Jiaxi Hu 1,  Yiming Shi 1,  Jiaming Zhang 1,  Xinfeng Huang 1,  Qian Wang 1,  Hang Zhao 1,  Jiawei Shen 1,  Zhiping Chen 1,  Wei Song 2,  Ping Zheng 2,  Shulu Zhan 3,  Yanping Sun 1,  Pengfei Cai 1,  Kai An 1,  Changjie Ouyang 1,  Baizhen Zhao 4,  Qixin Zhou 4,  Lin Xu 4,  Wei Xiong 1,  Zhi Zhang 1,  Jianjun Meng 1,  Jutao Chen 1,  Yuqian Ma 1,  Huan Zhao 1,  Mei Zhang 1,  Kun Qu 1,  Ji Hu 3,  Minhua Luo 5,  Fuqiang Xu 6,  Xiaowei Chen 7,  Ying Xiong 1,  Jin Bao 8,  Tian Xue 9

Affiliations

• 1Hefei National Research Center for Physical Sciences at the Microscale, CAS Key Laboratory of Brain Function and Disease, Biomedical Sciences and Health Laboratory of Anhui Province, School of Life Sciences, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei 230026, China.
• 2Technical Center for Hefei Customs, Hefei 230029, China.
• 3School of Life Science and Technology, ShanghaiTech University, Shanghai 201210, China.
• 4Key Laboratory of Animal Models and Human Disease Mechanisms, Laboratory of Learning and Memory, KIZ-SU Joint Laboratory of Animal Model and Drug Development, and State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, the Chinese Academy of Sciences (CAS), Kunming 650223, China.
• 5State Key Laboratory of Virology, CAS Center for Excellence in Brain Science and Intelligence Technology, Center for Biosafety Mega-Science, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan 430071, China.
• 6Brain Connectome and Behavior, CAS Key Laboratory of Brain Connectome and Manipulation, the Brain Cognition and Brain Disease Institute, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen-Hong Kong Institute of Brain Science-Shenzhen Fundamental Research Institutions, Shenzhen 518055, China.
• 7Brain Research Center, Third Military Medical University, and Chongqing Institute for Brain and Intelligence, Guangyang Bay Laboratory, Chongqing 400038, China.
• 8Hefei National Research Center for Physical Sciences at the Microscale, CAS Key Laboratory of Brain Function and Disease, Biomedical Sciences and Health Laboratory of Anhui Province, School of Life Sciences, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei 230026, China. Electronic address: baojin@ustc.edu.cn.
• 9Hefei National Research Center for Physical Sciences at the Microscale, CAS Key Laboratory of Brain Function and Disease, Biomedical Sciences and Health Laboratory of Anhui Province, School of Life Sciences, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei 230026, China. Electronic address: xuetian@ustc.edu.cn.

PMID: 35944541   DOI: 10.1016/j.cell.2022.07.009

Abstract

During development, melanopsin-expressing intrinsically photosensitive retinal ganglion cells (ipRGCs) become LIGHT sensitive much earlier than rods and cones. IpRGCs project to many subcortical areas, whereas physiological functions of these projections are yet to be fully elucidated. Here, we found that ipRGC-mediated LIGHT sensation promotes synaptogenesis of pyramidal neurons in various cortices and the hippocampus. This phenomenon depends on activation of ipRGCs and is mediated by the release of oxytocin from the supraoptic nucleus (SON) and the paraventricular nucleus (PVN) into cerebral-spinal fluid. We further characterized a direct connection between ipRGCs and oxytocin neurons in the SON and mutual projections between oxytocin neurons in the SON and PVN. Moreover, we showed that the lack of ipRGC-mediated, light-promoted early cortical synaptogenesis compromised learning ability in adult mice. Our results highlight the importance of LIGHT sensation early in life on the development of learning ability and therefore call attention to suitable LIGHT environment for infant care.