A single photoreceptor splits perception and entrainment by cotransmission

Na Xiao, Shuang Xu, Ze-Kai Li, Min Tang, Renbo Mao, Tian Yang, Si-Xing Ma, Peng-Hao Wang, Meng-Tong Li, Ajay Sunilkumar, François Rouyer, Li-Hui Cao and Dong-Gen Luo ()
Additional contact information
Na Xiao: Peking University
Shuang Xu: Peking University
Ze-Kai Li: Peking University
Min Tang: Peking University
Renbo Mao: Peking University
Tian Yang: Peking University
Si-Xing Ma: Peking University
Peng-Hao Wang: Peking University
Meng-Tong Li: Peking University
Ajay Sunilkumar: Université Paris-Sud, Université Paris-Saclay, CNRS
François Rouyer: Université Paris-Sud, Université Paris-Saclay, CNRS
Li-Hui Cao: Capital Medical University
Dong-Gen Luo: Peking University

Nature, 2023, vol. 623, issue 7987, 562-570

Abstract: Abstract Vision enables both image-forming perception, driven by a contrast-based pathway, and unconscious non-image-forming circadian photoentrainment, driven by an irradiance-based pathway1,2. Although two distinct photoreceptor populations are specialized for each visual task3–6, image-forming photoreceptors can additionally contribute to photoentrainment of the circadian clock in different species7–15. However, it is unknown how the image-forming photoreceptor pathway can functionally implement the segregation of irradiance signals required for circadian photoentrainment from contrast signals required for image perception. Here we report that the Drosophila R8 photoreceptor separates image-forming and irradiance signals by co-transmitting two neurotransmitters, histamine and acetylcholine. This segregation is further established postsynaptically by histamine-receptor-expressing unicolumnar retinotopic neurons and acetylcholine-receptor-expressing multicolumnar integration neurons. The acetylcholine transmission from R8 photoreceptors is sustained by an autocrine negative feedback of the cotransmitted histamine during the light phase of light–dark cycles. At the behavioural level, elimination of histamine and acetylcholine transmission impairs R8-driven motion detection and circadian photoentrainment, respectively. Thus, a single type of photoreceptor can achieve the dichotomy of visual perception and circadian photoentrainment as early as the first visual synapses, revealing a simple yet robust mechanism to segregate and translate distinct sensory features into different animal behaviours.

Date: 2023
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DOI: 10.1038/s41586-023-06681-6

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