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Sleep-promoting neurons remodel their response properties to calibrate sleep drive with environmental demands

Falling asleep at the wrong time can place an individual at risk of immediate physical harm. However, not sleeping degrades cognition and adaptive behavior. To understand how animals match sleep need with environmental demands, we used live-brain imaging to examine the physiological response propert...

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Autores principales: Dissel, Stephane, Klose, Markus K., van Swinderen, Bruno, Cao, Lijuan, Ford, Melanie, Periandri, Erica M., Jones, Joseph D., Li, Zhaoyi, Shaw, Paul J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9521806/
https://www.ncbi.nlm.nih.gov/pubmed/36173939
http://dx.doi.org/10.1371/journal.pbio.3001797
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author Dissel, Stephane
Klose, Markus K.
van Swinderen, Bruno
Cao, Lijuan
Ford, Melanie
Periandri, Erica M.
Jones, Joseph D.
Li, Zhaoyi
Shaw, Paul J.
author_facet Dissel, Stephane
Klose, Markus K.
van Swinderen, Bruno
Cao, Lijuan
Ford, Melanie
Periandri, Erica M.
Jones, Joseph D.
Li, Zhaoyi
Shaw, Paul J.
author_sort Dissel, Stephane
collection PubMed
description Falling asleep at the wrong time can place an individual at risk of immediate physical harm. However, not sleeping degrades cognition and adaptive behavior. To understand how animals match sleep need with environmental demands, we used live-brain imaging to examine the physiological response properties of the dorsal fan-shaped body (dFB) following interventions that modify sleep (sleep deprivation, starvation, time-restricted feeding, memory consolidation) in Drosophila. We report that dFB neurons change their physiological response-properties to dopamine (DA) and allatostatin-A (AstA) in response to different types of waking. That is, dFB neurons are not simply passive components of a hard-wired circuit. Rather, the dFB neurons intrinsically regulate their response to the activity from upstream circuits. Finally, we show that the dFB appears to contain a memory trace of prior exposure to metabolic challenges induced by starvation or time-restricted feeding. Together, these data highlight that the sleep homeostat is plastic and suggests an underlying mechanism.
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spelling pubmed-95218062022-09-30 Sleep-promoting neurons remodel their response properties to calibrate sleep drive with environmental demands Dissel, Stephane Klose, Markus K. van Swinderen, Bruno Cao, Lijuan Ford, Melanie Periandri, Erica M. Jones, Joseph D. Li, Zhaoyi Shaw, Paul J. PLoS Biol Research Article Falling asleep at the wrong time can place an individual at risk of immediate physical harm. However, not sleeping degrades cognition and adaptive behavior. To understand how animals match sleep need with environmental demands, we used live-brain imaging to examine the physiological response properties of the dorsal fan-shaped body (dFB) following interventions that modify sleep (sleep deprivation, starvation, time-restricted feeding, memory consolidation) in Drosophila. We report that dFB neurons change their physiological response-properties to dopamine (DA) and allatostatin-A (AstA) in response to different types of waking. That is, dFB neurons are not simply passive components of a hard-wired circuit. Rather, the dFB neurons intrinsically regulate their response to the activity from upstream circuits. Finally, we show that the dFB appears to contain a memory trace of prior exposure to metabolic challenges induced by starvation or time-restricted feeding. Together, these data highlight that the sleep homeostat is plastic and suggests an underlying mechanism. Public Library of Science 2022-09-29 /pmc/articles/PMC9521806/ /pubmed/36173939 http://dx.doi.org/10.1371/journal.pbio.3001797 Text en © 2022 Dissel et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Dissel, Stephane
Klose, Markus K.
van Swinderen, Bruno
Cao, Lijuan
Ford, Melanie
Periandri, Erica M.
Jones, Joseph D.
Li, Zhaoyi
Shaw, Paul J.
Sleep-promoting neurons remodel their response properties to calibrate sleep drive with environmental demands
title Sleep-promoting neurons remodel their response properties to calibrate sleep drive with environmental demands
title_full Sleep-promoting neurons remodel their response properties to calibrate sleep drive with environmental demands
title_fullStr Sleep-promoting neurons remodel their response properties to calibrate sleep drive with environmental demands
title_full_unstemmed Sleep-promoting neurons remodel their response properties to calibrate sleep drive with environmental demands
title_short Sleep-promoting neurons remodel their response properties to calibrate sleep drive with environmental demands
title_sort sleep-promoting neurons remodel their response properties to calibrate sleep drive with environmental demands
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9521806/
https://www.ncbi.nlm.nih.gov/pubmed/36173939
http://dx.doi.org/10.1371/journal.pbio.3001797
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