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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
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“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].”
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“High-fat diets could be detrimental to immune function compared to high carbohydrate diets [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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“We propose that one needs to take a systems biology approach to correlate the complex functional dynamic in the gut ecosystem as a modulator of the gut-brain axis in the human host [14].”
BackgroundThe microbiome: stress, health and disease
Moloney, R. D., Desbonnet, L., Clarke, G., Dinan, T. G., & Cryan, J. F. (2014) · Mammalian Genome · doi:10.1007/s00335-013-9488-5 · Cited by 430
“…and the subject of microbiota–brain–gut axis dysregulation in stress-related CNS disorders has been the subject of a number of excellent recent reviews (Bested et al. 2013a, b; Bravo et al. 2012; Collins et al. 2012; Cryan and Dinan 2012; Foster and McVey Neufeld 2013; Scott et al. 2013).”
BackgroundInfluentialMetagenome Sequencing of the Hadza Hunter-Gatherer Gut Microbiota
Rampelli, S., Schnorr, S. L., Consolandi, C., Turroni, S., Severgnini, M., Peano, C., Brigidi, P., Crittenden, A. N., Henry, A. G., & Candela, M. (2015) · Current Biology · doi:10.1016/j.cub.2015.04.055 · Cited by 399
“In particular, phenylalanine, tyrosine, tryptophan, histidine, and glutamate are important precursors for neurotransmitters and signaling transduction proteins and therefore could contribute to epithelial crosstalk and GM-mediated modulation of the host central nervous system through the vagus nerve [17].”
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Melancholic microbes: a link between gut microbiota and depression
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Immunological Consequences of Intestinal Fungal Dysbiosis
Wheeler, M. L., Limon, J. J., Bar, A. S., Leal, C. A., Gargus, M. D., Tang, J., Brown, J. S., Funari, V. A., Wang, H. L., Crother, T. R., et al. (2016) · Cell Host & Microbe · doi:10.1016/j.chom.2016.05.003 · Cited by 427
“Microbial communities associated with mucosal surfaces of the body play essential roles in diverse biological processes ranging from digestion to behavior and are increasingly recognized as integral components of normal physiology (Clemente et al., 2012; Collins et al., 2012).”
BackgroundThe progress of gut microbiome research related to brain disorders
Zhu, S., Jiang, Y., Xu, K., Cui, M., Ye, W., Zhao, G., Jin, L., & Chen, X. (2020) · Journal of Neuroinflammation · doi:10.1186/s12974-020-1705-z · Cited by 419
“The microbiota of different habitats contribute to bidirectional brain-gut signaling through humoral, neural, and immunological pathogenic pathways [14].”
BackgroundGut microbiota in autism and mood disorders
Mangiola, F. (2016) · World Journal of Gastroenterology · doi:10.3748/wjg.v22.i1.361 · Cited by 413
(Dis)Trust your gut: the gut microbiome in age-related inflammation, health, and disease
Buford, T. W. (2017) · Microbiome · doi:10.1186/s40168-017-0296-0 · Cited by 409
“microbiota, as evidenced by the fact that 70% of the body’s lymphocytes reside in the gut-associated lymphoid tissue [49].”
Sharkey, K. A., & Mawe, G. M. (2022) · Physiological Reviews · doi:10.1152/physrev.00018.2022 · Cited by 447
Gut microbiome and depression: what we know and what we need to know
Winter, G., Hart, R. A., Charlesworth, R. P. G., & Sharpley, C. F. (2018) · Reviews in the Neurosciences · doi:10.1515/revneuro-2017-0072 · Cited by 394
Stress and the Microbiota–Gut–Brain Axis in Visceral Pain: Relevance to Irritable Bowel Syndrome
Moloney, R. D., Johnson, A. C., O’Mahony, S. M., Dinan, T. G., Meerveld, B. G., & Cryan, J. F. (2015) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.12490 · Cited by 412
“More recently, the role of the gut microbiota in the bidirectional communication along the gut–brain axis, and subsequent changes in behavior, has emerged [15,16].”
BackgroundRole of microbiota-derived short-chain fatty acids in nervous system disorders
Mirzaei, R., Bouzari, B., Hosseini‐Fard, S. R., Mazaheri, M., Ahmadyousefi, Y., Abdi, M., Jalalifar, S., Karimitabar, Z., Teimoori, A., Keyvani, H., et al. (2021) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2021.111661 · Cited by 408
Diet, Stress and Mental Health
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Recognizing Depression from the Microbiota–Gut–Brain Axis
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“Scientists have started to pay attention to the role of the brain–gut axis in depression since 2009 [14,18,23,62,164,165].”
