The neuroendocrinology of the microbiota-gut-brain axis: a behavioural perspective
Open accessAbstract
The human gut harbours trillions of symbiotic bacteria that play a key role in programming different aspects of host physiology in health and disease. These intestinal microbes are also key components of the gut-brain axis, the bidirectional communication pathway between the gut and the central nervous system (CNS). In addition, the CNS is closely interconnected with the endocrine system to regulate many physiological processes. An expanding body of evidence is supporting the notion that gut microbiota modifications and/or manipulations may also play a crucial role in the manifestation of specific behavioural responses regulated by neuroendocrine pathways. In this review, we will focus on how the intestinal microorganisms interact with elements of the host neuroendocrine system to modify behaviours relevant to stress, eating behaviour, sexual behaviour, social behaviour, cognition and addiction.
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The development of the blood-brain barrier is contingent upon the presence of commensal gut flora.
“The development of the blood-brain barrier is now well established to be contingent upon the presence of commensal gut flora (10, 11).”
From Association Between Gut Microbiota and Autism Spectrum Disorder: A Systematic Review and Meta-Analysis (2019) · cites this paper as [10]
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“basal noradrenaline levels in the brainstem, however, there were no differences in corticosterone concentrations between groups (Desbonnet et al., 2008; Desbonnet et al., 2010).”
BackgroundMicrobial community profiling for human microbiome projects: Tools, techniques, and challengesPreprint
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BackgroundThe microbiome-gut-brain axis: from bowel to behavior
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BackgroundSex-Specific Programming of Offspring Emotionality after Stress Early in Pregnancy
Mueller, B. R., & Bale, T. L. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.1424-08.2008 · Cited by 988 · see citing works
Pyrosequencing study of fecal microflora of autistic and control children
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“microbiota in children with ASD are limited in quantity and quality; however, some have pointed out differences in the microbiota composition between ASD and healthy children (Finegold et al., 2010; Kang et al., 2013; Parracho et al., 2005).”
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“bacterial fermentation of proteins and carbohydrates in the intestine (Macfarlane and Macfarlane, 2012) and their molar ratios in the colon are approximately 20:20:60”
BackgroundDesbonnet, 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 · cited 2× · see citing works
“basal noradrenaline levels in the brainstem, however, there were no differences in corticosterone concentrations between groups (Desbonnet et al., 2008; Desbonnet et al., 2010).”
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“In addition, the prebiotic combination was able to normalise the effects of chronic psychological stress on the microbiota (Burokas et al., 2017).”
BackgroundInfluentialRole of serotonin in the pathophysiology of depression: focus on the serotonin transporter
Owens, M. J., & Nemeroff, C. B. (1994) · Clinical Chemistry · doi:10.1093/clinchem/40.2.288 · Cited by 934 · cited 1× · see citing works
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BackgroundDiet and feeding pattern affect the diurnal dynamics of the gut microbiome
Zarrinpar, A., Chaix, A., Yooseph, S., & Panda, S. (2014) · Cell Metabolism · doi:10.1016/j.cmet.2014.11.008 · Cited by 926 · cited 1× · see citing works
“fluctuations in composition and in the production of key metabolic mediators (Leone et al., 2015; Liang et al., 2015; Thaiss et al., 2014; Zarrinpar et al., 2014).”
BackgroundTowards a more comprehensive concept for prebiotics
Bindels, L. B., Delzenne, N. M., Cani, P. D., & Walter, J. (2015) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2015.47 · Cited by 914 · cited 1× · see citing works
“host by selectively stimulating the growth and/or activity of one or a limited number of bacteria in the colon, thus improving host health” (Gibson and Roberfroid, 1995) but this concept has been expanded more recently (Bindels et al., 2015).”
BackgroundEnterochromaffin cells are gut chemosensors that couple to sensory neural pathways
Bellono, N. W., Bayrer, J. R., Leitch, D. B., Castro, J., Zhang, C., O’Donnell, T. A., Brierley, S. M., Ingraham, H. A., & Julius, D. (2017) · Cell · doi:10.1016/j.cell.2017.05.034 · Cited by 910 · see citing works
Bacterial infection causes stress-induced memory dysfunction in mice
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“rodentium in conventionally colonised mice was able to generate stress-induced memory dysfunction (Gareau et al., 2011).”
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“fluctuations in composition and in the production of key metabolic mediators (Leone et al., 2015; Liang et al., 2015; Thaiss et al., 2014; Zarrinpar et al., 2014).”
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The neuropharmacology of butyrate: the bread and butter of the microbiota-gut-brain axis
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Comparative metagenomics revealed commonly enriched gene sets in human gut microbiomes
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“The intestinal microbiota does not remain stable throughout lifespan, in fact the microbiota of newborn infants, acquired at delivery, is characterised by low diversity and a relative dominance of the phyla Proteobacteria and Actinobacteria (Kurokawa et al., 2007).”
BackgroundMicrobiota is essential for social development in the mouse
Desbonnet, L., Clarke, G., Shanahan, F., Dinan, T. G., & Cryan, J. F. (2014) · Molecular Psychiatry · doi:10.1038/mp.2013.65 · Cited by 866 · cited 1× · see citing works
“, 2011) and demonstrated that germfree animals suffer a social impairment, which is reversed by re-colonisation with a normal microbiota (Desbonnet et al., 2014).”
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New insights into symptoms and neurocircuit function of anorexia nervosa
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Socially transmitted gut microbiota protect bumble bees against an intestinal parasite
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“, 2014), bumblebees (Koch and Schmid-Hempel, 2011), hyenas (Theis et al.”
Commensal bacteria play a role in mating preference of Drosophila melanogaster
Sharon, G., Segal, D., Ringo, J. M., Hefetz, A., Zilber‐Rosenberg, I., & ROSENBERG, E. B. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1009906107 · Cited by 825 · cited 8× · see citing works
“The microbiota has been linked to social status across a variety of species including Drosophila (Lize et al., 2014; Venu et al., 2014), bumblebees (Koch and Schmid-Hempel, 2011), hyenas (Theis et al., 2013), non-human primates in the wild (Tung et al., 2015) and rodents.”
BackgroundInfluentialGut 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 · cited 1× · see citing works
“which the brain regulates the activity of the gut and vice versa and is critical for homeostasis of the host system (De Vadder et al., 2014; Dinan and Cryan, 2017; Holzer et al., 2012; Montiel-Castro et al., 2013; Rhee et al., 2009; Sherwin et al., 2017).”
BackgroundAutism‐like behavioral phenotypes in BTBR T+tf/J mice
McFarlane, H. G., Kusek, G. K., Yang, M., Phoenix, J. L., Bolivar, V. J., & Crawley, J. N. (2008) · Genes, Brain and Behavior · doi:10.1111/j.1601-183x.2007.00330.x · Cited by 812 · see citing works
Effects of sodium butyrate, a new pharmacological agent, on cells in culture
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“In fact, one of the most recognised cellular mechanism of action of butyrate is its ability to inhibit the histone deacetylases (Kruh, 1982).”
