Experimentally induced active and quiet sleep engage non-overlapping transcriptional programs in Drosophila

Sleep in mammals can be broadly classified into two different physiological categories: rapid eye movement (REM) sleep and slow-wave sleep (SWS), and accordingly REM and SWS are thought to achieve a different set of functions. The fruit fly Drosophila melanogaster is increasingly being used as a mod...

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Main Authors: Niki Anthoney, Lucy Tainton-Heap, Hang Luong, Eleni Notaras, Amber B Kewin, Qiongyi Zhao, Trent Perry, Philip Batterham, Paul J Shaw, Bruno van Swinderen
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2023-11-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/88198
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author Niki Anthoney
Lucy Tainton-Heap
Hang Luong
Eleni Notaras
Amber B Kewin
Qiongyi Zhao
Trent Perry
Philip Batterham
Paul J Shaw
Bruno van Swinderen
author_facet Niki Anthoney
Lucy Tainton-Heap
Hang Luong
Eleni Notaras
Amber B Kewin
Qiongyi Zhao
Trent Perry
Philip Batterham
Paul J Shaw
Bruno van Swinderen
author_sort Niki Anthoney
collection DOAJ
description Sleep in mammals can be broadly classified into two different physiological categories: rapid eye movement (REM) sleep and slow-wave sleep (SWS), and accordingly REM and SWS are thought to achieve a different set of functions. The fruit fly Drosophila melanogaster is increasingly being used as a model to understand sleep functions, although it remains unclear if the fly brain also engages in different kinds of sleep as well. Here, we compare two commonly used approaches for studying sleep experimentally in Drosophila: optogenetic activation of sleep-promoting neurons and provision of a sleep-promoting drug, gaboxadol. We find that these different sleep-induction methods have similar effects on increasing sleep duration, but divergent effects on brain activity. Transcriptomic analysis reveals that drug-induced deep sleep (‘quiet’ sleep) mostly downregulates metabolism genes, whereas optogenetic ‘active’ sleep upregulates a wide range of genes relevant to normal waking functions. This suggests that optogenetics and pharmacological induction of sleep in Drosophila promote different features of sleep, which engage different sets of genes to achieve their respective functions.
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spelling doaj.art-e75b510d1f4f41b19288111cbb75b78a2023-11-01T13:46:21ZengeLife Sciences Publications LtdeLife2050-084X2023-11-011210.7554/eLife.88198Experimentally induced active and quiet sleep engage non-overlapping transcriptional programs in DrosophilaNiki Anthoney0Lucy Tainton-Heap1Hang Luong2Eleni Notaras3Amber B Kewin4Qiongyi Zhao5Trent Perry6https://orcid.org/0000-0002-8045-0487Philip Batterham7Paul J Shaw8Bruno van Swinderen9https://orcid.org/0000-0001-6552-7418Queensland Brain Institute, The University of Queensland, Brisbane, AustraliaQueensland Brain Institute, The University of Queensland, Brisbane, AustraliaSchool of BioSciences, The University of Melbourne, Melbourne, AustraliaQueensland Brain Institute, The University of Queensland, Brisbane, AustraliaQueensland Brain Institute, The University of Queensland, Brisbane, AustraliaQueensland Brain Institute, The University of Queensland, Brisbane, AustraliaSchool of BioSciences, The University of Melbourne, Melbourne, AustraliaSchool of BioSciences, The University of Melbourne, Melbourne, AustraliaDepartment of Neuroscience, School of Medicine, Washington University in St. Louis, St Louis, United StatesQueensland Brain Institute, The University of Queensland, Brisbane, AustraliaSleep in mammals can be broadly classified into two different physiological categories: rapid eye movement (REM) sleep and slow-wave sleep (SWS), and accordingly REM and SWS are thought to achieve a different set of functions. The fruit fly Drosophila melanogaster is increasingly being used as a model to understand sleep functions, although it remains unclear if the fly brain also engages in different kinds of sleep as well. Here, we compare two commonly used approaches for studying sleep experimentally in Drosophila: optogenetic activation of sleep-promoting neurons and provision of a sleep-promoting drug, gaboxadol. We find that these different sleep-induction methods have similar effects on increasing sleep duration, but divergent effects on brain activity. Transcriptomic analysis reveals that drug-induced deep sleep (‘quiet’ sleep) mostly downregulates metabolism genes, whereas optogenetic ‘active’ sleep upregulates a wide range of genes relevant to normal waking functions. This suggests that optogenetics and pharmacological induction of sleep in Drosophila promote different features of sleep, which engage different sets of genes to achieve their respective functions.https://elifesciences.org/articles/88198sleepoptogeneticsgaboxadolcalcium imagingRNA seq
spellingShingle Niki Anthoney
Lucy Tainton-Heap
Hang Luong
Eleni Notaras
Amber B Kewin
Qiongyi Zhao
Trent Perry
Philip Batterham
Paul J Shaw
Bruno van Swinderen
Experimentally induced active and quiet sleep engage non-overlapping transcriptional programs in Drosophila
eLife
sleep
optogenetics
gaboxadol
calcium imaging
RNA seq
title Experimentally induced active and quiet sleep engage non-overlapping transcriptional programs in Drosophila
title_full Experimentally induced active and quiet sleep engage non-overlapping transcriptional programs in Drosophila
title_fullStr Experimentally induced active and quiet sleep engage non-overlapping transcriptional programs in Drosophila
title_full_unstemmed Experimentally induced active and quiet sleep engage non-overlapping transcriptional programs in Drosophila
title_short Experimentally induced active and quiet sleep engage non-overlapping transcriptional programs in Drosophila
title_sort experimentally induced active and quiet sleep engage non overlapping transcriptional programs in drosophila
topic sleep
optogenetics
gaboxadol
calcium imaging
RNA seq
url https://elifesciences.org/articles/88198
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