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The interplay between the intestinal microbiota and the brain
Abstract
The intestinal microbiota consists of a vast bacterial community that resides primarily in the lower gut and lives in a symbiotic relationship with the host. A bidirectional neurohumoral communication system, known as the gut-brain axis, integrates the host gut and brain activities. Here, we describe the recent advances in our understanding of how the intestinal microbiota communicates with the brain via this axis to influence brain development and behaviour. We also review how this extended communication system might influence a broad spectrum of diseases, including irritable bowel syndrome, psychiatric disorders and demyelinating conditions such as multiple sclerosis.
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“the bacterial family Porphyromonadaceae has been linked to declines in cognition and affective disorders”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Collins et al., 2012
In the citing paper
“Accumulating evidence from experimental studies supports the hypothesis that; via affecting inflammation, endocrine system, and neurotransmission; the gut microbiome takes a crucial role in the CNS function (Collins et al., 2012; Dinan and Cryan, 2013).”
From Effect of Probiotic Supplementation on Cognitive Function and Metabolic Status in Alzheimer's Disease: A Randomized, Double-Blind and Controlled Trial (2016) · cites this paper as Collins et al., 2012
In the citing paper
“recent studies suggest that changes in the gut microbiota may be responsible for underlying mechanisms associated with IBS such as visceral hypersensitivity, altered barrier function, gastrointestinal motility and the gut-brain axis90–93.”
From Update on Fecal Microbiota Transplantation 2015: Indications, Methodologies, Mechanisms, and Outlook (2015) · cites this paper as [91]
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“However, during exercise, serotonin levels might also be increased through other known pathways: (i) kynurenine pathway [21], and (ii) gut microbiota synthesis [85, 86].”
From Exercise-induced stress behavior, gut-microbiota-brain axis and diet: a systematic review for athletes (2016) · cites this paper as [85]
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“High-fat diets could be detrimental to immune function compared to high carbohydrate diets [85].”
From Exercise-induced stress behavior, gut-microbiota-brain axis and diet: a systematic review for athletes (2016) · cites this paper as [85]
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“Mounting evidence suggests that the gastrointestinal microbiota influences host behaviour via bi-directional communication through what has been coined the microbiota-gut-brain axis [17, 18, 20, 29, 50, 60, 71].”
From Distinct actions of the fermented beverage kefir on host behaviour, immunity and microbiome gut-brain modules in the mouse (2020) · cites this paper as [17]
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“Recent discoveries in germ-free animal models have highlighted the role of gut microbiome in influencing behaviors, brain neurochemistry, and physiology (Cryan and Dinan, 2012).”
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“A bidirectional neurohumoral communication system, known as the gut-brain axis, integrates 61 the host gut and brain activities (Collins et al., 2012; Cryan et al., 2019).”
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The impact of gut microbiota on the occurrence, treatment, and prognosis of ischemic stroke
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“explained that the intestinal microbiota and its products can affect the brain function through blood circulation and other ways [64] and may as well stimulate intestinal endocrine cells to secrete 5-HT, BDNF, NE, and other substances to affect the brain function, thereby reducing stress and mood, and alleviating depr…”
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Philip, V., Newton, D. F., Oh, H., Collins, S. M., Berčík, P., & Sibille, E. L. (2021) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2021.01.021 · Cited by 14
“Microbiota show a profound influence on numerous host processes, including immune system development, brain function, and behaviour (Bercik et al., 2011; Collins et al., 2012; McVey Neufeld et al., 2019; Sharon et al., 2019; Valles-Colomer et al., 2019).”
BackgroundSelf-citationDiCarlo, G. E., Mabry, S. J., Cao, X., McMillan, C., Woynaroski, T. G., Harrison, F. E., Reddy, I. A., Matthies, H. J. G., Flynn, C. R., Wallace, M. T., et al. (2021) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2021.655451 · Cited by 15
“As communication between the brain and the gut is bidirectional, it is conceivable that dysfunction of key regulators of CNS function associated with ASD may also drive dysfunction of the ENS and thus changes in the composition of the oral and GI microbiota (51, 52).”
