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

Ze Zhang (), Corinne Beier, Tenley Weil and Samer Hattar ()
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Ze Zhang: Section on Light and Circadian Rhythms, National Institute of Mental Health (NIMH), National Institutes of Health (NIH)
Corinne Beier: Section on Light and Circadian Rhythms, National Institute of Mental Health (NIMH), National Institutes of Health (NIH)
Tenley Weil: Section on Light and Circadian Rhythms, National Institute of Mental Health (NIMH), National Institutes of Health (NIH)
Samer Hattar: Section on Light and Circadian Rhythms, National Institute of Mental Health (NIMH), National Institutes of Health (NIH)

Nature Communications, 2021, vol. 12, issue 1, 1-11

Abstract: Abstract 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.

Date: 2021
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DOI: 10.1038/s41467-021-25378-w

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