The Orbitofrontal Cortex: Novelty, Deviation from Expectation, and Memory

Abstract:  The orbitofrontal cortex is strongly connected with limbic areas of the medial temporal lobe that are critically involved in the establishment of declarative memories (entorhinal and perirhinal cortex and the hippocampal region) as well as the amygdala and the hypothalamus that are involved in emotional and motivational states. The present article reviews evidence regarding the role of the orbitofrontal cortex in the processing of novel information, breaches of expectation, and memory. Functional neuroimaging evidence is provided that there is a difference between the anterior and posterior orbitofrontal cortex in such processing. Exposure to novel information gives rise to a selective increase of activity in the granular anterior part of the orbitofrontal cortex (area 11) and this activity increases when subjects attempt to encode this information in memory. If the stimuli violate expectations (e.g., inspection of graffiti‐like stimuli in the context of other regular stimuli) or are unpleasant (i.e., exposure to the sounds of car crashes), there is increased response in the posteromedial agranular/dysgranular area 13 of the orbitofrontal region. The anatomic data provide a framework within which to understand these functional neuroimaging findings.

[1]  G. Smith,et al.  Die Cytoarchitektonik der Hirnrinde des erwachsenen Menschen. , 1927 .

[2]  M. Keschner,et al.  MENTAL SYMPTOMS IN CASES OF TUMOR OF THE FRONTAL LOBE , 1935 .

[3]  W. Sweet,et al.  EFFECTS ON RESPIRATION, BLOOD PRESSURE AND GASTRIC MOTILITY OF STIMULATION OF ORBITAL SURFACE OF FRONTAL LOBE , 1940 .

[4]  R. Livingston,et al.  Stimulation of orbital surface of man prior to frontal lobotomy. , 1948, Research publications - Association for Research in Nervous and Mental Disease.

[5]  R. Livingston,et al.  Some respiratory, vascular and thermal responses to stimulation of orbital surface of frontal lobe. , 1948, Journal of neurophysiology.

[6]  W. Nauta,et al.  Fibre degeneration following lesions of the amygdaloid complex in the monkey. , 1961, Journal of anatomy.

[7]  W. Nauta,et al.  Neural associations of the amygdaloid complex in the monkey. , 1962, Brain : a journal of neurology.

[8]  C. Butter,et al.  Habituation of Responses to Novel Stimuli in Monkeys with Selective Frontal Lesions , 1964, Science.

[9]  G. Lindqvist,et al.  KORSAKOFF'S SYNDROME AFTER OPERATION ON RUPTURED ANEURYSM OF THE ANTERIOR COMMUNICATING ARTERY , 1966, Acta psychiatrica Scandinavica.

[10]  W. Sweet,et al.  AMNESIC SYNDROME WITH ANTERIOR COMMUNICATING ARTERY ANEURYSM , 1967, The Journal of nervous and mental disease.

[11]  H. Stephan,et al.  The septum in the human brain , 1968, The Journal of comparative neurology.

[12]  D. R. Snyder,et al.  Effects of orbital frontal lesions on aversive and aggressive behaviors in rhesus monkeys. , 1970, Journal of comparative and physiological psychology.

[13]  T. Avery Seven Cases of Frontal Tumour with Psychiatric Presentation , 1971, British Journal of Psychiatry.

[14]  B. Milner,et al.  Disorders of learning and memory after temporal lobe lesions in man. , 1972, Clinical neurosurgery.

[15]  N Butters,et al.  Cortical Afferents to the Entorhinal Cortex of the Rhesus Monkey , 1972, Science.

[16]  Deepak N. Pandya,et al.  Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. III. Efferent connections , 1975, Brain Research.

[17]  Deepak N. Pandya,et al.  Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. II. Frontal lobe afferents , 1975, Brain Research.

[18]  T. J. Tobias,et al.  Afferents to prefrontal cortex from the thalamic mediodorsal nucleus in the rhesus monkey , 1975, Brain Research.

[19]  R. E. Hall,et al.  Role of the orbital cortex in cardiac dysfunction in unanesthetized rhesus monkey , 1977, Experimental Neurology.

[20]  G. V. Van Hoesen,et al.  Hippocampal efferents reach widespread areas of cerebral cortex and amygdala in the rhesus monkey. , 1977, Science.

[21]  R. Livingston,et al.  Orbital cortical influences on cardiovascular dynamics and myocardial structure in conscious monkeys. , 1977, Journal of neurosurgery.

[22]  R. E. Passingham,et al.  Cortical and subcortical afferents to the amygdala of the rhesus monkey (Macaca mulatta) , 1980, Brain Research.

[23]  J. Eccles The emotional brain. , 1980, Bulletin et memoires de l'Academie royale de medecine de Belgique.

