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Sleep deprivation, sleep fragmentation, and social jet lag increase temperature preference in Drosophila

Despite the fact that sleep deprivation substantially affects the way animals regulate their body temperature, the specific mechanisms behind this phenomenon are not well understood. In both mammals and flies, neural circuits regulating sleep and thermoregulation overlap, suggesting an interdependen...

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Autores principales: Roach, S. Tanner, Ford, Melanie C., Simhambhatla, Vikram, Loutrianakis, Vasilios, Farah, Hamza, Li, Zhaoyi, Periandri, Erica M., Abdalla, Dina, Huang, Irene, Kalra, Arjan, Shaw, Paul J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10237294/
https://www.ncbi.nlm.nih.gov/pubmed/37274220
http://dx.doi.org/10.3389/fnins.2023.1175478
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author Roach, S. Tanner
Ford, Melanie C.
Simhambhatla, Vikram
Loutrianakis, Vasilios
Farah, Hamza
Li, Zhaoyi
Periandri, Erica M.
Abdalla, Dina
Huang, Irene
Kalra, Arjan
Shaw, Paul J.
author_facet Roach, S. Tanner
Ford, Melanie C.
Simhambhatla, Vikram
Loutrianakis, Vasilios
Farah, Hamza
Li, Zhaoyi
Periandri, Erica M.
Abdalla, Dina
Huang, Irene
Kalra, Arjan
Shaw, Paul J.
author_sort Roach, S. Tanner
collection PubMed
description Despite the fact that sleep deprivation substantially affects the way animals regulate their body temperature, the specific mechanisms behind this phenomenon are not well understood. In both mammals and flies, neural circuits regulating sleep and thermoregulation overlap, suggesting an interdependence that may be relevant for sleep function. To investigate this relationship further, we exposed flies to 12 h of sleep deprivation, or 48 h of sleep fragmentation and evaluated temperature preference in a thermal gradient. Flies exposed to 12 h of sleep deprivation chose warmer temperatures after sleep deprivation. Importantly, sleep fragmentation, which prevents flies from entering deeper stages of sleep, but does not activate sleep homeostatic mechanisms nor induce impairments in short-term memory also resulted in flies choosing warmer temperatures. To identify the underlying neuronal circuits, we used RNAi to knock down the receptor for Pigment dispersing factor, a peptide that influences circadian rhythms, temperature preference and sleep. Expressing UAS-Pdfr(RNAi) in subsets of clock neurons prevented sleep fragmentation from increasing temperature preference. Finally, we evaluated temperature preference after flies had undergone a social jet lag protocol which is known to disrupt clock neurons. In this protocol, flies experience a 3 h light phase delay on Friday followed by a 3 h light advance on Sunday evening. Flies exposed to social jet lag exhibited an increase in temperature preference which persisted for several days. Our findings identify specific clock neurons that are modulated by sleep disruption to increase temperature preference. Moreover, our data indicate that temperature preference may be a more sensitive indicator of sleep disruption than learning and memory.
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spelling pubmed-102372942023-06-03 Sleep deprivation, sleep fragmentation, and social jet lag increase temperature preference in Drosophila Roach, S. Tanner Ford, Melanie C. Simhambhatla, Vikram Loutrianakis, Vasilios Farah, Hamza Li, Zhaoyi Periandri, Erica M. Abdalla, Dina Huang, Irene Kalra, Arjan Shaw, Paul J. Front Neurosci Neuroscience Despite the fact that sleep deprivation substantially affects the way animals regulate their body temperature, the specific mechanisms behind this phenomenon are not well understood. In both mammals and flies, neural circuits regulating sleep and thermoregulation overlap, suggesting an interdependence that may be relevant for sleep function. To investigate this relationship further, we exposed flies to 12 h of sleep deprivation, or 48 h of sleep fragmentation and evaluated temperature preference in a thermal gradient. Flies exposed to 12 h of sleep deprivation chose warmer temperatures after sleep deprivation. Importantly, sleep fragmentation, which prevents flies from entering deeper stages of sleep, but does not activate sleep homeostatic mechanisms nor induce impairments in short-term memory also resulted in flies choosing warmer temperatures. To identify the underlying neuronal circuits, we used RNAi to knock down the receptor for Pigment dispersing factor, a peptide that influences circadian rhythms, temperature preference and sleep. Expressing UAS-Pdfr(RNAi) in subsets of clock neurons prevented sleep fragmentation from increasing temperature preference. Finally, we evaluated temperature preference after flies had undergone a social jet lag protocol which is known to disrupt clock neurons. In this protocol, flies experience a 3 h light phase delay on Friday followed by a 3 h light advance on Sunday evening. Flies exposed to social jet lag exhibited an increase in temperature preference which persisted for several days. Our findings identify specific clock neurons that are modulated by sleep disruption to increase temperature preference. Moreover, our data indicate that temperature preference may be a more sensitive indicator of sleep disruption than learning and memory. Frontiers Media S.A. 2023-05-19 /pmc/articles/PMC10237294/ /pubmed/37274220 http://dx.doi.org/10.3389/fnins.2023.1175478 Text en Copyright © 2023 Roach, Ford, Simhambhatla, Loutrianakis, Farah, Li, Periandri, Abdalla, Huang, Kalra and Shaw. 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
Roach, S. Tanner
Ford, Melanie C.
Simhambhatla, Vikram
Loutrianakis, Vasilios
Farah, Hamza
Li, Zhaoyi
Periandri, Erica M.
Abdalla, Dina
Huang, Irene
Kalra, Arjan
Shaw, Paul J.
Sleep deprivation, sleep fragmentation, and social jet lag increase temperature preference in Drosophila
title Sleep deprivation, sleep fragmentation, and social jet lag increase temperature preference in Drosophila
title_full Sleep deprivation, sleep fragmentation, and social jet lag increase temperature preference in Drosophila
title_fullStr Sleep deprivation, sleep fragmentation, and social jet lag increase temperature preference in Drosophila
title_full_unstemmed Sleep deprivation, sleep fragmentation, and social jet lag increase temperature preference in Drosophila
title_short Sleep deprivation, sleep fragmentation, and social jet lag increase temperature preference in Drosophila
title_sort sleep deprivation, sleep fragmentation, and social jet lag increase temperature preference in drosophila
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10237294/
https://www.ncbi.nlm.nih.gov/pubmed/37274220
http://dx.doi.org/10.3389/fnins.2023.1175478
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