The DOI matches its Crossref record; 55 of the 55 references it cites were found in a registry or an index.
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]
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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]
Citations
Cites
A human gut microbial gene catalogue established by metagenomic sequencing
MetaHIT Consortium, Qin, J., Li, R., Raes, J., Arumugam, M., Burgdorf, K. S., Manichanh, C., Nielsen, T., Pons, N., Levenez, F., et al. (2010) · Nature · doi:10.1038/nature08821 · Cited by 11,624
Bravo, J. A., Forsythe, P., Chew, M. V., Escaravage, E., Savignac, H. M., Dinan, T. G., Bienenstock, J., & Cryan, J. F. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1102999108 · Cited by 3,888
Bacterial Community Variation in Human Body Habitats Across Space and Time
Costello, E. K., Lauber, C. L., Hamady, M., Fierer, N., Gordon, J. I., & Knight, R. (2009) · Science · doi:10.1126/science.1177486 · Cited by 3,231
Normal gut microbiota modulates brain development and behavior
Heijtz, R. D., Wang, S., Anuar, F., Qian, Y., Björkholm, B., Samuelsson, A., Hibberd, M. L., Forssberg, H., & Pettersson, S. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1010529108 · Cited by 3,228
Sudo, N., Chida, Y., Aiba, Y., Sonoda, J., Oyama, N., Yu, X., Kubo, C., & Koga, Y. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.063388 · Cited by 2,735
Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites
Wikoff, W. R., Anfora, A. T., Liu, J., Schultz, P. G., Lesley, S. A., Peters, E. C., & Siuzdak, G. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0812874106 · Cited by 2,677
Bercik, P., Denou, E., Collins, J., Jackson, W., Lu, J., Jury, J., Deng, Y., Blennerhassett, P., Macri, J., McCoy, K. D., et al. (2011) · Gastroenterology · doi:10.1053/j.gastro.2011.04.052 · Cited by 1,748
Self-citationGut feelings: the emerging biology of gut-brain communication
Mayer, E. A. (2011) · Nature Reviews Neuroscience · doi:10.1038/nrn3071 · Cited by 1,726
Interactions between commensal intestinal bacteria and the immune system
Macpherson, A. J., & Harris, N. L. (2004) · Nature reviews. Immunology · doi:10.1038/nri1373 · Cited by 1,683
O’Mahony, L., McCarthy, J., Kelly, P., Hurley, G., Luo, F., Chen, K., O’Sullivan, G. C., Kiely, B., Collins, J. K., Shanahan, F., et al. (2005) · Gastroenterology · doi:10.1053/j.gastro.2004.11.050 · Cited by 1,448
Neufeld, K. M., Kang, N., Bienenstock, J., & Foster, J. A. (2011) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2010.01620.x · Cited by 1,392
Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis
Lee, Y. K., Menezes, J. S., Umesaki, Y., & Mazmanian, S. K. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1000082107 · Cited by 1,323
Commensal microbiota and myelin autoantigen cooperate to trigger autoimmune demyelination
Berer, K., Mues, M., Koutrolos, M., Rasbi, Z. A., Boziki, M., Johner, C., Wekerle, H., & Krishnamoorthy, G. (2011) · Nature · doi:10.1038/nature10554 · Cited by 1,251
γ-Aminobutyric acid production by culturable bacteria from the human intestine
Barrett, E., Ross, R. P., O'Toole, P. W., Fitzgerald, G. F., & Stanton, C. (2012) · Journal of Applied Microbiology · doi:10.1111/j.1365-2672.2012.05344.x · Cited by 1,156
Tracey, K. J. (2009) · Nature Reviews Immunology · doi:10.1038/nri2566 · Cited by 1,154
Bailey, M. T., Dowd, S. E., Galley, J. D., Hufnagle, A. R., Allen, R. G., & Lyte, M. (2011) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2010.10.023 · Cited by 1,123
Bercik, P., Park, A. J., Sinclair, D., Khoshdel, A., Lu, J., Huang, X., Deng, Y., Blennerhassett, P. A., Fahnestock, M., Moine, D., et al. (2011) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2011.01796.x · Cited by 1,018
Self-citationEffects of the probiotic Bifidobacterium infantis in the maternal separation model of depression
Desbonnet, L., Garrett, L., Clarke, G., Kiely, B., Cryan, J. F., & Dinan, T. G. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.08.005 · Cited by 999
