A central amygdala input to the dorsal vagal complex controls gastric motility in mice under restraint stress
Background/aims: Psychological and physiological stress can cause gastrointestinal motility disorders. Acupuncture has a benign regulatory effect on gastrointestinal motility. However, the mechanisms underlying these processes remain unclear.Methods: Herein, we established a gastric motility disorde...
| Main Authors: | , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2023-02-01
|
| Series: | Frontiers in Physiology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fphys.2023.1074979/full |
| _version_ | 1797924470788194304 |
|---|---|
| author | Hao Wang Hao Wang Wen-Jian Liu Xi-Yang Wang Xiao-Qi Chen Rong-Lin Cai Meng-Ting Zhang Hai-Tao Wang Guang-Wei He Zhi Zhang Guo-Ming Shen |
| author_facet | Hao Wang Hao Wang Wen-Jian Liu Xi-Yang Wang Xiao-Qi Chen Rong-Lin Cai Meng-Ting Zhang Hai-Tao Wang Guang-Wei He Zhi Zhang Guo-Ming Shen |
| author_sort | Hao Wang |
| collection | DOAJ |
| description | Background/aims: Psychological and physiological stress can cause gastrointestinal motility disorders. Acupuncture has a benign regulatory effect on gastrointestinal motility. However, the mechanisms underlying these processes remain unclear.Methods: Herein, we established a gastric motility disorder (GMD) model in the context of restraint stress (RS) and irregular feeding. The activity of emotional center—central amygdala (CeA) GABAergic neurons and gastrointestinal center—dorsal vagal complex (DVC) neurons were recorded by electrophysiology. Virus tracing and patch clamp analysis of the anatomical and functional connection between the CeAGABA → dorsal vagal complex pathways were performed. Optogenetics inhibiting or activating CeAGABA neurons or the CeAGABA → dorsal vagal complex pathway were used to detect changes in gastric function.Results: We found that restraint stress induced delayed gastric emptying and decreased gastric motility and food intake. Simultaneously, restraint stress activated CeA GABAergic neurons, inhibiting dorsal vagal complex neurons, with electroacupuncture (EA) reversing this phenomenon. In addition, we identified an inhibitory pathway in which CeA GABAergic neurons project into the dorsal vagal complex. Furthermore, the use of optogenetic approaches inhibited CeAGABA neurons and the CeAGABA → dorsal vagal complex pathway in gastric motility disorder mice, which enhanced gastric movement and gastric emptying, whereas activation of the CeAGABA and CeAGABA → dorsal vagal complex pathway mimicked the symptoms of weakened gastric movement and delayed gastric emptying in naïve mice.Conclusion: Our findings indicate that the CeAGABA → dorsal vagal complex pathway may be involved in regulating gastric dysmotility under restraint stress conditions, and partially reveals the mechanism of electroacupuncture. |
| first_indexed | 2024-04-10T15:02:53Z |
| format | Article |
| id | doaj.art-384d7b583fb54e14a924b8f4ead965a4 |
| institution | Directory Open Access Journal |
| issn | 1664-042X |
| language | English |
| last_indexed | 2024-04-10T15:02:53Z |
| publishDate | 2023-02-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Physiology |
| spelling | doaj.art-384d7b583fb54e14a924b8f4ead965a42023-02-15T09:40:52ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2023-02-011410.3389/fphys.2023.10749791074979A central amygdala input to the dorsal vagal complex controls gastric motility in mice under restraint stressHao Wang0Hao Wang1Wen-Jian Liu2Xi-Yang Wang3Xiao-Qi Chen4Rong-Lin Cai5Meng-Ting Zhang6Hai-Tao Wang7Guang-Wei He8Zhi Zhang9Guo-Ming Shen10College of Integrated Chinese and Western Medicine (School of Life Sciences), Anhui University of Chinese Medicine, Hefei, Anhui, ChinaHefei Institute of Pharmaceutical Industry Co., Ltd., Hefei, Anhui, ChinaDepartment of Thoracic Surgery, The First Affiliated Hospital of Anhui Medical University, Hefei, Anhui, ChinaCollege of Integrated Chinese and Western Medicine (School of Life Sciences), Anhui University of Chinese Medicine, Hefei, Anhui, ChinaCollege of Integrated Chinese and Western Medicine (School of Life Sciences), Anhui University of Chinese Medicine, Hefei, Anhui, ChinaResearch Institute of Acupuncture and Meridian, Anhui University of Chinese Medicine, Hefei, Anhui, ChinaCollege of Integrated Chinese and Western Medicine (School of Life Sciences), Anhui University of Chinese Medicine, Hefei, Anhui, ChinaCollege of Integrated Chinese and Western Medicine (School of Life Sciences), Anhui University of Chinese Medicine, Hefei, Anhui, ChinaHefei Institute of Pharmaceutical Industry Co., Ltd., Hefei, Anhui, ChinaHefei National Laboratory for Physical Sciences at the Microscale, Division of Life Sciences and Medicine, Department of Biophysics and Neurobiology, University of Science and Technology of China, Hefei, Anhui, ChinaCollege of Integrated Chinese and Western Medicine (School of Life Sciences), Anhui University of Chinese Medicine, Hefei, Anhui, ChinaBackground/aims: Psychological and physiological stress can cause gastrointestinal motility disorders. Acupuncture has a benign regulatory effect on gastrointestinal motility. However, the mechanisms underlying these processes remain unclear.Methods: Herein, we established a gastric motility disorder (GMD) model in the context of restraint stress (RS) and