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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...
Autores principales: | , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
eLife Sciences Publications, Ltd
2018
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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. |
format | Online Article Text |
id | pubmed-5931800 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2018 |
publisher | eLife Sciences Publications, Ltd |
record_format | MEDLINE/PubMed |
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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