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Behavioral and genetic features of sleep ontogeny in Drosophila.

ABSTRACT: The fruit fly Drosophila melanogaster, like most organisms, exhibits increased sleep amount and depth in young compared to mature animals. While the fly has emerged as a powerful model for studying sleep during development, qualitative behavioral features of sleep ontogeny and its genetic control are poorly understood. Here we find that, in addition to increased sleep time and intensity, young flies sleep with less place preference than mature adults, and, like mammals, exhibit more motor twitches during sleep. In addition, we show that ontogenetic changes in sleep amount, twitch, and place preference are preserved across sleep mutants with lesions in distinct molecular pathways. Our results demonstrate that sleep ontogeny is characterized by multifaceted behavioral changes, including quantitative and qualitative alterations to sleep as animals mature. Further, the preservation of sleep ontogenetic changes despite mutations that alter sleep time suggests independent genetic control mechanisms for sleep maturation.

SUBMITTER: Dilley LC

PROVIDER: S-EPMC6047415 | biostudies-literature | 2018 Jul

REPOSITORIES: biostudies-literature

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Behavioral and genetic features of sleep ontogeny in Drosophila.

Dilley Leela C LC Vigderman Abigail A Williams Charlette E CE Kayser Matthew S MS

Sleep 20180701 7

The fruit fly Drosophila melanogaster, like most organisms, exhibits increased sleep amount and depth in young compared to mature animals. While the fly has emerged as a powerful model for studying sleep during development, qualitative behavioral features of sleep ontogeny and its genetic control are poorly understood. Here we find that, in addition to increased sleep time and intensity, young flies sleep with less place preference than mature adults, and, like mammals, exhibit more motor twitch ...[more]

PMID: 29746663

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Project description:Study objectivesSleep rebound-the increase in sleep that follows sleep deprivation-is a hallmark of homeostatic sleep regulation that is conserved across the animal kingdom. However, both the mechanisms that underlie sleep rebound and its relationship to habitual daily sleep remain unclear. To address this, we developed an efficient thermogenetic method of inducing sleep deprivation in Drosophila that produces a substantial rebound, and applied the newly developed method to assess sleep rebound in a screen of 1,741 mutated lines. We used data generated by this screen to identify lines with reduced sleep rebound following thermogenetic sleep deprivation, and to probe the relationship between habitual sleep amount and sleep following thermogenetic sleep deprivation in Drosophila.MethodsTo develop a thermogenetic method of sleep deprivation suitable for screening, we thermogenetically stimulated different populations of wake-promoting neurons labeled by Gal4 drivers. Sleep rebound following thermogenetically-induced wakefulness varies across the different sets of wake-promoting neurons that were stimulated, from very little to quite substantial. Thermogenetic activation of neurons marked by the c584-Gal4 driver produces both strong sleep loss and a substantial rebound that is more consistent within genotypes than rebound following mechanical or caffeine-induced sleep deprivation. We therefore used this driver to induce sleep deprivation in a screen of 1,741 mutagenized lines generated by the Drosophila Gene Disruption Project. Flies were subjected to 9 h of sleep deprivation during the dark period and released from sleep deprivation 3 h before lights-on. Recovery was measured over the 15 h following sleep deprivation. Following identification of lines with reduced sleep rebound, we characterized baseline sleep and sleep depth before and after sleep deprivation for these hits.ResultsWe identified two lines that consistently exhibit a blunted increase in the duration and depth of sleep after thermogenetic sleep deprivation. Neither of the two genotypes has reduced total baseline sleep. Statistical analysis across all screened lines shows that genotype is a strong predictor of recovery sleep, independent from effects of genotype on baseline sleep.ConclusionsOur data show that rebound sleep following thermogenetic sleep deprivation can be genetically separated from sleep at baseline. This suggests that genetically controlled mechanisms of sleep regulation not manifest under undisturbed conditions contribute to sleep rebound following thermogenetic sleep deprivation.

Dataset Information

Behavioral and genetic features of sleep ontogeny in Drosophila.

Publications

Behavioral and genetic features of sleep ontogeny in Drosophila.

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