Cargando…

Nitric Oxide Synthase Neurons in the Preoptic Hypothalamus Are NREM and REM Sleep-Active and Lower Body Temperature

When mice are exposed to external warmth, nitric oxide synthase (NOS1) neurons in the median and medial preoptic (MnPO/MPO) hypothalamus induce sleep and concomitant body cooling. However, how these neurons regulate baseline sleep and body temperature is unknown. Using calcium photometry, we show th...

Descripción completa

Detalles Bibliográficos
Autores principales: Harding, Edward C., Ba, Wei, Zahir, Reesha, Yu, Xiao, Yustos, Raquel, Hsieh, Bryan, Lignos, Leda, Vyssotski, Alexei L., Merkle, Florian T., Constandinou, Timothy G., Franks, Nicholas P., Wisden, William
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8551479/
https://www.ncbi.nlm.nih.gov/pubmed/34720852
http://dx.doi.org/10.3389/fnins.2021.709825
_version_ 1784591166778376192
author Harding, Edward C.
Ba, Wei
Zahir, Reesha
Yu, Xiao
Yustos, Raquel
Hsieh, Bryan
Lignos, Leda
Vyssotski, Alexei L.
Merkle, Florian T.
Constandinou, Timothy G.
Franks, Nicholas P.
Wisden, William
author_facet Harding, Edward C.
Ba, Wei
Zahir, Reesha
Yu, Xiao
Yustos, Raquel
Hsieh, Bryan
Lignos, Leda
Vyssotski, Alexei L.
Merkle, Florian T.
Constandinou, Timothy G.
Franks, Nicholas P.
Wisden, William
author_sort Harding, Edward C.
collection PubMed
description When mice are exposed to external warmth, nitric oxide synthase (NOS1) neurons in the median and medial preoptic (MnPO/MPO) hypothalamus induce sleep and concomitant body cooling. However, how these neurons regulate baseline sleep and body temperature is unknown. Using calcium photometry, we show that NOS1 neurons in MnPO/MPO are predominantly NREM and REM active, especially at the boundary of wake to NREM transitions, and in the later parts of REM bouts, with lower activity during wakefulness. In addition to releasing nitric oxide, NOS1 neurons in MnPO/MPO can release GABA, glutamate and peptides. We expressed tetanus-toxin light-chain in MnPO/MPO NOS1 cells to reduce vesicular release of transmitters. This induced changes in sleep structure: over 24 h, mice had less NREM sleep in their dark (active) phase, and more NREM sleep in their light (sleep) phase. REM sleep episodes in the dark phase were longer, and there were fewer REM transitions between other vigilance states. REM sleep had less theta power. Mice with synaptically blocked MnPO/MPO NOS1 neurons were also warmer than control mice at the dark-light transition (ZT0), as well as during the dark phase siesta (ZT16-20), where there is usually a body temperature dip. Also, at this siesta point of cooled body temperature, mice usually have more NREM, but mice with synaptically blocked MnPO/MPO NOS1 cells showed reduced NREM sleep at this time. Overall, MnPO/MPO NOS1 neurons promote both NREM and REM sleep and contribute to chronically lowering body temperature, particularly at transitions where the mice normally enter NREM sleep.
format Online
Article
Text
id pubmed-8551479
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-85514792021-10-29 Nitric Oxide Synthase Neurons in the Preoptic Hypothalamus Are NREM and REM Sleep-Active and Lower Body Temperature Harding, Edward C. Ba, Wei Zahir, Reesha Yu, Xiao Yustos, Raquel Hsieh, Bryan Lignos, Leda Vyssotski, Alexei L. Merkle, Florian T. Constandinou, Timothy G. Franks, Nicholas P. Wisden, William Front Neurosci Neuroscience When mice are exposed to external warmth, nitric oxide synthase (NOS1) neurons in the median and medial preoptic (MnPO/MPO) hypothalamus induce sleep and concomitant body cooling. However, how these neurons regulate baseline sleep and body temperature is unknown. Using calcium photometry, we show that NOS1 neurons in MnPO/MPO are predominantly NREM and REM active, especially at the boundary of wake to NREM transitions, and in the later parts of REM bouts, with lower activity during wakefulness. In addition to releasing nitric oxide, NOS1 neurons in MnPO/MPO