Abstract
The ability to generalize behaviour-guiding principles and concepts from experience is key to intelligent, goal-directed behaviour. It allows us to deal efficiently with a complex world and to adapt readily to novel situations. We review evidence that the prefrontal cortex-the cortical area that reaches its greatest elaboration in primates-plays a central part in acquiring and representing this information. The prefrontal cortex receives highly processed information from all major forebrain systems, and neurophysiological studies suggest that it synthesizes this into representations of learned task contingencies, concepts and task rules. In short, the prefrontal cortex seems to underlie our internal representations of the 'rules of the game'. This may provide the necessary foundation for the complex behaviour of primates, in whom this structure is most elaborate.
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Selected References
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- Asaad W. F., Rainer G., Miller E. K. Neural activity in the primate prefrontal cortex during associative learning. Neuron. 1998 Dec;21(6):1399–1407. doi: 10.1016/s0896-6273(00)80658-3. [DOI] [PubMed] [Google Scholar]
- Asaad W. F., Rainer G., Miller E. K. Task-specific neural activity in the primate prefrontal cortex. J Neurophysiol. 2000 Jul;84(1):451–459. doi: 10.1152/jn.2000.84.1.451. [DOI] [PubMed] [Google Scholar]
- Baddeley A., Della Sala S. Working memory and executive control. Philos Trans R Soc Lond B Biol Sci. 1996 Oct 29;351(1346):1397–1404. doi: 10.1098/rstb.1996.0123. [DOI] [PubMed] [Google Scholar]
- Beymer D., Poggio T. Image representations for visual learning. Science. 1996 Jun 28;272(5270):1905–1909. doi: 10.1126/science.272.5270.1905. [DOI] [PubMed] [Google Scholar]
- Bichot N. P., Schall J. D. Effects of similarity and history on neural mechanisms of visual selection. Nat Neurosci. 1999 Jun;2(6):549–554. doi: 10.1038/9205. [DOI] [PubMed] [Google Scholar]
- Bichot N. P., Schall J. D., Thompson K. G. Visual feature selectivity in frontal eye fields induced by experience in mature macaques. Nature. 1996 Jun 20;381(6584):697–699. doi: 10.1038/381697a0. [DOI] [PubMed] [Google Scholar]
- Cohen J. D., Servan-Schreiber D. Context, cortex, and dopamine: a connectionist approach to behavior and biology in schizophrenia. Psychol Rev. 1992 Jan;99(1):45–77. doi: 10.1037/0033-295x.99.1.45. [DOI] [PubMed] [Google Scholar]
- Desimone R., Albright T. D., Gross C. G., Bruce C. Stimulus-selective properties of inferior temporal neurons in the macaque. J Neurosci. 1984 Aug;4(8):2051–2062. doi: 10.1523/JNEUROSCI.04-08-02051.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Desimone R., Duncan J. Neural mechanisms of selective visual attention. Annu Rev Neurosci. 1995;18:193–222. doi: 10.1146/annurev.ne.18.030195.001205. [DOI] [PubMed] [Google Scholar]
- Dias R., Robbins T. W., Roberts A. C. Primate analogue of the Wisconsin Card Sorting Test: effects of excitotoxic lesions of the prefrontal cortex in the marmoset. Behav Neurosci. 1996 Oct;110(5):872–886. doi: 10.1037//0735-7044.110.5.872. [DOI] [PubMed] [Google Scholar]
- Duncan J., Emslie H., Williams P., Johnson R., Freer C. Intelligence and the frontal lobe: the organization of goal-directed behavior. Cogn Psychol. 1996 Jun;30(3):257–303. doi: 10.1006/cogp.1996.0008. [DOI] [PubMed] [Google Scholar]
- Eacott M. J., Gaffan David. Inferotemporal-frontal Disconnection: The Uncinate Fascicle and Visual Associative Learning in Monkeys. Eur J Neurosci. 1992;4(12):1320–1332. doi: 10.1111/j.1460-9568.1992.tb00157.x. [DOI] [PubMed] [Google Scholar]
- Fabre-Thorpe M., Richard G., Thorpe S. J. Rapid categorization of natural images by rhesus monkeys. Neuroreport. 1998 Jan 26;9(2):303–308. doi: 10.1097/00001756-199801260-00023. [DOI] [PubMed] [Google Scholar]