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The Microbiome–Gut–Brain Axis and Dementia: A Bibliometric Analysis
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BackgroundNeural Mechanisms of Exercise: Effects on Gut Miccrobiota and Depression
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Sulfated dietary fiber protects gut microbiota from antibiotics
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“19 Previous research has often considered neurological diseases and gastrointestinal issues as separate entities.”
BackgroundBreivik, T. J., Gjermo, P. E., Gundersen, Y., Opstad, P. K., Murison, R. C. C., Hugoson, A., von Hörsten, S., & Fristad, I. (2024) · Periodontology 2000 · doi:10.1111/prd.12610 · Cited by 15
“A 9–12 This includes immune responses that control the composition of micro-organisms in the microbiota and the microbial tissue load (Figures 1 and 2).”
The gut microbiome and the brain
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“In turn, the brain controls gut function and the intraluminal milieu via the autonomic and enteric nervous system modulating motility, secretion, and permeability [43,44,47].”
Can Gut Microbiota and Lifestyle Help Us in the Handling of Anorexia Nervosa Patients?
Mendez-Figueroa, V., Fernández, J. M. B., del Pozo, R. B. M., Fernández, A. B., Bailén, M., Bressa, C., Larrosa, M., & González-Soltero, R. (2019) · Microorganisms · doi:10.3390/microorganisms7020058 · Cited by 14
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“On the other hand, the CNS can affect the composition of the microbiota by governing processes like gut movement, secretion, permeability, and inflammation in the gastrointestinal tract through its autonomic interactions with ENS, intestinal muscle layers, and mucosa [71].”
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“…due to the recognition of the importance of the microbiota in regulating health, the GBA has been expanded to include the microbiota–gut–brain axis [118], which represents a complex network of communication between the gut microbiota and the brain in the regulation of immune, gastrointestinal, and…”
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Lai, M., Chang, Y., Lee, C., & Neonatal Microbiome Outcomes Study Group (NEMO) (2024) · The Kaohsiung Journal of Medical Sciences · doi:10.1002/kjm2.12878 · Cited by 12
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López‐Tello, J., Kiu, R., Schofield, Z., Zhang, C. X. W., van Sinderen, D., Gall, G. L., Hall, L. J., & Sferruzzi-Perri, A. N. (2024) · Molecular Metabolism · doi:10.1016/j.molmet.2024.102004 · Cited by 14
“Previous studies have established that the gut microbiome can in fl u-ence brain function and behaviour [56,57], including a recent murine model study revealing that the maternal gut microbiota can modulate fetal axonogenesis via microbially regulated metabolites [18].”
Thakur, P., Baraskar, K., Shrivastava, V. K., & Medhi, B. (2024) · Brain Research · doi:10.1016/j.brainres.2024.149176 · Cited by 12
Understanding neurotropic enteric viruses: routes of infection and mechanisms of attenuation
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“…overview of the different cells and the interactions between the different layers, we refer to more comprehensive reviews focused on this topic [29–31] Box 1 The gut-microbiome-brain axis Colonization of the intestine, amongst other sites, by microbes starts at birth and plays a critical role in…”
MethodThe impact of gut microbiome and diet on post-acute sequelae of SARS-CoV-2 infection
Reyes, Z., Stovall, M. C., Punyamurthula, S., Longo, M. T., Maraganore, D. M., & Solch-Ottaiano, R. J. (2024) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2024.123295 · Cited by 13
López-Santamarina, A., Cardelle‐Cobas, A., Mondragón, A. D. C., Sáez, A. C., & Miranda, J. M. (2025) · Food Chemistry · doi:10.1016/j.foodchem.2025.143437 · Cited by 12
Ex Vivo Analysis of Tryptophan Metabolism Using 19F NMR
Tombari, R. J., Saunders, C. M., Wu, C., Dunlap, L. E., Tantillo, D. J., & Olson, D. E. (2019) · ACS Chemical Biology · doi:10.1021/acschembio.9b00548 · Cited by 12
Angiotensin (1–7) Expressing Probiotic as a Potential Treatment for Dementia
Hernandez, A. R., Banerjee, A., Carter, C. S., & Buford, T. W. (2021) · Frontiers in Aging · doi:10.3389/fragi.2021.629164 · Cited by 12
“Notably, the majority of the body’s constitutive immune function is dedicated to maintaining homeostasis with the microbiota—evidenced by the fact that 70% of the body’s lymphocytes reside in the gut-associated lymphoid tissue (Collins et al., 2012).”
