Functional localization within the prefrontal cortex: missing the forest for the trees?

Anatomical and functional studies of the prefrontal cortex (PFC) have identified multiple PFC subregions. We argue that the PFC is involved in cognitive functions exceeding the sum of specific functions attributed to its subregions. These can be revealed either by lesions of the whole PFC, or more specifically by selective disconnection of the PFC from certain types of information (for example, visual) allowing the investigation of PFC function in toto. Recent studies in macaque monkeys using the latter approach lead to a second conclusion: that the PFC, as a whole, could be fundamentally specialized for representing events that are extended in time. The representation of temporally complex events might underlie PFC involvement in general intelligence, decision-making, and executive function.

[1]  Steven P. Wise,et al.  Forward frontal fields: phylogeny and fundamental function , 2008, Trends in Neurosciences.

[2]  S. Carmichael,et al.  Connectional networks within the orbital and medial prefrontal cortex of macaque monkeys , 1996 .

[3]  Amanda Parker,et al.  Crossed unilateral lesions of medial forebrain bundle and either inferior temporal or frontal cortex impair object recognition memory in Rhesus monkeys , 2001, Behavioural Brain Research.

[4]  E. Murray,et al.  Prospective memory in the formation of learning sets by rhesus monkeys (Macaca mulatta). , 2006, Journal of experimental psychology. Animal behavior processes.

[5]  A. Walker,et al.  A cytoarchitectural study of the prefrontal area of the macaque monkey , 1940 .

[6]  J. Duncan,et al.  Common regions of the human frontal lobe recruited by diverse cognitive demands , 2000, Trends in Neurosciences.

[7]  P. Goldman-Rakic Cellular basis of working memory , 1995, Neuron.

[8]  J. Price,et al.  Architectonic subdivision of the orbital and medial prefrontal cortex in the macaque monkey , 1994, The Journal of comparative neurology.

[9]  K. Pribram,et al.  Analysis of the effects of frontal lesions in monkey. I. Variations of delayed alternation. , 1955, Journal of comparative and physiological psychology.

[10]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

[11]  Y. Miyashita,et al.  Functional MRI of Macaque Monkeys Performing a Cognitive Set-Shifting Task , 2002, Science.

[12]  D. Gaffan,et al.  Crossed unilateral lesions of the medial forebrain bundle and either inferior temporal or frontal cortex impair object–reward association learning in Rhesus monkeys , 2001, Neuropsychologia.

[13]  Anthony D. Wagner,et al.  Neural Priming in Human Frontal Cortex: Multiple Forms of Learning Reduce Demands on the Prefrontal Executive System , 2009, Journal of Cognitive Neuroscience.

[14]  M. Mishkin,et al.  Perseverative interference in monkeys following selective lesions of the inferior prefrontal convexity , 1970, Experimental Brain Research.

[15]  A. Baddeley The psychology of memory , 1976 .

[16]  B. Milner Effects of Different Brain Lesions on Card Sorting: The Role of the Frontal Lobes , 1963 .

[17]  D. Pandya,et al.  The cerebrocerebellar system. , 1997, International review of neurobiology.

[18]  A. Collins The Psychology of Memory. , 2001 .

[19]  D. Gaffan Associative and perceptual learning and the concept of memory systems. , 1996, Brain research. Cognitive brain research.

[20]  M. Mishkin,et al.  Non-spatial memory after selective prefrontal lesions in monkeys , 1978, Brain Research.

[21]  T. Powell,et al.  An anatomical study of converging sensory pathways within the cerebral cortex of the monkey. , 1970, Brain : a journal of neurology.

[22]  Amanda Parker,et al.  Memory after frontal/temporal disconnection in monkeys: conditional and non-conditional tasks, unilateral and bilateral frontal lesions , 1998, Neuropsychologia.

[23]  Richard N A Henson,et al.  The Scale of Functional Specialization within Human Prefrontal Cortex , 2010, The Journal of Neuroscience.

