Control of brain development, function, and behavior by the microbiome

Sampson, Timothy R.; Mazmanian, Sarkis K.

doi:10.1016/j.chom.2015.04.011

Cited by 1,093Gut microbiota and healthTryptophan and brain disordersGastrointestinal motility and disorders

Control of brain development, function, and behavior by the microbiome

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Sampson, Timothy R., Mazmanian, Sarkis K.·2015·Cell Host & Microbe

DOI 10.1016/j.chom.2015.04.011PMC PMC4442490

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Abstract

Animals share an intimate and life-long partnership with a myriad of resident microbial species, collectively referred to as the microbiota. Symbiotic microbes have been shown to regulate nutrition and metabolism and are critical for the development and function of the immune system. More recently, studies have suggested that gut bacteria can impact neurological outcomes--altering behavior and potentially affecting the onset and/or severity of nervous system disorders. In this review, we highlight emerging evidence that the microbiome extends its influence to the brain via various pathways connecting the gut to the central nervous system. While understanding and appreciation of a gut microbial impact on neurological function is nascent, unraveling gut-microbiome-brain connections holds the promise of transforming the neurosciences and revealing potentially novel etiologies for psychiatric and neurodegenerative disorders.

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In animal experimentation and some small human studies, dysbiosis has been shown to impact brain and behavioral parameters including cortisol regulation, depressive and anxious symptomatology, and social functioning.
“In animal experimentation and some small human studies, dysbiosis has also been shown to impact relevant brain and behavioral parameters, including cortisol regulation, depressive and anxious symptomatology, and social functioning [77, 79].”
From Biological embedding of childhood adversity: from physiological mechanisms to clinical implications (2017) · cites this paper as [79]
The section “Role of the Microbiota in Mood and Individual Behaviors” reports animal findings on stress hormones and depression-like behavior, plus small human probiotic studies reporting reduced anxiety, sadness, and urinary cortisol. “The Link between Gut Bacteria and Disorders Involving Social Impairment” reports improved communication-related behavior in a mouse model, but describes the proposed microbial role in autism as still requiring validation. The claim overstates these findings by treating dysbiosis as a demonstrated cause across the listed outcomes, particularly social functioning in humans. (LLM, conf=0.86)
Experimental — accuracy not yet measured
The GM influences the stress system, behavior, and cognition in animals.
“Studies in animals have demonstrated the effect that the GM has on neural development and neurochemistry in the host, influencing the stress system, behavior, and cognition (42–47).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [45]
Animal studies suggest that the GM plays a crucial role in regulating early brain development.
“Animal studies suggest that the GM plays a crucial role in regulating early brain development (19, 45, 60, 114–117).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [45]

