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      Increased cortical surface area and gyrification following long-term survival from early monocular enucleation

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          Abstract

          Purpose

          Retinoblastoma is typically diagnosed before 5 years of age and is often treated by enucleation (surgical removal) of the cancerous eye. Here, we sought to characterize morphological changes of the cortex following long-term survival from early monocular enucleation.

          Methods

          Nine adults with early right-eye enucleation (≤48 months of age) due to retinoblastoma were compared to 18 binocularly intact controls. Surface area, cortical thickness, and gyrification estimates were obtained from T 1 weighted images and group differences were examined.

          Results

          Early monocular enucleation was associated with increased surface area and/or gyrification in visual (i.e., V1, inferior temporal), auditory (i.e., supramarginal), and multisensory (i.e., superior temporal, inferior parietal, superior parietal) cortices compared with controls. Visual cortex increases were restricted to the right hemisphere contralateral to the remaining eye, consistent with previous subcortical data showing asymmetrical lateral geniculate nucleus volume following early monocular enucleation.

          Conclusions

          Altered morphological development of visual, auditory, and multisensory regions occurs subsequent to long-time survival from early eye loss.

          Highlights

          • Cortical morphology in early monocular enucleation was assessed.

          • Enucleation resulted in increased surface area and gyrification of the cortex.

          • Visual cortex increases were exhibited contralateral to the remaining eye.

          • Non-visual cortex increases in surface area and gyrification were also found.

          • Altered cortical development occurs following early monocular enucleation.

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          Most cited references78

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          Distributed and overlapping representations of faces and objects in ventral temporal cortex.

          The functional architecture of the object vision pathway in the human brain was investigated using functional magnetic resonance imaging to measure patterns of response in ventral temporal cortex while subjects viewed faces, cats, five categories of man-made objects, and nonsense pictures. A distinct pattern of response was found for each stimulus category. The distinctiveness of the response to a given category was not due simply to the regions that responded maximally to that category, because the category being viewed also could be identified on the basis of the pattern of response when those regions were excluded from the analysis. Patterns of response that discriminated among all categories were found even within cortical regions that responded maximally to only one category. These results indicate that the representations of faces and objects in ventral temporal cortex are widely distributed and overlapping.
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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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                Author and article information

                Contributors
                Journal
                Neuroimage Clin
                Neuroimage Clin
                NeuroImage : Clinical
                Elsevier
                2213-1582
                3 December 2014
                3 December 2014
                2015
                : 7
                : 297-305
                Affiliations
                [a ]Department of Psychology, York University, Toronto, Canada
                [b ]Centre for Vision Research, York University, Toronto, Canada
                [c ]Department of Ophthalmology and Visual Sciences, The Hospital for Sick Children, Toronto, Canada
                Author notes
                [* ]Corresponding author at: Department of Psychology and Centre for Vision Research, York University, 4700 Keele St, Toronto, ON M3J 1P3, Canada. Tel.: +1 416 736 2100×20452; fax: +1 416 736 5814. steeves@ 123456yorku.ca
                Article
                S2213-1582(14)00185-5
                10.1016/j.nicl.2014.11.020
                4300017
                25610793
                dd4428dd-1ad3-427c-b702-3c65aef41154
                © 2015 The Authors. Published by Elsevier Inc. All rights reserved.

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/3.0/).

                History
                : 24 September 2014
                : 26 November 2014
                : 29 November 2014
                Categories
                Article

                monocular enucleation,morphological development,early visual deprivation,visual cortex,brain plasticity,hemisphere asymmetry

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