Fecal Microbiota Composition as a Metagenomic Biomarker of Dietary Intake
Melo, N. C. D. O., Cuevas‐Sierra, A., Cruz, E. F., Víctor de la, O., & Martínez, J. A. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24054918 · Cited by 13
“In fact, Bacteroides, Escherichia, Shigella, and Streptococcus are associated with higher levels of stress [57].”
BackgroundFood Science – Yesterday, Today and Tomorrow
Smithers, G. W. (2015) · Elsevier eBooks · doi:10.1016/b978-0-08-100596-5.03337-0 · Cited by 12
Intestinal microbiota, metabolome and gender dimorphism in autism spectrum disorders
Kushak, R. I., & Winter, H. S. (2018) · Research in Autism · doi:10.1016/j.rasd.2018.01.009 · Cited by 15
Tracking a dysregulated gut-brain axis with biomarkers of the microbiome
Severance, E. G., & Yolken, R. H. (2019) · Biomarkers in Neuropsychiatry · doi:10.1016/j.bionps.2019.100009 · Cited by 12
Elective Deliveries and the Risk of AutismPreprint
Liu, K., Teitler, J. O., Rajananda, S., Chegwin, V., Bearman, P., Hegyi, T., & Reichman, N. E. (2021) · SSRN Electronic Journal · doi:10.1016/j.amepre.2022.01.024 · Cited by 14
Hagerty, S. L., Ellingson, J. M., Helmuth, T. B., Bidwell, L. C., Hutchison, K. E., & Bryan, A. D. (2019) · Perspectives on Psychological Science · doi:10.1177/1745691619827010 · Cited by 12
Chataigner, M., Lucas, C., Miceli, M. D., Pallet, V., Layé, S., Mehaignerie, A., Bouvret, E., Dinel, A., & Joffre, C. (2021) · Frontiers in Nutrition · doi:10.3389/fnut.2021.750292 · Cited by 13
“These changes impact the gut-brain axis thereby impairing neural, endocrine, and immunological signals between the gut and the brain via the enteric nervous system and could play a role in diseases of the CNS (98, 99).”
BackgroundXiang, X., Gomez, A. A. V., Blomberg, S. P., Yuan, H., Degnan, B. M., & Degnan, B. M. (2023) · Frontiers in Neural Circuits · doi:10.3389/fncir.2023.1250694 · Cited by 11
“Conversely, the host can also shape the composition of the gut microbiota via these same signalling molecules (Collins et al., 2012; Galland, 2014; Miri et al., 2023).”
BackgroundImpact of Larval Food Source on the Stability of the Bactrocera dorsalis Microbiome
Kempraj, V., Auth, J., Cha, D. H., & Mason, C. J. (2024) · Microbial Ecology · doi:10.1007/s00248-024-02352-9 · Cited by 11
“They share common niches with insects and often engage in intricate ecological interactions that influence an insect’s overall fitness [1] by affecting their growth, fecundity, lifespan, and mate selection [2–4].”
Applied physiology: gut microbiota and antimicrobial therapy
Suslov, A. V., Panas, A., Sinelnikov, M. Y., Maslennikov, R. V., Trishina, A. S., Zharikova, T. S., Zharova, N. V., Kalinin, D. V., Pontes‐Silva, A., & Zharikov, Y. O. (2024) · European Journal of Applied Physiology · doi:10.1007/s00421-024-05496-1 · Cited by 11
“Many studies have shown that the interaction of gut bacteria with the brain is realised through the gut–brain axis, through the activation of neural pathways and the influence of neurohumoral factors (Collins et al. 2012; Clarke et al. 2014; Sorboni et al. 2022).”
