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      Quantitative assessment of prefrontal cortex in humans relative to nonhuman primates

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          Significance

          A longstanding controversy in neuroscience pertains to differences in human prefrontal cortex (PFC) compared with other primate species; specifically, is human PFC disproportionately large? Distinctively human behavioral capacities related to higher cognition and affect presumably arose from evolutionary modifications since humans and great apes diverged from a common ancestor about 6–8 Mya. Accurate determination of regional differences in the amount of cortical gray and subcortical white matter content in humans, great apes, and Old World monkeys can further our understanding of the link between structure and function of the human brain. Using tissue volume analyses, we show a disproportionately large amount of gray and white matter corresponding to PFC in humans compared with nonhuman primates.

          Abstract

          Humans have the largest cerebral cortex among primates. The question of whether association cortex, particularly prefrontal cortex (PFC), is disproportionately larger in humans compared with nonhuman primates is controversial: Some studies report that human PFC is relatively larger, whereas others report a more uniform PFC scaling. We address this controversy using MRI-derived cortical surfaces of many individual humans, chimpanzees, and macaques. We present two parcellation-based PFC delineations based on cytoarchitecture and function and show that a previously used morphological surrogate (cortex anterior to the genu of the corpus callosum) substantially underestimates PFC extent, especially in humans. We find that the proportion of cortical gray matter occupied by PFC in humans is up to 1.9-fold greater than in macaques and 1.2-fold greater than in chimpanzees. The disparity is even more prominent for the proportion of subcortical white matter underlying the PFC, which is 2.4-fold greater in humans than in macaques and 1.7-fold greater than in chimpanzees.

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          Most cited references47

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          Emotion, decision making and the orbitofrontal cortex.

          The somatic marker hypothesis provides a systems-level neuroanatomical and cognitive framework for decision making and the influence on it by emotion. The key idea of this hypothesis is that decision making is a process that is influenced by marker signals that arise in bioregulatory processes, including those that express themselves in emotions and feelings. This influence can occur at multiple levels of operation, some of which occur consciously and some of which occur non-consciously. Here we review studies that confirm various predictions from the hypothesis. The orbitofrontal cortex represents one critical structure in a neural system subserving decision making. Decision making is not mediated by the orbitofrontal cortex alone, but arises from large-scale systems that include other cortical and subcortical components. Such structures include the amygdala, the somatosensory/insular cortices and the peripheral nervous system. Here we focus only on the role of the orbitofrontal cortex in decision making and emotional processing, and the relationship between emotion, decision making and other cognitive functions of the frontal lobe, namely working memory.
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            MSM: a new flexible framework for Multimodal Surface Matching.

            Surface-based cortical registration methods that are driven by geometrical features, such as folding, provide sub-optimal alignment of many functional areas due to variable correlation between cortical folding patterns and function. This has led to the proposal of new registration methods using features derived from functional and diffusion imaging. However, as yet there is no consensus over the best set of features for optimal alignment of brain function. In this paper we demonstrate the utility of a new Multimodal Surface Matching (MSM) algorithm capable of driving alignment using a wide variety of descriptors of brain architecture, function and connectivity. The versatility of the framework originates from adapting the discrete Markov Random Field (MRF) registration method to surface alignment. This has the benefit of being very flexible in the choice of a similarity measure and relatively insensitive to local minima. The method offers significant flexibility in the choice of feature set, and we demonstrate the advantages of this by performing registrations using univariate descriptors of surface curvature and myelination, multivariate feature sets derived from resting fMRI, and multimodal descriptors of surface curvature and myelination. We compare the results with two state of the art surface registration methods that use geometric features: FreeSurfer and Spherical Demons. In the future, the MSM technique will allow explorations into the best combinations of features and alignment strategies for inter-subject alignment of cortical functional areas for a wide range of neuroimaging data sets.
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              Architectonic subdivision of the human orbital and medial prefrontal cortex.

