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      Asymmetrical Interhemispheric Connections Develop in Cat Visual Cortex after Early Unilateral Convergent Strabismus: Anatomy, Physiology, and Mechanisms

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          Abstract

          In the mammalian primary visual cortex, the corpus callosum contributes to the unification of the visual hemifields that project to the two hemispheres. Its development depends on visual experience. When this is abnormal, callosal connections must undergo dramatic anatomical and physiological changes. However, data concerning these changes are sparse and incomplete. Thus, little is known about the impact of abnormal postnatal visual experience on the development of callosal connections and their role in unifying representation of the two hemifields. Here, the effects of early unilateral convergent strabismus (a model of abnormal visual experience) were fully characterized with respect to the development of the callosal connections in cat visual cortex, an experimental model for humans. Electrophysiological responses and 3D reconstruction of single callosal axons show that abnormally asymmetrical callosal connections develop after unilateral convergent strabismus, resulting from an extension of axonal branches of specific orders in the hemisphere ipsilateral to the deviated eye and a decreased number of nodes and terminals in the other (ipsilateral to the non-deviated eye). Furthermore this asymmetrical organization prevents the establishment of a unifying representation of the two visual hemifields. As a general rule, we suggest that crossed and uncrossed retino-geniculo-cortical pathways contribute successively to the development of the callosal maps in visual cortex.

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          Most cited references72

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          Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry.

          Endogenous cytochrome oxidase activity within the mitochondria of neurons and neuropil was demonstrated histochemically under normal and experimental conditions. Since enzymatic changes were noted with chronic neuronal inactivity in the auditory system (Wong-Riley et al), the present study sought to examine functionally induced enzymatic changes in the visual system of kittens. Eight kittens were used experimentally: 5 had monocular lid suture for varying periods of time; one had binocular lid suture followed by monocular suture followed by binocular opening; two had monocular enucleation. All initial procedures were performed before eye opening. Materials from other normal kittens and cats were also used as controls. At the end of the experiments, the animals were perfused with aldehyde solutions and frozen sections of the brains were incubated for cytochrome oxidase activity (a detailed protocol was outlined). The results indicated that the deprivation caused by monocular suture produced a decrease in the cytochrome oxidase staining of the binocular segment of the deprived geniculate laminae. Enucleation yielded a greater decrease in the cytochrome oxidase activity in the affected geniculate laminae. However, the staining in the 'normal' lamina extended across the interlaminar border to include a row of surviving large cells in the 'denervated' lamina. The staining of the monocular segment appeared not to be affected by lid suture, but was decreased by enucleation. At the cortical level, lamina IV in area 17 of normal cats was stained darkly as a continuous band. Following lid suture, this pattern was replaced in part by alternating columns of light and dark staining, suggestive of ocular dominance columns. Thus, a decrease in neuronal activity due to reduced visual stimulation or destruction of the primary afferent nerves led to a significant decrease in the level of oxidative enzyme activity one to several synapses away.
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            Binocular interaction in striate cortex of kittens reared with artificial squint.

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              The retinotopic organization of area 17 (striate cortex) in the cat.

              The location and retinotopic organization of visual areas in the cat cortex were determined by systematically mapping visual cortex in over 100 cats. The positions of the receptive fields of single neurons or small clusters of neurons were related to the locations of the corresponding recording sites in the cortex to determine the representations of the visual field in these cortical areas. In this report, the first of a series, we describe the organization of area 17. A single representation of the cat's entire visual field corresponds closely to the cytoarchitectonically defined area 17. This area has the largest cortical surface area (380 mm2) and the highest cortical magnification factor (3.6 mm2/degree2 at area centralis) of all the cortical areas we have studied. There was perfect agreement between the borders of area 17 determined electrophysiologically and cytoarchitecturally. This area contains a first order transformation of the visual hemifield in which every adjacent point in the visual field is represented as an adjacent point in the cortex. Some variability exists among cats in the extent and retinotopic representation of the visual field in area 17.
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                Author and article information

                Journal
                Front Neuroanat
                Front. Neuroanat.
                Frontiers in Neuroanatomy
                Frontiers Research Foundation
                1662-5129
                11 October 2011
                11 January 2012
                2011
                : 5
                : 68
                Affiliations
                [1] 1simpleLaboratoire de Physiologie de la Perception et de l’Action, Collège de France Paris, France
                [2] 2simpleLaboratoire de Physiologie de la Perception et de l’Action, CNRS UMR 7152 Paris, France
                [3] 3simpleService d’Ophtalmologie, Hôpital Robert Debré Paris, France
                Author notes

                Edited by: Zoltan F. Kisvarday, University of Debrecen, Hungary

                Reviewed by: Alino Martinez-Marcos, Universidad de Castilla, Spain; Zoltan F. Kisvarday, University of Debrecen, Hungary

                *Correspondence: Chantal Milleret, Laboratoire de Physiologie de la Perception et de l’Action, Collège de France, CNRS UMR 7152, 11 Place Marcelin Berthelot, 75005 Paris, France. e-mail: chantal.milleret@ 123456college-de-france.fr

                Emmanuel Bui Quoc and Jérôme Ribot have contributed equally to this work.

                Article
                10.3389/fnana.2011.00068
                3257851
                22275883
                b4be3f3a-cb81-44b9-ba5f-f9dfe509c9ed
                Copyright © 2012 Bui Quoc, Ribot, Quenech’Du, Doutremer, Lebas, Grantyn, Aushana and Milleret.

                This is an open-access article distributed under the terms of the Creative Commons Attribution Non Commercial License, which permits non-commercial use, distribution, and reproduction in other forums, provided the original authors and source are credited.

                History
                : 19 September 2011
                : 19 December 2011
                Page count
                Figures: 10, Tables: 6, Equations: 0, References: 83, Pages: 29, Words: 20530
                Categories
                Neuroscience
                Original Research

                Neurosciences
                strabismus,cerebral asymmetry,visual interhemispheric integration,higher mammals
                Neurosciences
                strabismus, cerebral asymmetry, visual interhemispheric integration, higher mammals

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