Compartment specific regulation of sleep by mushroom body requires GABA and dopaminergic signaling

Abstract Sleep is a fundamental behavioral state important for survival and is universal in animals with sufficiently complex nervous systems. As a highly conserved neurobehavioral state, sleep has been described in species ranging from jellyfish to humans. Biogenic amines like dopamine, serotonin a...

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Autores principales:	Margaret Driscoll, Steven N Buchert, Victoria Coleman, Morgan McLaughlin, Amanda Nguyen, Divya Sitaraman
Formato:	article
Lenguaje:	EN
Publicado:	Nature Portfolio 2021
Materias:	Medicine R Science Q
Acceso en línea:	https://doaj.org/article/63385cbd2f004b0f9144866f19b08540
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spelling	oai:doaj.org-article:63385cbd2f004b0f9144866f19b085402021-12-02T18:37:09ZCompartment specific regulation of sleep by mushroom body requires GABA and dopaminergic signaling10.1038/s41598-021-99531-22045-2322https://doaj.org/article/63385cbd2f004b0f9144866f19b085402021-10-01T00:00:00Zhttps://doi.org/10.1038/s41598-021-99531-2https://doaj.org/toc/2045-2322Abstract Sleep is a fundamental behavioral state important for survival and is universal in animals with sufficiently complex nervous systems. As a highly conserved neurobehavioral state, sleep has been described in species ranging from jellyfish to humans. Biogenic amines like dopamine, serotonin and norepinephrine have been shown to be critical for sleep regulation across species but the precise circuit mechanisms underlying how amines control persistence of sleep, arousal and wakefulness remain unclear. The fruit fly, Drosophila melanogaster, provides a powerful model system for the study of sleep and circuit mechanisms underlying state transitions and persistence of states to meet the organisms motivational and cognitive needs. In Drosophila, two neuropils in the central brain, the mushroom body (MB) and the central complex (CX) have been shown to influence sleep homeostasis and receive aminergic neuromodulator input critical to sleep–wake switch. Dopamine neurons (DANs) are prevalent neuromodulator inputs to the MB but the mechanisms by which they interact with and regulate sleep- and wake-promoting neurons within MB are unknown. Here we investigate the role of subsets of PAM-DANs that signal wakefulness and project to wake-promoting compartments of the MB. We find that PAM-DANs are GABA responsive and require GABAA-Rdl receptor in regulating sleep. In mapping the pathways downstream of PAM neurons innervating γ5 and β′2 MB compartments we find that wakefulness is regulated by both DopR1 and DopR2 receptors in downstream Kenyon cells (KCs) and mushroom body output neurons (MBONs). Taken together, we have identified and characterized a dopamine modulated sleep microcircuit within the mushroom body that has previously been shown to convey information about positive and negative valence critical for memory formation. These studies will pave way for understanding how flies balance sleep, wakefulness and arousal.Margaret DriscollSteven N BuchertVictoria ColemanMorgan McLaughlinAmanda NguyenDivya SitaramanNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 11, Iss 1, Pp 1-18 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Medicine R Science Q
spellingShingle	Medicine R Science Q Margaret Driscoll Steven N Buchert Victoria Coleman Morgan McLaughlin Amanda Nguyen Divya Sitaraman Compartment specific regulation of sleep by mushroom body requires GABA and dopaminergic signaling
description	Abstract Sleep is a fundamental behavioral state important for survival and is universal in animals with sufficiently complex nervous systems. As a highly conserved neurobehavioral state, sleep has been described in species ranging from jellyfish to humans. Biogenic amines like dopamine, serotonin and norepinephrine have been shown to be critical for sleep regulation across species but the precise circuit mechanisms underlying how amines control persistence of sleep, arousal and wakefulness remain unclear. The fruit fly, Drosophila melanogaster, provides a powerful model system for the study of sleep and circuit mechanisms underlying state transitions and persistence of states to meet the organisms motivational and cognitive needs. In Drosophila, two neuropils in the central brain, the mushroom body (MB) and the central complex (CX) have been shown to influence sleep homeostasis and receive aminergic neuromodulator input critical to sleep–wake switch. Dopamine neurons (DANs) are prevalent neuromodulator inputs to the MB but the mechanisms by which they interact with and regulate sleep- and wake-promoting neurons within MB are unknown. Here we investigate the role of subsets of PAM-DANs that signal wakefulness and project to wake-promoting compartments of the MB. We find that PAM-DANs are GABA responsive and require GABAA-Rdl receptor in regulating sleep. In mapping the pathways downstream of PAM neurons innervating γ5 and β′2 MB compartments we find that wakefulness is regulated by both DopR1 and DopR2 receptors in downstream Kenyon cells (KCs) and mushroom body output neurons (MBONs). Taken together, we have identified and characterized a dopamine modulated sleep microcircuit within the mushroom body that has previously been shown to convey information about positive and negative valence critical for memory formation. These studies will pave way for understanding how flies balance sleep, wakefulness and arousal.
format	article
author	Margaret Driscoll Steven N Buchert Victoria Coleman Morgan McLaughlin Amanda Nguyen Divya Sitaraman
author_facet	Margaret Driscoll Steven N Buchert Victoria Coleman Morgan McLaughlin Amanda Nguyen Divya Sitaraman
author_sort	Margaret Driscoll
title	Compartment specific regulation of sleep by mushroom body requires GABA and dopaminergic signaling
title_short	Compartment specific regulation of sleep by mushroom body requires GABA and dopaminergic signaling
title_full	Compartment specific regulation of sleep by mushroom body requires GABA and dopaminergic signaling
title_fullStr	Compartment specific regulation of sleep by mushroom body requires GABA and dopaminergic signaling
title_full_unstemmed	Compartment specific regulation of sleep by mushroom body requires GABA and dopaminergic signaling
title_sort	compartment specific regulation of sleep by mushroom body requires gaba and dopaminergic signaling
publisher	Nature Portfolio
publishDate	2021
url	https://doaj.org/article/63385cbd2f004b0f9144866f19b08540
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Compartment specific regulation of sleep by mushroom body requires GABA and dopaminergic signaling

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