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. 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.
Sleep and Circadian Neuroscience Institute (SCNi), Nuffield Department of Clinical Neurosciences, Oxford Molecular Pathology Institute, Dunn School of Pathology, University of Oxford, Oxford, United Kingdom.
Violetta
0000-0003-0474-8975
V
Pilorz
Sleep and Circadian Neuroscience Institute (SCNi), Nuffield Department of Clinical Neurosciences, Oxford Molecular Pathology Institute, Dunn School of Pathology, University of Oxford, Oxford, United Kingdom.
Shu K E
SK
Tam
Sleep and Circadian Neuroscience Institute (SCNi), Nuffield Department of Clinical Neurosciences, Oxford Molecular Pathology Institute, Dunn School of Pathology, University of Oxford, Oxford, United Kingdom.
Steven
S
Hughes
Sleep and Circadian Neuroscience Institute (SCNi), Nuffield Department of Clinical Neurosciences, Oxford Molecular Pathology Institute, Dunn School of Pathology, University of Oxford, Oxford, United Kingdom.
Carina A
0000-0001-8759-9404
CA
Pothecary
Sleep and Circadian Neuroscience Institute (SCNi), Nuffield Department of Clinical Neurosciences, Oxford Molecular Pathology Institute, Dunn School of Pathology, University of Oxford, Oxford, United Kingdom.
Aarti
A
Jagannath
Sleep and Circadian Neuroscience Institute (SCNi), Nuffield Department of Clinical Neurosciences, Oxford Molecular Pathology Institute, Dunn School of Pathology, University of Oxford, Oxford, United Kingdom.
Mark W
MW
Hankins
Department of Experimental Psychology, University of Oxford, Oxford, United Kingdom.
David M
DM
Bannerman
Henry Wellcome Laboratories for Integrative Neuroscience and Endocrinology, University of Bristol, Bristol, United Kingdom.
Stafford L
SL
Lightman
Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford, United Kingdom.
Vladyslav V
VV
Vyazovskiy
MRC Harwell, Harwell Science and Innovation Campus, Oxfordshire, United Kingdom.
Patrick M
PM
Nolan
Sleep and Circadian Neuroscience Institute (SCNi), Nuffield Department of Clinical Neurosciences, Oxford Molecular Pathology Institute, Dunn School of Pathology, University of Oxford, Oxford, United Kingdom.
Russell G
RG
Foster
Sleep and Circadian Neuroscience Institute (SCNi), Nuffield Department of Clinical Neurosciences, Oxford Molecular Pathology Institute, Dunn School of Pathology, University of Oxford, Oxford, United Kingdom.
Stuart N
SN
Peirson
D000818:Animals; D001143:Arousal / Q000502:physiology / Q000528:radiation effects*; D003345:Corticosterone / Q000097:blood / Q000378:metabolism; D015870:Gene Expression / Q000528:radiation effects; D008027:Light; D008810:Mice, Inbred C57BL; D018345:Mice, Knockout; D008954:Models, Biological; D056950:Period Circadian Proteins / Q000235:genetics; D020419:Photoreceptor Cells, Vertebrate / Q000378:metabolism / Q000528:radiation effects; D011301:Preoptic Area / Q000378:metabolism / Q000528:radiation effects; D016760:Proto-Oncogene Proteins c-fos / Q000235:genetics; D012165:Retinal Ganglion Cells / Q000378:metabolism / Q000528:radiation effects; D017299:Rod Opsins / Q000235:genetics / Q000378:metabolism*; D012890:Sleep / Q000502:physiology / Q000528:radiation effects*; D013493:Suprachiasmatic Nucleus / Q000378:metabolism / Q000528:radiation effects; D013997:Time Factors; D000099210:Melanopsin
D003345:Corticosterone; D056950:Period Circadian Proteins; D016760:Proto-Oncogene Proteins c-fos; D017299:Rod Opsins; D000099210:Melanopsin; C539023:Per1 protein, mouse; C513312:Per2 protein, mouse