BackgroundAlzheimer’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
The gut microbiome and diet in psychiatry: focus on depression
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Bifidobacteria modulate cognitive processes in an anxious mouse strain
Savignac, H. M., Tramullas, M., Kiely, B., Dinan, T. G., & Cryan, J. F. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.02.044 · Cited by 365
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Microbiota controls the homeostasis of glial cells in the gut lamina propria
Kabouridis, P. S., Lasrado, R., McCallum, S., Chng, S. H., Snippert, H. J., Clevers, H., Pettersson, S., & Pachnis, V. (2015) · Neuron · doi:10.1016/j.neuron.2014.12.037 · Cited by 358
“The ENS regulates most aspects of GI physiology, such as peristalsis, blood supply to the gut wall, and secretion (Furness, 2006), and constitutes a relay station in the bi-directional neuro-endocrine pathways that connect the digestive system and the brain (gut-brain axis) (Collins et al., 2012).”
A role for the gut microbiota in IBS
Collins, S. M. (2014) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2014.40 · Cited by 351
Self-citationGut Microbiome Dysbiosis and Immunometabolism: New Frontiers for Treatment of Metabolic Diseases
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“Some of these factors act as major neurotransmitters and modulators of the brain-gut axis, and serotonin has central roles in sexuality, substance addiction, appetite, emotions, and stress response [18].”
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Bacterial Neuroactive Compounds Produced by Psychobiotics
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Microbiome-Gut-Brain Axis and Toll-Like Receptors in Parkinson’s Disease
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Fan, P. F., Liu, P., Song, P., Chen, X., & Ma, X. (2017) · Scientific Reports · doi:10.1038/srep43412 · Cited by 363
Solfrizzi, V., Custodero, C., Lozupone, M., Imbimbo, B. P., Valiani, V., Agosti, P., Schilardi, A., D’Introno, A., Montagna, M. L., Calvani, M., et al. (2017) · Journal of Alzheimer s Disease · doi:10.3233/jad-170248 · Cited by 358
“In the past five years, there has been an increasing interest in the role that gut microbiota may play in the modulation of the bidirectional signaling underlying the gut–brain axis [112, 113].”
Dogra, S. K., Sakwińska, O., Soh, S., Ngom‐Bru, C., Brück, W. M., Berger, B. W., Brüssow, H., Lee, Y. S., Yap, F. K. P., Chong, Y. S., et al. (2015) · mBio · doi:10.1128/mbio.02419-14 · Cited by 359
“Variation in the microbiota of the adult human gut has been linked to many outcomes, including a risk of autoimmune disease (1), response to toxins (2), and behavior (3).”
BackgroundThe impact of the microbiota-gut-brain axis on Alzheimer’s disease pathophysiology
Doifode, T., Giridharan, V. V., Generoso, J. S., Bhatti, G., Collodel, A., Schulz, P. E., Forlenza, O. V., & Barichello, T. (2021) · Pharmacological Research · doi:10.1016/j.phrs.2020.105314 · Cited by 347
A review of the relationship between the gut microbiota and amino acid metabolism
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Gut dysbiosis impairs recovery after spinal cord injury
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“Recent data indicate that gut microbes also regulate both normal development and disease pathogenesis in the central nervous system (CNS; Collins et al., 2012; Wang and Kasper, 2014; Benakis et al., 2016; Winek et al., 2016).”
BackgroundEffect of probiotics on central nervous system functions in animals and humans: a systematic review
Wang, H., Lee, I.-S., Braun, C., & Enck, P. (2016) · Journal of Neurogastroenterology and Motility · doi:10.5056/jnm16018 · Cited by 334
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“Furthermore, it is being increasingly recognized that the gut–brain axis provides a bidirectional route of communication that employs neural, hormonal and immunological pathways, and that dysfunction of this axis can have pathophysiological consequences (Collins et al., 2012; Cryan and Dinan, 2012).”
The Impact of Microbiota on Brain and Behavior: Mechanisms & Therapeutic Potential
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“Many papers have explored the links among gut microbes, brain and behaviour (e.g. Collins et al., 2012; Mayer, 2011; Thakur et al., 2014).”
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“secretion of 5-HT from enteroendocrine cells.(41) The efficacy of the non-absorbable antibiotic rifaximin in IBS in about a third of cases is consistent(42) with the hypothesis”
Background
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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