Brain regulation of gastric dysfunction induced by stress

doi:10.1038/s42255-023-00866-z

. 2023 Sep;5(9):1494-1505.

doi: 10.1038/s42255-023-00866-z. Epub 2023 Aug 17.

Brain regulation of gastric dysfunction induced by stress

Wan-Ying Dong^#¹, Xia Zhu^#¹, Hao-Di Tang^#^{1

2}, Ji-Ye Huang^#¹, Meng-Yu Zhu^{3

4}, Ping-Kai Cheng¹, Hao Wang⁵, Xi-Yang Wang⁵, Haitao Wang⁵, Yu Mao¹, Wan Zhao⁶, Yan Zhang⁷, Wen-Juan Tao^{8

9}, Zhi Zhang^{10

11}

Affiliations

¹ Department of Anesthesiology, The First Affiliated Hospital of University of Science and Technology of China, Hefei National Laboratory for Physical Sciences at the Microscale, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei, People's Republic of China.
² Laboratory of Anesthesia and Critical Care Medicine, National-Local Joint Engineering Research Center of Translational Medicine of Anesthesiology, West China Hospital, Sichuan University, Chengdu, People's Republic of China.
³ College & Hospital of Stomatology, Anhui Medical University, Key laboratory of Oral Diseases Research of Anhui Province, Hefei, People's Republic of China.
⁴ Department of Physiology, School of Basic Medical Sciences, Anhui Medical University, Hefei, People's Republic of China.
⁵ School of Integrated Chinese and Western Medicine, Anhui University of Chinese Medicine, Hefei, People's Republic of China.
⁶ Department of Otolaryngology-Head and Neck Surgery, The First Affiliated Hospital of the University of Science and Technique of China, Hefei, People's Republic of China.
⁷ Stroke Center and Department of Neurology, The First Affiliated Hospital of the University of Science and Technique of China, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei, People's Republic of China.
⁸ College & Hospital of Stomatology, Anhui Medical University, Key laboratory of Oral Diseases Research of Anhui Province, Hefei, People's Republic of China. wjtao01@ahmu.edu.cn.
⁹ Department of Physiology, School of Basic Medical Sciences, Anhui Medical University, Hefei, People's Republic of China. wjtao01@ahmu.edu.cn.
¹⁰ Department of Anesthesiology, The First Affiliated Hospital of University of Science and Technology of China, Hefei National Laboratory for Physical Sciences at the Microscale, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei, People's Republic of China. zhizhang@ustc.edu.cn.
¹¹ The Center for Advanced Interdisciplinary Science and Biomedicine, Institute of Health and Medicine, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei, People's Republic of China. zhizhang@ustc.edu.cn.

^# Contributed equally.

PMID: 37592008
DOI: 10.1038/s42255-023-00866-z

Brain regulation of gastric dysfunction induced by stress

Wan-Ying Dong et al. Nat Metab. 2023 Sep.

. 2023 Sep;5(9):1494-1505.

doi: 10.1038/s42255-023-00866-z. Epub 2023 Aug 17.

Authors

Affiliations

¹ Department of Anesthesiology, The First Affiliated Hospital of University of Science and Technology of China, Hefei National Laboratory for Physical Sciences at the Microscale, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei, People's Republic of China.
² Laboratory of Anesthesia and Critical Care Medicine, National-Local Joint Engineering Research Center of Translational Medicine of Anesthesiology, West China Hospital, Sichuan University, Chengdu, People's Republic of China.
³ College & Hospital of Stomatology, Anhui Medical University, Key laboratory of Oral Diseases Research of Anhui Province, Hefei, People's Republic of China.
⁴ Department of Physiology, School of Basic Medical Sciences, Anhui Medical University, Hefei, People's Republic of China.
⁵ School of Integrated Chinese and Western Medicine, Anhui University of Chinese Medicine, Hefei, People's Republic of China.
⁶ Department of Otolaryngology-Head and Neck Surgery, The First Affiliated Hospital of the University of Science and Technique of China, Hefei, People's Republic of China.
⁷ Stroke Center and Department of Neurology, The First Affiliated Hospital of the University of Science and Technique of China, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei, People's Republic of China.
⁸ College & Hospital of Stomatology, Anhui Medical University, Key laboratory of Oral Diseases Research of Anhui Province, Hefei, People's Republic of China. wjtao01@ahmu.edu.cn.
⁹ Department of Physiology, School of Basic Medical Sciences, Anhui Medical University, Hefei, People's Republic of China. wjtao01@ahmu.edu.cn.
¹⁰ Department of Anesthesiology, The First Affiliated Hospital of University of Science and Technology of China, Hefei National Laboratory for Physical Sciences at the Microscale, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei, People's Republic of China. zhizhang@ustc.edu.cn.
¹¹ The Center for Advanced Interdisciplinary Science and Biomedicine, Institute of Health and Medicine, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei, People's Republic of China. zhizhang@ustc.edu.cn.

