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  3. Midbrain glutamatergic circuit mechanism of resilience to socially transferred allodynia in male mice

Midbrain glutamatergic circuit mechanism of resilience to socially transferred allodynia in male mice

  • Nat Commun. 2024 Jun 10;15(1):4947. doi: 10.1038/s41467-024-49340-8.
Yi Han # 1 2 3,  Lin Ai # 1 2 3,  Lingzhen Song # 1 2 3,  Yu Zhou # 1 2 3,  Dandan Chen 1 2 3,  Sha Sha 1 2 3,  Ran Ji 1 2 3,  Qize Li 1 2 3,  Qingyang Bu 1 2 3,  Xiangyu Pan 1 2 3,  Xiaojing Zhai 1 2 3,  Mengqiao Cui 1 2 3,  Jiawen Duan 4,  Junxia Yang 1 2 3,  Dipesh Chaudhury 5,  Ankang Hu 6,  He Liu 7,  Ming-Hu Han 8 9,  Jun-Li Cao 10 11 12 13,  Hongxing Zhang 14 15 16
Affiliations

Affiliations

  • 1 Jiangsu Province Key Laboratory of Anesthesiology, Xuzhou Medical University, Xuzhou, Jiangsu, 221004, PR China.
  • 2 Jiangsu Province Key Laboratory of Anesthesia and Analgesia Application Technology, Xuzhou Medical University, Xuzhou, Jiangsu, 221004, PR China.
  • 3 NMPA Key Laboratory for Research and Evaluation of Narcotic and Psychotropic Drugs, Xuzhou Medical University, Xuzhou, Jiangsu, 221004, PR China.
  • 4 Department of Mental Health and Public Health, Faculty of Life and Health Sciences, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen, Guangdong, 518055, PR China.
  • 5 Division of Science, New York University Abu Dhabi (NYUAD), Saadiyat Island, 129188, United Arab Emirates.
  • 6 The Animal Facility of Xuzhou Medical University, Xuzhou Medical University, Xuzhou, Jiangsu, 221004, PR China.
  • 7 Department of Anesthesiology, Huzhou Central Hospital, Huzhou, Zhejiang, 313000, PR China.
  • 8 Department of Mental Health and Public Health, Faculty of Life and Health Sciences, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen, Guangdong, 518055, PR China. hanmh@siat.ac.cn.
  • 9 Department of Pharmacological Sciences, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA. hanmh@siat.ac.cn.
  • 10 Jiangsu Province Key Laboratory of Anesthesiology, Xuzhou Medical University, Xuzhou, Jiangsu, 221004, PR China. caojl0310@aliyun.com.
  • 11 Jiangsu Province Key Laboratory of Anesthesia and Analgesia Application Technology, Xuzhou Medical University, Xuzhou, Jiangsu, 221004, PR China. caojl0310@aliyun.com.
  • 12 NMPA Key Laboratory for Research and Evaluation of Narcotic and Psychotropic Drugs, Xuzhou Medical University, Xuzhou, Jiangsu, 221004, PR China. caojl0310@aliyun.com.
  • 13 Department of Anesthesiology, The Affiliated Hospital of Xuzhou Medical University, Xuzhou, Jiangsu, 221004, PR China. caojl0310@aliyun.com.
  • 14 Jiangsu Province Key Laboratory of Anesthesiology, Xuzhou Medical University, Xuzhou, Jiangsu, 221004, PR China. hongxing.zhang@xzhmu.edu.cn.
  • 15 Jiangsu Province Key Laboratory of Anesthesia and Analgesia Application Technology, Xuzhou Medical University, Xuzhou, Jiangsu, 221004, PR China. hongxing.zhang@xzhmu.edu.cn.
  • 16 NMPA Key Laboratory for Research and Evaluation of Narcotic and Psychotropic Drugs, Xuzhou Medical University, Xuzhou, Jiangsu, 221004, PR China. hongxing.zhang@xzhmu.edu.cn.
  • # Contributed equally.
PMID: 38858350 DOI: 10.1038/s41467-024-49340-8
Abstract

The potential brain mechanism underlying resilience to socially transferred allodynia remains unknown. Here, we utilize a well-established socially transferred allodynia paradigm to segregate male mice into pain-susceptible and pain-resilient subgroups. Brain screening results show that ventral tegmental area glutamatergic neurons are selectively activated in pain-resilient mice as compared to control and pain-susceptible mice. Chemogenetic manipulations demonstrate that activation and inhibition of ventral tegmental area glutamatergic neurons bi-directionally regulate resilience to socially transferred allodynia. Moreover, ventral tegmental area glutamatergic neurons that project specifically to the nucleus accumbens shell and lateral habenula regulate the development and maintenance of the pain-resilient phenotype, respectively. Together, we establish an approach to explore individual variations in pain response and identify ventral tegmental area glutamatergic neurons and related downstream circuits as critical targets for resilience to socially transferred allodynia and the development of conceptually innovative analgesics.

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