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Formation of retinal direction-selective circuitry initiated by starburst amacrine cell homotypic contact

A common strategy by which developing neurons locate their synaptic partners is through projections to circuit-specific neuropil sublayers. Once established, sublayers serve as a substrate for selective synapse formation, but how sublayers arise during neurodevelopment remains unknown. Here, we iden...

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Autores principales: Ray, Thomas A, Roy, Suva, Kozlowski, Christopher, Wang, Jingjing, Cafaro, Jon, Hulbert, Samuel W, Wright, Christopher V, Field, Greg D, Kay, Jeremy N
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5931800/
https://www.ncbi.nlm.nih.gov/pubmed/29611808
http://dx.doi.org/10.7554/eLife.34241
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author Ray, Thomas A
Roy, Suva
Kozlowski, Christopher
Wang, Jingjing
Cafaro, Jon
Hulbert, Samuel W
Wright, Christopher V
Field, Greg D
Kay, Jeremy N
author_facet Ray, Thomas A
Roy, Suva
Kozlowski, Christopher
Wang, Jingjing
Cafaro, Jon
Hulbert, Samuel W
Wright, Christopher V
Field, Greg D
Kay, Jeremy N
author_sort Ray, Thomas A
collection PubMed
description A common strategy by which developing neurons locate their synaptic partners is through projections to circuit-specific neuropil sublayers. Once established, sublayers serve as a substrate for selective synapse formation, but how sublayers arise during neurodevelopment remains unknown. Here, we identify the earliest events that initiate formation of the direction-selective circuit in the inner plexiform layer of mouse retina. We demonstrate that radially migrating newborn starburst amacrine cells establish homotypic contacts on arrival at the inner retina. These contacts, mediated by the cell-surface protein MEGF10, trigger neuropil innervation resulting in generation of two sublayers comprising starburst-cell dendrites. This dendritic scaffold then recruits projections from circuit partners. Abolishing MEGF10-mediated contacts profoundly delays and ultimately disrupts sublayer formation, leading to broader direction tuning and weaker direction-selectivity in retinal ganglion cells. Our findings reveal a mechanism by which differentiating neurons transition from migratory to mature morphology, and highlight this mechanism’s importance in forming circuit-specific sublayers.
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spelling pubmed-59318002018-05-03 Formation of retinal direction-selective circuitry initiated by starburst amacrine cell homotypic contact Ray, Thomas A Roy, Suva Kozlowski, Christopher Wang, Jingjing Cafaro, Jon Hulbert, Samuel W Wright, Christopher V Field, Greg D Kay, Jeremy N eLife Neuroscience A common strategy by which developing neurons locate their synaptic partners is through projections to circuit-specific neuropil sublayers. Once established, sublayers serve as a substrate for selective synapse formation, but how sublayers arise during neurodevelopment remains unknown. Here, we identify the earliest events that initiate formation of the direction-selective circuit in the inner plexiform layer of mouse retina. We demonstrate that radially migrating newborn starburst amacrine cells establish homotypic contacts on arrival at the inner retina. These contacts, mediated by the cell-surface protein MEGF10, trigger neuropil innervation resulting in generation of two sublayers comprising starburst-cell dendrites. This dendritic scaffold then recruits projections from circuit partners. Abolishing MEGF10-mediated contacts profoundly delays and ultimately disrupts sublayer formation, leading to broader direction tuning and weaker direction-selectivity in retinal ganglion cells. Our findings reveal a mechanism by which differentiating neurons transition from migratory to mature morphology, and highlight this mechanism’s importance in forming circuit-specific sublayers. eLife Sciences Publications, Ltd 2018-04-03 /pmc/articles/PMC5931800/ /pubmed/29611808 http://dx.doi.org/10.7554/eLife.34241 Text en © 2018, Ray et al http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Ray, Thomas A
Roy, Suva
Kozlowski, Christopher
Wang, Jingjing
Cafaro, Jon
Hulbert, Samuel W
Wright, Christopher V
Field, Greg D
Kay, Jeremy N
Formation of retinal direction-selective circuitry initiated by starburst amacrine cell homotypic contact
title Formation of retinal direction-selective circuitry initiated by starburst amacrine cell homotypic contact
title_full Formation of retinal direction-selective circuitry initiated by starburst amacrine cell homotypic contact
title_fullStr Formation of retinal direction-selective circuitry initiated by starburst amacrine cell homotypic contact
title_full_unstemmed Formation of retinal direction-selective circuitry initiated by starburst amacrine cell homotypic contact
title_short Formation of retinal direction-selective circuitry initiated by starburst amacrine cell homotypic contact
title_sort formation of retinal direction-selective circuitry initiated by starburst amacrine cell homotypic contact
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5931800/
https://www.ncbi.nlm.nih.gov/pubmed/29611808
http://dx.doi.org/10.7554/eLife.34241
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