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Energy Scarcity Promotes a Brain-wide Sleep State Modulated by Insulin Signaling in C. elegans

Neural information processing entails a high energetic cost, but its maintenance is crucial for animal survival. However, the brain’s energy conservation strategies are incompletely understood. Employing functional brain-wide imaging and quantitative behavioral assays, we describe a neuronal strateg...

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Detalles Bibliográficos
Autores principales: Skora, Susanne, Mende, Fanny, Zimmer, Manuel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cell Press 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5846868/
https://www.ncbi.nlm.nih.gov/pubmed/29386137
http://dx.doi.org/10.1016/j.celrep.2017.12.091
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author Skora, Susanne
Mende, Fanny
Zimmer, Manuel
author_facet Skora, Susanne
Mende, Fanny
Zimmer, Manuel
author_sort Skora, Susanne
collection PubMed
description Neural information processing entails a high energetic cost, but its maintenance is crucial for animal survival. However, the brain’s energy conservation strategies are incompletely understood. Employing functional brain-wide imaging and quantitative behavioral assays, we describe a neuronal strategy in Caenorhabditis elegans that balances energy availability and expenditure. Upon acute food deprivation, animals exhibit a transiently elevated state of arousal, indicated by foraging behaviors and increased responsiveness to food-related cues. In contrast, long-term starvation suppresses these behaviors and biases animals to intermittent sleep episodes. Brain-wide neuronal population dynamics, which are likely energetically costly but important for behavior, are robust to starvation while animals are awake. However, during starvation-induced sleep, brain dynamics are systemically downregulated. Neuromodulation via insulin-like signaling is required to transiently maintain the animals’ arousal state upon acute food deprivation. Our data suggest that the regulation of sleep and wakefulness supports optimal energy allocation.
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spelling pubmed-58468682018-03-13 Energy Scarcity Promotes a Brain-wide Sleep State Modulated by Insulin Signaling in C. elegans Skora, Susanne Mende, Fanny Zimmer, Manuel Cell Rep Article Neural information processing entails a high energetic cost, but its maintenance is crucial for animal survival. However, the brain’s energy conservation strategies are incompletely understood. Employing functional brain-wide imaging and quantitative behavioral assays, we describe a neuronal strategy in Caenorhabditis elegans that balances energy availability and expenditure. Upon acute food deprivation, animals exhibit a transiently elevated state of arousal, indicated by foraging behaviors and increased responsiveness to food-related cues. In contrast, long-term starvation suppresses these behaviors and biases animals to intermittent sleep episodes. Brain-wide neuronal population dynamics, which are likely energetically costly but important for behavior, are robust to starvation while animals are awake. However, during starvation-induced sleep, brain dynamics are systemically downregulated. Neuromodulation via insulin-like signaling is required to transiently maintain the animals’ arousal state upon acute food deprivation. Our data suggest that the regulation of sleep and wakefulness supports optimal energy allocation. Cell Press 2018-01-28 /pmc/articles/PMC5846868/ /pubmed/29386137 http://dx.doi.org/10.1016/j.celrep.2017.12.091 Text en © 2017 The Author(s) http://creativecommons.org/licenses/by-nc-nd/4.0/ This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
spellingShingle Article
Skora, Susanne
Mende, Fanny
Zimmer, Manuel
Energy Scarcity Promotes a Brain-wide Sleep State Modulated by Insulin Signaling in C. elegans
title Energy Scarcity Promotes a Brain-wide Sleep State Modulated by Insulin Signaling in C. elegans
title_full Energy Scarcity Promotes a Brain-wide Sleep State Modulated by Insulin Signaling in C. elegans
title_fullStr Energy Scarcity Promotes a Brain-wide Sleep State Modulated by Insulin Signaling in C. elegans
title_full_unstemmed Energy Scarcity Promotes a Brain-wide Sleep State Modulated by Insulin Signaling in C. elegans
title_short Energy Scarcity Promotes a Brain-wide Sleep State Modulated by Insulin Signaling in C. elegans
title_sort energy scarcity promotes a brain-wide sleep state modulated by insulin signaling in c. elegans
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5846868/
https://www.ncbi.nlm.nih.gov/pubmed/29386137
http://dx.doi.org/10.1016/j.celrep.2017.12.091
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