Original Article

Commensal microbiota modulate murine behaviors in a strictly contamination-free environment confirmed by culture-based methods

  1. R. Nishino1,2,*,
  2. K. Mikami1,2,
  3. H. Takahashi1,
  4. S. Tomonaga3,4,
  5. M. Furuse3,
  6. T. Hiramoto5,
  7. Y. Aiba1,
  8. Y. Koga1,
  9. N. Sudo5

Article first published online: 11 MAR 2013

DOI: 10.1111/nmo.12110

Issue

Neurogastroenterology & Motility

Neurogastroenterology & Motility

Volume 25, Issue 6, pages 521–528, June 2013

Additional Information

How to Cite

Nishino, R., Mikami, K., Takahashi, H., Tomonaga, S., Furuse, M., Hiramoto, T., Aiba, Y., Koga, Y. and Sudo, N. (2013), Commensal microbiota modulate murine behaviors in a strictly contamination-free environment confirmed by culture-based methods. Neurogastroenterology & Motility, 25: 521–528. doi: 10.1111/nmo.12110

Author Information

  1. 1

    Laboratory for Infectious Diseases, Isehara, Kanagawa, Japan

  2. 2

    Department of Psychiatry, Tokai University School of Medicine, Isehara, Kanagawa, Japan

  3. 3

    Laboratory of Regulation in Metabolism and Behavior, Graduate School of Bioresource and Bioenvironmental Sciences, Kyushu University, Fukuoka, Japan

  4. 4

    Laboratory of Nutritional Science for Animals, Division of Applied Biosciences, Graduate School of Agriculture, Kyoto University, Kyoto, Japan

  5. 5

    Department of Psychosomatic Medicine, Graduate School of Medical Science, Kyushu University, Fukuoka, Japan

* Address for Correspondence
Ryo Nishino, Laboratory for Infectious Diseases and Department of Psychiatry, Tokai University School of Medicine, 143 Shimokasuya, Isehara, 259-1193 Kanagawa, Japan.
Tel: 81 463 93 1121 (ext 5451); fax: 81 463 94 5532;
e-mail: nishinoryo@tokai-u.jp

Publication History

  1. Issue published online: 14 MAY 2013
  2. Article first published online: 11 MAR 2013
  3. Manuscript Accepted: 5 FEB 2013
  4. Manuscript Received: 25 JUN 2012

Funded by

  • Research Fund of Tokai University School of Medicine
  • General Scientific Research from the Ministry of Education, Culture, Sports, Science, and Technology in Japan. Grant Numbers: 19390192, 22659144, 24659350
  • Yakult Bioscience Research Foundation

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Keywords:

  • behavior;
  • germfree;
  • microbiota;
  • stress

Abstract

Background

There is increasing evidence suggesting the existence of an interaction between commensal microbiota, the gut and the brain. The aim of this study was to examine the influence of commensal microbiota on the host behaviors in a contamination-free environment, which was verified by culture-based methods.

Methods

Open-field and marble-burying tests were used to analyze anxiety-like behaviors and locomotor activity in gnotobiotic BALB/c mice with a common genetic background in a sterile isolator. The monoamine levels in several regions of the brain were measured in germfree (GF) mice and commensal fecal microbiota-associated mice (EX-GF).

Key Results

A 24-h exposure to the environment outside the sterile isolators rendered GF mice less anxious than those not contaminated, while there was no change in the locomotion. EX-GF mice, the gnotobiotic mice with normal specific pathogen-free microbiota, were less anxious and active than GF mice using open-field and marble-burying tests. The norepinephrine, dopamine, and serotonin turnover rates were higher in the EX-GF mice than in the GF mice in most regions of the brain, suggesting that monoaminergic neurotransmission might increase in the EX-GF mice comparing the GF mice. Monoassociation with Brautia coccoides reduced the anxiety level, but it did not affect the locomotor activity. In contrast, colonization with Bifidobacterium infantis decreased the locomotor activity, while having little effect on the anxiety level.

Conclusions & Inferences

These results strongly support the current view that gut microorganisms modulate brain development and behavior.

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