Specialized Elements of Orbitofrontal Cortex in Primates

Abstract: The orbitofrontal cortex is associated with encoding the significance of stimuli within an emotional context, and its connections can be understood in this light. This large cortical region is architectonically heterogeneous, but its connections and functions can be summarized by a broad grouping of areas by cortical type into posterior and anterior sectors. The posterior (limbic) orbitofrontal region is composed of agranular and dysgranular‐type cortices and has unique connections with primary olfactory areas and rich connections with high‐order sensory association cortices. Posterior orbitofrontal areas are further distinguished by dense and distinct patterns of connections with the amygdala and memory‐related anterior temporal lobe structures that may convey signals about emotional import and their memory. The special sets of connections suggest that the posterior orbitofrontal cortex is the primary region for the perception of emotions. In contrast to orbitofrontal areas, posterior medial prefrontal areas in the anterior cingulate are not multi‐modal, but have strong connections with auditory association cortices, brain stem vocalization, and autonomic structures, in pathways that may mediate emotional communication and autonomic activation in emotional arousal. Posterior orbitofrontal areas communicate with anterior orbitofrontal areas and, through feedback projections, with lateral prefrontal and other cortices, suggesting a sequence of information processing for emotions. Pathology in orbitofrontal cortex may remove feedback input to sensory cortices, dissociating emotional context from sensory content and impairing the ability to interpret events.

[1]  Joseph E LeDoux Emotion circuits in the brain. , 2009, Annual review of neuroscience.

[2]  G. Shepherd Perspectives on Olfactory Processing, Conscious Perception, and Orbitofrontal Cortex , 2007, Annals of the New York Academy of Sciences.

[3]  J. Price Definition of the Orbital Cortex in Relation to Specific Connections with Limbic and Visceral Structures and Other Cortical Regions , 2007, Annals of the New York Academy of Sciences.

[4]  Claus C. Hilgetag,et al.  Sequence of information processing for emotions based on the anatomic dialogue between prefrontal cortex and amygdala , 2007, NeuroImage.

[5]  H. Barbas,et al.  Sequential and parallel circuits for emotional processing in primate orbitofrontal cortex , 2006 .

[6]  M. Petrides,et al.  The orbitofrontal cortex: sulcal and gyral morphology and architecture , 2006 .

[7]  H. Barbas,et al.  Prefrontal Projections to the Thalamic Reticular Nucleus form a Unique Circuit for Attentional Mechanisms , 2006, The Journal of Neuroscience.

[8]  Helen Barbas,et al.  Synaptic distinction of laminar-specific prefrontal-temporal pathways in primates. , 2006, Cerebral cortex.

[9]  Claus C. Hilgetag,et al.  Role of Mechanical Factors in the Morphology of the Primate Cerebral Cortex , 2006, PLoS Comput. Biol..

[10]  H. Barbas,et al.  Diversity of laminar connections linking periarcuate and lateral intraparietal areas depends on cortical structure , 2006, The European journal of neuroscience.

[11]  H. Barbas,et al.  Relationship of prefrontal connections to inhibitory systems in superior temporal areas in the rhesus monkey. , 2005, Cerebral cortex.

[12]  Claus C Hilgetag,et al.  Graded classes of cortical connections: quantitative analyses of laminar projections to motion areas of cat extrastriate cortex , 2005, The European journal of neuroscience.

[13]  H. Barbas,et al.  Parallel organization of contralateral and ipsilateral prefrontal cortical projections in the rhesus monkey , 2005, BMC Neuroscience.

[14]  Geoffrey Schoenbaum,et al.  Rapid Associative Encoding in Basolateral Amygdala Depends on Connections with Orbitofrontal Cortex , 2005, Neuron.

[15]  E. Murray,et al.  Bilateral Orbital Prefrontal Cortex Lesions in Rhesus Monkeys Disrupt Choices Guided by Both Reward Value and Reward Contingency , 2004, The Journal of Neuroscience.

[16]  E. Rolls,et al.  The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology , 2004, Progress in Neurobiology.

[17]  P. Goldman-Rakic,et al.  Division of labor among distinct subtypes of inhibitory neurons in a cortical microcircuit of working memory. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[18]  R. R. Sturrock,et al.  The Human Nervous System , 2004 .

[19]  B. Everitt,et al.  Lesions of the Orbitofrontal but not Medial Prefrontal Cortex Disrupt Conditioned Reinforcement in Primates , 2003, The Journal of Neuroscience.

