A Paradoxical Kind of Sleep in Drosophila melanogaster

• Published in: Current biology Vol. 31; no. 3; pp. 578 - 590.e6
• Main Authors: Tainton-Heap, Lucy A.L., Kirszenblat, Leonie C., Notaras, Eleni T., Grabowska, Martyna J., Jeans, Rhiannon, Feng, Kai, Shaw, Paul J., van Swinderen, Bruno
• Format: Journal Article
• Language: English
• Published: England Elsevier Inc 08-02-2021
• Subjects: Animals; brain; calcium imaging; dorsal fan-shaped body; Drosophila melanogaster - genetics; optogenetics; REM sleep; Sleep; Sleep Deprivation; sleep stages; two-photon microscopy; visual attention; Wakefulness; visual attention; sleep stages; optogenetics; two-photon microscopy; brain; calcium imaging; dorsal fan-shaped body; REM sleep
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2020.10.081

The dynamic nature of sleep in many animals suggests distinct stages that serve different functions. Genetic sleep induction methods in animal models provide a powerful way to disambiguate these stages and functions, although behavioral methods alone are insufficient to accurately identify what kind of sleep is being engaged. In Drosophila, activation of the dorsal fan-shaped body (dFB) promotes sleep, but it remains unclear what kind of sleep this is, how the rest of the fly brain is behaving, or if any specific sleep functions are being achieved. Here, we developed a method to record calcium activity from thousands of neurons across a volume of the fly brain during spontaneous sleep and compared this to dFB-induced sleep. We found that spontaneous sleep typically transitions from an active “wake-like” stage to a less active stage. In contrast, optogenetic activation of the dFB promotes sustained wake-like levels of neural activity even though flies become unresponsive to mechanical stimuli. When we probed flies with salient visual stimuli, we found that the activity of visually responsive neurons in the central brain was blocked by transient dFB activation, confirming an acute disconnect from the external environment. Prolonged optogenetic dFB activation nevertheless achieved a key sleep function by correcting visual attention defects brought on by sleep deprivation. These results suggest that dFB activation promotes a distinct form of sleep in Drosophila, where brain activity appears similar to wakefulness, but responsiveness to external sensory stimuli is profoundly suppressed.
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•Calcium imaging reveals distinct spontaneous sleep stages in the fly brain•Short bouts of quiescence in Drosophila may involve an active sleep stage•Optogenetic activation of a sleep switch promotes wake-like brain activity•Prolonged activation of the sleep switch corrects visual attention defects
Tainton-Heap et al. track calcium activity in neurons across the fly brain to compare spontaneous and optogenetically induced sleep. They uncover an active, wake-like sleep stage as well as a less active deep sleep stage. Induced sleep appears to promote wake-like levels of brain activity while suppressing responsiveness to external stimuli.