Circadian gating of light-induced arousal in Drosophila sleep

Abstract

Circadian rhythms and sleep homeostasis constitute the two-process model for daily sleep regulation. However, evidence for circadian control of sleep-wake cycles has been relatively short since clock-less animals often show sleep behaviors quantitatively comparable to wild-type. Here we examine Drosophila sleep behaviors under different light-dark regimes and demonstrate that circadian clocks gate light-induced arousal. Genetic excitation of tyrosine decarboxylase 2 (TDC2)-expressing neurons suppressed sleep more evidently at night, causing nocturnal activity. The arousal effects were likely mediated in part by glutamate transmission from the octopaminergic neurons and substantially masked by light. Application of T12 cycles (6-h light: 6-h dark) further showed that the light-sensitive effects of TDC2 neurons depended on the time of the day. In particular, light-sensing via visual input pathway led to strong sleep suppression at subjective night, and such an effect disappeared in clock-less mutants. Transgenic mapping revealed that light-induced arousal and free-running behavioral rhythms require distinct groups of circadian pacemaker neurons. These results provide convincing evidence that circadian control of sleep is mediated by the dedicated clock neurons for light-induced arousal.

Keywords:

• Drosophila melanogaster
• circadian rhythms
• sleep
• light
• arousal

Acknowledgements

We thank R. Allada, J. Choe, E.Y. Kim, Y. Li, Bloomington Drosophila Stock Center, Korea Drosophila Resource Center, and NIG-Fly Stock Center for reagents.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Additional information

Funding

This work was supported by the National Research Foundation (NRF) funded by the Ministry of Science and Information & Communication Technology, Republic of Korea (NRF-2021K2A9A2A08000057[C.L.]]; NRF-2019R1A6A3A13091965[H.L.]).