Circadian neuron feedback controls the Drosophila sleep–activity profile

• Published in: Nature (London) 2016-08, Vol.536 (7616), p.292-297
• Main Authors: Guo, Fang, Yu, Junwei, Jung, Hyung Jae, Abruzzi, Katharine C., Luo, Weifei, Griffith, Leslie C., Rosbash, Michael
• Format: Article
• Language: English
• Subjects: 13/1; 13/89; 13/95; 14/19; 14/5; 38/35; 45/90; 631/1647/2253; 631/378/1385/2640; 631/378/1385/519; 631/61/32; 64/24; Animal behavior; Animals; Biological Clocks - physiology; Calcium - metabolism; Circadian rhythm; Circadian Rhythm - physiology; Circadian rhythms; Drosophila melanogaster - cytology; Drosophila melanogaster - physiology; Environmental information; Feedback, Physiological; Female; Glutamic Acid - metabolism; High temperature; Humanities and Social Sciences; Insects; Light; Male; Motor Activity; multidisciplinary; Neurons; Neurons - physiology; Optogenetics; Science; Sex Characteristics; Sleep; Sleep - physiology; Temperature; Wakefulness - physiology
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/nature19097

Little is known about the ability of Drosophila circadian neurons to promote sleep. Here we show, using optogenetic manipulation and video recording, that a subset of dorsal clock neurons (DN1s) are potent sleep-promoting cells that release glutamate to directly inhibit key pacemaker neurons. The pacemakers promote morning arousal by activating these DN1s, implying that a late-day feedback circuit drives midday siesta and night-time sleep. To investigate more plastic aspects of the sleep program, we used a calcium assay to monitor and compare the real-time activity of DN1 neurons in freely behaving males and females. Our results revealed that DN1 neurons were more active in males than in females, consistent with the finding that male flies sleep more during the day. DN1 activity is also enhanced by elevated temperature, consistent with the ability of higher temperatures to increase sleep. These new approaches indicate that DN1s have a major effect on the fly sleep–wake profile and integrate environmental information with the circadian molecular program. A subset of dorsal clock neurons are identified in Drosophila as sleep-promoting cells, which participate in a feedback loop with pacemaker neurons to drive both midday siesta and night-time sleep. Sleep-promoting cells in the fruit fly Specific Drosophila circadian neurons — whose activity cycles over the 24-hour period — are known to promote morning and evening peak locomotor activity, but their involvement in sleep control has been unclear. Now, Michael Rosbash and colleagues identify a subset of dorsal clock neurons, called DN1s, as sleep-promoting cells, participating in a feedback loop with pacemaker neurons to drive both midday siesta and night-time sleep. They further observe that DN1 neuronal activity differs between males and females and responds to temperature, consistent with a role for these factors in daytime sleep. Also in this issue of Nature , Gero Miesenböck and colleagues report that sleep-promoting dopaminergic neurons that innervate the Drosophila fan-shaped body switch between electrical activity and silence as a function of sleep requirement.