Dataset Information

Differential regulation of the Drosophila sleep homeostat by circadian and arousal inputs.

ABSTRACT: One output arm of the sleep homeostat in Drosophila appears to be a group of neurons with projections to the dorsal fan-shaped body (dFB neurons) of the central complex in the brain. However, neurons that regulate the sleep homeostat remain poorly understood. Using neurogenetic approaches combined with Ca2+ imaging, we characterized synaptic connections between dFB neurons and distinct sets of upstream sleep-regulatory neurons. One group of the sleep-promoting upstream neurons is a set of circadian pacemaker neurons that activates dFB neurons via direct glutaminergic excitatory synaptic connections. Opposing this population, a group of arousal-promoting neurons downregulates dFB axonal output with dopamine. Co-activating these two inputs leads to frequent shifts between sleep and wake states. We also show that dFB neurons release the neurotransmitter GABA and inhibit octopaminergic arousal neurons. We propose that dFB neurons integrate synaptic inputs from distinct sets of upstream sleep-promoting circadian clock neurons, and arousal neurons.

SUBMITTER: Ni JD

PROVIDER: S-EPMC6363385 | biostudies-literature | 2019 Feb

REPOSITORIES: biostudies-literature

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Differential regulation of the Drosophila sleep homeostat by circadian and arousal inputs.

Ni Jinfei D JD Gurav Adishthi S AS Liu Weiwei W Ogunmowo Tyler H TH Hackbart Hannah H Elsheikh Ahmed A Verdegaal Andrew A AA Montell Craig C

eLife 20190205

One output arm of the sleep homeostat in Drosophila appears to be a group of neurons with projections to the dorsal fan-shaped body (dFB neurons) of the central complex in the brain. However, neurons that regulate the sleep homeostat remain poorly understood. Using neurogenetic approaches combined with Ca2+ imaging, we characterized synaptic connections between dFB neurons and distinct sets of upstream sleep-regulatory neurons. One group of the sleep-promoting upstream neurons ...[more]

PMID: 30719975

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Project description:The need to sleep is sensed and discharged in a poorly understood process that is homeostatically controlled over time. In flies, different contributions to this process have been attributed to peripheral ppk and central brain neurons, with the former serving as hypothetical inputs to the sleep homeostat and the latter reportedly serving as the homeostat itself. Here we re-evaluate these distinctions in light of new findings using female flies. First, activating neurons targeted by published ppk and brain drivers elicits similar phenotypes - namely sleep deprivation followed by rebound sleep. Second, inhibiting activity or synaptic output with one type of driver suppresses sleep homeostasis induced using the other type of driver. Third, drivers previously used to implicate central neurons in sleep homeostasis unexpectedly also label ppk neurons. Fourth, activating only this subset of co-labeled neurons is sufficient to elicit sleep homeostasis. Thus, many published contributions of central neurons to sleep homeostasis can be explained by previously unrecognized expression of brain drivers in peripheral ppk neurons, most likely those in the legs that promote walking. Lastly, we show that activation of certain non-ppk neurons can also induce sleep homeostasis. Notably, axons of these as well as ppk neurons terminate in the same ventral brain region, suggesting that a previously undefined neural circuit element of a sleep homeostat may lie nearby.SIGNIFICANCE STATEMENT:The biological need(s) that sleep fulfills are unknown, but they are reflected by an animal's ability to compensate for prior sleep loss in a process called sleep homeostasis. Researchers have searched for the neural circuitry that comprises the sleep homeostat so that the information it conveys can shed light on the nature of sleep need. Here we demonstrate that neurons originating outside of the brain are responsible for phenotypes previously attributed to the proposed central brain sleep homeostat in flies. Our results support a revised neural circuit model for sensing and discharging sleep need in which peripheral inputs connect to a sleep homeostat through previously unrecognized neural circuit elements in the ventral brain.

Dataset Information

Differential regulation of the Drosophila sleep homeostat by circadian and arousal inputs.

Publications

Differential regulation of the <i>Drosophila</i> sleep homeostat by circadian and arousal inputs.

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