BackgroundOxytocin, vasopressin, and human social behavior
Heinrichs, M., von Dawans, B., & Domes, G. (2009) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2009.05.005 · Cited by 799 · see citing works
Enteric dysbiosis associated with a mouse model of alcoholic liver disease
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“microbiota in children with ASD are limited in quantity and quality; however, some have pointed out differences in the microbiota composition between ASD and healthy children (Finegold et al., 2010; Kang et al., 2013; Parracho et al., 2005).”
BackgroundTargeting gut microbiota in obesity: effects of prebiotics and probiotics
Delzenne, N. M., Neyrinck, A. M., Bäckhed, F., & Cani, P. D. (2011) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2011.126 · Cited by 783 · cited 1× · see citing works
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BackgroundColonic microbiome is altered in alcoholism
Mutlu, E. A., Gillevet, P. M., Rangwala, H., Sikaroodi, M., Naqvi, A., Engen, P. A., Kwasny, M., Lau, C. K., & Keshavarzian, A. (2012) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00380.2011 · Cited by 775 · see citing works
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“The increased satiety and reduced hunger caused by highly fermented prebiotics were associated with changes in plasma GLP-1 and PYY levels (Cani et al., 2009).”
BackgroundGut microbiota depletion from early adolescence in mice: implications for brain and behaviour
Desbonnet, L., Clarke, G., Traplin, A., O’Sullivan, O., Crispie, F., Moloney, R. D., Cotter, P. D., Dinan, T. G., & Cryan, J. F. (2015) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2015.04.004 · Cited by 760 · cited 4× · see citing works
“compared to non-treated mice, suggesting that gut microbes are able to modulate the activity of these hormones (Desbonnet et al., 2015).”
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“Receptors sensitive to glucocorticoids are expressed throughout the CNS including in the same brain regions involved in the mounting of a stress-mediated neuroendocrine response (Sapolsky et al., 1984).”
BackgroundWhy are autism spectrum conditions more prevalent in males?
Baron-Cohen, S., Lombardo, M. V., Auyeung, B., Ashwin, E., Chakrabarti, B., & Knickmeyer, R. (2011) · PLoS Biology · doi:10.1371/journal.pbio.1001081 · Cited by 754 · cited 1× · see citing works
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Functional Cross‐Talk Between the Hypothalamic‐Pituitary‐Gonadal and ‐Adrenal Axes
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BackgroundInfluentialStress, Glucocorticoids, and Damage to the Nervous System: The Current State of Confusion
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BackgroundCentral Command Neurons of the Sympathetic Nervous System: Basis of the Fight-or-Flight Response
Jansen, A. S. P., Nguyen, X. V., Karpitskiy, V. V., Mettenleiter, T. C., & Loewy, A. D. (1995) · Science · doi:10.1126/science.270.5236.644 · Cited by 730 · cited 1× · see citing works
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Beneficial metabolic effects of a probiotic via butyrate-induced GLP-1 hormone secretion
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Maternal gut bacteria promote neurodevelopmental abnormalities in mouse offspring
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Influence of a high-fat diet on gut microbiota, intestinal permeability and metabolic endotoxaemia
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The role of testosterone in social interaction
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Stress as a Common Risk Factor for Obesity and Addiction
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The GABA system in anxiety and depression and its therapeutic potential
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“Some intestinal bacteria are also able to produce ɣ-aminobutyric acid (GABA), the main inhibitory neurotransmitter in the CNS that is also associated to pathological scenarios such as depression and anxiety (Mohler, 2012).”
BackgroundAutomated Three‐Chambered Social Approach Task for Mice
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“through the three-chambered sociability test (Yang et al., 2011) and demonstrated that germfree animals suffer a social impairment, which is reversed by re-colonisation with a normal microbiota (Desbonnet et al.”
MethodCrumeyrolle-Arias, M., Jaglin, M., Bruneau, A., Vancassel, S., Cardona, A., Daugé, V., Naudon, L., & Rabot, S. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.01.014 · Cited by 581 · cited 1× · see citing works
“animals have high levels of ACTH and corticosterone following a stressful stimulus (Clarke et al., 2013; Crumeyrolle-Arias et al., 2014; Neufeld et al., 2011; Sudo et al., 2004).”
BackgroundRhythmicity of the intestinal microbiota is regulated by gender and the host circadian clock
Liang, X., Bushman, F. D., & FitzGerald, G. A. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1501305112 · Cited by 578 · cited 1× · see citing works
“fluctuations in composition and in the production of key metabolic mediators (Leone et al., 2015; Liang et al., 2015; Thaiss et al., 2014; Zarrinpar et al., 2014).”
BackgroundNøhr, M. K., Pedersen, M. H., Gille, A., Egerod, K. L., Engelstoft, M. S., Husted, A. S., Sichlau, R. M., Grunddal, K. V., Poulsen, S. S., Han, S., et al. (2013) · Endocrinology · doi:10.1210/en.2013-1142 · Cited by 575 · see citing works
Anxiety, depression, and the microbiome: A role for gut peptides
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“Another class of molecules, gut-derived peptides, can reach the systemic circulation and bind receptors on immune cells and vagus nerve terminals thereby enabling indirect gut-brain communication (Lach et al., 2017).”
BackgroundStress and the HPA axis: role of glucocorticoids in alcohol dependence
Stephens, M. (2012) · Alcohol Research: Current Reviews · doi:10.35946/arcr.v34.4.11 · Cited by 571 · cited 1× · see citing works
“adrenal cortex produces glucocorticoid hormones: cortisol in humans and corticosterone in rodents (Stephens and Wand, 2012).”
BackgroundCollective unconscious: How gut microbes shape human behavior
Dinan, T. G., Stilling, R. M., Stanton, C., & Cryan, J. F. (2015) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2015.02.021 · Cited by 571 · cited 1× · see citing works
“This bidirectional axis functions through a series of different routes (Bercik et al., 2012; Dinan et al., 2015; Rhee et al., 2009) and comprises an afferent and an efferent pathway.”
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Frodl, T., & O'Keane, V. (2013) · Neurobiology of Disease · doi:10.1016/j.nbd.2012.03.012 · Cited by 555 · see citing works
Antidepressant-Like Effects of the Histone Deacetylase Inhibitor, Sodium Butyrate, in the Mouse
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“Indeed, when administered systemically, sodium butyrate induced a transient histone acetylation in the frontal cortex and hippocampus, resulting in an antidepressant-like behaviour (Schroeder et al., 2007).”