Ultra-Processed Foods Consumption and Asthma in the Western Diet
Frontela‐Saseta, C., Finlayson, G., Sánchez‐Moya, T., Lorenzetti, S., & López‐Nicolás, R. (2024) · Dietetics · doi:10.3390/dietetics3020012 · Cited by 11
“…(a Western diet) have effects on the intestinal microbiota and the immune response, explaining the increase in the prevalence of non-communicable diseases such as cardiovascular diseases [106], type 2 diabetes [107], obesity [108], cancer [109], asthma [110], and neurological disorders [111].”
BackgroundNirmalkar, K., Patel, J., Kang, D., Bellinghiere, A., Bowes, D. A., Qureshi, F. A., Adams, J. B., & Krajmalnik‐Brown, R. (2024) · Gut Microbes Reports · doi:10.1080/29933935.2024.2358324 · Cited by 12
Early depletion of gut microbiota shape oligodendrocyte response after traumatic brain injury
Shumilov, K., Ni, A., García‐Bonilla, M., Celorrio, M., & Friess, S. H. (2024) · Journal of Neuroinflammation · doi:10.1186/s12974-024-03158-9 · Cited by 12
“This complex interplay is known as the gut-brain axis, a bidirectional communication that includes neuro-endo-crine-immunological activity [15].”
BackgroundTomassini, A., Vitalone, A., Marini, F., Praticò, G., Sciubba, F., Bevilacqua, M., Delfini, M., Sotto, A. D., Giacomo, S. D., Mariani, P., et al. (2014) · Journal of Proteome Research · doi:10.1021/pr500748r · Cited by 11
Agostoni, C. V., Mazzocchi, A., Leone, L., Ciappolino, V., Delvecchio, G., Altamura, C. A., & Brambilla, P. (2017) · Journal of Affective Disorders · doi:10.1016/j.jad.2017.01.001 · Cited by 11
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Lima‐Ojeda, J. M., Rupprecht, R., & Baghai, T. C. (2020) · Der Nervenarzt · doi:10.1007/s00115-020-01029-1 · Cited by 11
Intriguing Role of Gut-Brain Axis on Cognition with an Emphasis on Interaction with Papez Circuit
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Exploring the association between microbiota and behaviour in suckling piglets
Choudhury, R., Middelkoop, A., Bolhuis, J. E., & Kleerebezem, M. (2022) · Scientific Reports · doi:10.1038/s41598-022-16259-3 · Cited by 14
“1 were considered significant and the associated microbial groups (genus level), having (1) a minimum response scores ≥ 0.”
BackgroundMethodIf microbial ecosystem therapy can change your life, what's the problem?
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An overview of addiction to sugar
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Effect of gut microbiome on minor complications after a colonoscopy
Kim, J. H., Choi, Y. J., Kwon, H. J., Jung, K., Kim, S. E., Moon, W., Park, M. I., & Park, S. J. (2020) · Intestinal Research · doi:10.5217/ir.2020.00057 · Cited by 11
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Metadata
- Authors
- Collins, S. M., Surette, M., & Bercik, P.
- Affiliations
- McMaster University (CA)
- Corresponding author
- Collins, Stephen M.
- Venue
- Nature Reviews Microbiology
- Published
- 2012-09-24
- Volume
- 10
- Issue
- 11
- Pages
- 735-742
- ISSN
- 1740-1526 (ISSN-L)
- 1740-1534
- OpenAlex
- W2010055058
- Cited by
- 1,611
- References
- 55
- Citations by year
- 2026: 56 · 2025: 105 · 2024: 128 · 2023: 127 · 2022: 134 · 2021: 172 · 2020: 129 · 2019: 135 · 2018: 134 · 2017: 123 · 2016: 116 · 2015: 90 · 2014: 111 · 2013: 49 · 2012: 2
- FWCI
- 7.35
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Reviews Microbiology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Crohn's and Colitis Foundation of Canada
- Canadian Institutes of Health Research
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Keywords
- gut microbiota, gut-brain axis, host-microbe symbiosis, brain development, animal behavior, irritable bowel syndrome, mental illness, multiple sclerosis, demyelinating disease
- MeSH terms
- Animals, Autonomic Nervous System, Brain, Humans, Intestines, Multiple Sclerosis, Stress, Physiological, Inflammatory Bowel Diseases, Signal Transduction, Enteric Nervous System, Irritable Bowel Syndrome, Mice, Metagenome
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