Cell Reports (Oct 2022)
A non-canonical retina-ipRGCs-SCN-PVT visual pathway for mediating contagious itch behavior
- Fang Gao,
- Jun Ma,
- Yao-Qing Yu,
- Xiao-Fei Gao,
- Yang Bai,
- Yi Sun,
- Juan Liu,
- Xianyu Liu,
- Devin M. Barry,
- Steven Wilhelm,
- Tyler Piccinni-Ash,
- Na Wang,
- Dongyang Liu,
- Rachel A. Ross,
- Yan Hao,
- Xu Huang,
- Jin-Jing Jia,
- Qianyi Yang,
- Hao Zheng,
- Johan van Nispen,
- Jun Chen,
- Hui Li,
- Jiayi Zhang,
- Yun-Qing Li,
- Zhou-Feng Chen
Affiliations
- Fang Gao
- Center for the Study of Itch and Sensory Disorders, Washington University School of Medicine, St. Louis, MO 63110, USA; Departments of Anesthesiology, Medicine, Psychiatry and Developmental Biology, Washington University School of Medicine, St. Louis, MO 63110, USA
- Jun Ma
- Center for the Study of Itch and Sensory Disorders, Washington University School of Medicine, St. Louis, MO 63110, USA; Departments of Anesthesiology, Medicine, Psychiatry and Developmental Biology, Washington University School of Medicine, St. Louis, MO 63110, USA
- Yao-Qing Yu
- Center for the Study of Itch and Sensory Disorders, Washington University School of Medicine, St. Louis, MO 63110, USA; Departments of Anesthesiology, Medicine, Psychiatry and Developmental Biology, Washington University School of Medicine, St. Louis, MO 63110, USA; Institute for Biomedical Sciences of Pain, Tangdu Hospital, Fourth Military Medical University, Xi’an 710038, P. R. China
- Xiao-Fei Gao
- Center for the Study of Itch and Sensory Disorders, Washington University School of Medicine, St. Louis, MO 63110, USA; Departments of Anesthesiology, Medicine, Psychiatry and Developmental Biology, Washington University School of Medicine, St. Louis, MO 63110, USA
- Yang Bai
- Center for the Study of Itch and Sensory Disorders, Washington University School of Medicine, St. Louis, MO 63110, USA; Department of Anatomy, Histology and Embryology & K.K. Leung Brain Research Centre, Fourth Military Medical University, Xi’an 710032, P. R. China
- Yi Sun
- Center for the Study of Itch and Sensory Disorders, Washington University School of Medicine, St. Louis, MO 63110, USA; Department of Anatomy, Histology and Embryology & K.K. Leung Brain Research Centre, Fourth Military Medical University, Xi’an 710032, P. R. China
- Juan Liu
- Center for the Study of Itch and Sensory Disorders, Washington University School of Medicine, St. Louis, MO 63110, USA; Departments of Anesthesiology, Medicine, Psychiatry and Developmental Biology, Washington University School of Medicine, St. Louis, MO 63110, USA
- Xianyu Liu
- Center for the Study of Itch and Sensory Disorders, Washington University School of Medicine, St. Louis, MO 63110, USA; Departments of Anesthesiology, Medicine, Psychiatry and Developmental Biology, Washington University School of Medicine, St. Louis, MO 63110, USA
- Devin M. Barry
- Center for the Study of Itch and Sensory Disorders, Washington University School of Medicine, St. Louis, MO 63110, USA; Departments of Anesthesiology, Medicine, Psychiatry and Developmental Biology, Washington University School of Medicine, St. Louis, MO 63110, USA
- Steven Wilhelm
- Center for the Study of Itch and Sensory Disorders, Washington University School of Medicine, St. Louis, MO 63110, USA; Departments of Anesthesiology, Medicine, Psychiatry and Developmental Biology, Washington University School of Medicine, St. Louis, MO 63110, USA
- Tyler Piccinni-Ash
- Center for the Study of Itch and Sensory Disorders, Washington University School of Medicine, St. Louis, MO 63110, USA; Departments of Anesthesiology, Medicine, Psychiatry and Developmental Biology, Washington University School of Medicine, St. Louis, MO 63110, USA
- Na Wang
- Center for the Study of Itch and Sensory Disorders, Washington University School of Medicine, St. Louis, MO 63110, USA; Departments of Anesthesiology, Medicine, Psychiatry and Developmental Biology, Washington University School of Medicine, St. Louis, MO 63110, USA
- Dongyang Liu
