The DOI matches its Crossref record; 69 of the 71 references it cites were found in a registry or an index.
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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Microbial memories: Sex‐dependent impact of the gut microbiome on hippocampal plasticity
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The multifaceted role of CARD9 in inflammatory bowel disease
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“For example, psychological stress has been linked to both changes in intestinal barrier function and food allergies [48].”
BackgroundHuman intestinal microbiota: Role in development and functioning of the nervous system
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The Role of Amyloid-Beta and Tau in the Early Pathogenesis of Alzheimer’s Disease
Yin, X., Qiu, Y., Zhao, C., Zhou, Z., Bao, J., & Qian, W. (2021) · Medical Science Monitor · doi:10.12659/msm.933084 · Cited by 48
“Eubacterium rectale, Porphyromonas gingivalis, and Lactobacillus rhamnosus are important in the origination of AD [81-85].”
BackgroundHattori, N., & Yamashiro, Y. (2021) · Annals of Nutrition and Metabolism · doi:10.1159/000512226 · Cited by 54
The Link between Gut Dysbiosis Caused by a High-Fat Diet and Hearing Loss
Kociszewska, D., Chan, J., Thorne, P. R., & Vlajkovic, S. M. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222413177 · Cited by 51
Nelson, E. D., Ramberg, J. E., Best, T., & Sinnott, R. (2012) · Nutritional Neuroscience · doi:10.1179/1476830512y.0000000004 · Cited by 46
Probiotics protect against gut dysbiosis associated decline in learning and memory
Sarkar, S. R., Mazumder, P. M., & Banerjee, S. (2020) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2020.577390 · Cited by 49
Wang, H., He, S., Xin, J., Zhang, T., Sun, N., Li, L., Ni, X., Zeng, D., Ma, H., & Bai, Y. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.662148 · Cited by 47
Influence of the Microbiota-Gut-Brain Axis on Cognition in Alzheimer’s Disease
Escobar, Y.-N. H., O’Piela, D., Wold, L. E., & Mackos, A. R. (2022) · Journal of Alzheimer s Disease · doi:10.3233/jad-215290 · Cited by 52
“Furthermore, GF mice have been shown to lack a working and non-spatial memory as measured by a T-Maze and novel object recognition test [116].”
The Brain-Gut Axis: A Target for Treating Stress-Related Disorders
Scott, L. V., Clarke, G. A., & Dinan, T. G. (2013) · Modern trends in psychiatry · doi:10.1159/000343971 · Cited by 46
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“…non-neurotropic and neurotropic infectious agents, have been examined for their effects on the CNS (Jurgens et al., 2012; Evans et al., 2014; Monje et al., 2003; Ekdahl et al., 2003; Gareau et al., 2011; Hermes et al., 2008; Vyas et al., 2007; de Miranda et al., 2012; Jurgens and Johnson, 2012).”
BackgroundInfluentialRios, A. C., Maurya, P. K., Pedrini, M., Zeni‐Graiff, M., Asevedo, E. D. M., Mansur, R. B., Wieck, A., Grassi‐Oliveira, R., McIntyre, R. S., Hayashi, M. A. F., et al. (2017) · Reviews in the Neurosciences · doi:10.1515/revneuro-2017-0001 · Cited by 45
“Interestingly, pretreatment with probiotics was capable of preventing the cognitive deficit, partly by restoring the hippocampal brain-derived neurotrophic factor (BDNF) and c-Fos expression (Gareau et al., 2011).”
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“Germ-free mice have been shown to have impaired working memory compared to specific pathogen-free mice [10].”
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Into the wild: microbiome transplant studies need broader ecological reality
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“This revelation, ushered in by advances in sequencing and computing technology, is grounded in a growing understanding that microbiomes profoundly shape their host’s biology, influencing factors such as immunity [2], adiposity [3], thermogenesis [4], hormonal regulation [5], physiological development [6], memory [7] a…”
BackgroundIs adolescence the missing developmental link in Microbiome–Gut–Brain axis communication?
