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Bacterial infection causes stress-induced memory dysfunction in mice
Open accessAbstract
BACKGROUND: The brain-gut axis is a key regulator of normal intestinal physiology; for example, psychological stress is linked to altered gut barrier function, development of food allergies and changes in behaviour. Whether intestinal events, such as enteric bacterial infections and bacterial colonisation, exert a reciprocal effect on stress-associated behaviour is not well established. OBJECTIVE: To determine the effects of either acute enteric infection or absence of gut microbiota on behaviour, including anxiety and non-spatial memory formation. METHODS: Behaviour was assessed following infection with the non-invasive enteric pathogen, Citrobacter rodentium in both C57BL/6 mice and germ-free Swiss-Webster mice, in the presence or absence of acute water avoidance stress. Whether daily treatment with probiotics normalised behaviour was assessed, and potential mechanisms of action evaluated. RESULTS: No behavioural abnormalities were observed, either at the height of infection (10 days) or following bacterial clearance (30 days), in C rodentium-infected C57BL/6 mice. When infected mice were exposed to acute stress, however, memory dysfunction was apparent after infection (10 days and 30 days). Memory dysfunction was prevented by daily treatment of infected mice with probiotics. Memory was impaired in germ-free mice, with or without exposure to stress, in contrast to conventionally reared, control Swiss-Webster mice with an intact intestinal microbiota. CONCLUSIONS: The intestinal microbiota influences the ability to form memory. Memory dysfunction occurs in infected mice exposed to acute stress, while in the germ-free setting memory is altered at baseline.
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“Firstly, studies in germ-free (GF) animals showed that the brain is affected in the absence of microbiota (see Table 2) (Clarke et al., 2013;Diaz Heijtz et al., 2011;Gareau et al., 2011;Hegstrand and Hine, 1986;Neufeld et al., 2011;Sudo et al., 2004).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Gareau et al., 2011
In the citing paper
“In addition, these animals exhibit altered BDNF expression in the hippocampus (Bercik et al., 2011a;Diaz Heijtz et al., 2011;Gareau et al., 2011), which as stated earlier has an important role in synaptic plasticity and cognition (Baj et al., 2013;Lu et al., 2014;Neufeld et al., 2011), suggesting a crucial involvement of microbes in regulating hippocampal-dependent memory function.”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Gareau et al., 2011
In the citing paper
“In addition, these animals exhibit altered BDNF expression in the hippocampus (Bercik et al., 2011a;Diaz Heijtz et al., 2011;Gareau et al., 2011), which as stated earlier has an important role in synaptic plasticity and cognition (Baj et al., 2013;Lu et al., 2014;Neufeld et al., 2011), suggesting a crucial involvement of microbes in regulating hippocampal-dependent memory function.”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Gareau et al., 2011
In the citing paper
“It has been shown that GF mice exhibit an impaired ability to remember a familiar object when presented with a novel object (Gareau et al., 2011;Luk et al., 2018), as well as impaired working memory in remembering a familiar environment in the spontaneous alternation task (Gareau et al., 2011).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Gareau et al., 2011
In the citing paper
“It has been shown that GF mice exhibit an impaired ability to remember a familiar object when presented with a novel object (Gareau et al., 2011;Luk et al., 2018), as well as impaired working memory in remembering a familiar environment in the spontaneous alternation task (Gareau et al., 2011).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Gareau et al., 2011
In the citing paper
“Indeed, different Lactobacillus strains were capable of restoring deficits in object recognition memory induced by chronic restraint stress (Liang et al., 2015a), as well as preventing these deficits in GF mice (Gareau et al., 2011), in a mouse model of colitis (Emge et al., 2016), and in immunodeficient mice (Smith et al., 2014).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Gareau et al., 2011
In the citing paper
“BDNF expression as measured by immunohistochemistry was decreased in the CA1 hippocampal brain area in GF stressed mice compared to stressed controls (Gareau et al., 2011).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Gareau et al., 2011
In the citing paper
“An increasing body of preclinical and human evidence demonstrates that the MGB axis plays important roles in the development and maintenance of various components of cognition (191, 362, 375).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [362]
In the citing paper
“The introduction of pathogenic bacteria reduced cognitive abilities and heightened anxiety-like behaviors (362, 363).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [362]
In the citing paper
“This deficit was prevented by daily administration of a Lactobacillus sp. probiotic combination before infection.”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [362]
In the citing paper
“Gareau et al. demonstrated impaired short-term recognition and working memory in 5 to 6-week-old germ-free mice when compared to conventionally reared counterparts (362).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [362]
In the citing paper
“Studies in germ-free mice have shown that, in the absence of microbes, the brain is markedly affected, exhibiting deficits in learning, memory formation and recognition, and social and emotional behaviors (58, 123, 124, 362).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [362]
In the citing paper
“Germ-free mice present with social cognitive deficits, which may be associated with biochemical changes, such as decreased hippocampal BDNF and c-FOS expression, important in memory (124, 362, 376, 377).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [362]
In the citing paper
“Administration of C. rodentium, combined with acute stress, led to memory dysfunction in young adult germ-free mice (362).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [362]
In the citing paper
“For example, Gareau et al. demonstrated a lack of memory in germ-free mice in the T-maze test and novel object test in situations with or without stress (362).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [362]
In the citing paper
“These studies show that rodents lacking all gut bacteria from birth (germ-free animals) have memory deficits28 and behavioral abnormalities29, 30 when compared to animals with normal gut microbiota.”
