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Curr Biol. 2019 Jun 17;29(12):1976-1987.e4. doi: 10.1016/j.cub.2019.05.009. Epub 2019 May 30.

Dynamic REM Sleep Modulation by Ambient Temperature and the Critical Role of the Melanin-Concentrating Hormone System.

Author information

1
Bern University Hospital (Inselspital), University of Bern, 3010 Bern, Switzerland.
2
Center for Experimental Neurology, Department of Neurology, Bern University Hospital (Inselspital), University of Bern, 3010 Bern, Switzerland.
3
Department of Neurology, Bern University Hospital (Inselspital), University of Bern, Freiburgstrasse 18, 3010 Bern, Switzerland.
4
Center for Experimental Neurology, Department of Neurology, Bern University Hospital (Inselspital), University of Bern, 3010 Bern, Switzerland; Department of Biomedical Research (DBMR), Bern University Hospital (Inselspital), University of Bern, 3010 Bern, Switzerland.
5
Center for Experimental Neurology, Department of Neurology, Bern University Hospital (Inselspital), University of Bern, 3010 Bern, Switzerland; Department of Neurology, Bern University Hospital (Inselspital), University of Bern, Freiburgstrasse 18, 3010 Bern, Switzerland; Ohio Sleep Medicine Institute, 4975 Bradenton Avenue, Dublin, OH 43017, USA. Electronic address: markus.schmidt@insel.ch.

Abstract

Ambient temperature (Ta) warming toward the high end of the thermoneutral zone (TNZ) preferentially increases rapid eye movement (REM) sleep over non-REM (NREM) sleep across species. The control and function of this temperature-induced REM sleep expression have remained unknown. Melanin-concentrating hormone (MCH) neurons play an important role in REM sleep control. We hypothesize that the MCH system may modulate REM sleep as a function of Ta. Here, we show that wild-type (WT) mice dynamically increased REM sleep durations specifically during warm Ta pulsing within the TNZ, compared to both the TNZ cool and baseline constant Ta conditions, without significantly affecting either wake or NREM sleep durations. However, genetically engineered MCH receptor-1 knockout (MCHR1-KO) mice showed no significant changes in REM sleep as a function of Ta, even with increased sleep pressure following a 4-h sleep deprivation. Using MCH-cre mice transduced with channelrhodopsin, we then optogenetically activated MCH neurons time locked with Ta warming, showing an increase in REM sleep expression beyond what Ta warming in yellow fluorescent protein (YFP) control mice achieved. Finally, in mice transduced with archaerhodopsin-T, semi-chronic optogenetic MCH neuronal silencing during Ta warming completely blocked the increase in REM sleep seen in YFP controls. These data demonstrate a previously unknown role for the MCH system in the dynamic output expression of REM sleep during Ta manipulation. These findings are consistent with the energy allocation hypothesis of sleep function, suggesting that endotherms have evolved neural circuits to opportunistically express REM sleep when the need for thermoregulatory defense is minimized.

KEYWORDS:

MCH; NREM sleep; REM sleep; energy allocation hypothesis; lateral hypothalamus; melanin-concentrating hormone; rapid eye movement sleep; resource optimization; sleep function; thermoregulation

PMID:
31155350
DOI:
10.1016/j.cub.2019.05.009

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