[24]  F Mauguiere,et al.  The duality of the cingulate gyrus in monkey. Neuroanatomical study and functional hypothesis. , 1980, Brain : a journal of neurology.

[25]  P. Goldman-Rakic,et al.  Direct and indirect pathways from the amygdala to the frontal lobe in rhesus monkeys , 1981, The Journal of comparative neurology.

[26]  M. Mishkin A memory system in the monkey. , 1982, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[27]  A. Gade,et al.  Amnesia after operations on aneurysms of the anterior communicating artery. , 1982, Surgical neurology.

[28]  B. Volpe,et al.  Amnesia following the rupture and repair of an anterior communicating artery aneurysm. , 1983, Journal of neurology, neurosurgery, and psychiatry.

[29]  A. Levey,et al.  Cholinergic innervation of cortex by the basal forebrain: Cytochemistry and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (Substantia innominata), and hypothalamus in the rhesus monkey , 1983, The Journal of comparative neurology.

[30]  M Freedman,et al.  Amnesia after anterior communicating artery aneurysm rupture , 1984, Neurology.

[31]  D. Amaral,et al.  Amygdalo‐cortical projections in the monkey (Macaca fascicularis) , 1984, The Journal of comparative neurology.

[32]  M Mishkin,et al.  Projections of the amygdala to the thalamus in the cynomolgus monkey , 1984, The Journal of comparative neurology.

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

[34]  A R Damasio,et al.  Amnesia following basal forebrain lesions. , 1985, Archives of neurology.

[35]  N. J. Cohen,et al.  Analyses of Global Memory Impairments of Different Etiologies a , 1985, Annals of the New York Academy of Sciences.

[36]  T Hamanaka,et al.  [Neuropsychology of memory]. , 1985, No to shinkei = Brain and nerve.

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

[38]  M Mishkin,et al.  The origin, course, and termination of the hippocampothalamic projections in the macaque , 1986, The Journal of comparative neurology.

[39]  A. Damasio,et al.  Severe disturbance of higher cognition after bilateral frontal lobe ablation: Patient EVR , 1986 .

[40]  D. Amaral,et al.  The afferent input to the magnocellular division of the mediodorsal thalamic nucleus in the monkey, Macaca fascicularis , 1987, The Journal of comparative neurology.

[41]  S. Phillips,et al.  Basal forebrain infarction. A clinicopathologic correlation. , 1987, Archives of neurology.

[42]  M. Mesulam,et al.  Neural inputs into the temporopolar cortex of the rhesus monkey , 1987, The Journal of comparative neurology.

[43]  M. Mishkin,et al.  A selective mnemonic role for the hippocampus in monkeys: memory for the location of objects , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  H. Barbas Anatomic organization of basoventral and mediodorsal visual recipient prefrontal regions in the rhesus monkey , 1988, The Journal of comparative neurology.

[45]  P. Goldman-Rakic,et al.  Posterior parietal cortex in rhesus monkey: II. Evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe , 1989, The Journal of comparative neurology.

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

[47]  B. Milner,et al.  Right hippocampal impairment in the recall of spatial location: Encoding deficit or rapid forgetting? , 1989, Neuropsychologia.

[48]  H. Barbas,et al.  Projections from the amygdala to basoventral and mediodorsal prefrontal regions in the rhesus monkey , 1990, The Journal of comparative neurology.

[49]  C. Papagno,et al.  A case of amnesia after excision of the septum pellucidum. , 1990, Journal of neurology, neurosurgery, and psychiatry.

[50]  H. Eichenbaum,et al.  Hippocampal representation in place learning , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[51]  J. Bartlett,et al.  Neuropsychological correlates of stereotactic subcaudate tractotomy. A prospective study. , 1991, Brain : a journal of neurology.

[52]  L. Squire,et al.  The medial temporal lobe memory system , 1991, Science.

[53]  C. Geula,et al.  Cytoarchitecture and neural afferents of orbitofrontal cortex in the brain of the monkey , 1992, The Journal of comparative neurology.

[54]  K M Heilman,et al.  Amnesia following a discrete basal forebrain lesion. , 1992, Brain : a journal of neurology.

[55]  D. Amaral,et al.  Lesions of the perirhinal and parahippocampal cortices in the monkey produce long-lasting memory impairment in the visual and tactual modalities , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[56]  H. Markowitsch,et al.  The possible contribution of the septal region to memory , 1993, Neuropsychologia.

[57]  M. Mishkin,et al.  Effects on visual recognition of combined and separate ablations of the entorhinal and perirhinal cortex in rhesus monkeys , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[58]  H. Barbas,et al.  Organization of cortical afferent input to orbitofrontal areas in the rhesus monkey , 1993, Neuroscience.