From The relation between cesarean birth and child cognitive development (2017) · cites this paper as [28]
In the citing paper
“Interestingly, these cognitive deficits in rodents can be corrected through the colonization of the intestine via a fecal transplant from the control group, but only if it occurs early in life.”
From The relation between cesarean birth and child cognitive development (2017) · cites this paper as [28]
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MethodSite and Strain-Specific Variation in Gut Microbiota Profiles and Metabolism in Experimental Mice
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“conditioned fear test.(51) Furthermore, the hippocampus is highly responsive to glucocorticoids.”
BackgroundHippocampal c-fos is necessary for long-term memory of a socially transmitted food preference
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“in the CA1 region of the hippocampus. c-Fos expression is necessary for the consolidation of non-spatial hippocampus-dependent memory, as demonstrated in rats using a socially transmitted food preference model.”
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“Probiotics also have extra-intestinal effects, such as prevention of myocardial infarctinduced apoptosis in the limbic region of the brain.(39) To determine the mechanism of action of microbe-induced memory deficits, the hippocampus was studied.”
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“Previous studies in rats with colitis indicate that altered memory is observed in association with inflammation-induced visceral pain.”
BackgroundSelective affective biasing in recognition memory in the irritable bowel syndrome.
Gomborone, J., Dewsnap, P., Libby, G., & Farthing, M. J. G. (1993) · Gut · doi:10.1136/gut.34.9.1230 · Cited by 67 · cited 1×
“Furthermore, patients with IBS have a bias in recognition memory, similar to subjects with depression.(60) Administration of probiotics ameliorates colonic disease resulting from C rodentium infection(24) 26 and in models of psychological stress.”
BackgroundUpdates on treatment of irritable bowel syndrome
Hammerle, C. W., & Surawicz, C. M. (2008) · World Journal of Gastroenterology · doi:10.3748/wjg.14.2639 · Cited by 65 · cited 1×
“The brain–gut axis is important for maintaining normal gut function, with alterations in the axis implicated in both IBS and chronic inflammatory bowel diseases.”
BackgroundProbiotics Prevent Death Caused byCitrobacter rodentiumInfection in Neonatal Mice
Gareau, M. G., Wine, E., Reardon, C., & Sherman, P. M. (2009) · The Journal of Infectious Diseases · doi:10.1086/648614 · Cited by 59 · cited 2×
“Trends towards changes were also seen in the C rodentiuminfected, placebo-treated group, suggesting a potential prebiotic effect, as has been described previously.(26) Probiotics also have extra-intestinal effects, such as prevention of myocardial infarctinduced apoptosis in the limbic region of the brain.”
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Metadata
- Authors
- Gareau, M. G., Wine, E., Rodrigues, D. M., Cho, J. H., Whary, M. T., Philpott, D. J., MacQueen, G., & Sherman, P. M.
- Affiliations
- Hospital for Sick Children (CA)
- University of Alberta (CA)
- University of Toronto (CA)
- Massachusetts Institute of Technology (US)
- University of Calgary (CA)
- Corresponding author
- Sherman, Philip M
- ORCID
- Venue
- Gut
- Publisher
- BMJ
- Published
- 2010-10-21
- Volume
- 60
- Issue
- 3
- Pages
- 307-317
- ISSN
- 0017-5749 (ISSN-L)
- 1468-3288
- OpenAlex
- W2170856053
- Cited by
- 909
- References
- 71
- Citations by year
- 2026: 19 · 2025: 53 · 2024: 72 · 2023: 60 · 2022: 94 · 2021: 91 · 2020: 113 · 2019: 79 · 2018: 73 · 2017: 62 · 2016: 60 · 2015: 36 · 2014: 41 · 2013: 22 · 2012: 17
- FWCI
- 7.17
- Type
- journal article
- Language
- en
- Open access
- green
- hdl.handle.net
- Licence
- cc-by-nc
- Locations
- Gut (publishedVersion)
- PubMed (publishedVersion)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc)
- HighWire Press Open Archive (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Keywords
- enteric bacterial infection, Citrobacter rodentium, gut microbiota, germ-free mice, non-spatial memory, anxiety, water avoidance stress, probiotics, gut-brain axis, acute stress
- MeSH terms
- Animals, Anxiety, Behavior, Animal, Colon, Corticosterone, Enterobacteriaceae Infections, Feces, Female, Germ-Free Life, Hippocampus, Hyperplasia, Memory Disorders, Mice, Inbred C57BL, Stress, Psychological, Cytokines, Proto-Oncogene Proteins c-fos, Inflammation Mediators, Brain-Derived Neurotrophic Factor, Probiotics, Citrobacter rodentium, Mice
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