Flannery, J., Callaghan, B. L., Sharpton, T. J., Fisher, P. A., & Pfeifer, J. H. (2019) · Developmental Psychobiology · doi:10.1002/dev.21821 · Cited by 48
Glinert, A., Turjeman, S., Elliott, E., & Koren, O. (2021) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12812 · Cited by 48
“Gareau et al. (2011) introduced Citrobacter rodentium to GF and conventional mice and tested memory impairment in the presence or absence of an added stressor in the form of water avoidance stress (WAS).”
BackgroundLiu, Y., Du, T., Zhang, W., Lu, W., Peng, Z., Huang, S., Sun, X., Zhu, X., Chen, C., Qian, L., et al. (2019) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2019/8340192 · Cited by 44
“Several bacterium taxa have been reported to be correlated with AD, such as Citrobacter rodentium , Chlamydia pneumoniae , and Helicobacter [66 – 68].”
Curdlan Prevents the Cognitive Deficits Induced by a High-Fat Diet in Mice via the Gut-Brain Axis
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“work suggested that the gut microbiome influences the ability to form memory, especially for the GF mice [19].”
BackgroundThe Microbiota-Gut Axis in Premature Infants: Physio-Pathological Implications
Bresesti, I., Salvatore, S., Valetti, G., Baj, A., Giaroni, C., & Agosti, M. A. (2022) · Cells · doi:10.3390/cells11030379 · Cited by 51
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“index of HPA axis activity [41,89,100], the elevated corticosterone”
BackgroundProbiotics in human mental health and diseases—A minireview
Sivamaruthi, B. S., Prasanth, M. I., Kesika, P., & Chaiyasut, C. (2021) · Tropical Journal of Pharmaceutical Research · doi:10.4314/tjpr.v18i4.29 · Cited by 44
“rhamnosus) have been found to prevent memory dysfunction in Citrobacter rodentium infected mice (C57BL/6) by improving the expression of brain-derived neurotrophic factor (BDNF) [27].”
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Lactobacillus rhamnosus: An emerging probiotic with therapeutic potential for depression
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Yang, C., Fu, X., Hao, W., Xiang, X., Liu, T., Yang, B., & Zhang, X. (2020) · Addiction Biology · doi:10.1111/adb.12975 · Cited by 45
“The increased intestinal permeability and gut dysbiosis play important roles in the pathophysiology of stress, depression, and cognitive decline.(1,38,43,44) All of these symptoms are very common in MA users.”
BackgroundKar, F., Hacioglu, C., Kar, E., Donmez, D. B., & Kanbak, G. (2022) · Metabolic Brain Disease · doi:10.1007/s11011-022-00964-z · Cited by 42
Smith, L. K., & Wissel, E. F. (2019) · Perspectives on Psychological Science · doi:10.1177/1745691618809379 · Cited by 46
Probiotic alleviate fluoride-induced memory impairment by reconstructing gut microbiota in mice
Xin, J., Wang, H., Sun, N., Bughio, S., Zeng, D., Li, L., Wang, Y., Khalique, A., Zeng, Y., Pan, K., et al. (2021) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2021.112108 · Cited by 42
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Inflammation in Mental Disorders: Is the Microbiota the Missing Link?
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Experimental gastritis leads to anxiety- and depression-like behaviors in female but not male rats
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“Although this can be important, the short duration of the estrous cycle in rats coupled with the duration of the study and the fact that female rats housed in the same room can phase into the same estrous cycle stage [84] would most likely result in not having a differential predominance of animals in any one particul…”
BackgroundGut microbiota in common elderly diseases affecting activities of daily living
Shimizu, Y. (2018) · World Journal of Gastroenterology · doi:10.3748/wjg.v24.i42.4750 · Cited by 40
Agnihotri, N., & Mohajeri, M. H. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232415934 · Cited by 47
“Three reports [47,59,68] studied the effect of unpredictable chronic mild stress (a model of stress-induced depression) on the gut microbiota and neurogenesis or BDNF.”
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The Many Faces of Microbiota-Gut-Brain Axis in Autism Spectrum Disorder
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Association between the oral microbiome and brain resting state connectivity in smokers
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“Inversely, gastrointestinal microbial perturbations have been shown to impair recognition memory and cognitive function in hippocampus (Gareau et al., 2011).”
Background
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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