Ventral hippocampal CA1 modulates pain behaviors in mice with peripheral inflammation

Summary: Chronic pain is one of the most significant medical problems throughout the world. Recent evidence has confirmed the hippocampus as an active modulator of pain chronicity, but the underlying mechanisms remain unclear. Using in vivo electrophysiology, we identify a neural ensemble in the ven...

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Main Authors: Shan Shao, Yawen Zheng, Zibing Fu, Jiaxin Wang, Yu Zhang, Cheng Wang, Xuetao Qi, Tingting Gong, Longyu Ma, Xi Lin, Haitao Yu, Shulu Yuan, You Wan, Haolin Zhang, Ming Yi
Format: Article
Language:English
Published: Elsevier 2023-01-01
Series:Cell Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124723000281
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author Shan Shao
Yawen Zheng
Zibing Fu
Jiaxin Wang
Yu Zhang
Cheng Wang
Xuetao Qi
Tingting Gong
Longyu Ma
Xi Lin
Haitao Yu
Shulu Yuan
You Wan
Haolin Zhang
Ming Yi
author_facet Shan Shao
Yawen Zheng
Zibing Fu
Jiaxin Wang
Yu Zhang
Cheng Wang
Xuetao Qi
Tingting Gong
Longyu Ma
Xi Lin
Haitao Yu
Shulu Yuan
You Wan
Haolin Zhang
Ming Yi
author_sort Shan Shao
collection DOAJ
description Summary: Chronic pain is one of the most significant medical problems throughout the world. Recent evidence has confirmed the hippocampus as an active modulator of pain chronicity, but the underlying mechanisms remain unclear. Using in vivo electrophysiology, we identify a neural ensemble in the ventral hippocampal CA1 (vCA1) that shows inhibitory responses to noxious but not innocuous stimuli. Following peripheral inflammation, this ensemble becomes responsive to innocuous stimuli, representing hypersensitivity. Mimicking the inhibition of vCA1 neurons using chemogenetics induces chronic pain-like behaviors in naive mice, whereas activating vCA1 neurons in mice with peripheral inflammation results in a reduction of pain-related behaviors. Pathway-specific manipulation of vCA1 projections to basolateral amygdala (BLA) and infralimbic cortex (IL) shows that these pathways are differentially involved in pain modulation at different temporal stages of chronic inflammatory pain. These results confirm a crucial role of the vCA1 and its circuits in modulating the development of chronic pain.
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spelling doaj.art-95cb23894769448986a11c1db8cab3f62023-01-21T04:20:43ZengElsevierCell Reports2211-12472023-01-01421112017Ventral hippocampal CA1 modulates pain behaviors in mice with peripheral inflammationShan Shao0Yawen Zheng1Zibing Fu2Jiaxin Wang3Yu Zhang4Cheng Wang5Xuetao Qi6Tingting Gong7Longyu Ma8Xi Lin9Haitao Yu10Shulu Yuan11You Wan12Haolin Zhang13Ming Yi14Neuroscience Research Institute and Department of Neurobiology, School of Basic Medical Sciences, Peking University, Beijing 100083, P.R. ChinaNeuroscience Research Institute and Department of Neurobiology, School of Basic Medical Sciences, Peking University, Beijing 100083, P.R. ChinaNeuroscience Research Institute and Department of Neurobiology, School of Basic Medical Sciences, Peking University, Beijing 100083, P.R. ChinaNeuroscience Research Institute and Department of Neurobiology, School of Basic Medical Sciences, Peking University, Beijing 100083, P.R. ChinaNeuroscience Research Institute and Department of Neurobiology, School of Basic Medical Sciences, Peking University, Beijing 100083, P.R. China; Institute of Laboratory Animal Sciences, Chinese Academy of Medical Sciences (CAMS), Comparative Medicine Center, Peking Union Medical College (PUMC), Beijing 100021, P.R. ChinaNeuroscience Research Institute and Department of Neurobiology, School of Basic Medical Sciences, Peking University, Beijing 100083, P.R. China; Chinese Institute for