- Freedman D. J., Riesenhuber M., Poggio T., Miller E. K. Categorical representation of visual stimuli in the primate prefrontal cortex. Science. 2001 Jan 12;291(5502):312–316. doi: 10.1126/science.291.5502.312. [DOI] [PubMed] [Google Scholar]
- Fuster J. M., Bodner M., Kroger J. K. Cross-modal and cross-temporal association in neurons of frontal cortex. Nature. 2000 May 18;405(6784):347–351. doi: 10.1038/35012613. [DOI] [PubMed] [Google Scholar]
- Fuster J. M. The prefrontal cortex, mediator of cross-temporal contingencies. Hum Neurobiol. 1985;4(3):169–179. [PubMed] [Google Scholar]
- Gaffan D., Harrison S. Auditory-visual associations, hemispheric specialization and temporal-frontal interaction in the rhesus monkey. Brain. 1991 Oct;114(Pt 5):2133–2144. doi: 10.1093/brain/114.5.2133. [DOI] [PubMed] [Google Scholar]
- Gaffan D., Harrison S. Inferotemporal-frontal disconnection and fornix transection in visuomotor conditional learning by monkeys. Behav Brain Res. 1988 Dec 1;31(2):149–163. doi: 10.1016/0166-4328(88)90018-6. [DOI] [PubMed] [Google Scholar]
- Gainotti G. What the locus of brain lesion tells us about the nature of the cognitive defect underlying category-specific disorders: a review. Cortex. 2000 Sep;36(4):539–559. doi: 10.1016/s0010-9452(08)70537-9. [DOI] [PubMed] [Google Scholar]
- Hoshi E., Shima K., Tanji J. Task-dependent selectivity of movement-related neuronal activity in the primate prefrontal cortex. J Neurophysiol. 1998 Dec;80(6):3392–3397. doi: 10.1152/jn.1998.80.6.3392. [DOI] [PubMed] [Google Scholar]
- Miller E. K., Cohen J. D. An integrative theory of prefrontal cortex function. Annu Rev Neurosci. 2001;24:167–202. doi: 10.1146/annurev.neuro.24.1.167. [DOI] [PubMed] [Google Scholar]
- Miller E. K. The prefrontal cortex: complex neural properties for complex behavior. Neuron. 1999 Jan;22(1):15–17. doi: 10.1016/s0896-6273(00)80673-x. [DOI] [PubMed] [Google Scholar]
- Mishkin M. A memory system in the monkey. Philos Trans R Soc Lond B Biol Sci. 1982 Jun 25;298(1089):83–95. doi: 10.1098/rstb.1982.0074. [DOI] [PubMed] [Google Scholar]
- Murray E. A., Bussey T. J., Wise S. P. Role of prefrontal cortex in a network for arbitrary visuomotor mapping. Exp Brain Res. 2000 Jul;133(1):114–129. doi: 10.1007/s002210000406. [DOI] [PubMed] [Google Scholar]
- Nauta W. J. The problem of the frontal lobe: a reinterpretation. J Psychiatr Res. 1971 Aug;8(3):167–187. doi: 10.1016/0022-3956(71)90017-3. [DOI] [PubMed] [Google Scholar]
- Orlov T., Yakovlev V., Hochstein S., Zohary E. Macaque monkeys categorize images by their ordinal number. Nature. 2000 Mar 2;404(6773):77–80. doi: 10.1038/35003571. [DOI] [PubMed] [Google Scholar]
- Parker A., Gaffan D. Memory after frontal/temporal disconnection in monkeys: conditional and non-conditional tasks, unilateral and bilateral frontal lesions. Neuropsychologia. 1998 Mar;36(3):259–271. doi: 10.1016/s0028-3932(97)00112-7. [DOI] [PubMed] [Google Scholar]
- Petrides M. Deficits in non-spatial conditional associative learning after periarcuate lesions in the monkey. Behav Brain Res. 1985 Aug;16(2-3):95–101. doi: 10.1016/0166-4328(85)90085-3. [DOI] [PubMed] [Google Scholar]
- Petrides M. Deficits on conditional associative-learning tasks after frontal- and temporal-lobe lesions in man. Neuropsychologia. 1985;23(5):601–614. doi: 10.1016/0028-3932(85)90062-4. [DOI] [PubMed] [Google Scholar]
- Petrides M. Nonspatial conditional learning impaired in patients with unilateral frontal but not unilateral temporal lobe excisions. Neuropsychologia. 1990;28(2):137–149. doi: 10.1016/0028-3932(90)90096-7. [DOI] [PubMed] [Google Scholar]