              The structure of the human orbital and medial prefrontal cortex (OMPFC) was investigated using five histological and immunohistochemical stains and was correlated with a previous analysis in macaque monkeys [Carmichael and Price (1994) J. Comp. Neurol. 346:366-402]. A cortical area was recognized if it was distinct with at least two stains and was found in similar locations in different brains. All of the areas recognized in the macaque OMPFC have counterparts in humans. Areas 11, 13, and 14 were subdivided into areas 11m, 11l, 13a, 13b, 13m, 13l, 14r, and 14c. Within area 10, the region corresponding to area 10m in monkeys was divided into 10m and 10r, and area 10o (orbital) was renamed area 10p (polar). Areas 47/12r, 47/12m, 47/12l, and 47/12s occupy the lateral orbital cortex, corresponding to monkey areas 12r, 12m, 12l, and 12o. The agranular insula (areas Iam, Iapm, Iai, and Ial) extends onto the caudal orbital surface and into the horizontal ramus of the lateral sulcus. The growth of the frontal pole in humans has pushed area 25 and area 32pl, which corresponds to the prelimbic area 32 in Brodmann's monkey brain map, caudal and ventral to the genu of the corpus callosum. Anterior cingulate areas 24a and 24b also extend ventral to the genu of the corpus callosum. Area 32ac, corresponding to the dorsal anterior cingulate area 32 in Brodmann's human brain map, is anterior and dorsal to the genu. The parallel organization of the OMPFC in monkeys and humans allows experimental data from monkeys to be applied to studies of the human cortex. Copyright 2003 Wiley-Liss, Inc.
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                Author and article information

                Journal
                Proc Natl Acad Sci U S A
                Proc. Natl. Acad. Sci. U.S.A
                pnas
                pnas
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                29 May 2018
                8 May 2018
                8 May 2018
                : 115
                : 22
                : E5183-E5192
                Affiliations
                [1] aDepartment of Neuroscience, Washington University School of Medicine , St. Louis, MO 63110;
                [2] bSt. Luke’s Hospital , St. Louis, MO 63017;
                [3] cDivision of Neuropharmacology and Neurologic Diseases, Emory University , Atlanta, GA 30329;
                [4] dCenter for Translational Social Neuroscience, Emory University , Atlanta, GA 30329;
                [5] eYerkes National Primate Research Center, Emory University , Atlanta, GA 30329;
                [6] fDepartment of Anthropology, Emory University , Atlanta, GA 30329;
                [7] gCenter for Behavioral Neuroscience, Emory University , Atlanta, GA 30329;
                [8] hDepartment of Psychiatry and Behavioral Sciences, Emory University , Atlanta, GA 30329
                Author notes
                1To whom correspondence may be addressed. Email: donahuec@ 123456wustl.edu or vanessen@ 123456wustl.edu .

                Contributed by David C. Van Essen, March 22, 2018 (sent for review December 14, 2017; reviewed by Leah A. Krubitzer, Rogier Mars, and Jeroen B. Smaers)

                Author contributions: C.J.D., M.F.G., and D.C.V.E. designed research; C.J.D. performed research; C.J.D., M.F.G., T.M.P., J.K.R., and D.C.V.E. analyzed data; and C.J.D., M.F.G., T.M.P., J.K.R., and D.C.V.E. wrote the paper.

                Reviewers: L.A.K., University of California, Davis; R.M., Radboud University Nijmegen; and J.B.S., Stony Brook University.

                Author information
                http://orcid.org/0000-0002-6440-7892
                http://orcid.org/0000-0001-7044-4721
                Article
                201721653
                10.1073/pnas.1721653115
                5984508
                29739891
                20a7659c-2ed5-40fc-a0d9-0a24fd79921f
                Copyright © 2018 the Author(s). Published by PNAS.

                This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

                History
                Page count
                Pages: 10
                Funding
                Funded by: HHS | NIH | National Institute of Biomedical Imaging and Bioengineering (NIBIB) 100000070
                Award ID: 2T32EB014855
                Funded by: HHS | NIH | National Institute of Mental Health (NIMH) 100000025
                Award ID: F30MH097312
                Funded by: HHS | NIH | National Institute of Mental Health (NIMH) 100000025
                Award ID: RO1MH60974
                Funded by: HHS | NIH | National Institute of Mental Health (NIMH) 100000025
                Award ID: U54MH091657
                Funded by: HHS | NIH | National Institute on Aging (NIA) 100000049
                Award ID: P01AG026423
                Funded by: HHS | NIH | National Center for Research Resources (NCRR) 100000097
                Award ID: P51RR165
                Funded by: HHS | NIH | National Institute of Neurological Disorders and Stroke (NINDS) 100000065
                Award ID: R24NS092988
                Categories
                PNAS Plus
                Biological Sciences
                Neuroscience
                PNAS Plus

                neuroanatomy,prefrontal cortex,evolution,cortical parcellation,chimpanzee

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