Cargando…

A circuit suppressing retinal drive to the optokinetic system during fast image motion

Optokinetic nystagmus (OKN) assists stabilization of the retinal image during head rotation. OKN is driven by ON direction selective retinal ganglion cells (ON DSGCs), which encode both the direction and speed of global retinal slip. The synaptic circuits responsible for the direction selectivity of...

Descripción completa

Detalles Bibliográficos
Autores principales: Mani, Adam, Yang, Xinzhu, Zhao, Tiffany A., Leyrer, Megan L., Schreck, Daniel, Berson, David M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10447436/
https://www.ncbi.nlm.nih.gov/pubmed/37612305
http://dx.doi.org/10.1038/s41467-023-40527-z
_version_ 1785094553229852672
author Mani, Adam
Yang, Xinzhu
Zhao, Tiffany A.
Leyrer, Megan L.
Schreck, Daniel
Berson, David M.
author_facet Mani, Adam
Yang, Xinzhu
Zhao, Tiffany A.
Leyrer, Megan L.
Schreck, Daniel
Berson, David M.
author_sort Mani, Adam
collection PubMed
description Optokinetic nystagmus (OKN) assists stabilization of the retinal image during head rotation. OKN is driven by ON direction selective retinal ganglion cells (ON DSGCs), which encode both the direction and speed of global retinal slip. The synaptic circuits responsible for the direction selectivity of ON DSGCs are well understood, but those sculpting their slow-speed preference remain enigmatic. Here, we probe this mechanism in mouse retina through patch clamp recordings, functional imaging, genetic manipulation, and electron microscopic reconstructions. We confirm earlier evidence that feedforward glycinergic inhibition is the main suppressor of ON DSGC responses to fast motion, and reveal the source for this inhibition—the VGluT3 amacrine cell, a dual neurotransmitter, excitatory/inhibitory interneuron. Together, our results identify a role for VGluT3 cells in limiting the speed range of OKN. More broadly, they suggest VGluT3 cells shape the response of many retinal cell types to fast motion, suppressing it in some while enhancing it in others.
format Online
Article
Text
id pubmed-10447436
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Nature Publishing Group UK
record_format MEDLINE/PubMed
spelling pubmed-104474362023-08-25 A circuit suppressing retinal drive to the optokinetic system during fast image motion Mani, Adam Yang, Xinzhu Zhao, Tiffany A. Leyrer, Megan L. Schreck, Daniel Berson, David M. Nat Commun Article Optokinetic nystagmus (OKN) assists stabilization of the retinal image during head rotation. OKN is driven by ON direction selective retinal ganglion cells (ON DSGCs), which encode both the direction and speed of global retinal slip. The synaptic circuits responsible for the direction selectivity of ON DSGCs are well understood, but those sculpting their slow-speed preference remain enigmatic. Here, we probe this mechanism in mouse retina through patch clamp recordings, functional imaging, genetic manipulation, and electron microscopic reconstructions. We confirm earlier evidence that feedforward glycinergic inhibition is the main suppressor of ON DSGC responses to fast motion, and reveal the source for this inhibition—the VGluT3 amacrine cell, a dual neurotransmitter, excitatory/inhibitory interneuron. Together, our results identify a role for VGluT3 cells in limiting the speed range of OKN. More broadly, they suggest VGluT3 cells shape the response of many retinal cell types to fast motion, suppressing it in some while enhancing it in others. Nature Publishing Group UK 2023-08-23 /pmc/articles/PMC10447436/ /pubmed/37612305 http://dx.doi.org/10.1038/s41467-023-40527-z Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Mani, Adam
Yang, Xinzhu
Zhao, Tiffany A.
Leyrer, Megan L.
Schreck, Daniel
Berson, David M.
A circuit suppressing retinal drive to the optokinetic system during fast image motion
title A circuit suppressing retinal drive to the optokinetic system during fast image motion
title_full A circuit suppressing retinal drive to the optokinetic system during fast image motion
title_fullStr A circuit suppressing retinal drive to the optokinetic system during fast image motion
title_full_unstemmed A circuit suppressing retinal drive to the optokinetic system during fast image motion
title_short A circuit suppressing retinal drive to the optokinetic system during fast image motion
title_sort circuit suppressing retinal drive to the optokinetic system during fast image motion
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10447436/
https://www.ncbi.nlm.nih.gov/pubmed/37612305
http://dx.doi.org/10.1038/s41467-023-40527-z
work_keys_str_mv AT maniadam acircuitsuppressingretinaldrivetotheoptokineticsystemduringfastimagemotion
AT yangxinzhu acircuitsuppressingretinaldrivetotheoptokineticsystemduringfastimagemotion
AT zhaotiffanya acircuitsuppressingretinaldrivetotheoptokineticsystemduringfastimagemotion
AT leyrermeganl acircuitsuppressingretinaldrivetotheoptokineticsystemduringfastimagemotion
AT schreckdaniel acircuitsuppressingretinaldrivetotheoptokineticsystemduringfastimagemotion
AT bersondavidm acircuitsuppressingretinaldrivetotheoptokineticsystemduringfastimagemotion
AT maniadam circuitsuppressingretinaldrivetotheoptokineticsystemduringfastimagemotion
AT yangxinzhu circuitsuppressingretinaldrivetotheoptokineticsystemduringfastimagemotion
AT zhaotiffanya circuitsuppressingretinaldrivetotheoptokineticsystemduringfastimagemotion
AT leyrermeganl circuitsuppressingretinaldrivetotheoptokineticsystemduringfastimagemotion
AT schreckdaniel circuitsuppressingretinaldrivetotheoptokineticsystemduringfastimagemotion
AT bersondavidm circuitsuppressingretinaldrivetotheoptokineticsystemduringfastimagemotion