[20]  H. Barbas,et al.  Serial pathways from primate prefrontal cortex to autonomic areas may influence emotional expression , 2003, BMC Neuroscience.

[21]  J. Wallis,et al.  Neuronal activity in primate dorsolateral and orbital prefrontal cortex during performance of a reward preference task , 2003, The European journal of neuroscience.

[22]  G. Schoenbaum,et al.  Encoding Predicted Outcome and Acquired Value in Orbitofrontal Cortex during Cue Sampling Depends upon Input from Basolateral Amygdala , 2003, Neuron.

[23]  M. Bar A Cortical Mechanism for Triggering Top-Down Facilitation in Visual Object Recognition , 2003, Journal of Cognitive Neuroscience.

[24]  H. Mayberg Modulating dysfunctional limbic-cortical circuits in depression: towards development of brain-based algorithms for diagnosis and optimised treatment. , 2003, British medical bulletin.

[25]  D. Zald The human amygdala and the emotional evaluation of sensory stimuli , 2003, Brain Research Reviews.

[26]  M. Mishkin,et al.  Functional Mapping of the Primate Auditory System , 2003, Science.

[27]  H. Barbas,et al.  Pathways for emotion: interactions of prefrontal and anterior temporal pathways in the amygdala of the rhesus monkey , 2002, Neuroscience.

[28]  E. Murray,et al.  The amygdala and reward , 2002, Nature Reviews Neuroscience.

[29]  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.

[30]  R. Davidson Anxiety and affective style: role of prefrontal cortex and amygdala , 2002, Biological Psychiatry.

[31]  L. Swanson,et al.  Combinatorial amygdalar inputs to hippocampal domains and hypothalamic behavior systems , 2001, Brain Research Reviews.

[32]  C C Hilgetag,et al.  Quantitative architecture distinguishes prefrontal cortical systems in the rhesus monkey. , 2001, Cerebral cortex.

[33]  R. Insausti,et al.  Cortical projections of the non‐entorhinal hippocampal formation in the cynomolgus monkey (Macaca fascicularis) , 2001, The European journal of neuroscience.

[34]  H. Barbas,et al.  Neural interaction between the basal forebrain and functionally distinct prefrontal cortices in the rhesus monkey , 2001, Neuroscience.

[35]  M. Raichle,et al.  Emotion-induced changes in human medial prefrontal cortex: II. During anticipatory anxiety. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[36]  M. Raichle,et al.  Emotion-induced changes in human medial prefrontal cortex: I. During cognitive task performance. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[37]  K. Nakano,et al.  Efferent projections of infralimbic and prelimbic areas of the medial prefrontal cortex in the Japanese monkey, Macaca fuscata , 2001, Brain Research.

[38]  H. Barbas,et al.  The laminar pattern of connections between prefrontal and anterior temporal cortices in the Rhesus monkey is related to cortical structure and function. , 2000, Cerebral cortex.

[39]  T. Batten,et al.  A GABAergic projection from the central nucleus of the amygdala to the nucleus of the solitary tract: a combined anterograde tracing and electron microscopic immunohistochemical study , 2000, Neuroscience.

[40]  G. Schoenbaum,et al.  Changes in Functional Connectivity in Orbitofrontal Cortex and Basolateral Amygdala during Learning and Reversal Training , 2000, The Journal of Neuroscience.

[41]  E. Murray,et al.  Control of Response Selection by Reinforcer Value Requires Interaction of Amygdala and Orbital Prefrontal Cortex , 2000, The Journal of Neuroscience.

[42]  W. Schultz,et al.  Reward-related neuronal activity during go-nogo task performance in primate orbitofrontal cortex. , 2000, Journal of neurophysiology.

[43]  J. Hollerman,et al.  Reward processing in primate orbitofrontal cortex and basal ganglia. , 2000, Cerebral cortex.

[44]  K. Hikosaka,et al.  Delay activity of orbital and lateral prefrontal neurons of the monkey varying with different rewards. , 2000, Cerebral cortex.

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

[46]  E. Rolls The orbitofrontal cortex and reward. , 2000, Cerebral cortex.

[47]  H. Barbas,et al.  Medial Prefrontal Cortices Are Unified by Common Connections With Superior Temporal Cortices and Distinguished by Input From Memory‐Related Areas in the Rhesus Monkey , 1999, The Journal of comparative neurology.

[48]  E. Rolls The functions of the orbitofrontal cortex , 1999, Brain and Cognition.

