Published August 15, 2022 | Version Supplemental Material
Journal Article Open

Oral short-chain fatty acids administration regulates innate anxiety in adult microbiome-depleted mice

  • 1. ROR icon National Cheng Kung University
  • 2. ROR icon Chia-Yi Christian Hospital
  • 3. ROR icon National Taiwan University
  • 4. ROR icon Kaohsiung Medical University
  • 5. ROR icon National Cheng Kung University Hospital
  • 6. ROR icon California Institute of Technology

Abstract

Anxiety is characterized by feelings of tension and worry even in the absence of threatening stimulus. Pathological condition of anxiety elicits defensive behavior and aversive reaction ultimately impacting individuals and society. The gut microbiota has been shown to contribute to the modulation of anxiety-like behavior in rodents through the gut-brain axis. Several studies observed that germ-free (GF) and the broad spectrum of antibiotic cocktail (ABX)-treated rodents display lowered anxiety-like behavior. We speculate that gut microbial short-chain fatty acids (SCFA) modulate the innate anxiety response. Herein, we administered SCFA in the drinking water in adult mice treated with ABX to deplete the microbiota and tested their anxiety-like behavior. To further augment the innate fear response, we enhanced the aversive stimulus of the anxiety-like behavior tests. Strikingly, we found that the anxiety-like behavior in ABX mice was not altered when enhanced aversive stimulus, while control and ABX mice supplemented with SCFA displayed increased anxiety-like behavior. Vagus nerve serves as a promising signaling pathway in the gut-brain axis. We determined the role of vagus nerve by subdiaphragmatic vagotomy (SDV) in ABX mice supplemented with SCFA. We found that the restored anxiety-like behavior in ABX mice by SCFA was unaffected by SDV. These findings suggest that gut microbiota can regulate anxiety-like behavior through their fermentation products SCFA.

Additional Information

© 2022 Published by Elsevier. Received 8 December 2021, Revised 5 May 2022, Accepted 14 May 2022, Available online 22 May 2022. We thank Prof. Chen-Chih Hsu's laboratory in Department of Chemistry at National Taiwan University and BIOTOOLS Co., Ltd. for the feces and brain SCFA measurements; Dr. Yen-Jung Lee and Center for Research Resources and Development of Kaohsiung Medical University for the serum SCFA measurement; the staff in the Laboratory Animal Center, National Cheng Kung University (NCKU) for caring of animals. This work was supported by the scholarship from Prof. Kun-Yen Huang Education Fund of CHENG-HSING Medical Foundation in Taiwan to T.-T.L. and C.-W.L.; the scholarship Pilot Program of Ministry of Science and Technology (MOST) to Subsidize Universities and Colleges to Cultivate Outstanding Doctoral Students at NCKU (MOST 110-2926-I-006-001-MY4) to T.-T.L.; the funds from the MOST in Taiwan: Undergraduate Research MOST 108-2813-C-006-130-B to J.-Y.X.; MOST 110-2636-M-002-014- to C.-C.H.; MOST 107-2320-B-006-072-MY3; 109-2314-B-006-046; 110-2314-B-006-114; 110-2320-B-006-018-MY3 to W.-LW.; Ministry of Health and Welfare of Taiwan (MOHW110-TDU-B-211-124003) to J.-H.H.; Ditmanson Medical Foundation Chia-yi Christian Hospital in Taiwan (CYC109002) to W.-L.W; National Cheng Kung University Hospital (NCKUH-11102004) to J.-H.H. and W.-L.W.; and the Higher Education Sprout Project, Ministry of Education to the Headquarters of University Advancement at National Cheng Kung Universtiy, Taiwan. CRediT authorship contribution statement: Jo-Ting Wu: Methodology, Investigation, Validation, Formal analysis, Data curation, Visualization, Writing – original draft. Chia-Ling Sun: Resources, Supervision, Funding acquisition. Tzu-Ting Lai: Methodology, Investigation, Validation, Formal analysis. Chia-Wei Liou: Validation, Formal analysis. Yuan-Yuan Lin: Validation, Formal analysis. Jia-Ying Xue: Validation. Hong-Wen Wang: Formal analysis. Laura Min Xuan Chai: Investigation, Formal analysis. Yen-Jung Lee: Investigation, Formal analysis. Shiou-Lan Chen: Supervision. Alice Y.W. Chang: Supervision. Jia-Horung Hung: Supervision, Funding acquisition. Cheng-Chih Hsu: Supervision, Funding acquisition. Wei-Li Wu: Conceptualization, Methodology, Investigation, Formal analysis, Data curation, Visualization, Writing – original draft, Writing – review & editing, Supervision, Project administration, Funding acquisition. All authors declare no conflicts of interest related to this work.

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Additional details

Identifiers

Eprint ID
114883
DOI
10.1016/j.neuropharm.2022.109140
Resolver ID
CaltechAUTHORS:20220523-165177000

Funding

CHENG-HSING Medical Foundation
Ministry of Science and Technology (Taipei)
MOST 110-2926-I-006-001-MY4
Ministry of Science and Technology (Taipei)
MOST 108-2813-C-006-130-B
Ministry of Science and Technology (Taipei)
MOST 110-2636-M-002-014
Ministry of Science and Technology (Taipei)
MOST 107-2320-B-006-072-MY3
Ministry of Science and Technology (Taipei)
109-2314-B-006-046
Ministry of Science and Technology (Taipei)
110-2314-B-006-114
Ministry of Science and Technology (Taipei)
110-2320-B-006-018-MY3
Ministry of Health and Welfare (Taipei)
MOHW110-TDU-B-211-124003
Ditmanson Medical Foundation
CYC109002
National Cheng Kung University Hospital
NCKUH-11102004
Ministry of Education (Taipei)

Dates

Created
2022-05-23
Created from EPrint's datestamp field
Updated
2022-06-27
Created from EPrint's last_modified field