Desbonnet, L., Garrett, L., Clarke, G., Bienenstock, J., & Dinan, T. G. (2008) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2008.03.009 · Cited by 952
Bacterial infection causes stress-induced memory dysfunction in mice
Gareau, M. G., Wine, E., Rodrigues, D. M., Cho, J. H., Whary, M. T., Philpott, D. J., MacQueen, G., & Sherman, P. M. (2011) · Gut · doi:10.1136/gut.2009.202515 · Cited by 909
Regulation of learning and memory by meningeal immunity: a key role for IL-4
Derecki, N. C., Cardani, A. N., Yang, C. H., Quinnies, K. M., Crihfield, A., Lynch, K. R., & Kipnis, J. (2010) · Journal of Experimental Medicine · doi:10.1084/jem.20091419 · Cited by 800
Bercik, P., Verdu, E. F., Foster, J. A., Macri, J., Potter, M., Huang, X., Malinowski, P., Jackson, W., Blennerhassett, P., Neufeld, K. A., et al. (2010) · Gastroenterology · doi:10.1053/j.gastro.2010.06.063 · Cited by 674
Self-citationPsychological stress in IBD: new insights into pathogenic and therapeutic implications
Mawdsley, J. E., & Rampton, D. S. (2005) · Gut · doi:10.1136/gut.2005.064261 · Cited by 622
Short-Term Benefit From Oral Vancomycin Treatment of Regressive-Onset Autism
Sandler, R. H., Finegold, S. M., Bolte, E. R., Buchanan, C. P., Maxwell, A. P., Väisänen, M.-L., Nelson, M. N., & Wexler, H. M. (2000) · Journal of Child Neurology · doi:10.1177/088307380001500701 · Cited by 614
Collins, S. M., & Bercik, P. (2009) · Gastroenterology · doi:10.1053/j.gastro.2009.01.075 · Cited by 612
Self-citationLyte, M. (2011) · BioEssays · doi:10.1002/bies.201100024 · Cited by 549
Linkage of gut microbiome with cognition in hepatic encephalopathy
Bajaj, J. S., Ridlon, J. M., Hylemon, P. B., Thacker, L. R., Heuman, D. M., Smith, S., Sikaroodi, M., & Gillevet, P. M. (2012) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00190.2011 · Cited by 547
MACFABE, D., CAIN, D., RODRIGUEZCAPOTE, K., FRANKLIN, A., HOFFMAN, J., BOON, F., TAYLOR, A., KAVALIERS, M., & OSSENKOPP, K. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.07.025 · Cited by 497
Williams, B. L., Hornig, M., Buie, T., Bauman, M. L., Cho Paik, M., Wick, I., Bennett, A., Jabado, O., Hirschberg, D. L., & Lipkin, W. I. (2011) · PLoS ONE · doi:10.1371/journal.pone.0024585 · Cited by 492
tana, C., umesaki, Y., imaoka, A., handa, T., kanazawa, M., & fukudo, S. (2009) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2009.01427.x · Cited by 474
Behavioral phenotyping strategies for mutant mice
Crawley, J. N. (2008) · Neuron · doi:10.1016/j.neuron.2008.03.001 · Cited by 439
Wang, L., Christophersen, C. T., Sorich, M. J., Gerber, J. P., Angley, M. T., & Conlon, M. A. (2011) · Applied and Environmental Microbiology · doi:10.1128/aem.05212-11 · Cited by 432
Williams, B. L., Hornig, M., Parekh, T., & Lipkin, W. I. (2012) · mBio · doi:10.1128/mbio.00261-11 · Cited by 378
Jalanka-Tuovinen, J., Salonen, A., Nikkilä, J., Immonen, O., Kekkonen, R., Lahti, L., Palva, A., & de Vos, W. M. (2011) · PLoS ONE · doi:10.1371/journal.pone.0023035 · Cited by 340
Kunze, W. A., Mao, Y., Wang, B., Huizinga, J. D., Ma, X., Forsythe, P., & Bienenstock, J. (2009) · Journal of Cellular and Molecular Medicine · doi:10.1111/j.1582-4934.2009.00686.x · Cited by 328
The intestinal microbiota and chronic disorders of the gut
Dupont, A. W., & DuPont, H. L. (2011) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2011.133 · Cited by 310
Microbial endocrinology: how stress influences susceptibility to infection
Freestone, P. P. E., Sandrini, S. M., Haigh, R. D., & Lyte, M. (2008) · Trends in Microbiology · doi:10.1016/j.tim.2007.11.005 · Cited by 299
Stress at the intestinal surface: catecholamines and mucosa–bacteria interactions
Lyte, M., Vulchanova, L., & Brown, D. R. (2011) · Cell and Tissue Research · doi:10.1007/s00441-010-1050-0 · Cited by 281
Gastrointestinal microbiota in irritable bowel syndrome: present state and perspectives