[59]  M. Petrides Comparative architectonic analysis of the human and the macaque frontal cortex , 1994 .

[60]  G. Lynch,et al.  Memory: Organization and locus of change , 1994 .

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

[62]  H. Damasio,et al.  Neuroanatomical correlates of electrodermal skin conductance responses. , 1994, Psychophysiology.

[63]  J. Price,et al.  Limbic connections of the orbital and medial prefrontal cortex in macaque monkeys , 1995, The Journal of comparative neurology.

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

[65]  M. Mishkin,et al.  Effects of orbital frontal and anterior cingulate lesions on object and spatial memory in rhesus monkeys , 1997, Neuropsychologia.

[66]  L. Nadel,et al.  Spatial memory deficits in patients with lesions to the right hippocampus and to the right parahippocampal cortex , 1998, Neuropsychologia.

[67]  J. Price,et al.  Prefrontal cortical projections to the hypothalamus in Macaque monkeys , 1998, The Journal of comparative neurology.

[68]  G. Schoenbaum,et al.  Orbitofrontal cortex and basolateral amygdala encode expected outcomes during learning , 1998, Nature Neuroscience.

[69]  E. Tulving,et al.  Episodic memory and the self in a case of isolated retrograde amnesia. , 1998 .

[70]  H. Barbas,et al.  Topographic Organization of Connections between the Hypothalamus and Prefrontal Cortex in the Rhesus Monkey , 2022 .

[71]  J. Price,et al.  Prefrontal cortical projections to longitudinal columns in the midbrain periaqueductal gray in Macaque monkeys , 1998, The Journal of comparative neurology.

[72]  E. Tulving,et al.  Episodic memory and the self in a case of isolated retrograde amnesia. , 1998, Brain : a journal of neurology.

[73]  M. Posner The Brain and Emotion , 1999, Nature Medicine.

[74]  M Petrides,et al.  Orbitofrontal cortex: A key prefrontal region for encoding information. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[75]  C. Cavada,et al.  The anatomical connections of the macaque monkey orbitofrontal cortex. A review. , 2000, Cerebral cortex.

[76]  M. Petrides,et al.  Orbitofrontal sulci of the human and macaque monkey brain , 2000, The Journal of comparative neurology.

[77]  H. Damasio,et al.  Characterization of the decision-making deficit of patients with ventromedial prefrontal cortex lesions. , 2000, Brain : a journal of neurology.

[78]  W. Schultz,et al.  Modifications of reward expectation-related neuronal activity during learning in primate orbitofrontal cortex. , 2000, Journal of neurophysiology.

[79]  M. Petrides,et al.  Orbitofrontal involvement in the processing of unpleasant auditory information , 2000, The European journal of neuroscience.

[80]  R. Henson,et al.  Neural activity associated with episodic memory for emotional context , 2001, Neuropsychologia.

[81]  M. Petrides,et al.  Differential activation of the human orbital, mid-ventrolateral, and mid-dorsolateral prefrontal cortex during the processing of visual stimuli , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[82]  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.

[83]  Michael Petrides,et al.  Orbitofrontal Cortex and Memory Formation , 2002, Neuron.

[84]  D. Pandya,et al.  Association pathways of the prefrontal cortex and functional observations , 2002 .

[85]  M. Petrides,et al.  Cognitive Strategies Dependent on the Hippocampus and Caudate Nucleus in Human Navigation: Variability and Change with Practice , 2003, The Journal of Neuroscience.

[86]  Michael Petrides,et al.  Greater orbitofrontal activity predicts better memory for faces , 2003, The European journal of neuroscience.

[87]  Gereon R Fink,et al.  Differential remoteness and emotional tone modulate the neural correlates of autobiographical memory. , 2003, Brain : a journal of neurology.

[88]  H. Lanfermann,et al.  Engagement of Lateral and Medial Prefrontal Areas in the Ecphory of Sad and Happy Autobiographical Memories , 2003, Cortex.

[89]  B. Milner Visual recognition and recall after right temporal-lobe excision in man , 1968, Epilepsy & Behavior.

[90]  Michael Petrides,et al.  Orbitofrontal contribution to auditory encoding , 2004, NeuroImage.

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

[92]  E. Rolls,et al.  Novel visual stimuli activate a population of neurons in the primate orbitofrontal cortex , 2005, Neurobiology of Learning and Memory.

[93]  T. Robbins,et al.  Neurochemical modulation of orbitofrontal cortex function , 2006 .

[94]  R. Cabeza,et al.  Cognitive neuroscience of emotional memory , 2006, Nature Reviews Neuroscience.