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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Main Authors: Violetta Pilorz, Shu K E Tam, Steven Hughes, Carina A Pothecary, Aarti Jagannath, Mark W Hankins, David M Bannerman, Stafford L Lightman, Vladyslav V Vyazovskiy, Patrick M Nolan, Russell G Foster, Stuart N Peirson
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2016-06-01
Series:PLoS Biology
Online Access:https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.1002482&type=printable
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author Violetta Pilorz
Shu K E Tam
Steven Hughes
Carina A Pothecary
Aarti Jagannath
Mark W Hankins
David M Bannerman
Stafford L Lightman
Vladyslav V Vyazovskiy
Patrick M Nolan
Russell G Foster
Stuart N Peirson
author_facet Violetta Pilorz
Shu K E Tam
Steven Hughes
Carina A Pothecary
Aarti Jagannath
Mark W Hankins
David M Bannerman
Stafford L Lightman
Vladyslav V Vyazovskiy
Patrick M Nolan
Russell G Foster
Stuart N Peirson
author_sort Violetta Pilorz
collection DOAJ
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 doaj-art-8e54a1b7d6d44bfe9da8ac8da5e6e8c22025-08-20T02:03:16ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852016-06-01146e100248210.1371/journal.pbio.1002482Melanopsin Regulates Both Sleep-Promoting and Arousal-Promoting Responses to Light.Violetta PilorzShu K E TamSteven HughesCarina A PothecaryAarti JagannathMark W HankinsDavid M BannermanStafford L LightmanVladyslav V VyazovskiyPatrick M NolanRussell G FosterStuart N PeirsonLight 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.https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.1002482&type=printable
spellingShingle Violetta Pilorz
Shu K E Tam
Steven Hughes
Carina A Pothecary
Aarti Jagannath
Mark W Hankins
David M Bannerman
Stafford L Lightman
Vladyslav V Vyazovskiy
Patrick M Nolan
Russell G Foster
Stuart N Peirson
Melanopsin Regulates Both Sleep-Promoting and Arousal-Promoting Responses to Light.
PLoS Biology
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
url https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.1002482&type=printable
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