Abstract
Both the structure and the amount of sleep are important for brain function. Entry into deep, restorative stages of sleep is time dependent; short sleep bouts selectively eliminate these states. Fragmentation-induced cognitive dysfunction is a feature of many common human sleep pathologies. Whether sleep structure is normally regulated independent of the amount of sleep is unknown. Here, we show that in Drosophila melanogaster, activation of a subset of serotonergic neurons fragments sleep without major changes in the total amount of sleep, dramatically reducing long episodes that may correspond to deep sleep states. Disruption of sleep structure results in learning deficits that can be rescued by pharmacologically or genetically consolidating sleep. We identify two reciprocally connected sets of ellipsoid body neurons that form the heart of a serotonin-modulated circuit that controls sleep architecture. Taken together, these findings define a circuit essential for controlling the structure of sleep independent of its amount.
Highlights
We show that the sleep/wake structure is regulated independently of the amount of sleep by a 5HT-modulated neural circuit in the ellipsoid body (EB), a prominent brain structure of the central complex, which mediates sensory integration and motor coordination
Activation with heat had no effect on total sleep compared to controls (Figures 1G and 1H), while light activation increased nighttime sleep compared to controls (Figures 1I and 1J). This total sleep effect with light was seen in tryptophan hydroxylase (Trh) lines but not in downstream circuit element lines (Figures S5F, S5H, S6F, and S6H), suggesting that it may be a dominant light-interaction phenotype from upstream of the fragmentation circuit
To explore the effects of activation of this subset of serotonergic neurons on sleep structure, we examined the distribution of sleep episode durations over the course of the day dTrpA1 activation of serotonergic neurons robustly decreased episode length, which is visualized by the shift of the cumulative distribution of the experimental population to the left
Summary
In both humans and Drosophila, nighttime sleep occurs in long consolidated bouts, while daytime sleep is much more fragmented [1, 2]. Long periods of consolidated sleep at night facilitate progression into the deep sleep stages that are associated with positive health and cognitive benefits. Fragmentation of sleep during the daytime active period may reflect maintaining a higher arousal state. Fragmentation decreases sleep quality and is associated with learning and memory deficits, attention deficit, hypertension, and diabetes [4], even when total sleep time is not significantly decreased [3, 5]. Sleep structure has importance that is independent of the total amount of sleep, and understanding its regulation will be critical to our understanding of the functions of sleep
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