Brain Research, Beijing 102206, P.R. ChinaNeuroscience Research Institute and Department of Neurobiology, School of Basic Medical Sciences, Peking University, Beijing 100083, P.R. ChinaNeuroscience Research Institute and Department of Neurobiology, School of Basic Medical Sciences, Peking University, Beijing 100083, P.R. ChinaNeuroscience Research Institute and Department of Neurobiology, School of Basic Medical Sciences, Peking University, Beijing 100083, P.R. ChinaDepartment of Civil Engineering, Tsinghua University, Beijing 100084, P.R. ChinaDepartment of Pathophysiology, Key Laboratory of Ministry of Education for Neurological Disorders, School of Basic Medicine, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, P.R. ChinaNeuroscience Research Institute and Department of Neurobiology, School of Basic Medical Sciences, Peking University, Beijing 100083, P.R. ChinaNeuroscience Research Institute and Department of Neurobiology, School of Basic Medical Sciences, Peking University, Beijing 100083, P.R. China; Key Laboratory for Neuroscience, Ministry of Education / National Health Commission, Peking University, Beijing 100083, P.R. ChinaDepartment of Traditional Chinese Medicine, Peking University Third Hospital, Beijing 100191, P.R. China; Corresponding authorNeuroscience Research Institute and Department of Neurobiology, School of Basic Medical Sciences, Peking University, Beijing 100083, P.R. China; Key Laboratory for Neuroscience, Ministry of Education / National Health Commission, Peking University, Beijing 100083, P.R. China; Corresponding authorSummary: Chronic pain is one of the most significant medical problems throughout the world. Recent evidence has confirmed the hippocampus as an active modulator of pain chronicity, but the underlying mechanisms remain unclear. Using in vivo electrophysiology, we identify a neural ensemble in the ventral hippocampal CA1 (vCA1) that shows inhibitory responses to noxious but not innocuous stimuli. Following peripheral inflammation, this ensemble becomes responsive to innocuous stimuli, representing hypersensitivity. Mimicking the inhibition of vCA1 neurons using chemogenetics induces chronic pain-like behaviors in naive mice, whereas activating vCA1 neurons in mice with peripheral inflammation results in a reduction of pain-related behaviors. Pathway-specific manipulation of vCA1 projections to basolateral amygdala (BLA) and infralimbic cortex (IL) shows that these pathways are differentially involved in pain modulation at different temporal stages of chronic inflammatory pain. These results confirm a crucial role of the vCA1 and its circuits in modulating the development of chronic pain.http://www.sciencedirect.com/science/article/pii/S2211124723000281CP: Neuroscience
spellingShingle Shan Shao
Yawen Zheng
Zibing Fu
Jiaxin Wang
Yu Zhang
Cheng Wang
Xuetao Qi
Tingting Gong
Longyu Ma
Xi Lin
Haitao Yu
Shulu Yuan
You Wan
Haolin Zhang
Ming Yi
Ventral hippocampal CA1 modulates pain behaviors in mice with peripheral inflammation
Cell Reports
CP: Neuroscience
title Ventral hippocampal CA1 modulates pain behaviors in mice with peripheral inflammation
title_full Ventral hippocampal CA1 modulates pain behaviors in mice with peripheral inflammation
title_fullStr Ventral hippocampal CA1 modulates pain behaviors in mice with peripheral inflammation
title_full_unstemmed Ventral hippocampal CA1 modulates pain behaviors in mice with peripheral inflammation
title_short Ventral hippocampal CA1 modulates pain behaviors in mice with peripheral inflammation
title_sort ventral hippocampal ca1 modulates pain behaviors in mice with peripheral inflammation
topic CP: Neuroscience
url http://www.sciencedirect.com/science/article/pii/S2211124723000281
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