Gut feelings: the emerging biology of gut-brain communication

Mayer, Emeran A.

doi:10.1038/nrn3071

Cited by 1,726Gastrointestinal motility and disordersRegulation of Appetite and ObesityGut microbiota and health

Gut feelings: the emerging biology of gut-brain communication

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Mayer, Emeran A.·2011·Nature Reviews Neuroscience

DOI 10.1038/nrn3071PMC PMC3845678

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Abstract

The concept that the gut and the brain are closely connected, and that this interaction plays an important part not only in gastrointestinal function but also in certain feeling states and in intuitive decision making, is deeply rooted in our language. Recent neurobiological insights into this gut–brain crosstalk have revealed a complex, bidirectional communication system that not only ensures the proper maintenance of gastrointestinal homeostasis and digestion but is likely to have multiple effects on affect, motivation and higher cognitive functions, including intuitive decision making. Moreover, disturbances of this system have been implicated in a wide range of disorders, including functional and inflammatory gastrointestinal disorders, obesity and eating disorders.

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Von Economo Neurons are primarily found in the interoceptive network and the enteric nervous system.
“Interestingly, there are specialized neurons called Von Economo Neurons (VENs), which are primarily found in the interoceptive network (Craig, 2009) and the Enteric Nervous System (Mayer, 2011).”
From Mindfulness, Interoception, and the Body: A Contemporary Perspective (2019) · cites this paper as Mayer, 2011
The citation to Mayer (2011) is attached to the claim that von Economo neurons are primarily found in the enteric nervous system. In “Meta-representation of gut-related feeling states,” the paper instead locates VEN cells in the anterior insula; it says certain receptors and peptides they share are abundant in the ENS, not that the cells themselves are found there. (LLM, conf=0.86)
Checked by a reasoning model — may be wrong.
Experimental — accuracy not yet measured
Cyclic vomiting syndrome is a functional GI disorder that is thought to be due to altered brain‐gut interaction.
“Cyclic vomiting syndrome is a functional GI disorder that is thought to be due to altered brain‐gut interaction.87, 88, 89”
From Guidelines on management of cyclic vomiting syndrome in adults by the American Neurogastroenterology and Motility Society and the Cyclic Vomiting Syndrome Association (2019) · cites this paper as [88]
The ‘Brain–gut interactions in chronic disease’ section links functional gastrointestinal disorders generally to brain–gut axis dysregulation. It does not identify cyclic vomiting syndrome as one of those disorders or attribute its cause to altered brain–gut interaction; a search for ‘cyclic vomiting syndrome’ found no such passage. Page numbers were unavailable in our copy. (LLM, conf=0.84)
Experimental — accuracy not yet measured
The extended reward system involves regions associated with salience and cortical inhibition (prefrontal control) networks.
“The extended reward system involves regions associated with salience and cortical inhibition (prefrontal control) networks 39, 89, 90, 91.”
From History of early life adversity is associated with increased food addiction and sex-specific alterations in reward network connectivity in obesity (2019) · cites this paper as [89]
Bodily information, mediated by afferent visceral neural pathways, sometimes referred to as gut feelings, although largely unconscious, is an inseparable part of the organism's emotional state.
“Bodily information, mediated by afferent visceral neural pathways, sometimes referred to as”
From Exposed to events that never happen: generalized unsafety, the default stress response, and prolonged autonomic activity (2017) · cites this paper as Mayer, 2011
Specific cognitive changes in IBS relate to hippocampal-mediated visuospatial memory deficits that are linked to indices of HPA axis function.
“Cognitive alterations may be present in individuals with IBS, and evidence is emerging that specific changes relate to hippocampal-mediated visuospatial memory deficits, which are linked to indices of HPA axis function (20, 496–498).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [20]

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The microbiota–gut–brain axis: learning from intestinal bacteria?
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Plasticity of vagal brainstem circuits in the control of gastrointestinal function
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Advances in Imaging the Brain–Gut Axis: Functional Gastrointestinal Disorders
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Introduction
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IN THE CEREBRAL CORTEX
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Gastrointestinal disorders
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Unusual Case of Right Upper Quadrant Swelling
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This month in Gastroenterology
Chang, E. B., & Kim, K. C. (2004) · Gastroenterology · doi:10.1053/j.gastro.2003.12.044 · Cited by 1 · see citing works

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Research works printed but not linked: 3

[18]Bandler R Keay KA The Emotional Motor System. Progress in Brain Research Holstege G Bandler R Saper CB 285 300 Elsevier Amsterdam 1996 8782510
[19]Holstege G The Emotional Motor System Jones EG Peters A 3 6 Elsevier Amsterdam 1996
[28]Jaenig W The Integrative Action of the Autonomic Nervous System Jaenig W 317 318 Cambridge Univ. Press New York 2006

