Role of astrocytic mu-opioid receptors of the ventrolateral periaqueductal gray in modulating anxiety-like responses

Abstract Background Mu-opioid receptors (MORs) are critical regulators mediating the modulation of several behavioral reactions, including analgesia, addiction, and sedation. Recent studies have reported that MORs are closely associated with mood disorders or anxiety behaviors; however, the underlyi...

Full description

Saved in:
Bibliographic Details
Main Authors: Yinan Du, Aozhuo Zhang, Zhiwei Li, Yukui Zhao, Shuyi Liu, Chunling Wei, Qiaohua Zheng, Yanning Qiao, Yihui Liu, Wei Ren, Jing Han, Zhiqiang Liu, Fei Gao
Format: Article
Language:English
Published: BMC 2025-07-01
Series:Behavioral and Brain Functions
Subjects:
Online Access:https://doi.org/10.1186/s12993-025-00291-0
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849331721340715008
author Yinan Du
Aozhuo Zhang
Zhiwei Li
Yukui Zhao
Shuyi Liu
Chunling Wei
Qiaohua Zheng
Yanning Qiao
Yihui Liu
Wei Ren
Jing Han
Zhiqiang Liu
Fei Gao
author_facet Yinan Du
Aozhuo Zhang
Zhiwei Li
Yukui Zhao
Shuyi Liu
Chunling Wei
Qiaohua Zheng
Yanning Qiao
Yihui Liu
Wei Ren
Jing Han
Zhiqiang Liu
Fei Gao
author_sort Yinan Du
collection DOAJ
description Abstract Background Mu-opioid receptors (MORs) are critical regulators mediating the modulation of several behavioral reactions, including analgesia, addiction, and sedation. Recent studies have reported that MORs are closely associated with mood disorders or anxiety behaviors; however, the underlying neural mechanisms remain unclear. The periaqueductal gray (PAG), a key brain area, participates in the modulation of aversive emotional behaviors. MORs show a high expression in the ventrolateral PAG (vlPAG) region. This study explored the preliminary role of MORs expressed in the vlPAG in modulating emotional behaviors. Results Bilateral administration of DAMGO, an MOR-specific agonist, into the vlPAG of male mice elicited anxiety-like behaviors in elevated plus maze tests. This phenotype was reversed by conditional knockdown of astrocytic MORs. In contrast, glutamatergic or GABAergic MORs were not involved in vlPAG MOR-dependent anxiety-like behaviors. By using in vitro calcium imaging of vlPAG astrocytes and chemical genetic technologies, we found that vlPAG astrocytic MORs can promote astrocytic calcium signaling, which can efficiently induce anxiety-like behaviors. Accordingly, the interference of astrocytic calcium signaling by viral infection reversed vlPAG-dependent anxiety-like behaviors. Conclusion Our findings demonstrated that vlPAG astrocytic, but not glutamatergic or GABAergic, MORs are involved in modulating emotional reactions, and these effects are accomplished by MOR-elicited astrocytic calcium signaling mechanisms. The present study provides a theoretical basis for treating emotional dysfunctions during MOR-targeted management.
format Article
id doaj-art-192c74a6ce43403ebd87d186e38654bd
institution Kabale University
issn 1744-9081
language English
publishDate 2025-07-01
publisher BMC
record_format Article
series Behavioral and Brain Functions
spelling doaj-art-192c74a6ce43403ebd87d186e38654bd2025-08-20T03:46:25ZengBMCBehavioral and Brain Functions1744-90812025-07-0121111510.1186/s12993-025-00291-0Role of astrocytic mu-opioid receptors of the ventrolateral periaqueductal gray in modulating anxiety-like responsesYinan Du0Aozhuo Zhang1Zhiwei Li2Yukui Zhao3Shuyi Liu4Chunling Wei5Qiaohua Zheng6Yanning Qiao7Yihui Liu8Wei Ren9Jing Han10Zhiqiang Liu11Fei Gao12Department of Neurology, The First Affiliated Hospital of Xi’an Medical UniversityMOE Key Laboratory of Modern Teaching Technology, Shaanxi Normal UniversityMOE Key Laboratory of Modern Teaching Technology, Shaanxi Normal UniversityMOE Key Laboratory of Modern Teaching Technology, Shaanxi Normal UniversityMOE Key Laboratory of Modern Teaching Technology, Shaanxi Normal UniversityMOE Key Laboratory of Modern Teaching Technology, Shaanxi Normal UniversityMOE Key Laboratory of Modern Teaching Technology, Shaanxi Normal UniversityMOE Key Laboratory of Modern Teaching Technology, Shaanxi Normal UniversityMOE Key Laboratory of Modern Teaching Technology, Shaanxi Normal UniversityMOE Key Laboratory of Modern Teaching Technology, Shaanxi Normal UniversityMOE Key Laboratory of Modern Teaching Technology, Shaanxi Normal UniversityMOE Key Laboratory of Modern Teaching Technology, Shaanxi Normal UniversityDepartment of Neurology, The First Affiliated Hospital of Xi’an Medical UniversityAbstract Background Mu-opioid