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Cited by 334Vagus Nerve Stimulation ResearchTryptophan and brain disordersGastrointestinal motility and disorders

Induction of anxiety-like behavior in mice during the initial stages of infection with the agent of murine colonic hyperplasia citrobacter rodentium

LYTE, M, LI, W, OPITZ, N, GAYKEMA, R, GOEHLER, L·2006·Physiology & Behavior
DOI 10.1016/j.physbeh.2006.06.019
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Abstract

Symptoms of anxiety frequently occur concomitant to the development and persistence of inflammatory bowel disease (IBD) in patients. In the present study, we utilized an animal model of IBD, infection with Citrobacter rodentium, to determine whether the infection per se can drive anxiety-like behavior. Nine-week-old CF-1 male mice were challenged orally with either saline or C. rodentium. Early in the infective process (7-8 h later), mice were tested on a hole-board open field apparatus for anxiety-like behavior measurement. Immediately following behavioral testing, plasma samples were obtained for immune cytokine analysis and colons were excised for histological analysis. In additional animals, vagal ganglia were removed and processed for c-Fos protein detection. Challenge with C. rodentium significantly increased anxiety-like behavior as evidenced by avoidance of the center area and increased risk assessment behavior. Plasma levels of the cytokines IFN-gamma, TNF-alpha and IL-12 were not different. However vagal sensory ganglia from C. rodentium-treated animals evinced significantly more c-Fos protein-positive neurons, consistent with vagal afferent transmission of C. rodentium-related signals from gut to brain. Histological examination of the colon indicated a lack of overt inflammation at the 8 h post-challenge time point, indicating that the differences in behavior were unlikely to follow from inflammation-related stress. The results of the present study demonstrate that infection with C. rodentium can induce anxiety-like symptoms that are likely mediated via vagal sensory neurons.

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  • Microbes residing in the gut can activate stress circuits in the CNS through the vagus nerve and sensory neurons of the ENS.

    “There is also evidence for signaling between the GM and CNS, since microbes residing in the gut can activate stress circuits in the CNS through the vagus nerve and sensory neurons of the ENS (21, 49–54).”

    From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [49]

  • Evidence of activation of the afferent vagal system was reported, which suggests a possible vagus-mediated microbe to brain signaling pathway.

    “Evidence of activation of the afferent vagal system was reported, which suggests a possible vagus-mediated microbe to brain signaling pathway.”

    From Principles and clinical implications of the brain-gut-enteric microbiota axis (2009) · cites this paper as [73]

  • A possible role for gut infection in triggering brain responses, such as anxious behavior and mood changes, in the absence of overt gut inflammation or elevation of plasma cytokines has been described in mice.

    “A possible role for gut infection in triggering brain responses, such as anxious behavior and mood changes, in the absence of overt gut inflammation or elevation of plasma cytokines has been described in mice.73”

    From Principles and clinical implications of the brain-gut-enteric microbiota axis (2009) · cites this paper as [73]

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Authors
LYTE, M., LI, W., OPITZ, N., GAYKEMA, R., & GOEHLER, L.
Affiliations
  • Texas Tech University (US)
  • University of Minnesota (US)
  • University of Virginia (US)
Corresponding author
LYTE, M
ORCID
Venue
Physiology & Behavior
Publisher
Elsevier BV
Published
2006-10-30
Volume
89
Issue
3
Pages
350-357
ISSN
0031-9384 (ISSN-L)
DOI
10.1016/j.physbeh.2006.06.019
OpenAlex
W1968646392
Cited by
334
References
60
Citations by year
2026: 7 · 2025: 13 · 2024: 16 · 2023: 17 · 2022: 27 · 2021: 30 · 2020: 25 · 2019: 27 · 2018: 24 · 2017: 26 · 2016: 27 · 2015: 23 · 2014: 16 · 2013: 12 · 2012: 14
FWCI
2.63
Type
journal article
Language
en
Open access
closed
Licence
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations
  • Physiology & Behavior (publishedVersion)
  • PubMed (publishedVersion)
Funders
National Institute of Mental Health (MH-50431, R01MH050431)
Topics
  • Life Sciences › Neuroscience › Neurology › Vagus Nerve Stimulation Research
  • Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
  • Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
Keywords
anxiety-like behavior, Citrobacter rodentium, inflammatory bowel disease, gut-brain axis, vagal afferent neurons, c-fos, vagal ganglia, immune cytokines, early infection, colonic hyperplasia, risk assessment behavior
MeSH terms
Administration, Oral, Animals, Anxiety Disorders, Behavior, Animal, Colitis, Colon, Enterobacteriaceae Infections, Exploratory Behavior, Male, Proto-Oncogene Proteins c-fos, Citrobacter rodentium, Mice

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