4.8 Article

Chronic social isolation signals starvation and reduces sleep in Drosophila

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NATURE
卷 597, 期 7875, 页码 239-+

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NATURE PORTFOLIO
DOI: 10.1038/s41586-021-03837-0

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资金

  1. NIH grants [5R37 NS053087, 5R35 GM136237]
  2. Leon Levy Foundation
  3. Jane Coffin Childs Memorial Fund
  4. Grass Foundation
  5. NSF IOS [1656603]
  6. Kavli Foundation
  7. Division Of Integrative Organismal Systems
  8. Direct For Biological Sciences [1656603] Funding Source: National Science Foundation

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Social isolation can lead to chronic sleep loss and increased food consumption in Drosophila, mimicking the hyperphagia seen in lonely humans. Chronic social isolation alters the expression of metabolic genes and induces a brain state that signals starvation, promoting sleep loss and overconsumption of food. Neural activities in specific neurons play a crucial role in the link between chronic social isolation, metabolism, and sleep.
Social isolation and loneliness have potent effects on public health(1-4). Research in social psychology suggests that compromised sleep quality is a key factor that links persistent loneliness to adverse health conditions(5,6). Although experimental manipulations have been widely applied to studying the control of sleep and wakefulness in animal models, how normal sleep is perturbed by social isolation is unknown. Here we report that chronic, but not acute, social isolation reduces sleep in Drosophila. We use quantitative behavioural analysis and transcriptome profiling to differentiate between brain states associated with acute and chronic social isolation. Although the flies had uninterrupted access to food, chronic social isolation altered the expression of metabolic genes and induced a brain state that signals starvation. Chronically isolated animals exhibit sleep loss accompanied by overconsumption of food, which resonates with anecdotal findings of loneliness-associated hyperphagia in humans. Chronic social isolation reduces sleep and promotes feeding through neural activities in the peptidergic fan-shaped body columnar neurons of the fly. Artificial activation of these neurons causes misperception of acute social isolation as chronic social isolation and thereby results in sleep loss and increased feeding. These results present a mechanistic link between chronic social isolation, metabolism, and sleep, addressing a long-standing call for animal models focused on loneliness(7).

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