- Center for the Study of Itch and Sensory Disorders, Washington University School of Medicine, St. Louis, MO 63110, USA; Departments of Anesthesiology, Medicine, Psychiatry and Developmental Biology, Washington University School of Medicine, St. Louis, MO 63110, USA; Department of Pain Management, the State Key Clinical Specialty in Pain Medicine, the Second Affiliated Hospital, Guangzhou Medical University, Guangzhou 510260, P.R. China
- Rachel A. Ross
- Department of Neuroscience, Psychiatry and Medicine, Albert Einstein College of Medicine Rose F. Kennedy Center, Bronx, NY, USA
- Yan Hao
- Center for the Study of Itch and Sensory Disorders, Washington University School of Medicine, St. Louis, MO 63110, USA; Departments of Anesthesiology, Medicine, Psychiatry and Developmental Biology, Washington University School of Medicine, St. Louis, MO 63110, USA
- Xu Huang
- Institutes of Brain Science, State Key Laboratory of Medical Neurobiology, MOE Frontiers Center for Brain Science and Institute for Medical and Engineering Innovation, Eye & ENT Hospital, Fudan University, Shanghai 200031, P.R. China
- Jin-Jing Jia
- Center for the Study of Itch and Sensory Disorders, Washington University School of Medicine, St. Louis, MO 63110, USA; Departments of Anesthesiology, Medicine, Psychiatry and Developmental Biology, Washington University School of Medicine, St. Louis, MO 63110, USA
- Qianyi Yang
- Center for the Study of Itch and Sensory Disorders, Washington University School of Medicine, St. Louis, MO 63110, USA; Departments of Anesthesiology, Medicine, Psychiatry and Developmental Biology, Washington University School of Medicine, St. Louis, MO 63110, USA
- Hao Zheng
- Institutes of Brain Science, State Key Laboratory of Medical Neurobiology, MOE Frontiers Center for Brain Science and Institute for Medical and Engineering Innovation, Eye & ENT Hospital, Fudan University, Shanghai 200031, P.R. China
- Johan van Nispen
- Center for the Study of Itch and Sensory Disorders, Washington University School of Medicine, St. Louis, MO 63110, USA; Departments of Anesthesiology, Medicine, Psychiatry and Developmental Biology, Washington University School of Medicine, St. Louis, MO 63110, USA
- Jun Chen
- Institute for Biomedical Sciences of Pain, Tangdu Hospital, Fourth Military Medical University, Xi’an 710038, P. R. China
- Hui Li
- Department of Anatomy, Histology and Embryology & K.K. Leung Brain Research Centre, Fourth Military Medical University, Xi’an 710032, P. R. China
- Jiayi Zhang
- Institutes of Brain Science, State Key Laboratory of Medical Neurobiology, MOE Frontiers Center for Brain Science and Institute for Medical and Engineering Innovation, Eye & ENT Hospital, Fudan University, Shanghai 200031, P.R. China
- Yun-Qing Li
- Department of Anatomy, Histology and Embryology & K.K. Leung Brain Research Centre, Fourth Military Medical University, Xi’an 710032, P. R. China
- Zhou-Feng Chen
- Center for the Study of Itch and Sensory Disorders, Washington University School of Medicine, St. Louis, MO 63110, USA; Departments of Anesthesiology, Medicine, Psychiatry and Developmental Biology, Washington University School of Medicine, St. Louis, MO 63110, USA; Corresponding author
- Journal volume & issue
-
Vol. 41,
no. 1
p. 111444
Abstract
Summary: Contagious itch behavior informs conspecifics of adverse environment and is crucial for the survival of social animals. Gastrin-releasing peptide (GRP) and its receptor (GRPR) in the suprachiasmatic nucleus (SCN) of the hypothalamus mediates contagious itch behavior in mice. Here, we show that intrinsically photosensitive retina ganglion cells (ipRGCs) convey visual itch information, independently of melanopsin, from the retina to GRP neurons via PACAP-PAC1R signaling. Moreover, GRPR neurons relay itch information to the paraventricular nucleus of the thalamus (PVT). Surprisingly, neither the visual cortex nor superior colliculus is involved in contagious itch. In vivo calcium imaging and extracellular recordings reveal contagious itch-specific neural dynamics of GRPR neurons. Thus, we propose that the retina-ipRGC-SCN-PVT pathway constitutes a previously unknown visual pathway that probably evolved for motion vision that encodes salient environmental cues and enables animals to imitate behaviors of conspecifics as an anticipatory mechanism to cope with adverse conditions.
