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The retinal ipRGC-preoptic circuit mediates the acute effect of light on sleep

Light regulates daily sleep rhythms by a neural circuit that connects intrinsically photosensitive retinal ganglion cells (ipRGCs) to the circadian pacemaker, the suprachiasmatic nucleus. Light, however, also acutely affects sleep in a circadian-independent manner. The neural circuits involving the...

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Autores principales: Zhang, Ze, Beier, Corinne, Weil, Tenley, Hattar, Samer
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8387462/
https://www.ncbi.nlm.nih.gov/pubmed/34433830
http://dx.doi.org/10.1038/s41467-021-25378-w
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author Zhang, Ze
Beier, Corinne
Weil, Tenley
Hattar, Samer
author_facet Zhang, Ze
Beier, Corinne
Weil, Tenley
Hattar, Samer
author_sort Zhang, Ze
collection PubMed
description Light regulates daily sleep rhythms by a neural circuit that connects intrinsically photosensitive retinal ganglion cells (ipRGCs) to the circadian pacemaker, the suprachiasmatic nucleus. Light, however, also acutely affects sleep in a circadian-independent manner. The neural circuits involving the acute effect of light on sleep remain unknown. Here we uncovered a neural circuit that drives this acute light response, independent of the suprachiasmatic nucleus, but still through ipRGCs. We show that ipRGCs substantially innervate the preoptic area (POA) to mediate the acute light effect on sleep in mice. Consistently, activation of either the POA projecting ipRGCs or the light-responsive POA neurons increased non-rapid eye movement (NREM) sleep without influencing REM sleep. In addition, inhibition of the light-responsive POA neurons blocked the acute light effects on NREM sleep. The predominant light-responsive POA neurons that receive ipRGC input belong to the corticotropin-releasing hormone subpopulation. Remarkably, the light-responsive POA neurons are inhibitory and project to well-known wakefulness-promoting brain regions, such as the tuberomammillary nucleus and the lateral hypothalamus. Therefore, activation of the ipRGC-POA circuit inhibits arousal brain regions to drive light-induced NREM sleep. Our findings reveal a functional retina-brain circuit that is both necessary and sufficient for the acute effect of light on sleep.
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spelling pubmed-83874622021-09-22 The retinal ipRGC-preoptic circuit mediates the acute effect of light on sleep Zhang, Ze Beier, Corinne Weil, Tenley Hattar, Samer Nat Commun Article Light regulates daily sleep rhythms by a neural circuit that connects intrinsically photosensitive retinal ganglion cells (ipRGCs) to the circadian pacemaker, the suprachiasmatic nucleus. Light, however, also acutely affects sleep in a circadian-independent manner. The neural circuits involving the acute effect of light on sleep remain unknown. Here we uncovered a neural circuit that drives this acute light response, independent of the suprachiasmatic nucleus, but still through ipRGCs. We show that ipRGCs substantially innervate the preoptic area (POA) to mediate the acute light effect on sleep in mice. Consistently, activation of either the POA projecting ipRGCs or the light-responsive POA neurons increased non-rapid eye movement (NREM) sleep without influencing REM sleep. In addition, inhibition of the light-responsive POA neurons blocked the acute light effects on NREM sleep. The predominant light-responsive POA neurons that receive ipRGC input belong to the corticotropin-releasing hormone subpopulation. Remarkably, the light-responsive POA neurons are inhibitory and project to well-known wakefulness-promoting brain regions, such as the tuberomammillary nucleus and the lateral hypothalamus. Therefore, activation of the ipRGC-POA circuit inhibits arousal brain regions to drive light-induced NREM sleep. Our findings reveal a functional retina-brain circuit that is both necessary and sufficient for the acute effect of light on sleep. Nature Publishing Group UK 2021-08-25 /pmc/articles/PMC8387462/ /pubmed/34433830 http://dx.doi.org/10.1038/s41467-021-25378-w Text en © This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply 2021 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 license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license 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 license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Zhang, Ze
Beier, Corinne
Weil, Tenley
Hattar, Samer
The retinal ipRGC-preoptic circuit mediates the acute effect of light on sleep
title The retinal ipRGC-preoptic circuit mediates the acute effect of light on sleep
title_full The retinal ipRGC-preoptic circuit mediates the acute effect of light on sleep
title_fullStr The retinal ipRGC-preoptic circuit mediates the acute effect of light on sleep
title_full_unstemmed The retinal ipRGC-preoptic circuit mediates the acute effect of light on sleep
title_short The retinal ipRGC-preoptic circuit mediates the acute effect of light on sleep
title_sort retinal iprgc-preoptic circuit mediates the acute effect of light on sleep
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8387462/
https://www.ncbi.nlm.nih.gov/pubmed/34433830
http://dx.doi.org/10.1038/s41467-021-25378-w
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