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      Differential Tangential Expansion as a Mechanism for Cortical Gyrification

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          Abstract

          Gyrification, the developmental buckling of the cortex, is not a random process—the forces that mediate expansion do so in such a way as to generate consistent patterns of folds across individuals and even species. Although the origin of these forces is unknown, some theories have suggested that they may be related to external cortical factors such as axonal tension. Here, we investigate an alternative hypothesis, namely, whether the differential tangential expansion of the cortex alone can account for the degree and pattern-specificity of gyrification. Using intrinsic curvature as a measure of differential expansion, we initially explored whether this parameter and the local gyrification index (used to quantify the degree of gyrification) varied in a regional-specific pattern across the cortical surface in a manner that was replicable across independent datasets of neurotypicals. Having confirmed this consistency, we further demonstrated that within each dataset, the degree of intrinsic curvature of the cortex was predictive of the degree of cortical folding at a global and regional level. We conclude that differential expansion is a plausible primary mechanism for gyrification, and propose that this perspective offers a compelling mechanistic account of the co-localization of cytoarchitecture and cortical folds.

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          Most cited references44

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          Specification of cerebral cortical areas.

          P Rakic (1988)
          How the immense population of neurons that constitute the human cerebral neocortex is generated from progenitors lining the cerebral ventricle and then distributed to appropriate layers of distinctive cytoarchitectonic areas can be explained by the radial unit hypothesis. According to this hypothesis, the ependymal layer of the embryonic cerebral ventricle consists of proliferative units that provide a proto-map of prospective cytoarchitectonic areas. The output of the proliferative units is translated via glial guides to the expanding cortex in the form of ontogenetic columns, whose final number for each area can be modified through interaction with afferent input. Data obtained through various advanced neurobiological techniques, including electron microscopy, immunocytochemistry, [3H]thymidine and receptor autoradiography, retrovirus gene transfer, neural transplants, and surgical or genetic manipulation of cortical development, furnish new details about the kinetics of cell proliferation, their lineage relationships, and phenotypic expression that favor this hypothesis. The radial unit model provides a framework for understanding cerebral evolution, epigenetic regulation of the parcellation of cytoarchitectonic areas, and insight into the pathogenesis of certain cortical disorders in humans.
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            A tension-based theory of morphogenesis and compact wiring in the central nervous system.

            Many structural features of the mammalian central nervous system can be explained by a morphogenetic mechanism that involves mechanical tension along axons, dendrites and glial processes. In the cerebral cortex, for example, tension along axons in the white matter can explain how and why the cortex folds in a characteristic species-specific pattern. In the cerebellum, tension along parallel fibres can explain why the cortex is highly elongated but folded like an accordion. By keeping the aggregate length of axonal and dendritic wiring low, tension should contribute to the compactness of neural circuitry throughout the adult brain.
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              High-resolution intersubject averaging and a coordinate system for the cortical surface.

              The neurons of the human cerebral cortex are arranged in a highly folded sheet, with the majority of the cortical surface area buried in folds. Cortical maps are typically arranged with a topography oriented parallel to the cortical surface. Despite this unambiguous sheetlike geometry, the most commonly used coordinate systems for localizing cortical features are based on 3-D stereotaxic coordinates rather than on position relative to the 2-D cortical sheet. In order to address the need for a more natural surface-based coordinate system for the cortex, we have developed a means for generating an average folding pattern across a large number of individual subjects as a function on the unit sphere and of nonrigidly aligning each individual with the average. This establishes a spherical surface-based coordinate system that is adapted to the folding pattern of each individual subject, allowing for much higher localization accuracy of structural and functional features of the human brain.
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                Author and article information

                Journal
                Cereb Cortex
                Cereb. Cortex
                cercor
                cercor
                Cerebral Cortex (New York, NY)
                Oxford University Press
                1047-3211
                1460-2199
                August 2014
                29 March 2013
                29 March 2013
                : 24
                : 8
                : 2219-2228
                Affiliations
                [1 ]Brain Mapping Unit, Department of Psychiatry, University of Cambridge , Cambridge CB2 3EB, UK,
                [2 ]FMRIB Centre, Nuffield Department of Clinical Neurosciences, University of Oxford, OX3 9DU, UK
                [3 ]SANE POWIC, Department of Psychiatry, Warneford Hospital, University of Oxford, OX3 7JX
                [4 ]Highfield Adolescent Unit, Warneford Hospital , Oxford OX3 7JX, UK and
                [5 ]Child Psychiatry Branch, NIH, Bethesda MD, 20892, USA
                Author notes
                Address correspondence to Dr Lisa Ronan, Brain Mapping Unit, University of Cambridge, Sir William Hardy Building, Downing Site, Downing Street, Cambridge CB2 3EB, UK. Email: lr344@ 123456cam.ac.uk
                Article
                bht082
                10.1093/cercor/bht082
                4089386
                23542881
                92c24863-09b9-4eb6-aef8-f6097983a5a1
                © The Author 2013. Published by Oxford University Press

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by-nc/3.0/), which permits non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com.

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                Categories
                Articles

                Neurology
                cortical development,differential expansion,gyrification,intrinsic curvature
                Neurology
                cortical development, differential expansion, gyrification, intrinsic curvature

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