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Lateral Spread of Orientation Selectivity in V1 is Controlled by Intracortical Cooperativity

Neurons in the primary visual cortex receive subliminal information originating from the periphery of their receptive fields (RF) through a variety of cortical connections. In the cat primary visual cortex, long-range horizontal axons have been reported to preferentially bind to distant columns of s...

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Autores principales: Chavane, Frédéric, Sharon, Dahlia, Jancke, Dirk, Marre, Olivier, Frégnac, Yves, Grinvald, Amiram
Formato: Texto
Lenguaje:English
Publicado: Frontiers Research Foundation 2011
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3100672/
https://www.ncbi.nlm.nih.gov/pubmed/21629708
http://dx.doi.org/10.3389/fnsys.2011.00004
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author Chavane, Frédéric
Sharon, Dahlia
Jancke, Dirk
Marre, Olivier
Frégnac, Yves
Grinvald, Amiram
author_facet Chavane, Frédéric
Sharon, Dahlia
Jancke, Dirk
Marre, Olivier
Frégnac, Yves
Grinvald, Amiram
author_sort Chavane, Frédéric
collection PubMed
description Neurons in the primary visual cortex receive subliminal information originating from the periphery of their receptive fields (RF) through a variety of cortical connections. In the cat primary visual cortex, long-range horizontal axons have been reported to preferentially bind to distant columns of similar orientation preferences, whereas feedback connections from higher visual areas provide a more diverse functional input. To understand the role of these lateral interactions, it is crucial to characterize their effective functional connectivity and tuning properties. However, the overall functional impact of cortical lateral connections, whatever their anatomical origin, is unknown since it has never been directly characterized. Using direct measurements of postsynaptic integration in cat areas 17 and 18, we performed multi-scale assessments of the functional impact of visually driven lateral networks. Voltage-sensitive dye imaging showed that local oriented stimuli evoke an orientation-selective activity that remains confined to the cortical feedforward imprint of the stimulus. Beyond a distance of one hypercolumn, the lateral spread of cortical activity gradually lost its orientation preference approximated as an exponential with a space constant of about 1 mm. Intracellular recordings showed that this loss of orientation selectivity arises from the diversity of converging synaptic input patterns originating from outside the classical RF. In contrast, when the stimulus size was increased, we observed orientation-selective spread of activation beyond the feedforward imprint. We conclude that stimulus-induced cooperativity enhances the long-range orientation-selective spread.
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spelling pubmed-31006722011-05-31 Lateral Spread of Orientation Selectivity in V1 is Controlled by Intracortical Cooperativity Chavane, Frédéric Sharon, Dahlia Jancke, Dirk Marre, Olivier Frégnac, Yves Grinvald, Amiram Front Syst Neurosci Neuroscience Neurons in the primary visual cortex receive subliminal information originating from the periphery of their receptive fields (RF) through a variety of cortical connections. In the cat primary visual cortex, long-range horizontal axons have been reported to preferentially bind to distant columns of similar orientation preferences, whereas feedback connections from higher visual areas provide a more diverse functional input. To understand the role of these lateral interactions, it is crucial to characterize their effective functional connectivity and tuning properties. However, the overall functional impact of cortical lateral connections, whatever their anatomical origin, is unknown since it has never been directly characterized. Using direct measurements of postsynaptic integration in cat areas 17 and 18, we performed multi-scale assessments of the functional impact of visually driven lateral networks. Voltage-sensitive dye imaging showed that local oriented stimuli evoke an orientation-selective activity that remains confined to the cortical feedforward imprint of the stimulus. Beyond a distance of one hypercolumn, the lateral spread of cortical activity gradually lost its orientation preference approximated as an exponential with a space constant of about 1 mm. Intracellular recordings showed that this loss of orientation selectivity arises from the diversity of converging synaptic input patterns originating from outside the classical RF. In contrast, when the stimulus size was increased, we observed orientation-selective spread of activation beyond the feedforward imprint. We conclude that stimulus-induced cooperativity enhances the long-range orientation-selective spread. Frontiers Research Foundation 2011-02-23 /pmc/articles/PMC3100672/ /pubmed/21629708 http://dx.doi.org/10.3389/fnsys.2011.00004 Text en Copyright © 2011 Chavane, Sharon, Jancke, Marre, Frégnac and Grinvald. http://www.frontiersin.org/licenseagreement This is an open-access article subject to an exclusive license agreement between the authors and Frontiers Media SA, which permits unrestricted use, distribution, and reproduction in any medium, provided the original authors and source are credited.
spellingShingle Neuroscience
Chavane, Frédéric
Sharon, Dahlia
Jancke, Dirk
Marre, Olivier
Frégnac, Yves
Grinvald, Amiram
Lateral Spread of Orientation Selectivity in V1 is Controlled by Intracortical Cooperativity
title Lateral Spread of Orientation Selectivity in V1 is Controlled by Intracortical Cooperativity
title_full Lateral Spread of Orientation Selectivity in V1 is Controlled by Intracortical Cooperativity
title_fullStr Lateral Spread of Orientation Selectivity in V1 is Controlled by Intracortical Cooperativity
title_full_unstemmed Lateral Spread of Orientation Selectivity in V1 is Controlled by Intracortical Cooperativity
title_short Lateral Spread of Orientation Selectivity in V1 is Controlled by Intracortical Cooperativity
title_sort lateral spread of orientation selectivity in v1 is controlled by intracortical cooperativity
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3100672/
https://www.ncbi.nlm.nih.gov/pubmed/21629708
http://dx.doi.org/10.3389/fnsys.2011.00004
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