BackgroundInfant 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
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Prenatal stress and long-term consequences: implications of glucocorticoid hormones
Maccari, S., Darnaudéry, M., Morley‐Fletcher, S., Zuena, A. R., Cinque, C., & Reeth, O. V. (2003) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(03)00014-9 · Cited by 529 · cited 1× · see citing works
“In addition to neonatal stress, prenatal stress (PNS) also has powerful and enduring effects on behaviour (Beijers et al., 2010; Frye and Wawrzycki, 2003; Maccari et al., 2003; MorleyFletcher et al., 2003).”
BackgroundVagal immune-to-brain communication: a visceral chemosensory pathway
Goehler, L. E., Gaykema, R. P. A., Hansen, M. K., Anderson, K., Maier, S. F., & Watkins, L. R. (2000) · Autonomic Neuroscience · doi:10.1016/s1566-0702(00)00219-8 · Cited by 525 · cited 1× · see citing works
“The vagus nerve has received much attention as a conduit of signals from the gut to the brain and vice versa (Goehler et al., 2000; Goehler et al., 1999; Goehler et al., 2005).”
BackgroundSocial networks predict gut microbiome composition in wild baboons
Tung, J., Barreiro, L. B., Burns, M. B., Grenier, J., Lynch, J., Grieneisen, L., Jeanne Altmann, A., Alberts, S. C., Blekhman, R., & Archie, E. A. (2015) · eLife · doi:10.7554/elife.05224 · Cited by 524 · cited 2× · see citing works
“The microbiota has been linked to social status across a variety of species including Drosophila (Lize et al., 2014; Venu et al., 2014), bumblebees (Koch and Schmid-Hempel, 2011), hyenas (Theis et al., 2013), non-human primates in the wild (Tung et al., 2015) and rodents.”
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Tryptophan metabolism in the central nervous system: medical implications
Ruddick, J. P., Evans, A. K., Nutt, D. J., Lightman, S. L., Rook, G. A. W., & Lowry, C. A. (2006) · Expert Reviews in Molecular Medicine · doi:10.1017/s1462399406000068 · Cited by 519 · cited 2× · see citing works
“Tryptophan is an essential amino acid and is a precursor to many biologically active agents, such as serotonin (Ruddick et al., 2006).”
BackgroundMicrobiota and host determinants of behavioural phenotype in maternally separated mice
De Palma, G., Blennerhassett, P., Lu, J., Deng, Y., Park, A. J., Green, W., Denou, E., Silva, M. A., Santacruz, A., Sanz, Y., et al. (2015) · Nature Communications · doi:10.1038/ncomms8735 · Cited by 517 · see citing works
Allen, A. P., Hutch, W., Borre, Y. E., Kennedy, P. J., Temko, A., Boylan, G., Murphy, E., Cryan, J. F., Dinan, T. G., & Clarke, G. (2016) · Translational Psychiatry · doi:10.1038/tp.2016.191 · Cited by 513 · see citing works
The microbiota-gut-brain axis in obesity.
Torres-Fuentes, C., Schellekens, H., Dinan, T., & Cryan, J. (2017) · The Lancet Gastroenterology and Hepatology · doi:10.1016/s2468-1253(17)30147-4 · Cited by 506 · see citing works
Metabolism and Circadian Rhythms—Implications for Obesity
Froy, O. (2010) · Endocrine Reviews · doi:10.1210/er.2009-0014 · Cited by 505 · cited 1× · see citing works
“Circadian rhythms regulate several aspects of physiology including metabolism and play a critical role in obesity (Bray and Young, 2007; Froy, 2010).”
BackgroundInfant antibiotic exposures and early-life body mass
Trasande, L., Blustein, J., Liu, M., Corwin, E. J., Cox, L. M., & Blaser, M. J. (2012) · International Journal of Obesity · doi:10.1038/ijo.2012.132 · Cited by 503 · cited 1× · see citing works
“antibiotics during childhood increases the risk of obesity, thus demonstrating that the gut microbiota composition/stability may play a key role in the onset of obesity (Azad et al., 2014; Scott et al., 2016; Trasande et al., 2013).”
BackgroundNeuropeptide, Y, peptide YY and pancreatic polypeptide in the gut-brain axis
Holzer, P., Reichmann, F., & Farzi, A. (2012) · Neuropeptides · doi:10.1016/j.npep.2012.08.005 · Cited by 501 · cited 1× · see citing works
“which the brain regulates the activity of the gut and vice versa and is critical for homeostasis of the host system (De Vadder et al., 2014; Dinan and Cryan, 2017; Holzer et al., 2012; Montiel-Castro et al., 2013; Rhee et al., 2009; Sherwin et al., 2017).”
BackgroundQueipo-Ortuño, M. I., Seoane, L. M., Murri, M., Pardo, M., Gomez-Zumaquero, J. M., Cardona, F., Casanueva, F., & Tinahones, F. J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0065465 · Cited by 497 · cited 1× · see citing works
“33 microbiota composition (Conlon and Bird, 2014; De Filippo et al., 2010; Queipo-Ortuno et al., 2013; Wu et al., 2011); however the converse might also be true.”
BackgroundSex differences in human neonatal social perception
Connellan, J., Baron‐Cohen, S., Wheelwright, S. J., Bátki, A., & Ahluwalia, J. S. (2000) · Infant Behavior and Development · doi:10.1016/s0163-6383(00)00032-1 · Cited by 479 · cited 1× · see citing works
“however, should be interpreted with caution as females girls tend to be more socially driven than males (Christov-Moore et al., 2014; Connellan et al., 2000), therefore some mildly”
BackgroundRole of Corticotropin-Releasing Factor in Drug Addiction
Logrip, M. L., Koob, G. F., & Zorrilla, E. P. (2011) · CNS Drugs · doi:10.2165/11587790-000000000-00000 · Cited by 476 · see citing works
Persistent microbiome alterations modulate the rate of post-dieting weight regain
Thaiss, C. A., Itav, S., Rothschild, D., Meijer, M. T., Levy, M., Moresi, C., Dohnalová, L., Braverman, S., Rozin, S., Malitsky, S., et al. (2016) · Nature · doi:10.1038/nature20796 · Cited by 471 · cited 1× · see citing works
“signature that persisted after successful dieting of obese mice and contributed to faster weight regain upon re-exposure to obesity-promoting factors (Thaiss et al., 2016).”
BackgroundOxytocin in general anxiety and social fear: a translational approach
Neumann, I. D., & Slattery, D. A. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.06.004 · Cited by 468 · cited 1× · see citing works
“As mentioned above, the neuropeptides oxytocin (OXT) and arginine vasopressin (AVP) are key mediators of complex social behaviours including attachment, social recognition and aggression (Dölen et al., 2013; Heinrichs et al., 2009; Neumann and Slattery, 2016).”