Sorted by citations

The Microbiota-Gut-Brain Axis
Cryan, J. F., O'Riordan, K. J., Cowan, C. S. M., Sandhu, K. V., Bastiaanssen, T. F. S., Boehme, M., Codagnone, M. G., Cussotto, S., Fulling, C., Golubeva, A. V., et al. (2019) · Physiological Reviews · doi:10.1152/physrev.00018.2018 · Cited by 5,286 · see citing works
Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour
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The role of short-chain fatty acids in microbiota–gut–brain communication
Dalile, B., Van Oudenhove, L., Vervliet, B., & Verbeke, K. (2019) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-019-0157-3 · Cited by 3,357 · see citing works
Serotonin, tryptophan metabolism and the brain-gut-microbiome axis
O’Mahony, S. M., Clarke, G., Borre, Y. E., Dinan, T. G., & Cryan, J. F. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.07.027 · Cited by 2,012 · see citing works
The microbiome-gut-brain axis during early life regulates the hippocampal serotonergic system in a sex-dependent manner
Clarke, G., Grenham, S., Scully, P., Fitzgerald, P., Moloney, R. D., Shanahan, F., Dinan, T. G., & Cryan, J. F. (2013) · Molecular Psychiatry · doi:10.1038/mp.2012.77 · Cited by 1,893 · see citing works
The interplay between the intestinal microbiota and the brain
Collins, S. M., Surette, M., & Bercik, P. (2012) · Nature Reviews Microbiology · doi:10.1038/nrmicro2876 · Cited by 1,611 · see citing works
Gut/brain axis and the microbiota
Mayer, E. A., Tillisch, K., & Gupta, A. (2015) · Journal of Clinical Investigation · doi:10.1172/jci76304 · Cited by 1,503 · see citing works
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The brain-gut-microbiome axis
Martin, C. R., Osadchiy, V., Kalani, A., & Mayer, E. A. (2018) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2018.04.003 · Cited by 1,284 · see citing works
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Consumption of fermented milk product with probiotic modulates brain activity
Tillisch, K., Labus, J., Kilpatrick, L., Jiang, Z., Stains, J., Ebrat, B., Guyonnet, D., Legrain–Raspaud, S., Trotin, B., Naliboff, B., et al. (2013) · Gastroenterology · doi:10.1053/j.gastro.2013.02.043 · Cited by 1,192 · see citing works
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Current Understanding of Dysbiosis in Disease in Human and Animal Models
DeGruttola, A. K., Low, D., Mizoguchi, A., & Mizoguchi, E. (2016) · Inflammatory Bowel Diseases · doi:10.1097/mib.0000000000000750 · Cited by 1,122 · see citing works
Microbiota and neurodevelopmental windows: implications for brain disorders
Borre, Y. E., O’Keeffe, G. W., Clarke, G., Stanton, C., Dinan, T. G., & Cryan, J. F. (2014) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2014.05.002 · Cited by 1,089 · see citing works
Effects of probiotics on gut microbiota: mechanisms of intestinal immunomodulation and neuromodulation
Hemarajata, P., & Versalovic, J. (2013) · Therapeutic Advances in Gastroenterology · doi:10.1177/1756283x12459294 · Cited by 1,083 · see citing works
Symbiotic bacterial metabolites regulate gastrointestinal barrier function via the xenobiotic sensor PXR and Toll-like receptor 4
Venkatesh, M., Mukherjee, S., Wang, H., Li, H., Sun, K., Benechet, A. P., Qiu, Z., Maher, L., Redinbo, M. R., Phillips, R. S., et al. (2014) · Immunity · doi:10.1016/j.immuni.2014.06.014 · Cited by 1,066 · see citing works
Gut microbes and the brain: paradigm shift in neuroscience
Mayer, E. A., Knight, R., Mazmanian, S. K., Cryan, J. F., & Tillisch, K. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.3299-14.2014 · Cited by 1,033 · see citing works
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The microbiota-gut-brain axis: from motility to mood
Margolis, K. G., Cryan, J. F., & Mayer, E. A. (2021) · Gastroenterology · doi:10.1053/j.gastro.2020.10.066 · Cited by 999 · see citing works
Brain-gut-microbe communication in health and disease
Grenham, S., Clarke, G., Cryan, J. F., & Dinan, T. G. (2011) · Frontiers in Physiology · doi:10.3389/fphys.2011.00094 · Cited by 952 · see citing works
Interoception and emotion.
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“Additional information concerning the chemical and inflammatory environment of the gut and endocrine responses to food intake, are also signalled both neural and humorally to brain [31].”
Background
Microbiota-Brain-Gut Axis and Neurodegenerative Diseases
Quigley, E. M. M. (2017) · Current Neurology and Neuroscience Reports · doi:10.1007/s11910-017-0802-6 · Cited by 804 · see citing works