^# Contributed equally.

PMID: 37592008
DOI: 10.1038/s42255-023-00866-z

Abstract

Psychological and physical stressors have been implicated in gastric disorders in humans. The mechanism coupling the brain to the stomach underlying stress-induced gastric dysfunction has remained elusive. Here, we show that the stomach directly receives acetylcholinergic inputs from the dorsal motor nucleus of the vagus (ACh^DMV), which are innervated by serotonergic neurons in the dorsal raphe nucleus (5-HT^DRN). Microendoscopic calcium imaging and multi-tetrode electrophysiological recordings reveal that the 5-HT^DRN → ACh^DMV → stomach circuit is inhibited with chronic stress accompanied by hypoactivate gastric function. Artificial activation of this circuit reverses the gastric dysfunction induced by chronic stress in both male and female mice. Our study demonstrates that this 5-HT^DRN → ACh^DMV → stomach axis drives gastric dysfunction associated with stress, thus providing insights into the circuit basis for brain regulation of the stomach.

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References

1. Wolff, H. G. Emotions and gastric function. Science 98, 481–484 (1943). - PubMed - DOI
1. Jiang, Y. & Travagli, R. A. Hypothalamic–vagal oxytocinergic neurocircuitry modulates gastric emptying and motility following stress. J. Physiol. 598, 4941–4955 (2020). - PubMed - DOI
1. Skrobisz, K. et al. Imaging of morphological background in selected functional and inflammatory gastrointestinal diseases in fMRI. Front. Psychiatry 11, 461 (2020). - PubMed - PMC - DOI
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1. Huang, J. S., Terrones, L., Simmons, A. N., Kaye, W. & Strigo, I. Pilot study of functional magnetic resonance imaging responses to somatic pain stimuli in youth with functional and inflammatory gastrointestinal disease. J. Pediatr. Gastroenterol. Nutr. 63, 500–507 (2016). - PubMed - PMC - DOI

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[1] Wolff, H. G. Emotions and gastric function. Science 98, 481–484 (1943). - PubMed - DOI

[2] Wolff, H. G. Emotions and gastric function. Science 98, 481–484 (1943). - PubMed - DOI

[3] Jiang, Y. & Travagli, R. A. Hypothalamic–vagal oxytocinergic neurocircuitry modulates gastric emptying and motility following stress. J. Physiol. 598, 4941–4955 (2020). - PubMed - DOI

[4] Jiang, Y. & Travagli, R. A. Hypothalamic–vagal oxytocinergic neurocircuitry modulates gastric emptying and motility following stress. J. Physiol. 598, 4941–4955 (2020). - PubMed - DOI

[5] Skrobisz, K. et al. Imaging of morphological background in selected functional and inflammatory gastrointestinal diseases in fMRI. Front. Psychiatry 11, 461 (2020). - PubMed - PMC - DOI

[6] Skrobisz, K. et al. Imaging of morphological background in selected functional and inflammatory gastrointestinal diseases in fMRI. Front. Psychiatry 11, 461 (2020). - PubMed - PMC - DOI

[7] Mak, A. D. P. et al. Unaltered brain GABA concentrations and resting fMRI activity in functional dyspepsia with and without comorbid depression. Front. Psychiatry 11, 549749 (2020). - PubMed - PMC - DOI

[8] Mak, A. D. P. et al. Unaltered brain GABA concentrations and resting fMRI activity in functional dyspepsia with and without comorbid depression. Front. Psychiatry 11, 549749 (2020). - PubMed - PMC - DOI

[9] Huang, J. S., Terrones, L., Simmons, A. N., Kaye, W. & Strigo, I. Pilot study of functional magnetic resonance imaging responses to somatic pain stimuli in youth with functional and inflammatory gastrointestinal disease. J. Pediatr. Gastroenterol. Nutr. 63, 500–507 (2016). - PubMed - PMC - DOI

[10] Huang, J. S., Terrones, L., Simmons, A. N., Kaye, W. & Strigo, I. Pilot study of functional magnetic resonance imaging responses to somatic pain stimuli in youth with functional and inflammatory gastrointestinal disease. J. Pediatr. Gastroenterol. Nutr. 63, 500–507 (2016). - PubMed - PMC - DOI

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Brain regulation of gastric dysfunction induced by stress

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