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Interactions between the microbiota, immune and nervous systems in health and disease
Fung, T. C., Olson, C. A., & Hsiao, E. Y. (2017) · Nature Neuroscience · doi:10.1038/nn.4476 · Cited by 1,900 · see citing works
Stress & the gut-brain axis: Regulation by the microbiome
Foster, J. A., Rinaman, L., & Cryan, J. F. (2017) · Neurobiology of Stress · doi:10.1016/j.ynstr.2017.03.001 · Cited by 1,150 · see citing works
New evidences on the altered gut microbiota in autism spectrum disorders
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Gut microbiota from multiple sclerosis patients enables spontaneous autoimmune encephalomyelitis in mice
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The neuropharmacology of butyrate: the bread and butter of the microbiota-gut-brain axis
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Gut instincts: microbiota as a key regulator of brain development, ageing and neurodegeneration
Dinan, T. G., & Cryan, J. F. (2017) · The Journal of Physiology · doi:10.1113/jp273106 · Cited by 813 · see citing works
The gut-brain axis
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Impact of Omega-3 Fatty Acids on the Gut Microbiota
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Altered bile acid profile associates with cognitive impairment in Alzheimer's disease—An emerging role for gut microbiome
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Kynurenine pathway metabolism and the microbiota-gut-brain axis
Kennedy, P. J., Cryan, J. F., Dinan, T. G., & Clarke, G. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2016.07.002 · Cited by 724 · see citing works
Cognitive impairment by antibiotic-induced gut dysbiosis: analysis of gut microbiota-brain communication
Fröhlich, E. E., Farzi, A., Mayerhofer, R., Reichmann, F., Jačan, A., Wagner, B., Zinser, E., Bordag, N., Magnes, C., Fröhlich, E., et al. (2016) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2016.02.020 · Cited by 720 · see citing works
Biological embedding of childhood adversity: from physiological mechanisms to clinical implications
Berens, A. E., Jensen, S. K. G., & Nelson, C. A. (2017) · BMC Medicine · doi:10.1186/s12916-017-0895-4 · Cited by 657 · see citing works
“In animal experimentation and some small human studies, dysbiosis has also been shown to impact relevant brain and behavioral parameters, including cortisol regulation, depressive and anxious symptomatology, and social functioning [77, 79].”
Background
Growing up in a bubble: using germ-free animals to assess the influence of the gut microbiota on brain and behavior
Luczynski, P., McVey Neufeld, K.-A., Oriach, C. S., Clarke, G., Dinan, T. G., & Cryan, J. F. (2016) · International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyw020 · Cited by 632 · see citing works
The bowel and beyond: The enteric nervous system in neurological disorders
Rao, M., & Gershon, M. D. (2016) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2016.107 · Cited by 629 · see citing works
The Gut–Brain Axis and the Microbiome: Mechanisms and Clinical Implications
Osadchiy, V., Martin, C. R., & Mayer, E. A. (2019) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2018.10.002 · Cited by 555 · see citing works
The gut microbiome in human neurological disease: A review
Tremlett, H., Bauer, K. C., Appel‐Cresswell, S., Finlay, B. B., & Waubant, E. (2017) · Annals of Neurology · doi:10.1002/ana.24901 · Cited by 535 · see citing works
Infant gut microbiome associated with cognitive development
Carlson, A. L., Xia, K., Azcarate-Peril, M. A., Goldman, B. D., Ahn, M., Styner, M. A., Thompson, A. L., Geng, X., Gilmore, J. H., & Knickmeyer, R. C. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.06.021 · Cited by 541 · see citing works
Gut microbiota and dysbiosis in Alzheimer's disease: Implications for pathogenesis and treatment
Liu, S., Gao, J., Zhu, M., Liu, K., & Zhang, H.-L. (2020) · Molecular Neurobiology · doi:10.1007/s12035-020-02073-3 · Cited by 516 · see citing works
The microbiome: a key regulator of stress and neuroinflammation