Salonen, A., de Vos, W. M., & Palva, A. (2010) · Microbiology · doi:10.1099/mic.0.043257-0 · Cited by 264
Li, W., Dowd, S. E., Scurlock, B., Acosta-Martinez, V., & Lyte, M. (2009) · Physiology & Behavior · doi:10.1016/j.physbeh.2008.12.004 · Cited by 246
Kynurenines: from the perspective of major psychiatric disorders
Myint, A.-M. (2012) · FEBS Journal · doi:10.1111/j.1742-4658.2012.08551.x · Cited by 230
Microbiology of regressive autism
Finegold, S. M., Downes, J., & Summanen, P. H. (2012) · Anaerobe · doi:10.1016/j.anaerobe.2011.12.018 · Cited by 211
Bacterial Cell-to-Cell Signaling in the Gastrointestinal Tract
Kaper, J. B., & Sperandio, V. (2005) · Infection and Immunity · doi:10.1128/iai.73.6.3197-3209.2005 · Cited by 177
Microflora modulates endocrine cells in the gastrointestinal mucosa of the rat
Uribe, A., Alam, M., Johansson, O., Midtvedt, T., & Theodorsson, E. (1994) · Gastroenterology · doi:10.1016/0016-5085(94)90526-6 · Cited by 171
Antimicrobial-Induced Mania (Antibiomania): A Review of Spontaneous Reports
Abouesh, A., Stone, C., & Hobbs, W. R. (2002) · Journal of Clinical Psychopharmacology · doi:10.1097/00004714-200202000-00012 · Cited by 169
Wu, J. C. (2012) · Journal of Neurogastroenterology and Motility · doi:10.5056/jnm.2012.18.1.13 · Cited by 126
Rendeiro, C., Guerreiro, J. D. T., Williams, C. M., & Spencer, J. P. E. (2012) · Proceedings of The Nutrition Society · doi:10.1017/s0029665112000146 · Cited by 114
Regulatory mechanisms of immune responses to intestinal bacteria
Honda, K., & Takeda, K. (2009) · Mucosal Immunology · doi:10.1038/mi.2009.8 · Cited by 107
Microbiota–immune system interaction: an uneasy alliance
Salzman, N. H. (2011) · Current Opinion in Microbiology · doi:10.1016/j.mib.2010.09.018 · Cited by 96
Juárez, I., Gratton, A., & Flores, G. (2008) · Journal of Comparative Neurology · doi:10.1002/cne.21651 · Cited by 89
Lotrich, F. E., El-Gabalawy, H. S., Guenther, L., & Ware, C. F. (2011) · Journal of Rheumatology Supplement · doi:10.3899/jrheum.110903 · Cited by 76
Carbohydrate Malabsorption Syndromes and Early Signs of Mental Depression in Females
Ledochowski, M., Widner, B., Sperner‐Unterweger, B., Propst, T., Vogel, W., & Fuchs, D. (2000) · Digestive Diseases and Sciences · doi:10.1023/a:1005527230346 · Cited by 61
Increased plasma d-lactic acid associated with impaired memory in rats
Hanstock, T. L., Mallet, P. E., & Clayton, E. H. (2010) · Physiology & Behavior · doi:10.1016/j.physbeh.2010.09.018 · Cited by 41
Treatment Options for Hepatic Encephalopathy
Schiano, T. D. (2010) · Pharmacotherapy The Journal of Human Pharmacology and Drug Therapy · doi:10.1592/phco.30.pt2.16s · Cited by 33
Delivery modes and neonatal EEG: spatial pattern analysis
Kim, H.-R., Jung, K.-Y., Kim, S.-Y., Ko, K. O., Lee, Y., & Kim, J.-M. (2003) · Early Human Development · doi:10.1016/j.earlhumdev.2003.09.004 · Cited by 17
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“The bidirectional interactions of gut–brain mean that the brain can also alter gut microbiota composition [110].”
BackgroundHsiao, E. Y., McBride, S. W., Hsien, S., Sharon, G., Hyde, E. R., McCue, T., Codelli, J. A., Chow, J., Reisman, S. E., Petrosino, J. F., et al. (2013) · Cell · doi:10.1016/j.cell.2013.11.024 · Cited by 3,283
“Commensal bacteria affect a variety of complex behaviors, including social, emotional, and anxiety-like behaviors, and contribute to brain development and function in mice (Collins et al., 2012; Cryan and Dinan, 2012) and humans (Tillisch et al., 2013).”
Animals in a bacterial world, a new imperative for the life sciences
McFall‐Ngai, M., Hadfield, M. G., Bosch, T. C. G., Carey, H. V., Domazet‐Lošo, T., Douglas, A. E., Dubilier, N., Eberl, G., Fukami, T., Gilbert, S. F., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1218525110 · Cited by 2,879
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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