BackgroundFSH and testosterone signaling in Sertoli cells
Walker, W. H., & Cheng, J. (2005) · Reproduction · doi:10.1530/rep.1.00358 · Cited by 467 · cited 1× · see citing works
“In males, FSH and LH stimulate the production of testosterone, a hormone required for normal spermatogenesis (Huang et al., 2001; Walker and Cheng, 2005).”
BackgroundProbiotics, gut microbiota and health
Butel, M. J. (2013) · Médecine et Maladies Infectieuses · doi:10.1016/j.medmal.2013.10.002 · Cited by 459 · cited 2× · see citing works
“Probiotics are defined as living micro-organisms that, if administered in adequate amount, confer health benefits to the host (Butel, 2014).”
BackgroundAlcock, J., Maley, C. C., & Aktipis, C. A. (2014) · BioEssays · doi:10.1002/bies.201400071 · Cited by 454 · see citing works
Bezirtzoglou, E., Tsiotsias, A., & Welling, G. W. (2011) · Anaerobe · doi:10.1016/j.anaerobe.2011.03.009 · Cited by 453 · cited 1× · see citing works
“Interestingly, the microbiota of formula-fed infants is significantly different from the microbiota of breastfed infants (Bezirtzoglou et al., 2011; Lee et al., 2015; Wang et al., 2015).”
BackgroundCani, P. D., Dewever, C., & Delzenne, N. M. (2004) · British Journal Of Nutrition · doi:10.1079/bjn20041225 · Cited by 447 · cited 2× · see citing works
“Similarly, food intake, body weight and fat mass were all decreased in male Wistar rats after administration of three different prebiotics (Cani et al., 2004).”
BackgroundGoehler, L. E., Gaykema, R. P. A., Opitz, N., Reddaway, R., Badr, N., & Lyte, M. (2005) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2004.09.002 · Cited by 442 · cited 1× · see citing works
“The vagus nerve has received much attention as a conduit of signals from the gut to the brain and vice versa (Goehler et al., 2000; Goehler et al., 1999; Goehler et al., 2005).”
BackgroundMaternal prenatal stress is associated with the infant intestinal microbiota
Zijlmans, M. A. C., Korpela, K., Riksen-Walraven, J. M., de Vos, W. M., & de Weerth, C. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.01.006 · Cited by 438 · cited 1× · see citing works
“In a population-based study, maternal PNS was positively correlated with the infants' microbiota composition (Zijlmans et al., 2015), reinforcing the idea that PNS can affect microbial”
ResultAit‐Belgnaoui, A., Colom, A., Braniste, V., Ramalho, L., Marrot, A., Cartier, C., Houdeau, E., Theodorou, V., & Tompkins, T. (2014) · Neurogastroenterology & Motility · doi:10.1111/nmo.12295 · Cited by 434 · see citing works
Altered gut microbiota and activity in a murine model of autism spectrum disorders
de Theije, C. G. M., Wopereis, H., Ramadan, M., van Eijndthoven, T., Lambert, J., Knol, J., Garssen, J., Kraneveld, A. D., & Oozeer, R. (2014) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2013.12.005 · Cited by 433 · see citing works
Differences between trait fear and trait anxiety: Implications for psychopathology
Sylvers, P. D., Lilienfeld, S. O., & LaPrairie, J. L. (2010) · Clinical Psychology Review · doi:10.1016/j.cpr.2010.08.004 · Cited by 431 · cited 1× · see citing works
“disproportionate feelings of fear (Sylvers et al., 2011).”
The 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 · see citing works
Bos, P. A., Panksepp, J., Bluthé, R.-M., & Honk, J. V. (2012) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2011.01.002 · Cited by 429 · see citing works
Association of the oxytocin receptor gene (OXTR) in Caucasian children and adolescents with autism
Jacob, S., Brune, C. W., Carter, C. S., Leventhal, B. L., Lord, C., & Cook, E. H. (2007) · Neuroscience Letters · doi:10.1016/j.neulet.2007.02.001 · Cited by 425 · cited 1× · see citing works
“Especially because of its role in mediating social behaviours, oxytocin has been implicated in the aetiology of autism (Jacob et al., 2007; Wermter et al., 2010).”
BackgroundImmune Responses to the Microbiota at the Intestinal Mucosal Surface
Duerkop, B. A., Vaishnava, S., & Hooper, L. V. (2009) · Immunity · doi:10.1016/j.immuni.2009.08.009 · Cited by 424 · cited 15× · see citing works
“In response to stress, the sympathetic nervous system (SNS) increases the release of catecholamines into systemic circulation, while CRF is released from paraventricular neurons of the hypothalamus, which then stimulate the activation of the HPA axis ultimately resulting in a release of glucocorticoids from the adrena…”
BackgroundInfluentialMelancholic microbes: a link between gut microbiota and depression
Dinan, T. G., & Cryan, J. F. (2013) · Neurogastroenterology & Motility · doi:10.1111/nmo.12198 · Cited by 424 · cited 1× · see citing works
“only for the regulation of host physiology, but also for the appropriate development of central nervous system (CNS) and brain responses (Cryan and O'Mahony, 2011; Dinan and Cryan, 2013; Qin et al., 2010b).”
BackgroundModulation of social memory in male rats by neurohypophyseal peptides
Dantzer, R., Bluthe, R. M., Koob, G. F., & Le Moal, M. (1987) · Psychopharmacology · doi:10.1007/bf00518192 · Cited by 423 · see citing works
Microbes and the gut‐brain axis
Bercik, P., Collins, S. M., & Verdu, E. F. (2012) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2012.01906.x · Cited by 417 · cited 1× · see citing works
“This bidirectional axis functions through a series of different routes (Bercik et al., 2012; Dinan et al., 2015; Rhee et al., 2009) and comprises an afferent and an efferent pathway.”
BackgroundCarter, C. S. (1992) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(05)80176-9 · Cited by 417 · cited 1× · see citing works
“These behaviours have been selected for this review because they have been shown to be modulated by neuroendocrine routes (Bos et al., 2012; Carter, 1992; Kosten and Ambrosio, 2002; McCall and Singer, 2012; McEwen and Sapolsky, 1995; Murray et al., 2014; Sirinathsinghji, 1987; Smith et al., 2002;…”
MethodGeneral Background on the Hypothalamic-Pituitary-Thyroid (HPT) Axis
Zoeller, R. T., Tan, S. W., & Tyl, R. W. (2007) · Critical Reviews in Toxicology · doi:10.1080/10408440601123446 · Cited by 416 · cited 1× · see citing works
“The TSH, in turn, stimulates the thyroid to produce T3 and T4 until levels in the blood return to normal (Zoeller et al., 2007).”