irregular feeding. The activity of emotional center—central amygdala (CeA) GABAergic neurons and gastrointestinal center—dorsal vagal complex (DVC) neurons were recorded by electrophysiology. Virus tracing and patch clamp analysis of the anatomical and functional connection between the CeAGABA → dorsal vagal complex pathways were performed. Optogenetics inhibiting or activating CeAGABA neurons or the CeAGABA → dorsal vagal complex pathway were used to detect changes in gastric function.Results: We found that restraint stress induced delayed gastric emptying and decreased gastric motility and food intake. Simultaneously, restraint stress activated CeA GABAergic neurons, inhibiting dorsal vagal complex neurons, with electroacupuncture (EA) reversing this phenomenon. In addition, we identified an inhibitory pathway in which CeA GABAergic neurons project into the dorsal vagal complex. Furthermore, the use of optogenetic approaches inhibited CeAGABA neurons and the CeAGABA → dorsal vagal complex pathway in gastric motility disorder mice, which enhanced gastric movement and gastric emptying, whereas activation of the CeAGABA and CeAGABA → dorsal vagal complex pathway mimicked the symptoms of weakened gastric movement and delayed gastric emptying in naïve mice.Conclusion: Our findings indicate that the CeAGABA → dorsal vagal complex pathway may be involved in regulating gastric dysmotility under restraint stress conditions, and partially reveals the mechanism of electroacupuncture.https://www.frontiersin.org/articles/10.3389/fphys.2023.1074979/fullcentral amygdaladorsal vagal complexneural circuitgastric motility disorderelectroacupuncture |
| spellingShingle | Hao Wang Hao Wang Wen-Jian Liu Xi-Yang Wang Xiao-Qi Chen Rong-Lin Cai Meng-Ting Zhang Hai-Tao Wang Guang-Wei He Zhi Zhang Guo-Ming Shen A central amygdala input to the dorsal vagal complex controls gastric motility in mice under restraint stress Frontiers in Physiology central amygdala dorsal vagal complex neural circuit gastric motility disorder electroacupuncture |
| title | A central amygdala input to the dorsal vagal complex controls gastric motility in mice under restraint stress |
| title_full | A central amygdala input to the dorsal vagal complex controls gastric motility in mice under restraint stress |
| title_fullStr | A central amygdala input to the dorsal vagal complex controls gastric motility in mice under restraint stress |
| title_full_unstemmed | A central amygdala input to the dorsal vagal complex controls gastric motility in mice under restraint stress |
| title_short | A central amygdala input to the dorsal vagal complex controls gastric motility in mice under restraint stress |
| title_sort | central amygdala input to the dorsal vagal complex controls gastric motility in mice under restraint stress |
| topic | central amygdala dorsal vagal complex neural circuit gastric motility disorder electroacupuncture |
| url | https://www.frontiersin.org/articles/10.3389/fphys.2023.1074979/full |
| work_keys_str_mv | AT haowang acentralamygdalainputtothedorsalvagalcomplexcontrolsgastricmotilityinmiceunderrestraintstress AT haowang acentralamygdalainputtothedorsalvagalcomplexcontrolsgastricmotilityinmiceunderrestraintstress AT wenjianliu acentralamygdalainputtothedorsalvagalcomplexcontrolsgastricmotilityinmiceunderrestraintstress AT xiyangwang acentralamygdalainputtothedorsalvagalcomplexcontrolsgastricmotilityinmiceunderrestraintstress AT xiaoqichen acentralamygdalainputtothedorsalvagalcomplexcontrolsgastricmotilityinmiceunderrestraintstress AT ronglincai acentralamygdalainputtothedorsalvagalcomplexcontrolsgastricmotilityinmiceunderrestraintstress AT mengtingzhang acentralamygdalainputtothedorsalvagalcomplexcontrolsgastricmotilityinmiceunderrestraintstress AT haitaowang acentralamygdalainputtothedorsalvagalcomplexcontrolsgastricmotilityinmiceunderrestraintstress AT guangweihe acentralamygdalainputtothedorsalvagalcomplexcontrolsgastricmotilityinmiceunderrestraintstress AT zhizhang acentralamygdalainputtothedorsalvagalcomplexcontrolsgastricmotilityinmiceunderrestraintstress AT guomingshen acentralamygdalainputtothedorsalvagalcomplexcontrolsgastricmotilityinmiceunderrestraintstress AT haowang centralamygdalainputtothedorsalvagalcomplexcontrolsgastricmotilityinmiceunderrestraintstress AT haowang centralamygdalainputtothedorsalvagalcomplexcontrolsgastricmotilityinmiceunderrestraintstress AT wenjianliu centralamygdalainputtothedorsalvagalcomplexcontrolsgastricmotilityinmiceunderrestraintstress AT xiyangwang centralamygdalainputtothedorsalvagalcomplexcontrolsgastricmotilityinmiceunderrestraintstress AT xiaoqichen centralamygdalainputtothedorsalvagalcomplexcontrolsgastricmotilityinmiceunderrestraintstress AT ronglincai centralamygdalainputtothedorsalvagalcomplexcontrolsgastricmotilityinmiceunderrestraintstress AT mengtingzhang centralamygdalainputtothedorsalvagalcomplexcontrolsgastricmotilityinmiceunderrestraintstress AT haitaowang centralamygdalainputtothedorsalvagalcomplexcontrolsgastricmotilityinmiceunderrestraintstress AT guangweihe centralamygdalainputtothedorsalvagalcomplexcontrolsgastricmotilityinmiceunderrestraintstress AT zhizhang centralamygdalainputtothedorsalvagalcomplexcontrolsgastricmotilityinmiceunderrestraintstress AT guomingshen centralamygdalainputtothedorsalvagalcomplexcontrolsgastricmotilityinmiceunderrestraintstress |