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Retina-derived signals control pace of neurogenesis in visual brain areas but not circuit assembly

Brain development is orchestrated by both innate and experience-dependent mechanisms, but their relative contributions are difficult to disentangle. Here we asked if and how central visual areas are altered in a vertebrate brain depleted of any and all signals from retinal ganglion cells throughout...

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Autores principales: Sherman, Shachar, Arnold-Ammer, Irene, Schneider, Martin W., Kawakami, Koichi, Baier, Herwig
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10533834/
https://www.ncbi.nlm.nih.gov/pubmed/37758715
http://dx.doi.org/10.1038/s41467-023-40749-1
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author Sherman, Shachar
Arnold-Ammer, Irene
Schneider, Martin W.
Kawakami, Koichi
Baier, Herwig
author_facet Sherman, Shachar
Arnold-Ammer, Irene
Schneider, Martin W.
Kawakami, Koichi
Baier, Herwig
author_sort Sherman, Shachar
collection PubMed
description Brain development is orchestrated by both innate and experience-dependent mechanisms, but their relative contributions are difficult to disentangle. Here we asked if and how central visual areas are altered in a vertebrate brain depleted of any and all signals from retinal ganglion cells throughout development. We transcriptionally profiled neurons in pretectum, thalamus and other retinorecipient areas of larval zebrafish and searched for changes in lakritz mutants that lack all retinal connections. Although individual genes are dysregulated, the complete set of 77 neuronal types develops in apparently normal proportions, at normal locations, and along normal differentiation trajectories. Strikingly, the cell-cycle exits of proliferating progenitors in these areas are delayed, and a greater fraction of early postmitotic precursors remain uncommitted or are diverted to a pre-glial fate. Optogenetic stimulation targeting groups of neurons normally involved in processing visual information evokes behaviors indistinguishable from wildtype. In conclusion, we show that signals emitted by retinal axons influence the pace of neurogenesis in visual brain areas, but do not detectably affect the specification or wiring of downstream neurons.
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spelling pubmed-105338342023-09-29 Retina-derived signals control pace of neurogenesis in visual brain areas but not circuit assembly Sherman, Shachar Arnold-Ammer, Irene Schneider, Martin W. Kawakami, Koichi Baier, Herwig Nat Commun Article Brain development is orchestrated by both innate and experience-dependent mechanisms, but their relative contributions are difficult to disentangle. Here we asked if and how central visual areas are altered in a vertebrate brain depleted of any and all signals from retinal ganglion cells throughout development. We transcriptionally profiled neurons in pretectum, thalamus and other retinorecipient areas of larval zebrafish and searched for changes in lakritz mutants that lack all retinal connections. Although individual genes are dysregulated, the complete set of 77 neuronal types develops in apparently normal proportions, at normal locations, and along normal differentiation trajectories. Strikingly, the cell-cycle exits of proliferating progenitors in these areas are delayed, and a greater fraction of early postmitotic precursors remain uncommitted or are diverted to a pre-glial fate. Optogenetic stimulation targeting groups of neurons normally involved in processing visual information evokes behaviors indistinguishable from wildtype. In conclusion, we show that signals emitted by retinal axons influence the pace of neurogenesis in visual brain areas, but do not detectably affect the specification or wiring of downstream neurons. Nature Publishing Group UK 2023-09-27 /pmc/articles/PMC10533834/ /pubmed/37758715 http://dx.doi.org/10.1038/s41467-023-40749-1 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
Sherman, Shachar
Arnold-Ammer, Irene
Schneider, Martin W.
Kawakami, Koichi
Baier, Herwig
Retina-derived signals control pace of neurogenesis in visual brain areas but not circuit assembly
title Retina-derived signals control pace of neurogenesis in visual brain areas but not circuit assembly
title_full Retina-derived signals control pace of neurogenesis in visual brain areas but not circuit assembly
title_fullStr Retina-derived signals control pace of neurogenesis in visual brain areas but not circuit assembly
title_full_unstemmed Retina-derived signals control pace of neurogenesis in visual brain areas but not circuit assembly
title_short Retina-derived signals control pace of neurogenesis in visual brain areas but not circuit assembly
title_sort retina-derived signals control pace of neurogenesis in visual brain areas but not circuit assembly
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10533834/
https://www.ncbi.nlm.nih.gov/pubmed/37758715
http://dx.doi.org/10.1038/s41467-023-40749-1
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