BackgroundMaternal separation as a model of brain-gut axis dysfunction
O’Mahony, S. M., Hyland, N. P., Dinan, T. G., & Cryan, J. F. (2011) · Psychopharmacology · doi:10.1007/s00213-010-2010-9 · Cited by 415 · cited 1× · see citing works
“…effects of early life stress exposure in rodents is the maternal separation model, which has been shown to induce long-term changes in behaviour, HPA axis activity and alterations of the intestinal microbiota diversity/complexity (Lehmann et al., 2002; O'Mahony et al., 2011; Plotsky et al., 2005).”
BackgroundThe microbiota-gut-brain axis: neurobehavioral correlates, health and sociality
Montiel-Castro, A. J., González-Cervantes, R. M., Bravo-Ruiseco, G., & Pacheco-López, G. (2013) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2013.00070 · Cited by 413 · see citing works
Role of Monocarboxylate Transporters in Drug Delivery to the Brain
Vijay, N., & Morris, M. (2014) · Current Pharmaceutical Design · doi:10.2174/13816128113199990462 · Cited by 408 · cited 1× · see citing works
“SCFAs act as direct mediators between the gut and the brain in fact they circulate far from their production site and are carried by monocarboxylate transporters, which are expressed also on the blood-brain barrier (BBB) (Kekuda et al., 2013; Nisha Vijay, 2015).”
BackgroundResponses of gut microbiota to diet composition and weight loss in lean and obese mice
Ravussin, Y., Koren, O., Spor, A., LeDuc, C., Gutman, R., Stombaugh, J., Knight, R., Ley, R. E., & Leibel, R. L. (2012) · Obesity · doi:10.1038/oby.2011.111 · Cited by 406 · see citing works
Role of the gut microbiota in host appetite control: bacterial growth to animal feeding behaviour
Fetissov, S. O. (2017) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2016.150 · Cited by 403 · cited 2× · see citing works
“supports the concept that the gastrointestinal microbiota composition and richness may be responsible, together with other factors, for the host eating behaviour and appetite (Alcock et al., 2014; Fetissov, 2017; Goyal et al., 2015; Norris et al., 2013).”
BackgroundOligofructose Promotes Satiety in Rats Fed a High‐Fat Diet: Involvement of Glucagon‐Like Peptide‐1
Cani, P. D., Neyrinck, A. M., Maton, N., & Delzenne, N. M. (2005) · Obesity Research · doi:10.1038/oby.2005.117 · Cited by 382 · cited 1× · see citing works
“, 2012), confirming findings of others (Cani et al., 2004; Cani et al., 2005; Choi et al., 2010).”
Testosterone, Social Class, and Antisocial Behavior in a Sample of 4,462 Men
Dabbs, J. M., & Morris, R. (1990) · Psychological Science · doi:10.1111/j.1467-9280.1990.tb00200.x · Cited by 382 · see citing works
Oligofructose promotes satiety in healthy human: a pilot study
Cani, P. D., Joly, E., Horsmans, Y., & Delzenne, N. M. (2005) · European Journal of Clinical Nutrition · doi:10.1038/sj.ejcn.1602350 · Cited by 381 · cited 1× · see citing works
“satiety, reduced hunger and reduced the desire to ingest food in humans (Cani et al., 2006).”
BackgroundThe Role of Corticotropin-Releasing Factor in Drug Addiction
Sarnyai, Z., Shaham, Y., & Heinrichs, S. C. (2001) · Pharmacological Reviews · doi:10.1016/s0031-6997(24)01492-3 · Cited by 381 · see citing works
Mutlu, E., Keshavarzian, A., Engen, P. A., Forsyth, C. B., Sikaroodi, M., & Gillevet, P. M. (2009) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2009.01022.x · Cited by 371 · see citing works
Bacterial Neuroactive Compounds Produced by Psychobiotics
Wall, R., Cryan, J. F., Ross, R. P., Fitzgerald, G. F., Dinan, T. G., & Stanton, C. (2014) · Advances in experimental medicine and biology · doi:10.1007/978-1-4939-0897-4_10 · Cited by 362 · cited 12× · see citing works
“GABA transporters are localized on the blood-brain barrier (BBB) and allow gut- derived GABA to reach the CNS (Takanaga et al., 2001).”
BackgroundInfluentialGoehler, L. E., Gaykema, R. P. A., Nguyen, K. T., Lee, J. E., Tilders, F. J. H., Maier, S. F., & Watkins, L. R. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-07-02799.1999 · Cited by 357 · cited 1× · see citing works
“The vagus nerve has received much attention as a conduit of signals from the gut to the brain and vice versa (Goehler et al., 2000; Goehler et al., 1999; Goehler et al., 2005).”
BackgroundSanchez, M., Darimont, C., Drapeau, V., Emady-Azar, S., Lepage, M., Rezzonico, E., Ngom-Bru, C., Berger, B., Philippe, L., Ammon-Zuffrey, C., et al. (2014) · British Journal of Nutrition · doi:10.1017/s0007114513003875 · Cited by 351 · cited 1× · see citing works
“reductions in circulating leptin concentrations (Sanchez et al., 2014).”
Tannock, G. W., & Savage, D. C. (1974) · Infection and Immunity · doi:10.1128/iai.9.3.591-598.1974 · Cited by 349 · cited 1× · see citing works
“intestinal microbial populations in mice (Tannock and Savage, 1974).”
Glucocorticoids, stress, and fertility.
Whirledge, S., & Cidlowski, J. A. (2010) · PubMed · Cited by 347 · see citing works
Prenatal Stress Alters Bacterial Colonization of the Gut in Infant Monkeys
Bailey, M. T., Lubach, G. R., & Coe, C. L. (2004) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/00005176-200404000-00009 · Cited by 339 · see citing works
Recent developments in understanding the role of the gut microbiota in brain health and disease
Sherwin, E., Dinan, T. G., & Cryan, J. F. (2018) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.13416 · Cited by 338 · cited 1× · see citing works
“which the brain regulates the activity of the gut and vice versa and is critical for homeostasis of the host system (De Vadder et al., 2014; Dinan and Cryan, 2017; Holzer et al., 2012; Montiel-Castro et al., 2013; Rhee et al., 2009; Sherwin et al., 2017).”
BackgroundBailey, M. T., Dowd, S. E., Parry, N. M. A., Galley, J. D., Schauer, D. B., & Lyte, M. (2010) · Infection and Immunity · doi:10.1128/iai.00862-09 · Cited by 335 · cited 2× · see citing works
“29 enteric pathogen Citrobacter rodentium (Bailey et al., 2010).”
BackgroundInfant antibiotic exposure and the development of childhood overweight and central adiposity
Azad, M. B., Bridgman, S. L., Becker, A. B., & Kozyrskyj, A. L. (2014) · International Journal of Obesity · doi:10.1038/ijo.2014.119 · Cited by 331 · cited 4× · see citing works
“…et al. demonstrated that germ-free mice have less total body fat than conventionally reared mice and the colonisation of germ-free mice with a caecal microbiota harvested from conventionally raised animals produces an increase in body fat content and insulin resistance (Backhed et al., 2004).”
