Intrinsic maturation of sleep output neurons regulates sleep ontogeny in Drosophila

Gong, Naihua N.; Lương, Hằng Ngọc Bảo; Dang, An H.; Mainwaring, Benjamin; Shields, Emily; Schmeckpeper, Karl; Bonasio, Roberto; Kayser, Matthew S.

doi:10.1016/j.cub.2022.07.054

Cited by 12 publications

(14 citation statements)

References 60 publications

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“…One underlying assumption with focusing on sleep duration as the most relevant metric for understanding sleep function in Drosophila is that sleep is a unitary phenomenon in the fly model, meaning that primarily one set of functions and one form of brain activity are occurring when flies sleep. There is now substantial evidence that this is unlikely to be true, and that like other animals flies probably also experience distinct sleep stages that accomplish different functions [9, 10, 27, 50, 61, 62]. This does not mean that these functions are mutually exclusive; for example, both THIP provision and neuronal activation of central brain circuits have been found to promote memory consolidation in Drosophila [23].…”

Section: Discussionmentioning

confidence: 99%

“…Although many studies have shown that the R23E10-Gal4 circuit is sleep promoting (e.g. [19, 21, 62]), and we have shown that acute activation of these neurons produces a form of active sleep [10], it seems unlikely that active sleep regulation is limited to the dFB neurons alone [60]. Other circuits in the fly central brain are also sleep-promoting, including in the ellipsoid body [65] and the ventral fan-shaped body (vFB) [66], although it remains unknown if activation of these other circuits also promotes an active sleep stage, or whether a similar transcriptome might be engaged by these alternate approaches to optogenetic sleep induction in flies.…”

Section: Discussionmentioning

confidence: 99%

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Experimentally induced active and quiet sleep engage non-overlapping transcriptional programs inDrosophila

Anthoney

Tainton-Heap

Lương

et al. 2023

Preprint

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Sleep in mammals is broadly classified into two different categories: rapid eye movement (REM) sleep and slow wave sleep (SWS), and accordingly REM and SWS are thought to achieve a different set of functions. The fruit flyDrosophila melanogasteris increasingly being used as a model to understand sleep functions, although it remains unclear if the fly brain also engages in different kinds of sleep as well. Here, we compare two commonly used approaches for studying sleep experimentally inDrosophila: optogenetic activation of sleep-promoting neurons and provision of a sleep-promoting drug, Gaboxadol. We find that these different sleep-induction methods have similar effects on increasing sleep duration, but divergent effects on brain activity. Transcriptomic analysis reveals that drug-induced deep sleep (‘quiet’ sleep) mostly downregulates metabolism genes, whereas optogenetic ‘active’ sleep upregulates a wide range of genes relevant to normal waking functions. This suggests that optogenetics and pharmacological induction of sleep inDrosophilapromote different features of sleep, which engage different sets of genes to achieve their respective functions.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Experimentally induced active and quiet sleep engage non-overlapping transcriptional programs inDrosophila

Anthoney

Tainton-Heap

Lương

et al. 2023

Preprint

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“…During juvenile developmental periods across species, including early adulthood in Drosophila , sleep depth (and duration) are elevated 54,55 . Juvenile flies (Day 1 post eclosion) exhibit increased arousal threshold during the day and night compared to mature adults (Day 5-9) and an increase in sleep duration during the day period 54,55 . We next investigated if the knockdown of E93 in Type II NSCs affects juvenile adult sleep.…”

Section: Resultsmentioning

confidence: 99%

“…While much is known about the temporal patterning mechanisms of the Drosophila NSCs, genetic programs that regulate the formation of the adult central complex (CX) lineages are poorly understood. The insect CX is a higher-order brain center regulating complex behaviors such as navigation [28][29][30][31][32][33][34][35][36][37][38][39][40] , locomotion 29,[41][42][43][44][45][46] , feeding 47,48 , and sleep [49][50][51][52][53][54][55][56][57][58][59][60] . The CX is a centrally located brain region comprised of four major neuropils: a handlebar-shaped protocerebral bridge (PB), a Fan-shaped body (FB), a doughnut-shaped ellipsoid body (EB), and a pair of noduli (NO) 29,36,61,62 .…”

Section: Introductionmentioning

confidence: 99%

Stem cell-specific ecdysone signaling regulates the development and function of aDrosophilasleep homeostat

Wani,

Chowdhury,

Luong

et al. 2023

Preprint

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Complex behaviors arise from neural circuits that are assembled from diverse cell types. Sleep is a conserved and essential behavior, yet little is known regarding how the nervous system generates neuron types of the sleep-wake circuit. Here, we focus on the specification ofDrosophilasleep-promoting neurons—long-field tangential input neurons that project to the dorsal layers of the fan-shaped body neuropil in the central complex (CX). We use lineage analysis and genetic birth dating to identify two bilateral Type II neural stem cells that generate these dorsal fan-shaped body (dFB) neurons. We show that adult dFB neurons express Ecdysone-induced protein E93, and loss of Ecdysone signaling or E93 in Type II NSCs results in the misspecification of the adult dFB neurons. Finally, we show that E93 knockdown in Type II NSCs affects adult sleep behavior. Our results provide insight into how extrinsic hormonal signaling acts on NSCs to generate neuronal diversity required for adult sleep behavior. These findings suggest that some adult sleep disorders might derive from defects in stem cell-specific temporal neurodevelopmental programs.

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“…Numerous studies have shown the critical role of dFB-projecting neurons in sleep regulation under various conditions. Their activation leads to increased sleep by acting as effectors of homeostatic sleep needs 39,46 , and their enhanced activity underlies increased sleep in young flies 53 and in sickness 54 . They also receive information from neurons involved in sleep suppression due to chronic social isolation 55 , and GABAergic inputs to dFB contribute to temperature-dependent sleep plasticity 56 .…”

Section: Discussionmentioning

confidence: 99%

Modulation and Neural Correlates of Postmating Sleep Plasticity inDrosophilaFemales

Duhart

Buchler

Inami

et al. 2023

Preprint

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Sleep is essential, but animals may forgo sleep to engage in other critical behaviors, such as feeding and reproduction. Previous studies have shown that female flies show decreased sleep after mating, but our understanding of the process is limited. Here, we report that postmating nighttime sleep loss is modulated by diet and sleep deprivation, demonstrating a complex interaction among sleep, reproduction, and diet. We also report that female-specific pC1 neurons and sleep-promoting dorsal fan-shaped body (dFB) neurons are required for postmating sleep plasticity. Activating pC1 neurons leads to sleep suppression on standard fly culture media but has little sleep effect on sucrose-only food. Published connectome data suggest indirect, inhibitory connections among pC1 subtypes. Using calcium imaging, we show that activating the pC1e subtype inhibits dFB neurons. We propose that pC1 and dFB neurons integrate the mating status, food context, and sleep drive to modulate postmating sleep plasticity.

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Intrinsic maturation of sleep output neurons regulates sleep ontogeny in Drosophila

Cited by 12 publications

References 60 publications

Experimentally induced active and quiet sleep engage non-overlapping transcriptional programs inDrosophila

Experimentally induced active and quiet sleep engage non-overlapping transcriptional programs inDrosophila

Stem cell-specific ecdysone signaling regulates the development and function of aDrosophilasleep homeostat

Modulation and Neural Correlates of Postmating Sleep Plasticity inDrosophilaFemales

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