A central amygdala input to the dorsal vagal complex controls gastric motility in mice under restraint stress

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

doi:10.3389/fphys.2023.1074979

A central amygdala input to the dorsal vagal complex controls gastric motility in mice under restraint stress

Front Physiol. 2023 Feb 15:14:1074979. doi: 10.3389/fphys.2023.1074979. eCollection 2023.

Authors

Hao Wang^{1

2}, Wen-Jian Liu³, Xi-Yang Wang¹, Xiao-Qi Chen¹, Rong-Lin Cai⁴, Meng-Ting Zhang¹, Hai-Tao Wang¹, Guang-Wei He², Zhi Zhang⁵, Guo-Ming Shen¹

Affiliations

¹ College of Integrated Chinese and Western Medicine (School of Life Sciences), Anhui University of Chinese Medicine, Hefei, Anhui, China.
² Hefei Institute of Pharmaceutical Industry Co., Ltd., Hefei, Anhui, China.
³ Department of Thoracic Surgery, The First Affiliated Hospital of Anhui Medical University, Hefei, Anhui, China.
⁴ Research Institute of Acupuncture and Meridian, Anhui University of Chinese Medicine, Hefei, Anhui, China.
⁵ Hefei 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, China.

Abstract

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 CeA^GABA → dorsal vagal complex pathways were performed. Optogenetics inhibiting or activating CeA^GABA neurons or the CeA^GABA → 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 CeA^GABA neurons and the CeA^GABA → dorsal vagal complex pathway in gastric motility disorder mice, which enhanced gastric movement and gastric emptying, whereas activation of the CeA^GABA and CeA^GABA → dorsal vagal complex pathway mimicked the symptoms of weakened gastric movement and delayed gastric emptying in naïve mice. Conclusion: Our findings indicate that the CeA^GABA → dorsal vagal complex pathway may be involved in regulating gastric dysmotility under restraint stress conditions, and partially reveals the mechanism of electroacupuncture.

Keywords: central amygdala; dorsal vagal complex; electroacupuncture; gastric motility disorder; neural circuit.

Grants and funding

Support for this study was provided by the National Natural Science Foundation of China (Grant No. 81973936 to G-MS, 81704166 to HW, 81904095 to M-TZ), the Talent Support Project of Anhui University of TCM (Grant No. DT2100000552 to HW), the Excellent Youth Project of Anhui Universities (2022AH030065 to HW).