- Rainer G., Asaad W. F., Miller E. K. Selective representation of relevant information by neurons in the primate prefrontal cortex. Nature. 1998 Jun 11;393(6685):577–579. doi: 10.1038/31235. [DOI] [PubMed] [Google Scholar]
- Rainer G., Rao S. C., Miller E. K. Prospective coding for objects in primate prefrontal cortex. J Neurosci. 1999 Jul 1;19(13):5493–5505. doi: 10.1523/JNEUROSCI.19-13-05493.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rao S. C., Rainer G., Miller E. K. Integration of what and where in the primate prefrontal cortex. Science. 1997 May 2;276(5313):821–824. doi: 10.1126/science.276.5313.821. [DOI] [PubMed] [Google Scholar]
- Schultz W., Dayan P., Montague P. R. A neural substrate of prediction and reward. Science. 1997 Mar 14;275(5306):1593–1599. doi: 10.1126/science.275.5306.1593. [DOI] [PubMed] [Google Scholar]
- Schultz W., Dickinson A. Neuronal coding of prediction errors. Annu Rev Neurosci. 2000;23:473–500. doi: 10.1146/annurev.neuro.23.1.473. [DOI] [PubMed] [Google Scholar]
- Shallice T., Burgess P. W. Deficits in strategy application following frontal lobe damage in man. Brain. 1991 Apr;114(Pt 2):727–741. doi: 10.1093/brain/114.2.727. [DOI] [PubMed] [Google Scholar]
- Tanaka K., Saito H., Fukada Y., Moriya M. Coding visual images of objects in the inferotemporal cortex of the macaque monkey. J Neurophysiol. 1991 Jul;66(1):170–189. doi: 10.1152/jn.1991.66.1.170. [DOI] [PubMed] [Google Scholar]
- Tomita H., Ohbayashi M., Nakahara K., Hasegawa I., Miyashita Y. Top-down signal from prefrontal cortex in executive control of memory retrieval. Nature. 1999 Oct 14;401(6754):699–703. doi: 10.1038/44372. [DOI] [PubMed] [Google Scholar]
- Vaadia E., Benson D. A., Hienz R. D., Goldstein M. H., Jr Unit study of monkey frontal cortex: active localization of auditory and of visual stimuli. J Neurophysiol. 1986 Oct;56(4):934–952. doi: 10.1152/jn.1986.56.4.934. [DOI] [PubMed] [Google Scholar]
- Vogels R. Categorization of complex visual images by rhesus monkeys. Part 1: behavioural study. Eur J Neurosci. 1999 Apr;11(4):1223–1238. doi: 10.1046/j.1460-9568.1999.00530.x. [DOI] [PubMed] [Google Scholar]
- Vogels R. Categorization of complex visual images by rhesus monkeys. Part 2: single-cell study. Eur J Neurosci. 1999 Apr;11(4):1239–1255. doi: 10.1046/j.1460-9568.1999.00531.x. [DOI] [PubMed] [Google Scholar]
- Wallis J. D., Anderson K. C., Miller E. K. Single neurons in prefrontal cortex encode abstract rules. Nature. 2001 Jun 21;411(6840):953–956. doi: 10.1038/35082081. [DOI] [PubMed] [Google Scholar]
- Watanabe M. Frontal units of the monkey coding the associative significance of visual and auditory stimuli. Exp Brain Res. 1992;89(2):233–247. doi: 10.1007/BF00228241. [DOI] [PubMed] [Google Scholar]
- Watanabe M. Prefrontal unit activity during associative learning in the monkey. Exp Brain Res. 1990;80(2):296–309. doi: 10.1007/BF00228157. [DOI] [PubMed] [Google Scholar]
- White I. M., Wise S. P. Rule-dependent neuronal activity in the prefrontal cortex. Exp Brain Res. 1999 Jun;126(3):315–335. doi: 10.1007/s002210050740. [DOI] [PubMed] [Google Scholar]
- Wise S. P., Murray E. A., Gerfen C. R. The frontal cortex-basal ganglia system in primates. Crit Rev Neurobiol. 1996;10(3-4):317–356. doi: 10.1615/critrevneurobiol.v10.i3-4.30. [DOI] [PubMed] [Google Scholar]
- Wyttenbach R. A., May M. L., Hoy R. R. Categorical perception of sound frequency by crickets. Science. 1996 Sep 13;273(5281):1542–1544. doi: 10.1126/science.273.5281.1542. [DOI] [PubMed] [Google Scholar]
- Young M. E., Wasserman E. A. Entropy detection by pigeons: response to mixed visual displays after same-different discrimination training. J Exp Psychol Anim Behav Process. 1997 Apr;23(2):157–170. doi: 10.1037//0097-7403.23.2.157. [DOI] [PubMed] [Google Scholar]