[24]  E. Rolls,et al.  Emotion-related learning in patients with social and emotional changes associated with frontal lobe damage. , 1994, Journal of neurology, neurosurgery, and psychiatry.

[25]  A. Dickinson,et al.  Mediated Generalization in Discrimination Learning by Rhesus Monkeys , 2008, Quarterly journal of experimental psychology.

[26]  Anna S. Mitchell,et al.  Neurotoxic lesions of ventrolateral prefrontal cortex impair object-in-place scene memory , 2007, The European journal of neuroscience.

[27]  David Gaffan,et al.  Dorsolateral prefrontal lesions do not impair tests of scene learning and decision-making that require frontal–temporal interaction , 2008, The European journal of neuroscience.

[28]  H. Barbas,et al.  Topographically specific hippocampal projections target functionally distinct prefrontal areas in the rhesus monkey , 1995, Hippocampus.

[29]  S C Rao,et al.  Integration of what and where in the primate prefrontal cortex. , 1997, Science.

[30]  H. Spinnler The prefrontal cortex, Anatomy, physiology, and neuropsychology of the frontal lobe, J.M. Fuster. Raven Press, New York (1980), IX-222 pages , 1981 .

[31]  D. Pandya,et al.  Architecture and intrinsic connections of the prefrontal cortex in the rhesus monkey , 1989, The Journal of comparative neurology.

[32]  David Gaffan,et al.  The role of prefrontal cortex in object‐in‐place learning in monkeys , 2005, The European journal of neuroscience.

[33]  Charles M. Butter,et al.  Perseveration in extinction and in discrimination reversal tasks following selective frontal ablations in Macaca mulatta , 1969 .

[34]  J. M. Warren,et al.  THE FRONTAL GRANULAR CORTEX AND BEHAVIOR , 1964 .

[35]  D. Gaffan Scene-Specific Memory for Objects: A Model of Episodic Memory Impairment in Monkeys with Fornix Transection , 1994, Journal of Cognitive Neuroscience.

[36]  Mortimer Mishkin,et al.  Visual recognition impairment follows ventromedial but not dorsolateral prefrontal lesions in monkeys , 1986, Behavioural Brain Research.

[37]  M. Farah,et al.  Different underlying impairments in decision-making following ventromedial and dorsolateral frontal lobe damage in humans. , 2004, Cerebral cortex.

[38]  David Gaffan,et al.  Frontal-temporal disconnection abolishes object discrimination learning set in macaque monkeys. , 2006, Cerebral cortex.

[39]  P. Goldman-Rakic,et al.  Dissociation of object and spatial processing domains in primate prefrontal cortex. , 1993, Science.

[40]  J. Fuster The Prefrontal Cortex , 1997 .

[41]  Kuniyoshi L Sakai,et al.  Specialization in the Left Prefrontal Cortex for Sentence Comprehension , 2002, Neuron.

[42]  Jonathan D. Cohen,et al.  Prefrontal cortex and dynamic categorization tasks: representational organization and neuromodulatory control. , 2002, Cerebral cortex.

[43]  D. Gaffan,et al.  Interaction of frontal and perirhinal cortices in visual object recognition memory in monkeys , 1998, The European journal of neuroscience.

[44]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[45]  D. Gaffan,et al.  Dense amnesia in the monkey after transection of fornix, amygdala and anterior temporal stem , 2001, Neuropsychologia.

[46]  D. Gaffan,et al.  Interaction of Inferior Temporal Cortex with Frontal Cortex and Basal Forebrain: Double Dissociation in Strategy Implementation and Associative Learning , 2002, The Journal of Neuroscience.

[47]  K. Pribram,et al.  Analysis of the effects of frontal lesions in monkey. II. Variations of delayed response. , 1956, Journal of comparative and physiological psychology.

[48]  Philip G. F. Browning,et al.  Dissociable Components of Rule-Guided Behavior Depend on Distinct Medial and Prefrontal Regions , 2009, Science.

