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

Yi Han, Lin Ai, Lingzhen Song, Yu Zhou, Dandan Chen, Sha Sha, Ran Ji, Qize Li, Qingyang Bu, Xiangyu Pan, Xiaojing Zhai, Mengqiao Cui, Jiawen Duan, Junxia Yang, Dipesh Chaudhury, Ankang Hu, He Liu, Ming-Hu Han (), Jun-Li Cao () and Hongxing Zhang ()
Additional contact information
Yi Han: Xuzhou Medical University
Lin Ai: Xuzhou Medical University
Lingzhen Song: Xuzhou Medical University
Yu Zhou: Xuzhou Medical University
Dandan Chen: Xuzhou Medical University
Sha Sha: Xuzhou Medical University
Ran Ji: Xuzhou Medical University
Qize Li: Xuzhou Medical University
Qingyang Bu: Xuzhou Medical University
Xiangyu Pan: Xuzhou Medical University
Xiaojing Zhai: Xuzhou Medical University
Mengqiao Cui: Xuzhou Medical University
Jiawen Duan: Chinese Academy of Sciences
Junxia Yang: Xuzhou Medical University
Dipesh Chaudhury: New York University Abu Dhabi (NYUAD)
Ankang Hu: Xuzhou Medical University
He Liu: Huzhou Central Hospital
Ming-Hu Han: Chinese Academy of Sciences
Jun-Li Cao: Xuzhou Medical University
Hongxing Zhang: Xuzhou Medical University

Nature Communications, 2024, vol. 15, issue 1, 1-14

Abstract: 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.

Date: 2024
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DOI: 10.1038/s41467-024-49340-8

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