Rea, K., Dinan, T. G., & Cryan, J. F. (2016) · Neurobiology of Stress · doi:10.1016/j.ynstr.2016.03.001 · Cited by 508 · see citing works
Dysbiosis of gut microbiota and microbial metabolites in Parkinson's disease
Sun, M.-F., & Shen, Y.-Q. (2018) · Ageing Research Reviews · doi:10.1016/j.arr.2018.04.004 · Cited by 445 · see citing works
The role of the microbiome for human health: From basic science to clinical applications
Mohajeri, M. H., Brummer, R. J. M., Rastall, R. A., Weersma, R. K., Harmsen, H. J. M., Faas, M., & Eggersdorfer, M. (2018) · European Journal of Nutrition · doi:10.1007/s00394-018-1703-4 · Cited by 440 · see citing works
Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis
Rusch, J. A., Layden, B. T., & Dugas, L. R. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1130689 · Cited by 415 · see citing works
Relationship between the gut microbiome and brain function
Mohajeri, M. H., La Fata, G., Steinert, R. E., & Weber, P. (2018) · Nutrition Reviews · doi:10.1093/nutrit/nuy009 · Cited by 376 · see citing works
Alzheimer’s disease and gut microbiota
Hu, X., Wang, T., & Jin, F. (2016) · Science China Life Sciences · doi:10.1007/s11427-016-5083-9 · Cited by 371 · see citing works
Small metabolites, possible big changes: A microbiota-centered view of non-alcoholic fatty liver disease
Chu, H., Duan, Y., Yang, L., & Schnabl, B. (2019) · Gut · doi:10.1136/gutjnl-2018-316307 · Cited by 354 · see citing works
Why does the microbiome affect behaviour?
Johnson, K. V.-A., & Foster, K. R. (2018) · Nature Reviews Microbiology · doi:10.1038/s41579-018-0014-3 · Cited by 333 · see citing works
Probiotics and the microbiota-gut-brain axis: Focus on psychiatry
Mörkl, S., Butler, M. I., Holl, A., Cryan, J. F., & Dinan, T. G. (2020) · Current Nutrition Reports · doi:10.1007/s13668-020-00313-5 · Cited by 337 · see citing works
Transplantation of microbiota from drug-free patients with schizophrenia causes schizophrenia-like abnormal behaviors and dysregulated kynurenine metabolism in mice
Zhu, F., Guo, R., Wang, W., Ju, Y., Wang, Q., Ma, Q., Sun, Q., Fan, Y., Xie, Y., Yang, Z., et al. (2020) · Molecular Psychiatry · doi:10.1038/s41380-019-0475-4 · Cited by 323 · see citing works
Association Between Gut Microbiota and Autism Spectrum Disorder: A Systematic Review and Meta-Analysis
Xu, M., Xu, X., Li, J., & Li, F. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.00473 · Cited by 309 · see citing works
Probiotic Supplementation in Patients with Alzheimer’s Dementia - An Explorative Intervention Study
Leblhuber, F., Steiner, K., Schuetz, B., Fuchs, D., & Gostner, J. M. (2018) · Current Alzheimer Research · doi:10.2174/1389200219666180813144834 · Cited by 269 · see citing works
Omega-3 polyunsaturated fatty acids critically regulate behaviour and gut microbiota development in adolescence and adulthood
Robertson, R. C., Seira Oriach, C., Murphy, K., Moloney, G. M., Cryan, J. F., Dinan, T. G., Paul Ross, R., & Stanton, C. (2017) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2016.07.145 · Cited by 268 · see citing works
Gut feelings: a randomised, triple-blind, placebo-controlled trial of probiotics for depressive symptoms
Chahwan, B., Kwan, S., Isik, A., van Hemert, S., Burke, C., & Roberts, L. (2019) · Journal of Affective Disorders · doi:10.1016/j.jad.2019.04.097 · Cited by 256 · see citing works
Mannan oligosaccharide attenuates cognitive and behavioral disorders in the 5xFAD Alzheimer's disease mouse model via regulating the gut microbiota-brain axis
Liu, Q., Xi, Y., Wang, Q., Liu, J., Li, P., Meng, X., Liu, K., Chen, W., Liu, X., & Liu, Z. (2021) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2021.04.005 · Cited by 241 · see citing works
Microbiome, inflammation, epigenetic alterations, and mental diseases
Alam, R., Abdolmaleky, H. M., & Zhou, J. (2017) · American Journal of Medical Genetics Part B Neuropsychiatric Genetics · doi:10.1002/ajmg.b.32567 · Cited by 240 · see citing works
The function of gut microbiota in immune-related neurological disorders: a review
Sittipo, P., Choi, J., Lee, S., & Lee, Y. K. (2022) · Journal of Neuroinflammation · doi:10.1186/s12974-022-02510-1 · Cited by 221 · see citing works
