Quantitative demonstration of comparable architectonic areas within the ventromedial and lateral orbital frontal cortex in the human and the macaque monkey brains

The orbital and ventromedial frontal cortical regions of the human and the macaque monkey brains include several spatially discrete areas which are defined histologically by their distinctive laminar architecture. Although considerable information has been collected on the function and anatomical connections of specific architectonic areas within the orbital and ventromedial frontal cortex of the macaque monkey, the location of comparable areas in the human brain remains controversial. We re‐examined the comparability of orbital and ventromedial frontal areas across these two species and provide the first quantitative demonstration of architectonically comparable cortical areas in the human and the macaque brains. Images of Nissl‐stained sections of the cortex were obtained at low magnification. Differences in the typical size of neurons in alternating pyramidal and granule cell layers were exploited to segregate the cortical layers before sampling. Profiles of areal neuronal density were sampled across the width of the cortex. The location of individual cortical layers was identified on each profile by sampling a set of equally sized images on which the cortical layers had been manually traced. The rank order of sampled architectonic features in comparable architectonic areas in the two species was significantly correlated. The differences in measured features between gyral and sulcal parts of the same architectonic area are at a minimum 3–4 times smaller than the differences between architectonic areas for the areas examined. Furthermore, the quantified architectonic features arrange areas within the orbital and ventromedial frontal cortex along two dimensions: an anterior‐to‐posterior and a medial‐to‐lateral dimension. On the basis of these findings, and in light of known anatomical connections in the macaque, this region of the human cortex appears to comprise at least two hierarchically structured networks of areas.

[1]  M. Petrides,et al.  Architectonic mapping of the medial region of the human orbitofrontal cortex by density profiles , 2009, Neuroscience.

[2]  H. Barbas,et al.  Specialized Elements of Orbitofrontal Cortex in Primates , 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]  Trevor W Robbins,et al.  The Orbital Prefrontal Cortex and Drug Addiction in Laboratory Animals and Humans , 2007, Annals of the New York Academy of Sciences.

[5]  K. Ressler,et al.  Targeting abnormal neural circuits in mood and anxiety disorders: from the laboratory to the clinic , 2007, Nature Neuroscience.

[6]  J. O'Doherty,et al.  What We Know and Do Not Know about the Functions of the Orbitofrontal Cortex after 20 Years of Cross-Species Studies , 2007, The Journal of Neuroscience.

[7]  Dennis Velakoulis,et al.  The influence of sulcal variability on morphometry of the human anterior cingulate and paracingulate cortex , 2006, NeuroImage.

[8]  Jacob Jelsing,et al.  The prefrontal cortex in the Göttingen minipig brain defined by neural projection criteria and cytoarchitecture , 2006, Brain Research Bulletin.

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

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

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

[12]  S. B. Eickhoff,et al.  Quantitative architectural analysis: a new approach to cortical mapping , 2005, Anatomy and Embryology.

[13]  Timothy Edward John Behrens,et al.  Quantitative Investigation of Connections of the Prefrontal Cortex in the Human and Macaque using Probabilistic Diffusion Tractography , 2005, The Journal of Neuroscience.

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

[15]  S. Shipp.  The importance of being agranular: a comparative account of visual and motor cortex , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[16]  L. Negyessy,et al.  Morphometric characterization of synapses in the primate prefrontal cortex formed by afferents from the mediodorsal thalamic nucleus , 2005, Experimental Brain Research.

[17]  R. Shackleton.  A Quantitative Approach , 2005 .

[18]  Joseph E LeDoux,et al.  Extinction Learning in Humans Role of the Amygdala and vmPFC , 2004, Neuron.

[19]  R. Blair,et al.  The roles of orbital frontal cortex in the modulation of antisocial behavior , 2004, Brain and Cognition.

[20]  Stephen Grossberg,et al.  How laminar frontal cortex and basal ganglia circuits interact to control planned and reactive saccades , 2004, Neural Networks.

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

[22]  A. Hoff.  Objektive Registrierung der Myeloarchitekfonik der Hirnrinde , 1965, Naturwissenschaften.

[23]  J. Price,et al.  Architectonic subdivision of the human orbital and medial prefrontal cortex , 2003, The Journal of comparative neurology.

[24]  J. DeFelipe,et al.  Microstructure of the neocortex: Comparative aspects , 2002, Journal of neurocytology.

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

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

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

[28]  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.

[29]  N. Makris,et al.  Cortical abnormalities in schizophrenia identified by structural magnetic resonance imaging. , 1999, Archives of general psychiatry.

[30]  J. Harlow.  Passage of an Iron Rod Through the Head , 1999 .

[31]  P. Morosan,et al.  Observer-Independent Method for Microstructural Parcellation of Cerebral Cortex: A Quantitative Approach to Cytoarchitectonics , 1999, NeuroImage.

[32]  K Zilles,et al.  Limbic frontal cortex in hominoids: a comparative study of area 13. , 1998, American journal of physical anthropology.

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

[34]  E. Rolls,et al.  The Orbitofrontal Cortex , 2019 .

[35]  A. Damasio.  The somatic marker hypothesis and the possible functions of the prefrontal cortex. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[36]  E J Nestler,et al.  Under Siege: The Brain on Opiates , 1996, Neuron.

[37]  Alan C. Evans,et al.  Human cingulate and paracingulate sulci: pattern, variability, asymmetry, and probabilistic map. , 1996, Cerebral cortex.

[38]  B. Vogt,et al.  Human cingulate cortex: Surface features, flat maps, and cytoarchitecture , 1995, The Journal of comparative neurology.

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

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

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

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

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

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

[45]  Karl Zilles,et al.  A quantitative approach to cytoarchitectonics: software and hardware aspects of a system for the evaluation and analysis of structural inhomogeneities in nervous tissue , 1986, Journal of Neuroscience Methods.

[46]  I. Smart,et al.  Gyrus formation in the cerebral cortex of the ferret. II. Description of the internal histological changes. , 1986, Journal of anatomy.

[47]  Karl Zilles,et al.  Estimation of volume fractions in nervous tissue with an image analyzer , 1982, Journal of Neuroscience Methods.

[48]  A J Hudspeth,et al.  Cytoarchitectonic mapping by microdensitometry. , 1976, Proceedings of the National Academy of Sciences of the United States of America.

[49]  F. Sanides.  THE CYTO-MYELOARCHITECTURE OF THE HUMAN FRONTAL LOBE AND ITS RELATION TO PHYLOGENETIC DIFFERENTIATION OF THE CEREBRAL CORTEX. , 1964, Journal fur Hirnforschung.

[50]  S. Bok.  Histonomy of the cerebral cortex , 1959 .

[51]  M. Ryzen,et al.  A microphotometric method of cell enumeration within the cerebral cortex of man , 1956, The Journal of comparative neurology.

[52]  E. Beck.  A cytoarchitectural investigation into the boundaries of cortical areas 13 and 14 in the human brain. , 1949, Journal of anatomy.

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