Cell Reports
Volume 22, Issue 4, 23 January 2018, Pages 953-966
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Article
Energy Scarcity Promotes a Brain-wide Sleep State Modulated by Insulin Signaling in C. elegans

https://doi.org/10.1016/j.celrep.2017.12.091Get rights and content
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Highlights

  • Starvation shifts the behavioral strategy from exploration to intermittent sleep

  • Brain-wide neuronal population dynamics are robust to starvation

  • Neuromodulation via insulin signaling maintains wakefulness during short fasting

  • The insulin receptor DAF-2 acts in a network of sensory neurons and interneurons

Summary

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.

Keywords

energy homeostasis
starvation
insulin signaling
daf-2
whole-brain imaging
behavior
sleep
arousal
neuronal population dynamics
Caenorhabditis elegans

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2

Present address: Roche Pharmaceutical Research and Early Development, Roche Innovation Center Zurich, Roche Glycart AG, Wagistrasse 10, 8952 Schlieren, Switzerland

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