Network-specific synchronization of electrical slow-wave oscillations regulates sleep drive in Drosophila

Davide Raccuglia, Sheng Huang, Anatoli Ender, M.-Marcel Heim, Desiree Laber, Raquel Suárez-Grimalt, Agustin Liotta, Stephan J Sigrist, Jörg RP Geiger, David Owald

Slow-wave rhythms characteristic of deep sleep oscillate in the delta band (0.5–4 Hz) and can be foundacross various brain regions in vertebrates. Across phyla, however, an understanding of the mechanisms underlying oscillations and how these link to behavior remains limited. Here, we discover compound delta oscillations in the sleep-regulating R5 network of Drosophila. We find that the power of these slow-wave oscillations increases with sleep need and issubject to diurnal variation. Optical multi-unit voltagerecordings reveal that single R5 neurons get synchronized by activating circadian input pathways. Weshow that this synchronization depends on NMDA receptor (NMDAR) coincidence detector function, andthat an interplay of cholinergic and glutamatergic inputs regulates oscillatory frequency. Genetically targeting the coincidence detector function of NMDARsin R5, and thus the uncovered mechanism underlying synchronization, abolished network-specific compound slow-wave oscillations. It also disrupted sleepand facilitated light-induced wakening, establishing arole for slow-wave oscillations in regulating sleep andsensory gating. We therefore propose that the synchronization-based increase in oscillatory powerlikely represents an evolutionarily conserved, potentially ‘‘optimal,’’ strategy for constructing sleep-regulating sensory gates.

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Keywords

deep-sleepDrosophilasensory gatesleep regulationslow-wave oscillations
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