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Melanopsin Regulates Both Sleep-Promoting and Arousal-Promoting Responses to Light

Light plays a critical role in the regulation of numerous aspects of physiology and behaviour, including the entrainment of circadian rhythms and the regulation of sleep. These responses involve melanopsin (OPN4)-expressing photosensitive retinal ganglion cells (pRGCs) in addition to rods and cones....

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Autores principales: Pilorz, Violetta, Tam, Shu K. E., Hughes, Steven, Pothecary, Carina A., Jagannath, Aarti, Hankins, Mark W., Bannerman, David M., Lightman, Stafford L., Vyazovskiy, Vladyslav V., Nolan, Patrick M., Foster, Russell G., Peirson, Stuart N.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4898879/
https://www.ncbi.nlm.nih.gov/pubmed/27276063
http://dx.doi.org/10.1371/journal.pbio.1002482
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author Pilorz, Violetta
Tam, Shu K. E.
Hughes, Steven
Pothecary, Carina A.
Jagannath, Aarti
Hankins, Mark W.
Bannerman, David M.
Lightman, Stafford L.
Vyazovskiy, Vladyslav V.
Nolan, Patrick M.
Foster, Russell G.
Peirson, Stuart N.
author_facet Pilorz, Violetta
Tam, Shu K. E.
Hughes, Steven
Pothecary, Carina A.
Jagannath, Aarti
Hankins, Mark W.
Bannerman, David M.
Lightman, Stafford L.
Vyazovskiy, Vladyslav V.
Nolan, Patrick M.
Foster, Russell G.
Peirson, Stuart N.
author_sort Pilorz, Violetta
collection PubMed
description Light plays a critical role in the regulation of numerous aspects of physiology and behaviour, including the entrainment of circadian rhythms and the regulation of sleep. These responses involve melanopsin (OPN4)-expressing photosensitive retinal ganglion cells (pRGCs) in addition to rods and cones. Nocturnal light exposure in rodents has been shown to result in rapid sleep induction, in which melanopsin plays a key role. However, studies have also shown that light exposure can result in elevated corticosterone, a response that is not compatible with sleep. To investigate these contradictory findings and to dissect the relative contribution of pRGCs and rods/cones, we assessed the effects of light of different wavelengths on behaviourally defined sleep. Here, we show that blue light (470 nm) causes behavioural arousal, elevating corticosterone and delaying sleep onset. By contrast, green light (530 nm) produces rapid sleep induction. Compared to wildtype mice, these responses are altered in melanopsin-deficient mice (Opn4(-/-)), resulting in enhanced sleep in response to blue light but delayed sleep induction in response to green or white light. We go on to show that blue light evokes higher Fos induction in the SCN compared to the sleep-promoting ventrolateral preoptic area (VLPO), whereas green light produced greater responses in the VLPO. Collectively, our data demonstrates that nocturnal light exposure can have either an arousal- or sleep-promoting effect, and that these responses are melanopsin-mediated via different neural pathways with different spectral sensitivities. These findings raise important questions relating to how artificial light may alter behaviour in both the work and domestic setting.
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spelling pubmed-48988792016-06-16 Melanopsin Regulates Both Sleep-Promoting and Arousal-Promoting Responses to Light Pilorz, Violetta Tam, Shu K. E. Hughes, Steven Pothecary, Carina A. Jagannath, Aarti Hankins, Mark W. Bannerman, David M. Lightman, Stafford L. Vyazovskiy, Vladyslav V. Nolan, Patrick M. Foster, Russell G. Peirson, Stuart N. PLoS Biol Research Article Light plays a critical role in the regulation of numerous aspects of physiology and behaviour, including the entrainment of circadian rhythms and the regulation of sleep. These responses involve melanopsin (OPN4)-expressing photosensitive retinal ganglion cells (pRGCs) in addition to rods and cones. Nocturnal light exposure in rodents has been shown to result in rapid sleep induction, in which melanopsin plays a key role. However, studies have also shown that light exposure can result in elevated corticosterone, a response that is not compatible with sleep. To investigate these contradictory findings and to dissect the relative contribution of pRGCs and rods/cones, we assessed the effects of light of different wavelengths on behaviourally defined sleep. Here, we show that blue light (470 nm) causes behavioural arousal, elevating corticosterone and delaying sleep onset. By contrast, green light (530 nm) produces rapid sleep induction. Compared to wildtype mice, these responses are altered in melanopsin-deficient mice (Opn4(-/-)), resulting in enhanced sleep in response to blue light but delayed sleep induction in response to green or white light. We go on to show that blue light evokes higher Fos induction in the SCN compared to the sleep-promoting ventrolateral preoptic area (VLPO), whereas green light produced greater responses in the VLPO. Collectively, our data demonstrates that nocturnal light exposure can have either an arousal- or sleep-promoting effect, and that these responses are melanopsin-mediated via different neural pathways with different spectral sensitivities. These findings raise important questions relating to how artificial light may alter behaviour in both the work and domestic setting. Public Library of Science 2016-06-08 /pmc/articles/PMC4898879/ /pubmed/27276063 http://dx.doi.org/10.1371/journal.pbio.1002482 Text en © 2016 Pilorz et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Pilorz, Violetta
Tam, Shu K. E.
Hughes, Steven
Pothecary, Carina A.
Jagannath, Aarti
Hankins, Mark W.
Bannerman, David M.
Lightman, Stafford L.
Vyazovskiy, Vladyslav V.
Nolan, Patrick M.
Foster, Russell G.
Peirson, Stuart N.
Melanopsin Regulates Both Sleep-Promoting and Arousal-Promoting Responses to Light
title Melanopsin Regulates Both Sleep-Promoting and Arousal-Promoting Responses to Light
title_full Melanopsin Regulates Both Sleep-Promoting and Arousal-Promoting Responses to Light
title_fullStr Melanopsin Regulates Both Sleep-Promoting and Arousal-Promoting Responses to Light
title_full_unstemmed Melanopsin Regulates Both Sleep-Promoting and Arousal-Promoting Responses to Light
title_short Melanopsin Regulates Both Sleep-Promoting and Arousal-Promoting Responses to Light
title_sort melanopsin regulates both sleep-promoting and arousal-promoting responses to light
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4898879/
https://www.ncbi.nlm.nih.gov/pubmed/27276063
http://dx.doi.org/10.1371/journal.pbio.1002482
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