[49]  David Gaffan,et al.  Against memory systems. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[50]  M. Mishkin,et al.  OCCIPITOTEMPORAL CORTICOCORTICAL CONNECTIONS IN THE RHESUS MONKEY. , 1965, Experimental neurology.

[51]  Anna S. Mitchell,et al.  Orbital Prefrontal Cortex Is Required for Object-in-Place Scene Memory But Not Performance of a Strategy Implementation Task , 2007, The Journal of Neuroscience.

[52]  G. Ettlinger Visual discrimination following successive temporal ablations in monkeys. , 1959, Brain : a journal of neurology.

[53]  A. Benton,et al.  Frontal Lobe Function and Dysfunction , 1991 .

[54]  K. Brodmann Vergleichende Lokalisationslehre der Großhirnrinde : in ihren Prinzipien dargestellt auf Grund des Zellenbaues , 1985 .

[55]  Charles R. E. Wilson,et al.  Prefrontal–Inferotemporal Interaction Is Not Always Necessary for Reversal Learning , 2008, The Journal of Neuroscience.

[56]  Jeansok J Kim,et al.  Multiple brain-memory systems: the whole does not equal the sum of its parts , 2001, Trends in Neurosciences.

[57]  D. Pandya,et al.  Comparative cytoarchitectonic analysis of the human and the macaque ventrolateral prefrontal cortex and corticocortical connection patterns in the monkey , 2002, The European journal of neuroscience.

[58]  T. Bussey,et al.  Interaction of ventral and orbital prefrontal cortex with inferotemporal cortex in conditional visuomotor learning. , 2002, Behavioral neuroscience.

[59]  P. Goldman-Rakic,et al.  Prefrontal connections of medial motor areas in the rhesus monkey , 1993, The Journal of comparative neurology.

[60]  M. Petrides Lateral prefrontal cortex: architectonic and functional organization , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[61]  G. J. Romanes,et al.  The Neocortex of Macaca mulatta , 1948 .

[62]  T. Robbins,et al.  Inhibition and the right inferior frontal cortex , 2004, Trends in Cognitive Sciences.

[63]  D. Pandya,et al.  Dorsolateral prefrontal cortex: comparative cytoarchitectonic analysis in the human and the macaque brain and corticocortical connection patterns , 1999, The European journal of neuroscience.

[64]  Y. Miyashita,et al.  Common inhibitory mechanism in human inferior prefrontal cortex revealed by event-related functional MRI. , 1999, Brain : a journal of neurology.

[65]  M. Walton,et al.  Separate neural pathways process different decision costs , 2006, Nature Neuroscience.

[66]  J. Duncan An adaptive coding model of neural function in prefrontal cortex , 2001 .

[67]  Newell,et al.  A neural basis for general intelligence , 2000, American journal of ophthalmology.

[68]  T. Robbins,et al.  Differential effects of insular and ventromedial prefrontal cortex lesions on risky decision-making , 2008, Brain : a journal of neurology.

[69]  Philip G. F. Browning,et al.  Prefrontal Cortex Function in the Representation of Temporally Complex Events , 2008, The Journal of Neuroscience.

[70]  M. D’Esposito,et al.  Is the rostro-caudal axis of the frontal lobe hierarchical? , 2009, Nature Reviews Neuroscience.

[71]  T. Robbins,et al.  Dissociable Forms of Inhibitory Control within Prefrontal Cortex with an Analog of the Wisconsin Card Sort Test: Restriction to Novel Situations and Independence from “On-Line” Processing , 1997, The Journal of Neuroscience.

[72]  Philip G. F. Browning,et al.  Perseverative interference with object-in-place scene learning in rhesus monkeys with bilateral ablation of ventrolateral prefrontal cortex. , 2008, Learning & memory.

[73]  D. Pandya,et al.  Comparison of prefrontal architecture and connections. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[74]  P. Goldman-Rakic,et al.  The primate mediodorsal (MD) nucleus and its projection to the frontal lobe , 1985, The Journal of comparative neurology.