[49]  W. Schultz,et al.  Relative reward preference in primate orbitofrontal cortex , 1999, Nature.

[50]  G. Schoenbaum,et al.  Neural Encoding in Orbitofrontal Cortex and Basolateral Amygdala during Olfactory Discrimination Learning , 1999, The Journal of Neuroscience.

[51]  P. Hof,et al.  Cellular distribution of the calcium-binding proteins parvalbumin, calbindin, and calretinin in the neocortex of mammals: phylogenetic and developmental patterns , 1999, Journal of Chemical Neuroanatomy.

[52]  H. Eichenbaum,et al.  Crossmodal Associative Memory Representations in Rodent Orbitofrontal Cortex , 1999, Neuron.

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

[54]  D. Amaral,et al.  Evidence for a GABAergic projection from the central nucleus of the amygdala to the brainstem of the macaque monkey: a combined retrograde tracing and in situ hybridization study , 1998, The European journal of neuroscience.

[55]  H. Barbas,et al.  Topographic organization of connections between the hypothalamus and prefrontal cortex in the rhesus monkey , 1998, The Journal of comparative neurology.

[56]  Victor A. F. Lamme,et al.  Feedforward, horizontal, and feedback processing in the visual cortex , 1998, Current Opinion in Neurobiology.

[57]  S. Rauch,et al.  Masked Presentations of Emotional Facial Expressions Modulate Amygdala Activity without Explicit Knowledge , 1998, The Journal of Neuroscience.

[58]  H. Barbas,et al.  Cortical structure predicts the pattern of corticocortical connections. , 1997, Cerebral cortex.

[59]  E. Murray,et al.  Excitotoxic Lesions of the Amygdala Fail to Produce Impairment in Visual Learning for Auditory Secondary Reinforcement But Interfere with Reinforcer Devaluation Effects in Rhesus Monkeys , 1997, The Journal of Neuroscience.

[60]  R. Desimone,et al.  Object and place memory in the macaque entorhinal cortex. , 1997, Journal of neurophysiology.

[61]  L. Squire,et al.  Structure and function of declarative and nondeclarative memory systems. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

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

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

[64]  H. Barbas,et al.  Anatomic basis of cognitive-emotional interactions in the primate prefrontal cortex , 1995, Neuroscience & Biobehavioral Reviews.

[65]  J. Morrison,et al.  Human orbitofrontal cortex: Cytoarchitecture and quantitative immunohistochemical parcellation , 1995, The Journal of comparative neurology.

[66]  B. Leonard,et al.  Transient memory impairment in monkeys with bilateral lesions of the entorhinal cortex , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[67]  H Eichenbaum,et al.  Information coding in the rodent prefrontal cortex. I. Single-neuron activity in orbitofrontal cortex compared with that in pyriform cortex. , 1995, Journal of neurophysiology.

[68]  K. Nakamura,et al.  Mnemonic firing of neurons in the monkey temporal pole during a visual recognition memory task. , 1995, Journal of neurophysiology.

[69]  M. Gallagher,et al.  The amygdala complex: multiple roles in associative learning and attention. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

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

[71]  J. Price,et al.  Central olfactory connections in the macaque monkey , 1994, The Journal of comparative neurology.

[72]  H. Barbas,et al.  Contralateral thalamic projections predominantly reach transitional cortices in the rhesus monkey , 1994, The Journal of comparative neurology.

[73]  D. Paré,et al.  GABAergic projection from the intercalated cell masses of the amygdala to the basal forebrain in cats , 1994, The Journal of comparative neurology.

[74]  D. Amaral,et al.  The distribution of GABAergic cells, fibers, and terminals in the monkey amygdaloid complex: an immunohistochemical and in situ hybridization study , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[75]  D. Paré,et al.  The intercalated cell masses project to the central and medial nuclei of the amygdala in cats , 1993, Neuroscience.

[76]  D. Paré,et al.  Distribution of GABA immunoreactivity in the amygdaloid complex of the cat , 1993, Neuroscience.

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

[78]  Joseph E LeDoux,et al.  Equipotentiality of thalamo-amygdala and thalamo-cortico-amygdala circuits in auditory fear conditioning , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[80]  A. Berti Handbook of neuropsychology Edited by F. Boller, J. Grafman, G. Rizzolatti and H. Goodglass. Elsevier, New York, 1988, 441 pp , 1992, Neuropsychologia.

