Hub-organized parallel circuits of central circadian pacemaker neurons for visual photoentrainment in Drosophila

• Published in: Nature communications Vol. 9; no. 1; pp. 4247 - 14
• Main Authors: Li, Meng-Tong, Cao, Li-Hui, Xiao, Na, Tang, Min, Deng, Bowen, Yang, Tian, Yoshii, Taishi, Luo, Dong-Gen
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 12.10.2018; Nature Publishing Group; Nature Portfolio
• Subjects: 14/34; 14/69; 631/378/1385/1330; 631/378/3920; 64/24; 9/74; Animals; Biological Clocks - physiology; Circadian rhythm; Circadian Rhythm - genetics; Circadian Rhythm - physiology; Circadian rhythms; Circuits; Dendrites; Drosophila; Drosophila - cytology; Drosophila - metabolism; Drosophila - physiology; Drosophila Proteins - metabolism; Drosophila Proteins - physiology; Eye; Humanities and Social Sciences; Insects; Interneurons; Laser ablation; Light effects; Medulla oblongata; multidisciplinary; Neurons; Neurons - cytology; Neurons - metabolism; Neurons - physiology; Neuropil; Photoreceptors; Science; Science (multidisciplinary); Visual pathways; Visual Pathways - physiology
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-018-06506-5

Circadian rhythms are orchestrated by a master clock that emerges from a network of circadian pacemaker neurons. The master clock is synchronized to external light/dark cycles through photoentrainment, but the circuit mechanisms underlying visual photoentrainment remain largely unknown. Here, we report that Drosophila has eye-mediated photoentrainment via a parallel pacemaker neuron organization. Patch-clamp recordings of central circadian pacemaker neurons reveal that light excites most of them independently of one another. We also show that light-responding pacemaker neurons send their dendrites to a neuropil called accessary medulla (aMe), where they make monosynaptic connections with Hofbauer–Buchner eyelet photoreceptors and interneurons that transmit compound-eye signals. Laser ablation of aMe and eye removal both abolish light responses of circadian pacemaker neurons, revealing aMe as a hub to channel eye inputs to central circadian clock. Taken together, we demonstrate that the central clock receives eye inputs via hub-organized parallel circuits in Drosophila . The central circadian clock in Drosophila is made up of ~ 150 anatomically distributed neurons; the circuits underlying photoentrainment is unclear. This study describes ex vivo patch-clamp recording of the eye-mediated light response of all known circadian clock neurons, and shows that they are organized in parallel circuits centered around a hub.