L. G. & Mishkin, M. in Analysis of Visual Behavior (ed. Mansfield, R. J. W.) 549-586 (MIT Press, Cambridge, Massachusetts, 1982).
97. Haxby, J. V. et al. Dissociation of object and spatial visual processing pathways in human extrastriate cortex. Proc. Natl Acad. Sci. USA 88, 1621-1625 (1991).
98. Ettlinger, G. 'Object vision' and 'spatial vision': the neuropsychological evidence for the distinction. Cortex 26, 319-341 (1990).
99. Passingham, R. E. & Toni, I. Contrasting the dorsal and ventral visual systems: guidance of movement versus decision making. Neuroimage 14, S125-131 (2001).
100. Nobre, A. C., Coull, J. T., Frith, C. D. & Mesulam, M. M. Orbitofrontal cortex is activated during breaches of expectation in tasks of visual attention. Nature Neurosci. 2, 11-12 (1999)
101. Schultz, W., Tremblay, L. & Hollerman, J. R. Reward processing in primate orbitofrontal cortex and basal ganglia. Cereb. Cortex 10, 272-284 (2000).
102. Lu, T., Preston J. B. & Strick P. L. Interconnections between the prefrontal cortex and the premotor areas in the frontal lobe. J. Comp. Neurol. 341, 375-392 (1994).
103. Hadland, K. A., Rushworth, M. F., Passingham, R. E., Jahanshahi, M. & Rothwell, J. C. Interference with performance of a response selection task that has no working memory component: an rTMS comparison of the dorsolateral prefrontal and medial frontal cortex. J. Cogn. Neurosci. 13, 1097-1108 (2001).
104. Ramnani, N., Toni, I., Passingham, R. E. & Haggard, P. The cerebellum and parietal cortex play a specific role in coordination: a PET study. Neuroimage 14, 899-911 (2001).
105. Sarkissov, S. A., Filimonoff, I. N., Kononowa, E. P., Preopraschenskaja, I. S. & Kukuew, L. A. Atlas of the Cytoarchitectonics of the Human Cerebral Cortex (Medgiz, Moscow, 1955).
106. Petrides, M. & Pandya, D. N. in Handbook of Neuropsychology, Vol. 9 (ed. Grafman, J.) 17-58 (Elsevier, Amsterdam, 1994).