Current perspectives on gut microbiome dysbiosis and depression
Capuco, A., Urits, I., Hasoon, J., Chun, R., Gerald, B., Wang, J. K., Kassem, H., Ngo, A. L., Abd-Elsayed, A., Simopoulos, T., et al. (2020) · Advances in Therapy · doi:10.1007/s12325-020-01272-7 · Cited by 216 · see citing works
Autism, Gastrointestinal Symptoms and Modulation of Gut Microbiota by Nutritional Interventions
Ristori, M. V., Quagliariello, A., Reddel, S., Ianiro, G., Vicari, S., Gasbarrini, A., & Putignani, L. (2019) · Nutrients · doi:10.3390/nu11112812 · Cited by 214 · see citing works
Early-life adversity and brain development: Is the microbiome a missing piece of the puzzle?
O’Mahony, S. M., Clarke, G., Dinan, T. G., & Cryan, J. F. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2015.09.068 · Cited by 203 · see citing works
Probiotic treatment reduces depressive-like behaviour in rats independently of diet
Abildgaard, A., Elfving, B., Hokland, M., Wegener, G., & Lund, S. (2017) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2017.02.014 · Cited by 196 · see citing works
Epigenetic Regulation at the Interplay Between Gut Microbiota and Host Metabolism
Miro-Blanch, J., & Yanes, O. (2019) · Frontiers in Genetics · doi:10.3389/fgene.2019.00638 · Cited by 195 · see citing works
Gut microbial dysbiosis in indian children with autism spectrum disorders
Pulikkan, J., Maji, A., Dhakan, D. B., Saxena, R., Mohan, B., Anto, M. M., Agarwal, N., Grace, T., & Sharma, V. K. (2018) · Microbial Ecology · doi:10.1007/s00248-018-1176-2 · Cited by 189 · see citing works
The maternal vaginal microbiome partially mediates the effects of prenatal stress on offspring gut and hypothalamus
Jašarević, E., Howard, C. D., Morrison, K., Misic, A., Weinkopff, T., Scott, P., Hunter, C., Beiting, D., & Bale, T. L. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0182-5 · Cited by 189 · see citing works
Gut Microbiota: A Novel Therapeutic Target for Parkinson’s Disease
Zhu, M., Liu, X., Ye, Y., Yan, X., Cheng, Y., Zhao, L., Chen, F., & Ling, Z. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.937555 · Cited by 177 · see citing works
Bacterial Adrenergic Sensors Regulate Virulence of Enteric Pathogens in the Gut
Moreira, C. G., Russell, R., Mishra, A. A., Narayanan, S., Ritchie, J. M., Waldor, M. K., Curtis, M. M., Winter, S. E., Weinshenker, D., & Sperandio, V. (2016) · mBio · doi:10.1128/mbio.00826-16 · Cited by 157 · see citing works
“Neurological diseases, such as autism, depression, and neurodegenerative diseases, are often strongly inﬂuenced by intestinal factors (80).”
Administration of Non-Absorbable Antibiotics to Pregnant Mice to Perturb the Maternal Gut Microbiota Is Associated with Alterations in Offspring Behavior
Tochitani, S., Ikeno, T., Ito, T., Sakurai, A., Yamauchi, T., & Matsuzaki, H. (2016) · PLOS ONE · doi:10.1371/journal.pone.0138293 · Cited by 157 · see citing works
Gut microbiota composition is associated with temperament traits in infants
Aatsinki, A.-K., Lahti, L., Uusitupa, H.-M., Munukka, E., Keskitalo, A., Nolvi, S., O'Mahony, S., Pietilä, S., Elo, L. L., Eerola, E., et al. (2019) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2019.05.035 · Cited by 148 · see citing works
Probiotic consumption during puberty mitigates LPS-induced immune responses and protects against stress-induced depression- and anxiety-like behaviors in adulthood in a sex-specific manner
Murray, E., Sharma, R., Smith, K. B., Mar, K. D., Barve, R., Lukasik, M., Pirwani, A. F., Malette-Guyon, E., Lamba, S., Thomas, B. J., et al. (2019) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2019.06.016 · Cited by 150 · see citing works
Microbiome and nutrition in autism spectrum disorder: Current knowledge and research needs
Berding, K., & Donovan, S. M. (2016) · Nutrition Reviews · doi:10.1093/nutrit/nuw048 · Cited by 146 · see citing works
Relevance of gutmicrobiota in cognition, behaviour and Alzheimer’s disease
de J.R. De-Paula, V., Forlenza, A. S., & Forlenza, O. V. (2018) · Pharmacological Research · doi:10.1016/j.phrs.2018.07.007 · Cited by 145 · see citing works
Bile acids: a communication channel in the gut-brain axis