receptors (MORs) are critical regulators mediating the modulation of several behavioral reactions, including analgesia, addiction, and sedation. Recent studies have reported that MORs are closely associated with mood disorders or anxiety behaviors; however, the underlying neural mechanisms remain unclear. The periaqueductal gray (PAG), a key brain area, participates in the modulation of aversive emotional behaviors. MORs show a high expression in the ventrolateral PAG (vlPAG) region. This study explored the preliminary role of MORs expressed in the vlPAG in modulating emotional behaviors. Results Bilateral administration of DAMGO, an MOR-specific agonist, into the vlPAG of male mice elicited anxiety-like behaviors in elevated plus maze tests. This phenotype was reversed by conditional knockdown of astrocytic MORs. In contrast, glutamatergic or GABAergic MORs were not involved in vlPAG MOR-dependent anxiety-like behaviors. By using in vitro calcium imaging of vlPAG astrocytes and chemical genetic technologies, we found that vlPAG astrocytic MORs can promote astrocytic calcium signaling, which can efficiently induce anxiety-like behaviors. Accordingly, the interference of astrocytic calcium signaling by viral infection reversed vlPAG-dependent anxiety-like behaviors. Conclusion Our findings demonstrated that vlPAG astrocytic, but not glutamatergic or GABAergic, MORs are involved in modulating emotional reactions, and these effects are accomplished by MOR-elicited astrocytic calcium signaling mechanisms. The present study provides a theoretical basis for treating emotional dysfunctions during MOR-targeted management.https://doi.org/10.1186/s12993-025-00291-0AnxietyMu-opioid receptorsPeriaqueductal grayAstrocyteCalcium signaling
spellingShingle Yinan Du
Aozhuo Zhang
Zhiwei Li
Yukui Zhao
Shuyi Liu
Chunling Wei
Qiaohua Zheng
Yanning Qiao
Yihui Liu
Wei Ren
Jing Han
Zhiqiang Liu
Fei Gao
Role of astrocytic mu-opioid receptors of the ventrolateral periaqueductal gray in modulating anxiety-like responses
Behavioral and Brain Functions
Anxiety
Mu-opioid receptors
Periaqueductal gray
Astrocyte
Calcium signaling
title Role of astrocytic mu-opioid receptors of the ventrolateral periaqueductal gray in modulating anxiety-like responses
title_full Role of astrocytic mu-opioid receptors of the ventrolateral periaqueductal gray in modulating anxiety-like responses
title_fullStr Role of astrocytic mu-opioid receptors of the ventrolateral periaqueductal gray in modulating anxiety-like responses
title_full_unstemmed Role of astrocytic mu-opioid receptors of the ventrolateral periaqueductal gray in modulating anxiety-like responses
title_short Role of astrocytic mu-opioid receptors of the ventrolateral periaqueductal gray in modulating anxiety-like responses
title_sort role of astrocytic mu opioid receptors of the ventrolateral periaqueductal gray in modulating anxiety like responses
topic Anxiety
Mu-opioid receptors
Periaqueductal gray
Astrocyte
Calcium signaling
url https://doi.org/10.1186/s12993-025-00291-0
work_keys_str_mv AT yinandu roleofastrocyticmuopioidreceptorsoftheventrolateralperiaqueductalgrayinmodulatinganxietylikeresponses
AT aozhuozhang roleofastrocyticmuopioidreceptorsoftheventrolateralperiaqueductalgrayinmodulatinganxietylikeresponses
AT zhiweili roleofastrocyticmuopioidreceptorsoftheventrolateralperiaqueductalgrayinmodulatinganxietylikeresponses
AT yukuizhao roleofastrocyticmuopioidreceptorsoftheventrolateralperiaqueductalgrayinmodulatinganxietylikeresponses
AT shuyiliu roleofastrocyticmuopioidreceptorsoftheventrolateralperiaqueductalgrayinmodulatinganxietylikeresponses
AT chunlingwei roleofastrocyticmuopioidreceptorsoftheventrolateralperiaqueductalgrayinmodulatinganxietylikeresponses
AT qiaohuazheng roleofastrocyticmuopioidreceptorsoftheventrolateralperiaqueductalgrayinmodulatinganxietylikeresponses
AT yanningqiao roleofastrocyticmuopioidreceptorsoftheventrolateralperiaqueductalgrayinmodulatinganxietylikeresponses
AT yihuiliu roleofastrocyticmuopioidreceptorsoftheventrolateralperiaqueductalgrayinmodulatinganxietylikeresponses
AT weiren roleofastrocyticmuopioidreceptorsoftheventrolateralperiaqueductalgrayinmodulatinganxietylikeresponses
AT jinghan roleofastrocyticmuopioidreceptorsoftheventrolateralperiaqueductalgrayinmodulatinganxietylikeresponses
AT zhiqiangliu roleofastrocyticmuopioidreceptorsoftheventrolateralperiaqueductalgrayinmodulatinganxietylikeresponses
AT feigao roleofastrocyticmuopioidreceptorsoftheventrolateralperiaqueductalgrayinmodulatinganxietylikeresponses