[81]  F. Benes,et al.  Deficits in small interneurons in prefrontal and cingulate cortices of schizophrenic and schizoaffective patients. , 1991, Archives of general psychiatry.

[82]  H. Barbas,et al.  Diverse thalamic projections to the prefrontal cortex in the rhesus monkey , 1991, The Journal of comparative neurology.

[83]  P. Goldman-Rakic,et al.  Myelo‐ and cytoarchitecture of the granular frontal cortex and surrounding regions in the strepsirhine primate Galago and the anthropoid primate Macaca , 1991, The Journal of comparative neurology.

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

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

[86]  D. Amaral,et al.  Topographical organization of the entorhinal projection to the dentate gyrus of the monkey , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[87]  Y. Ben-Ari,et al.  Distribution of GABA‐like immunoreactivity in the rat amygdaloid complex , 1987, The Journal of comparative neurology.

[88]  H. Barbas Pattern in the laminar origin of corticocortical connections , 1986, The Journal of comparative neurology.

[89]  T. Gray,et al.  Peptidergic efferents from the intercalated nuclei of the amygdala to the parabrachial nucleus in the rat , 1985, Neuroscience Letters.

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

[91]  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.

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

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

[94]  J. Trojanowski,et al.  Amygdaloid projections to prefrontal granular cortex in rhesus monkey demonstrated with horseradish peroxidase , 1975, Brain Research.

[95]  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.

[96]  D. Pandya,et al.  A cingulo-amygdaloid projection in the rhesus monkey. , 1973, Brain research.

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

[98]  P. Yakovlev MOTILITY, BEHAVIOR AND THE BRAIN*: STEREODYNAMIC ORGANIZATION AND NEURAL CO‐ORDINATES OF BEHAVIOR , 1948, The Journal of nervous and mental disease.

[99]  M. Kennard Focal Autonomic Representation in the Cortex and its Relation to Sham Rage , 1945 .

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

[101]  J. W. Papez A PROPOSED MECHANISM OF EMOTION , 1937 .

[102]  S. Thorpe,et al.  The orbitofrontal cortex: Neuronal activity in the behaving monkey , 2004, Experimental Brain Research.

[103]  S. Grossberg,et al.  Towards a theory of the laminar architecture of cerebral cortex: computational clues from the visual system. , 2003, Cerebral cortex.

[104]  Michael Davis,et al.  The amygdala: vigilance and emotion , 2001, Molecular Psychiatry.

[105]  Masataka Watanabe,et al.  Cognitive and Motivational Operations in Primate Prefrontal Neurons , 1998, Reviews in the neurosciences.

[106]  J. Fuster,et al.  The association cortex : structure and function , 1997 .

[107]  D. Zald,et al.  Anatomy and function of the orbital frontal cortex, I: anatomy, neurocircuitry; and obsessive-compulsive disorder. , 1996, The Journal of neuropsychiatry and clinical neurosciences.

[108]  S. Carmichael,et al.  Connectional networks within the orbital and medial prefrontal cortex of macaque monkeys. , 1996, The Journal of comparative neurology.

[109]  L. Heimer,et al.  Theories of basal forebrain organization and the "emotional motor system". , 1996, Progress in brain research.

[110]  Gert Holstege,et al.  Chapter 1 The emotional motor system , 1996 .

[111]  G. Holstege,et al.  The emotional motor system. , 1996, Progress in brain research.

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

[113]  S Ullman,et al.  Sequence seeking and counter streams: a computational model for bidirectional information flow in the visual cortex. , 1995, Cerebral cortex.

[114]  G. Holstege,et al.  The emotional motor system. , 1992, European journal of morphology.

[115]  G. Holstege Descending motor pathways and the spinal motor system: limbic and non-limbic components. , 1991, Progress in brain research.

[116]  J. Price 29 – Olfactory System , 1990 .

[117]  Brent A. Vogt,et al.  Structure and Connections of the Cingulate Vocalization Region in the Rhesus Monkey , 1988 .

[118]  J. Newman The Physiological Control of Mammalian Vocalization , 1988, Springer US.

[119]  Douglas L. Rosene,et al.  The Hippocampal Formation of the Primate Brain , 1987 .

[120]  O MARBURG,et al.  The amygdaloid complex. , 1949, Confinia neurologica.

[121]  P. Broca,et al.  Anatomie comparée des circonvolutions cérébrales : le grand lobe limbique et la scissure limbique dans la série des mammifères , 1878 .