Monteiro-Cardoso, V. F., Corlianò, M., & Singaraja, R. R. (2021) · NeuroMolecular Medicine · doi:10.1007/s12017-020-08625-z · Cited by 145 · see citing works
Diet in Parkinson’s Disease: Critical Role for the Microbiome
Jackson, A., Forsyth, C. B., Shaikh, M., Voigt, R. M., Engen, P. A., Ramirez, V., & Keshavarzian, A. (2019) · Frontiers in Neurology · doi:10.3389/fneur.2019.01245 · Cited by 145 · see citing works
The gut microbiome: a key player in the complexity of amyotrophic lateral sclerosis (ALS)
Boddy, S. L., Giovannelli, I., Sassani, M., Cooper-Knock, J., Snyder, M. P., Segal, E., Elinav, E., Barker, L. A., Shaw, P. J., & McDermott, C. J. (2021) · BMC Medicine · doi:10.1186/s12916-020-01885-3 · Cited by 127 · see citing works
Enteric nervous system: the bridge between the gut microbiota and neurological disorders
Geng, Z.-H., Zhu, Y., Li, Q.-L., Zhao, C., & Zhou, P.-H. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.810483 · Cited by 144 · see citing works
Novel compound FLZ alleviates rotenone-induced PD mouse model by suppressing TLR4/MyD88/NF-κB pathway through microbiota–gut–brain axis
Zhao, Z., Li, F., Ning, J., Peng, R., Shang, J., Liu, H., Shang, M., Bao, X.-Q., & Zhang, D. (2021) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2021.03.020 · Cited by 137 · see citing works
The role of the microbiome in the neurobiology of social behaviour
Sarkar, A., Harty, S., Johnson, K. V. ‐., Moeller, A. H., Carmody, R. N., Lehto, S. M., Erdman, S. E., Dunbar, R. I. M., & Burnet, P. W. J. (2020) · Biological Reviews · doi:10.1111/brv.12603 · Cited by 135 · see citing works
Serum cortisol mediates the relationship between fecal Ruminococcus and brain N-acetylaspartate in the young pig
Mudd, A. T., Berding, K., Wang, M., Donovan, S. M., & Dilger, R. N. (2017) · Gut Microbes · doi:10.1080/19490976.2017.1353849 · Cited by 134 · see citing works
Fluoxetine ameliorates dysbiosis in a depression model induced by chronic unpredicted mild stress in mice
Sun, L., Zhang, H., Cao, Y., Wang, C., Zhao, C., Wang, H., Cui, G., Wang, M., Pan, Y., Shi, Y., et al. (2019) · International Journal of Medical Sciences · doi:10.7150/ijms.37322 · Cited by 127 · see citing works
Stress matters: randomized controlled trial on the effect of probiotics on neurocognition
Papalini, S., Michels, F., Kohn, N., Wegman, J., van Hemert, S., Roelofs, K., Arias-Vasquez, A., & Aarts, E. (2019) · Neurobiology of Stress · doi:10.1016/j.ynstr.2018.100141 · Cited by 123 · see citing works
Bile acids as key modulators of the brain-Gut-Microbiota axis in alzheimer’s disease
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Authors: Sampson, T. R., & Mazmanian, S. K.
Affiliations: California Institute of Technology (US)
Corresponding author: Mazmanian, Sarkis K.
ORCID: Sampson, Timothy R.
Mazmanian, Sarkis K.
Venue: Cell Host & Microbe
Publisher: Elsevier BV
Published: 2015-05
Volume: 17
Issue: 5
Pages: 565-576
ISSN: 1931-3128 (ISSN-L)
DOI: 10.1016/j.chom.2015.04.011
PMC: PMC4442490
OpenAlex: W2123097904
Cited by: 1,093
References: 107
Citations by year: 2026: 48 · 2025: 94 · 2024: 117 · 2023: 95 · 2022: 130 · 2021: 138 · 2020: 121 · 2019: 120 · 2018: 87 · 2017: 67 · 2016: 63 · 2015: 11
FWCI: 7.37
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 378 d)
Locations: Cell Host & Microbe (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
CaltechAUTHORS (California Institute of Technology) (submittedVersion)
Funders: National Institute of Mental Health (R01MH100556, MH100556)
National Institute of Diabetes and Digestive and Kidney Diseases (DK 078938, R01DK078938, R56DK078938)
National Institute of Neurological Disorders and Stroke (NS085910, R01NS085910)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
Keywords: gut microbiota, gut-brain axis, microbiota, brain development, neurobehavior, neurological disorders, neurodegenerative diseases, mental illness, central nervous system, immune system development, host-microbe symbiosis
MeSH terms: Gastrointestinal Microbiome, Animals, Behavior, Brain, Humans, Gastrointestinal Tract

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