BackgroundInfluentialNeurotransmitters as food supplements: the effects of GABA on brain and behavior
Boonstra, E., de Kleijn, R., Colzato, L. S., Alkemade, A., Forstmann, B. U., & Nieuwenhuis, S. (2015) · Frontiers in Psychology · doi:10.3389/fpsyg.2015.01520 · Cited by 330 · cited 1× · see citing works
“Whether the peripherally derived GABA is capable of crossing the BBB either through diffusion or through active transport remains a matter of dispute (Boonstra et al., 2015).”
BackgroundThyroid hormones, brain function and cognition: a brief review
Smith, J. A. (2002) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(01)00037-9 · Cited by 321 · see citing works
Breton, J., Tennoune, N., Lucas, N., Francois, M., Legrand, R., Jacquemot, J., Goichon, A., Guérin, C., Peltier, J., Pestel-Caron, M., et al. (2016) · Cell Metabolism · doi:10.1016/j.cmet.2015.10.017 · Cited by 321 · cited 2× · see citing works
“coli proteins was able to increase plasma PYY and GLP-1 levels enhancing satiety (Breton et al., 2016).”
BackgroundThe HPA and immune axes in stress: the involvement of the serotonergic system
Leonard, B. E. (2005) · European Psychiatry · doi:10.1016/s0924-9338(05)80180-4 · Cited by 317 · cited 2× · see citing works
“the immune system (Leonard, 2005) and the gonadal axis (Viau, 2002).”
BackgroundAlmey, A., Milner, T. A., & Brake, W. G. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.06.010 · Cited by 315 · see citing works
Luoto, R., Kalliomäki, M. A., Laitinen, K., & Isolauri, E. (2010) · International Journal of Obesity · doi:10.1038/ijo.2010.50 · Cited by 315 · cited 1× · see citing works
“rhamnosus administered to pregnant women has been found to modify the standard of weight gain in children during the first six months of life (Luoto et al., 2010) with no evidence, however, that this effect is mediated by the”
BackgroundCommensal bacteria and essential amino acids control food choice behavior and reproduction
Leitão-Gonçalves, R., Carvalho-Santos, Z., Francisco, A. P., Fioreze, G. T., Anjos, M., Baltazar, C., Elias, A. P., Itskov, P. M., Piper, M. D. W., & Ribeiro, C. (2017) · PLOS Biology · doi:10.1371/journal.pbio.2000862 · Cited by 315 · cited 2× · see citing works
“Specifically, the gut bacteria species that suppress protein appetite are Acetobacter pomorum and Lactobacilli (Leitao-Goncalves et al., 2017).”
BackgroundProgramming infant gut microbiota: influence of dietary and environmental factors
Marques, T. M., Wall, R., Ross, R. P., Fitzgerald, G. F., Ryan, C. A., & Stanton, C. (2010) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2010.03.020 · Cited by 314 · see citing works
Mack, I., Cuntz, U., Grämer, C., Niedermaier, S., Pohl, C., Schwiertz, A., Zimmermann, K., Zipfel, S., Enck, P., & Penders, J. (2016) · Scientific Reports · doi:10.1038/srep26752 · Cited by 313 · cited 2× · see citing works
“Interestingly, the microbial perturbations and gastrointestinal symptoms seen in anorexic patients did not recover after weight gain and/or normalisation of eating behaviour (Mack et al., 2016).”
BackgroundLê, A. D., Harding, S. E., Juzytsch, W., Watchus, J., Shalev, U., & Shaham, Y. (2000) · Psychopharmacology · doi:10.1007/s002130000411 · Cited by 310 · see citing works
Microbial symbionts accelerate wound healing via the neuropeptide hormone oxytocin
Poutahidis, T., Kearney, S. M., Levkovich, T., Qi, P., Varian, B. J., Lakritz, J. R., Ibrahim, Y. M., Chatzigiagkos, A., Alm, E. J., & Erdman, S. E. (2013) · PLoS ONE · doi:10.1371/journal.pone.0078898 · Cited by 310 · cited 2× · see citing works
“40 suggests that the gut microbiota is able to directly modulate the levels of host oxytocin (Poutahidis et al., 2013; Varian et al., 2017) and so it is interesting to speculate as to whether”
BackgroundShaham, Y., Funk, D., Erb, S., Brown, T. J., Walker, C.-D., & Stewart, J. (1997) · The Journal of Neuroscience · doi:10.1523/jneurosci.17-07-02605.1997 · Cited by 308 · cited 1× · see citing works
“In contrast, shock-induced reinstatement of heroin or alcohol seeking depends on CRF, but not on corticosterone (Le et al., 2000; O'Callaghan et al., 2005; Shaham et al., 1997).”
Background
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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
Global Impacts of Western Diet and Its Effects on Metabolism and Health: A Narrative Review
Clemente‐Suárez, V. J., Beltrán-Velasco, A. I., Redondo-Flórez, L., Martín-Rodríguez, A., & Tornero-Aguilera, J. F. (2023) · Nutrients · doi:10.3390/nu15122749 · Cited by 873 · see citing works
Impact of microbiota on central nervous system and neurological diseases: the gut-brain axis
Ma, Q., Xing, C., Long, W., Wang, H. Y., Liu, Q., & Wang, R. (2019) · Journal of Neuroinflammation · doi:10.1186/s12974-019-1434-3 · Cited by 752 · see citing works
“A notable role of human digestive system in brain development has been proposed [15, 50].”
BackgroundGut Microbiota and Energy Homeostasis in Fish
Butt, R. L., & Volkoff, H. (2019) · Frontiers in Endocrinology · doi:10.3389/fendo.2019.00009 · Cited by 621 · see citing works
McGuinness, A. J., Davis, J. A., Dawson, S. L., Loughman, A., Collier, F., O’Hely, M., Simpson, C. A., Green, J., Marx, W., Hair, C., et al. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01456-3 · Cited by 502 · see citing works
“They influence many aspects of physiology via neural, hormonal and immunological pathways [1, 2], so much so that some describe the gut microbiome as a ‘virtual organ’ [3, 4].”
BackgroundThe microbiota–gut–brain axis and neurodevelopmental disorders
Wang, Q., Yang, Q., & Liu, X. (2023) · Protein & Cell · doi:10.1093/procel/pwad026 · Cited by 407 · see citing works
The HPA axis dysregulation in severe mental illness: Can we shift the blame to gut microbiota?