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
Mayer, E. A., Nance, K., & Chen, S. (2022) · Annual Review of Medicine · doi:10.1146/annurev-med-042320-014032 · Cited by 813 · see citing works
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Discovery and characterization of gut microbiota decarboxylases that can produce the neurotransmitter tryptamine
Williams, B. B., Van Benschoten, A. H., Cimermancic, P., Donia, M. S., Zimmermann, M., Taketani, M., Ishihara, A., Kashyap, P. C., Fraser, J. S., & Fischbach, M. A. (2014) · Cell Host & Microbe · doi:10.1016/j.chom.2014.09.001 · Cited by 732 · see citing works
Neuroprotective effects of fecal microbiota transplantation on MPTP-induced Parkinson's disease mice: gut microbiota, glial reaction and TLR4/TNF-α signaling pathway
Sun, M.-F., Zhu, Y.-L., Zhou, Z.-L., Jia, X.-B., Xu, Y.-D., Yang, Q., Cui, C., & Shen, Y.-Q. (2018) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2018.02.005 · Cited by 736 · see citing works
Biological and psychological markers of stress in humans: Focus on the Trier Social Stress Test
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Active Inference, homeostatic regulation and adaptive behavioural control
Pezzulo, G., Rigoli, F., & Friston, K. (2015) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2015.09.001 · Cited by 650 · see citing works
“The lowest levels of these models might be reified in anatomy; for example, embodied in the functioning of the gastric system (Mayer, 2011).”
Leptin and the endocrine control of energy balance
Friedman, J. M. (2019) · Nature Metabolism · doi:10.1038/s42255-019-0095-y · Cited by 661 · see citing works
Evidence for a large-scale brain system supporting allostasis and interoception in humans
Kleckner, I. R., Zhang, J., Touroutoglou, A., Chanes, L., Xia, C., Simmons, W. K., Quigley, K. S., Dickerson, B. C., & Feldman Barrett, L. (2017) · Nature Human Behaviour · doi:10.1038/s41562-017-0069 · Cited by 641 · see citing works
A randomized controlled trial to test the effect of multispecies probiotics on cognitive reactivity to sad mood
Steenbergen, L., Sellaro, R., van Hemert, S., Bosch, J. A., & Colzato, L. S. (2015) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2015.04.003 · Cited by 671 · see citing works
“release immune activating and other signaling molecules that may play an important role in regulating the brain and subsequent behavior (Mayer, 2011; Cryan and Dinan, 2012; Foster and McVey Neufeld, 2013).”
Background
Gastrointestinal microbiota in children with autism in Slovakia
Tomova, A., Husarova, V., Lakatosova, S., Bakos, J., Vlkova, B., Babinska, K., & Ostatnikova, D. (2015) · Physiology & Behavior · doi:10.1016/j.physbeh.2014.10.033 · Cited by 632 · see citing works
Microbial genes, brain & behaviour – epigenetic regulation of the gut–brain axis
Stilling, R. M., Dinan, T. G., & Cryan, J. F. (2014) · Genes, Brain and Behavior · doi:10.1111/gbb.12109 · Cited by 637 · see citing works
Microfluidic Organ-on-a-Chip Models of Human Intestine
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Authors: Mayer, E. A.
Affiliations: University of California, Los Angeles (US)
Corresponding author: Mayer, Emeran A.
Venue: Nature Reviews Neuroscience
Publisher: Springer Science and Business Media LLC
Published: 2011-07-13
Volume: 12
Issue: 8
Pages: 453-466
ISSN: 1471-003X (ISSN-L)
1471-0048
DOI: 10.1038/nrn3071
PMC: PMC3845678
OpenAlex: W1993623582
Semantic Scholar: c3e26b9bfec3a313f48f1815e991934ebe53fab0
Cited by: 1,726
References: 160
Citations by year: 2026: 105 · 2025: 137 · 2024: 149 · 2023: 175 · 2022: 149 · 2021: 170 · 2020: 165 · 2019: 113 · 2018: 124 · 2017: 105 · 2016: 75 · 2015: 93 · 2014: 72 · 2013: 51 · 2012: 40
FWCI: 8.75
Type: journal article
Language: en
Open access: green
europepmc.org
Licence: www.springer.com/tdm (tdm)
Locations: Nature reviews. Neuroscience (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of Diabetes and Digestive and Kidney Diseases (DK048351, DK 082370, R01DK048351, DK 064539, U01DK082370, P50DK064539)
National Center for Complementary and Integrative Health (R24AT002681, AT002681)
Topics: Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Keywords: gut-brain axis, two-way communication, enteric nervous system, gastrointestinal homeostasis, affect, motivation, intuitive decision making, executive function, functional gastrointestinal disorders, obesity, eating disorders
MeSH terms: Brain, Homeostasis, Humans, Enteric Nervous System, Gastrointestinal Tract

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