A Serotonin-Modulated Circuit Controls Sleep Architecture to Regulate Cognitive Function Independent of Total Sleep in Drosophila

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...

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Published inCurrent biology Vol. 29; no. 21; pp. 3635 - 3646.e5
Main Authors Liu, Chang, Meng, Zhiqiang, Wiggin, Timothy D., Yu, Junwei, Reed, Martha L., Guo, Fang, Zhang, Yunpeng, Rosbash, Michael, Griffith, Leslie C.
Format Journal Article
LanguageEnglish
Published England Elsevier Ltd 04.11.2019
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Summary: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. •Serotonin plays a role in regulation of sleep architecture independent of total sleep•Serotonergic signaling to the ellipsoid body via 5HT7 receptors fragments sleep•Learning deficits resulting from fragmentation can be rescued by consolidating sleep•Two reciprocally connected sets of EB neurons control sleep architecture Liu et al. image, perturb, and analyze a serotonin-modulated circuit in the Drosophila brain that regulates sleep architecture without affecting the amount of sleep. Dysregulation of this circuit impairs cognitive function.
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These authors made equal contributions
Conceptualization, CL and LCG; Methodology, TDW; Investigation, CL, ZM, JW, MLR, FG, TDW, YZ; Writing-Original Draft, CL and ZM; Writing-Review & Editing, CL, TDW and LCG; Funding Acquisition, LCG and MR; Resources, MR, TDW; Supervision, LCG.
Lead Contact: Leslie C. Griffith, Brandeis University, Department of Biology MS008, 415 South Street, Waltham, MA, 02454-9110, USA
AUTHOR CONTRIBUTIONS
ISSN:0960-9822
1879-0445
DOI:10.1016/j.cub.2019.08.079