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Re-patterning sleep architecture in Drosophila through gustatory perception and nutritional quality.

ABSTRACT: Organisms perceive changes in their dietary environment and enact a suite of behavioral and metabolic adaptations that can impact motivational behavior, disease resistance, and longevity. However, the precise nature and mechanism of these dietary responses is not known. We have uncovered a novel link between dietary factors and sleep behavior in Drosophila melanogaster. Dietary sugar rapidly altered sleep behavior by modulating the number of sleep episodes during both the light and dark phase of the circadian period, independent of an intact circadian rhythm and without affecting total sleep, latency to sleep, or waking activity. The effect of sugar on sleep episode number was consistent with a change in arousal threshold for waking. Dietary protein had no significant effect on sleep or wakefulness. Gustatory perception of sugar was necessary and sufficient to increase the number of sleep episodes, and this effect was blocked by activation of bitter-sensing neurons. Further addition of sugar to the diet blocked the effects of sweet gustatory perception through a gustatory-independent mechanism. However, gustatory perception was not required for diet-induced fat accumulation, indicating that sleep and energy storage are mechanistically separable. We propose a two-component model where gustatory and metabolic cues interact to regulate sleep architecture in response to the quantity of sugar available from dietary sources. Reduced arousal threshold in response to low dietary availability may have evolved to provide increased responsiveness to cues associated with alternative nutrient-dense feeding sites. These results provide evidence that gustatory perception can alter arousal thresholds for sleep behavior in response to dietary cues and provide a mechanism by which organisms tune their behavior and physiology to environmental cues.

SUBMITTER: Linford NJ

PROVIDER: S-EPMC3342939 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Background and objectivesSleep disturbance is often associated with migraine. However, there is a paucity of research investigating objective and subjective measures of sleep in patients with migraine. This meta-analysis aims to determine whether there are differences in subjective sleep quality measured using the Pittsburgh Sleep Quality Index (PSQI) and objective sleep architecture measured using polysomnography (PSG) between adult and pediatric patients and healthy controls.MethodsThis review was preregistered on PROSPERO (CRD42020209325). A systematic search of 5 databases (Embase, MEDLINE, Global Health, APA PsycINFO, and APA PsycArticles, last searched on December 17, 2020) was conducted to find case-control studies that measured PSG or PSQI in patients with migraine. Pregnant participants and those with other headache disorders were excluded. Effect sizes (Hedges g) were entered into a random effects model meta-analysis. Study quality was evaluated with the Newcastle Ottawa Scale and publication bias with the Egger regression test.ResultsThirty-two studies were eligible, of which 21 measured PSQI or Migraine Disability Assessment Test in adults, 6 measured PSG in adults, and 5 measured PSG in children. The overall mean study quality score was 5/9; this did not moderate any of the results and there was no risk of publication bias. Overall, adults with migraine had higher PSQI scores than healthy controls (g = 0.75, p < 0.001, 95% confidence interval [CI] 0.54-0.96). This effect was larger in those with a chronic rather than episodic condition (g = 1.03, p < 0.001, 95% CI 0.37-1.01; g = 0.63, p < 0.001, 95% CI 0.38-0.88, respectively). For polysomnographic studies, adults and children with migraine displayed a lower percentage of rapid eye movement sleep (g = -0.22, p = 0.017, 95% CI -0.41 to -0.04; g = -0.71, p = 0.025, 95% CI -1.34 to -0.10, respectively) than controls. Pediatric patients displayed less total sleep time (g = -1.37, p = 0.039, 95% CI -2.66 to -0.10), more wake (g = 0.52, p < 0.001, 95% CI 0.08-0.79), and shorter sleep onset latency (g = -0.37, p < 0.001, 95% CI -0.54 to -0.21) than controls.DiscussionPeople with migraine have significantly poorer subjective sleep quality and altered sleep architecture compared to healthy individuals. Further longitudinal empirical studies are required to enhance our understanding of this relationship.

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Re-patterning sleep architecture in Drosophila through gustatory perception and nutritional quality.

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