Misiak, B., Łoniewski, I., Marlicz, W., Frydecka, D., Szulc, A., Rudzki, L., & Samochowiec, J. (2020) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2020.109951 · Cited by 343 · see citing works
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
The gut microbiota-immune-brain axis: therapeutic implications
O’Riordan, K. J., Moloney, G. M., Keane, L., Clarke, G., & Cryan, J. F. (2025) · Cell Reports Medicine · doi:10.1016/j.xcrm.2025.101982 · Cited by 333 · see citing works
“32 Immune-HPA interactions, demonstrated through microbial translocation and inflam-matory cytokine activation, underscore the gut microbiota’s role in HPA signaling.”
Xu, M., Xu, X., Li, J., & Li, F. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.00473 · Cited by 309 · see citing works
The Gut Microbiome Influences Host Endocrine Functions
Rastelli, M., Cani, P. D., & Knauf, C. (2019) · Endocrine Reviews · doi:10.1210/er.2018-00280 · Cited by 315 · see citing works
Gut-Brain Psychology: Rethinking Psychology From the Microbiota–Gut–Brain Axis
Liang, S., Wu, X., & Jin, F. (2018) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2018.00033 · Cited by 269 · see citing works
Obesity and gut–microbiota–brain axis: A narrative review
Asadi, A., Mehr, N. S., Mohamadi, M. H., Shokri, F., Heidary, M., Sadeghifard, N., & Khoshnood, S. (2022) · Journal of Clinical Laboratory Analysis · doi:10.1002/jcla.24420 · Cited by 254 · see citing works
Gut Microbiota and Their Neuroinflammatory Implications in Alzheimer’s Disease
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“Accumulating evidence suggests that the composition of the gut microbiota may also have a role in several other metabolic conditions involving the CNS [42,43].”
BackgroundFrom correlation to causality: the case of Subdoligranulum
Hul, M. V., Roy, T. L., Prifti, E., Dao, M. C., Paquot, A., Zucker, J., Delzenne, N. M., Muccioli, G. G., Clément, K., & Cani, P. D. (2020) · Gut Microbes · doi:10.1080/19490976.2020.1849998 · Cited by 221 · see citing works
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You’ve got male: Sex and the microbiota-gut-brain axis across the lifespan
Jaggar, M., Rea, K., Spichak, S., Dinan, T. G., & Cryan, J. F. (2020) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2019.100815 · Cited by 200 · see citing works
Self-citationWhen Rhythms Meet the Blues: Circadian Interactions with the Microbiota-Gut-Brain Axis
Teichman, E. M., O’Riordan, K. J., Gahan, C. G. M., Dinan, T. G., & Cryan, J. F. (2020) · Cell Metabolism · doi:10.1016/j.cmet.2020.02.008 · Cited by 198 · see citing works
Key role of gut microbiota in anhedonia-like phenotype in rodents with neuropathic pain
Yang, C., Fang, X., Zhan, G., Huang, N., Li, S., Bi, J., Jiang, R., Yang, L., Miao, L., Zhu, B., et al. (2019) · Translational Psychiatry · doi:10.1038/s41398-019-0379-8 · Cited by 176 · see citing works
Snigdha, S., Ha, K., Tsai, P., Dinan, T. G., Bartos, J. D., & Shahid, M. (2021) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2021.107978 · Cited by 171 · see citing works
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“It has been proposed that cross-talk between the gut and brain may impact several neurological [58] and behavioral [59] disorders.”
BackgroundThe Gut Microbiome and Sex Hormone-Related Diseases
He, S., Li, H., Yu, Z., Zhang, F., Liang, S., Liu, H., Chen, H., & Lü, M. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.711137 · Cited by 176 · see citing works
Checa-Ros, A., Jeréz-Calero, A., Molina-Carballo, A., Campoy, C., & Muñoz-Hoyos, A. (2021) · Nutrients · doi:10.3390/nu13010249 · Cited by 164 · see citing works
“The gut microbiome directly influences the production of glucocorticoids and immune mediators, such as tumor necrosis factor-alpha (TNF-α) and interleukins-1beta and 6 (IL-1β and IL-6), which in turn stimulates the HPA axis [69].”
BackgroundSepsis‐Induced Brain Dysfunction: Pathogenesis, Diagnosis, and Treatment
Pan, S., Lv, Z., Wang, R., Shu, H., Yuan, S., Yu, Y., & Shang, Y. (2022) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2022/1328729 · Cited by 160 · see citing works
“And other di ff erent kinds of hormones induced by enteroendo-crine cells also transmit peripheral in fl ammatory signals through the vagus nerve to the autonomic nervous system nucleus, neuroendocrine centers, and behavioral centers, driving corresponding changes [66, 74 – 76].”
Microbiota‐gut‐brain axis as a regulator of reward processes
García‐Cabrerizo, R., Carbia, C., O’Riordan, K. J., Schellekens, H., & Cryan, J. F. (2020) · Journal of Neurochemistry · doi:10.1111/jnc.15284 · Cited by 147 · see citing works
“Numerous preclinical evidence show that the intestinal microbiota can be altered under different chronic psychosocial stressors (Cussotto et al., 2018).”
BackgroundThe Relationship Between the Gut Microbiome-Immune System-Brain Axis and Major Depressive Disorder
Foster, J. A., Baker, G. B., & Dursun, S. M. (2021) · Frontiers in Neurology · doi:10.3389/fneur.2021.721126 · Cited by 153 · see citing works
“For example, exposure to various types of stress has been reported to alter the microbiota profile, and alteration of the gut microbiota can affect responses to stress, anxiety-like behavior and, as described below, activation of the hypothalamicpituitary-adrenal (HPA) axis [reviews: (40, 44)].”
BackgroundLignans and Gut Microbiota: An Interplay Revealing Potential Health Implications
Senizza, A., Rocchetti, G., Mosele, J. I., Patrone, V., Callegari, M. L., Morelli, L., & Lucini, L. (2020) · Molecules · doi:10.3390/molecules25235709 · Cited by 132 · see citing works
Spichak, S., Bastiaanssen, T. F. S., Berding, K., Vlckova, K., Clarke, G., Dinan, T. G., & Cryan, J. F. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.02.044 · Cited by 127 · see citing works
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“The gut microbiome also appears to be essential for the successful development of the HPA axis [106], with a developing microbiome stimulating inflammatory markers such as TNF-α , IL-1 β , and IL-6, which help mature the HPA axis [107]. and IL-6, which help mature the HPA axis [107].”
Pesticide exposure and the microbiota-gut-brain axis
Matsuzaki, R., Gunnigle, E., Geissen, V., Clarke, G. A., Nagpal, J. K., & Cryan, J. F. (2023) · The ISME Journal · doi:10.1038/s41396-023-01450-9 · Cited by 117 · see citing works
“, HPA axis), neuronal and immune pathways [46].”
