A Visual Circuit Related to the Nucleus Reuniens for the Spatial-Memory-Promoting Effects of Light Treatment

Xiaodan Huang; Pengcheng Huang; Lu Huang; Zhengfang Hu; Xianwei Liu; Jiawei Shen; Yue Xi; Yan Yang; Yunwei Fu; Qian Tao; Song Lin; Anding Xu; Fuqiang Xu; Tian Xue; Kwok-Fai So; Haohong Li; Chaoran Ren

doi:10.1016/j.neuron.2020.10.023

A Visual Circuit Related to the Nucleus Reuniens for the Spatial-Memory-Promoting Effects of Light Treatment

Neuron. 2021 Jan 20;109(2):347-362.e7. doi: 10.1016/j.neuron.2020.10.023. Epub 2020 Nov 9.

Authors

Xiaodan Huang¹, Pengcheng Huang², Lu Huang¹, Zhengfang Hu³, Xianwei Liu³, Jiawei Shen⁴, Yue Xi³, Yan Yang³, Yunwei Fu³, Qian Tao⁵, Song Lin⁶, Anding Xu⁷, Fuqiang Xu⁸, Tian Xue⁹, Kwok-Fai So¹⁰, Haohong Li¹¹, Chaoran Ren¹²

Affiliations

¹ Guangdong-Hongkong-Macau Institute of CNS Regeneration, Ministry of Education CNS Regeneration Collaborative Joint Laboratory, Jinan University, Guangzhou 510632, China; Department of Neurology and Stroke Center, The First Affiliated Hospital of Jinan University, Guangzhou 510632, China.
² Britton Chance Center for Biomedical Photonics, Wuhan National Laboratory for Optoelectronics, MoE Key Laboratory for Biomedical Photonics, Collaborative Innovation Center for Biomedical Engineering, School of Engineering Sciences, Huazhong University of Science and Technology, Wuhan 430074, China.
³ Guangdong-Hongkong-Macau Institute of CNS Regeneration, Ministry of Education CNS Regeneration Collaborative Joint Laboratory, Jinan University, Guangzhou 510632, China.
⁴ Hefei National Laboratory for Physical Sciences at the Microscale, Neurodegenerative Disorder Research Center, Chinese Academy of Sciences Key Laboratory of Brain Function and Disease, School of Life Sciences, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei 230026, China.
⁵ Psychology Department, School of Medicine, Jinan University, Guangzhou 510632, China.
⁶ Physiology Department, School of Medicine, Jinan University, Guangzhou 510632, China.
⁷ Department of Neurology and Stroke Center, The First Affiliated Hospital of Jinan University, Guangzhou 510632, China.
⁸ CAS Key Laboratory of Brain Connectome and Manipulation, the Brain Cognition and Brain Disease Institute (BCBDI), Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences (CAS), Shenzhen 518055, China.
⁹ Hefei National Laboratory for Physical Sciences at the Microscale, Neurodegenerative Disorder Research Center, Chinese Academy of Sciences Key Laboratory of Brain Function and Disease, School of Life Sciences, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei 230026, China; Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, Shanghai 200031, China.
¹⁰ Guangdong-Hongkong-Macau Institute of CNS Regeneration, Ministry of Education CNS Regeneration Collaborative Joint Laboratory, Jinan University, Guangzhou 510632, China; Bioland Laboratory (Guangzhou Regenerative Medicine and Health Guangdong Laboratory), Guangzhou 510530, China; Department of Ophthalmology and State Key Laboratory of Brain and Cognitive Sciences, The University of Hong Kong, Hong Kong, China; Center for Brain Science and Brain-Inspired Intelligence, Guangdong-Hong Kong-Macao Greater Bay Area, Guangzhou 510515, China; Co-innovation Center of Neuroregeneration, Nantong University, Nantong 226001, China. Electronic address: hrmaskf@hku.hk.
¹¹ Britton Chance Center for Biomedical Photonics, Wuhan National Laboratory for Optoelectronics, MoE Key Laboratory for Biomedical Photonics, Collaborative Innovation Center for Biomedical Engineering, School of Engineering Sciences, Huazhong University of Science and Technology, Wuhan 430074, China; The MOE Frontier Science Center for Brain Research and Brain-Machine Integration, Zhejiang University School of Brain Science and Brain Medicine, Hangzhou 310012, China. Electronic address: hxli@hust.edu.cn.
¹² Guangdong-Hongkong-Macau Institute of CNS Regeneration, Ministry of Education CNS Regeneration Collaborative Joint Laboratory, Jinan University, Guangzhou 510632, China; Bioland Laboratory (Guangzhou Regenerative Medicine and Health Guangdong Laboratory), Guangzhou 510530, China; Center for Brain Science and Brain-Inspired Intelligence, Guangdong-Hong Kong-Macao Greater Bay Area, Guangzhou 510515, China; Co-innovation Center of Neuroregeneration, Nantong University, Nantong 226001, China. Electronic address: tchaoran@jnu.edu.cn.

PMID: 33171117
DOI: 10.1016/j.neuron.2020.10.023

Abstract

Light exerts profound effects on cognitive functions across species, including humans. However, the neuronal mechanisms underlying the effects of light on cognitive functions are poorly understood. In this study, we show that long-term exposure to bright-light treatment promotes spatial memory through a di-synaptic visual circuit related to the nucleus reuniens (Re). Specifically, a subset of SMI-32-expressing ON-type retinal ganglion cells (RGCs) innervate CaMKIIα neurons in the thalamic ventral lateral geniculate nucleus and intergeniculate leaflet (vLGN/IGL), which in turn activate CaMKIIα neurons in the Re. Specific activation of vLGN/IGL-projecting RGCs, activation of Re-projecting vLGN/IGL neurons, or activation of postsynaptic Re neurons is sufficient to promote spatial memory. Furthermore, we demonstrate that the spatial-memory-promoting effects of light treatment are dependent on the activation of vLGN/IGL-projecting RGCs, Re-projecting vLGN/IGL neurons, and Re neurons. Our results reveal a dedicated subcortical visual circuit that mediates the spatial-memory-promoting effects of light treatment.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Lighting / methods*
Male
Mice
Mice, Inbred C57BL
Midline Thalamic Nuclei / chemistry
Midline Thalamic Nuclei / metabolism*
Nerve Net / chemistry
Nerve Net / metabolism*
Organ Culture Techniques
Photoperiod*
Spatial Memory / physiology*
Visual Pathways / chemistry
Visual Pathways / metabolism*