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A retinoraphe projection regulates serotonergic activity and looming-evoked defensive behaviour

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  • Lu Huang

    (Guangdong-Hongkong-Macau Institute of CNS Regeneration, Ministry of Education CNS Regeneration Collaborative Joint Laboratory, Jinan University
    Guangdong key Laboratory of Brain Function and Diseases, Jinan University)

  • Tifei Yuan

    (School of Psychology, Nanjing Normal University)

  • Minjie Tan

    (Guangdong-Hongkong-Macau Institute of CNS Regeneration, Ministry of Education CNS Regeneration Collaborative Joint Laboratory, Jinan University
    Guangdong key Laboratory of Brain Function and Diseases, Jinan University)

  • Yue Xi

    (Guangdong-Hongkong-Macau Institute of CNS Regeneration, Ministry of Education CNS Regeneration Collaborative Joint Laboratory, Jinan University
    Guangdong key Laboratory of Brain Function and Diseases, Jinan University)

  • Yu Hu

    (Guangdong-Hongkong-Macau Institute of CNS Regeneration, Ministry of Education CNS Regeneration Collaborative Joint Laboratory, Jinan University
    Guangdong key Laboratory of Brain Function and Diseases, Jinan University)

  • Qian Tao

    (School of Medicine, Jinan University)

  • Zhikai Zhao

    (Guangdong-Hongkong-Macau Institute of CNS Regeneration, Ministry of Education CNS Regeneration Collaborative Joint Laboratory, Jinan University
    Guangdong key Laboratory of Brain Function and Diseases, Jinan University)

  • Jiajun Zheng

    (Guangdong-Hongkong-Macau Institute of CNS Regeneration, Ministry of Education CNS Regeneration Collaborative Joint Laboratory, Jinan University
    Guangdong key Laboratory of Brain Function and Diseases, Jinan University)

  • Yushui Han

    (Guangdong-Hongkong-Macau Institute of CNS Regeneration, Ministry of Education CNS Regeneration Collaborative Joint Laboratory, Jinan University
    Guangdong key Laboratory of Brain Function and Diseases, Jinan University)

  • Fuqiang Xu

    (State Key Laboratory of Magnetic Resonance and Atomic and Molecular Physics, Wuhan Institute of Physics and Mathematics, Chinese Academy of Sciences)

  • Minmin Luo

    (National Institute of Biological Sciences, Zhongguancun Life Science)

  • Patricia J. Sollars

    (School of Veterinary Medicine and Biomedical Sciences, University of Nebraska)

  • Mingliang Pu

    (School of Basic Medical Sciences, Peking University)

  • Gary E. Pickard

    (School of Veterinary Medicine and Biomedical Sciences, University of Nebraska
    University of Nebraska Medical Center)

  • Kwok-Fai So

    (Guangdong-Hongkong-Macau Institute of CNS Regeneration, Ministry of Education CNS Regeneration Collaborative Joint Laboratory, Jinan University
    Guangdong key Laboratory of Brain Function and Diseases, Jinan University
    The University of Hong Kong
    Co-innovation Center of Neuroregeneration, Nantong University)

  • Chaoran Ren

    (Guangdong-Hongkong-Macau Institute of CNS Regeneration, Ministry of Education CNS Regeneration Collaborative Joint Laboratory, Jinan University
    Guangdong key Laboratory of Brain Function and Diseases, Jinan University
    Co-innovation Center of Neuroregeneration, Nantong University)

Abstract

Animals promote their survival by avoiding rapidly approaching objects that indicate threats. In mice, looming-evoked defensive responses are triggered by the superior colliculus (SC) which receives direct retinal inputs. However, the specific neural circuits that begin in the retina and mediate this important behaviour remain unclear. Here we identify a subset of retinal ganglion cells (RGCs) that controls mouse looming-evoked defensive responses through axonal collaterals to the dorsal raphe nucleus (DRN) and SC. Looming signals transmitted by DRN-projecting RGCs activate DRN GABAergic neurons that in turn inhibit serotoninergic neurons. Moreover, activation of DRN serotoninergic neurons reduces looming-evoked defensive behaviours. Thus, a dedicated population of RGCs signals rapidly approaching visual threats and their input to the DRN controls a serotonergic self-gating mechanism that regulates innate defensive responses. Our study provides new insights into how the DRN and SC work in concert to extract and translate visual threats into defensive behavioural responses.

Suggested Citation

  • Lu Huang & Tifei Yuan & Minjie Tan & Yue Xi & Yu Hu & Qian Tao & Zhikai Zhao & Jiajun Zheng & Yushui Han & Fuqiang Xu & Minmin Luo & Patricia J. Sollars & Mingliang Pu & Gary E. Pickard & Kwok-Fai So , 2017. "A retinoraphe projection regulates serotonergic activity and looming-evoked defensive behaviour," Nature Communications, Nature, vol. 8(1), pages 1-13, April.
  • Handle: RePEc:nat:natcom:v:8:y:2017:i:1:d:10.1038_ncomms14908
    DOI: 10.1038/ncomms14908
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    Cited by:

    1. Elyashiv Zangen & Shira Hadar & Christopher Lawrence & Mustafa Obeid & Hala Rasras & Ella Hanzin & Ori Aslan & Eyal Zur & Nadav Schulcz & Daniel Cohen-Hatab & Yona Samama & Sarah Nir & Yi Li & Irina D, 2024. "Prefrontal cortex neurons encode ambient light intensity differentially across regions and layers," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    2. Wei Shang & Shuangyi Xie & Wenbo Feng & Zhuangzhuang Li & Jingyan Jia & Xiaoxiao Cao & Yanting Shen & Jing Li & Haibo Shi & Yiran Gu & Shi-Jun Weng & Longnian Lin & Yi-Hsuan Pan & Xiao-Bing Yuan, 2024. "A non-image-forming visual circuit mediates the innate fear of heights in male mice," Nature Communications, Nature, vol. 15(1), pages 1-16, December.

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