can release GABA, glutamate and peptides. We expressed tetanus-toxin light-chain in MnPO/MPO NOS1 cells to reduce vesicular release of transmitters. This induced changes in sleep structure: over 24 h, mice had less NREM sleep in their dark (active) phase, and more NREM sleep in their light (sleep) phase. REM sleep episodes in the dark phase were longer, and there were fewer REM transitions between other vigilance states. REM sleep had less theta power. Mice with synaptically blocked MnPO/MPO NOS1 neurons were also warmer than control mice at the dark-light transition (ZT0), as well as during the dark phase siesta (ZT16-20), where there is usually a body temperature dip. Also, at this siesta point of cooled body temperature, mice usually have more NREM, but mice with synaptically blocked MnPO/MPO NOS1 cells showed reduced NREM sleep at this time. Overall, MnPO/MPO NOS1 neurons promote both NREM and REM sleep and contribute to chronically lowering body temperature, particularly at transitions where the mice normally enter NREM sleep. Frontiers Media S.A. 2021-10-14 /pmc/articles/PMC8551479/ /pubmed/34720852 http://dx.doi.org/10.3389/fnins.2021.709825 Text en Copyright © 2021 Harding, Ba, Zahir, Yu, Yustos, Hsieh, Lignos, Vyssotski, Merkle, Constandinou, Franks and Wisden. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Harding, Edward C.
Ba, Wei
Zahir, Reesha
Yu, Xiao
Yustos, Raquel
Hsieh, Bryan
Lignos, Leda
Vyssotski, Alexei L.
Merkle, Florian T.
Constandinou, Timothy G.
Franks, Nicholas P.
Wisden, William
Nitric Oxide Synthase Neurons in the Preoptic Hypothalamus Are NREM and REM Sleep-Active and Lower Body Temperature
title Nitric Oxide Synthase Neurons in the Preoptic Hypothalamus Are NREM and REM Sleep-Active and Lower Body Temperature
title_full Nitric Oxide Synthase Neurons in the Preoptic Hypothalamus Are NREM and REM Sleep-Active and Lower Body Temperature
title_fullStr Nitric Oxide Synthase Neurons in the Preoptic Hypothalamus Are NREM and REM Sleep-Active and Lower Body Temperature
title_full_unstemmed Nitric Oxide Synthase Neurons in the Preoptic Hypothalamus Are NREM and REM Sleep-Active and Lower Body Temperature
title_short Nitric Oxide Synthase Neurons in the Preoptic Hypothalamus Are NREM and REM Sleep-Active and Lower Body Temperature
title_sort nitric oxide synthase neurons in the preoptic hypothalamus are nrem and rem sleep-active and lower body temperature
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8551479/
https://www.ncbi.nlm.nih.gov/pubmed/34720852
http://dx.doi.org/10.3389/fnins.2021.709825
work_keys_str_mv AT hardingedwardc nitricoxidesynthaseneuronsinthepreoptichypothalamusarenremandremsleepactiveandlowerbodytemperature
AT bawei nitricoxidesynthaseneuronsinthepreoptichypothalamusarenremandremsleepactiveandlowerbodytemperature
AT zahirreesha nitricoxidesynthaseneuronsinthepreoptichypothalamusarenremandremsleepactiveandlowerbodytemperature
AT yuxiao nitricoxidesynthaseneuronsinthepreoptichypothalamusarenremandremsleepactiveandlowerbodytemperature
AT yustosraquel nitricoxidesynthaseneuronsinthepreoptichypothalamusarenremandremsleepactiveandlowerbodytemperature
AT hsiehbryan nitricoxidesynthaseneuronsinthepreoptichypothalamusarenremandremsleepactiveandlowerbodytemperature
AT lignosleda nitricoxidesynthaseneuronsinthepreoptichypothalamusarenremandremsleepactiveandlowerbodytemperature
AT vyssotskialexeil nitricoxidesynthaseneuronsinthepreoptichypothalamusarenremandremsleepactiveandlowerbodytemperature
AT merklefloriant nitricoxidesynthaseneuronsinthepreoptichypothalamusarenremandremsleepactiveandlowerbodytemperature
AT constandinoutimothyg nitricoxidesynthaseneuronsinthepreoptichypothalamusarenremandremsleepactiveandlowerbodytemperature
AT franksnicholasp nitricoxidesynthaseneuronsinthepreoptichypothalamusarenremandremsleepactiveandlowerbodytemperature
AT wisdenwilliam nitricoxidesynthaseneuronsinthepreoptichypothalamusarenremandremsleepactiveandlowerbodytemperature