BackgroundWang, S., Ishima, T., Qu, Y., Shan, J., Chang, L., Wei, Y., Zhang, J., Pu, Y., Fujita, Y., Tan, Y., et al. (2021) · Journal of Affective Disorders · doi:10.1016/j.jad.2021.06.006 · Cited by 116 · see citing works
Tirelle, P., Breton, J., Riou, G., Déchelotte, P., Coëffier, M., & Ribet, D. (2020) · BMC Microbiology · doi:10.1186/s12866-020-02018-9 · Cited by 113 · see citing works
Li, J., Fang, B., Pang, G., Zhang, M., & Ren, F. (2019) · Pesticide Biochemistry and Physiology · doi:10.1016/j.pestbp.2019.05.018 · Cited by 104 · see citing works
Wang, Y., An, Y., Ma, W., Yu, H., Lu, Y., Zhang, X., Wang, Y., Liu, W., Wang, T., & Xiao, R. (2020) · Journal of Neuroinflammation · doi:10.1186/s12974-020-01873-7 · Cited by 103 · see citing works
Visceral pain: gut microbiota, a new hope?
Pusceddu, M. M., & Gareau, M. G. (2018) · Journal of Biomedical Science · doi:10.1186/s12929-018-0476-7 · Cited by 100 · see citing works
Shobeiri, P., Kalantari, A., Teixeira, A. L., & Rezaei, N. (2022) · Biology of Sex Differences · doi:10.1186/s13293-022-00422-6 · Cited by 105 · see citing works
“Several studies reported on the potential mechanisms of microbiome–CNS crosstalk, including endocrine [28], the vagus nerve [29, 30], immune [31, 32] and neuropeptide/neurotransmitter systems [33, 34], and signaling molecules.”
BackgroundZhang, K., Fujita, Y., Chang, L., Qu, Y., Pu, Y., Wang, S., Shirayama, Y., & Hashimoto, K. (2019) · Translational Psychiatry · doi:10.1038/s41398-019-0571-x · Cited by 98 · see citing works
Wang, S., Qu, Y., Chang, L., Pu, Y., Zhang, K., & Hashimoto, K. (2019) · Journal of Affective Disorders · doi:10.1016/j.jad.2019.09.064 · Cited by 94 · see citing works
The effects of gut microbiota on appetite regulation and the underlying mechanisms
Yu, M., Yu, B., & Chen, D. (2024) · Gut Microbes · doi:10.1080/19490976.2024.2414796 · Cited by 98 · see citing works
“20,21 The gut microbiota plays a pivotal role in the regulation of appetite, as they can modulate physiological processes including insulin sensitivity, glucose homeostasis, and the balance of energy intake through the production of metabolites like short-chain fatty acids (SCFAs).”
BackgroundComplementary Feeding Methods—A Review of the Benefits and Risks
Boswell, N. (2021) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph18137165 · Cited by 93 · see citing works
Wang, J., Yang, Y., Shi, Y., Wei, L., Gao, L., & Liu, M. (2024) · Environment International · doi:10.1016/j.envint.2024.108523 · Cited by 96 · see citing works
The microbiota-gut-brain axis: Focus on the fundamental communication pathways
Bistoletti, M., Bosi, A., Banfi, D., Giaroni, C., & Baj, A. (2020) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2020.08.012 · Cited by 88 · see citing works
Pavlovian Conditioning of Immunological and Neuroendocrine Functions
Hadamitzky, M., Lückemann, L., Pacheco‐López, G., & Schedlowski, M. (2019) · Physiological Reviews · doi:10.1152/physrev.00033.2018 · Cited by 87 · see citing works
Xiao, S., Jiang, S., Qian, D., & Duan, J. (2019) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-019-10312-4 · Cited by 84 · see citing works
Baldi, S., Mundula, T., Nannini, G., & Amedei, A. (2021) · World Journal of Gastroenterology · doi:10.3748/wjg.v27.i39.6715 · Cited by 85 · see citing works
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A biological framework for emotional dysregulation in alcohol misuse: from gut to brain
Carbia, C., Lannoy, S., Maurage, P., López‐Caneda, E., O’Riordan, K. J., Dinan, T. G., & Cryan, J. F. (2020) · Molecular Psychiatry · doi:10.1038/s41380-020-00970-6 · Cited by 80 · see citing works
Ağagündüz, D., Bingöl, F. G., Çelik, E., Cemali, Ö., Özenir, Ç., Özoğul, F., & Capasso, R. (2022) · Journal of Translational Medicine · doi:10.1186/s12967-022-03609-y · Cited by 79 · see citing works
Regulation of endocrine systems by the microbiome: Perspectives from comparative animal models
Williams, C. L., García‐Reyero, N., Martyniuk, C. J., Tubbs, C. W., & Bisesi, J. H. (2020) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2020.113437 · Cited by 75 · see citing works
Guo, L., Xiao, P., Zhang, X., Yang, Y., Yang, M., Wang, T., Lu, H., Tian, H., Wang, H., & Liu, J. (2021) · Food & Function · doi:10.1039/d0fo02778b · Cited by 74 · see citing works
Precocious puberty and microbiota: The role of the sex hormone–gut microbiome axis
Calcaterra, V., Rossi, V., Massini, G., Regalbuto, C., Hruby, C., Panelli, S., Bandi, C., & Zuccotti, G. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.1000919 · Cited by 77 · see citing works
“More studies on humans are needed to better understand the underlying mechanisms of this axis (4, 75).”
BackgroundAcne and Stress: Impact of Catecholamines on Cutibacterium acnes
Borrel, V., THOMAS, P. A., Catovic, C., Racine, P., Konto‐Ghiorghi, Y., Lefeuvre, L., Poc, C. D., Zouboulis, C. C., & Feuilloley, M. G. J. (2019) · Frontiers in Medicine · doi:10.3389/fmed.2019.00155 · Cited by 70 · see citing works
Curcumin Alleviates DSS‐Induced Anxiety‐Like Behaviors via the Microbial‐Brain‐Gut Axis
Zhang, F., Zhou, Y., Chen, H., Jiang, H., Zhou, F., Lü, B., & Xu, M. (2022) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2022/6244757 · Cited by 69 · see citing works
“Therefore, some scholars suggest the MGB axis, which involves bidirectional communication between the microbiota and brain [12].”
BackgroundWu, Y., Wang, Y., Hu, A., Shu, X., Huang, W., Liu, J., Wang, B., Zhang, R., Yue, M., & Yang, C. (2022) · Frontiers in Nutrition · doi:10.3389/fnut.2022.946096 · Cited by 69 · see citing works
The role of the gut microbiome in opioid use
Ren, M., & Lotfipour, S. (2019) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000538 · Cited by 68 · see citing works
“An abundance of evidence in both humans and animals supports an essential role of gut microbiota in regulating brain function, mood, stress, and behavioral responses to rewards, including food and drugs of abuse (Collins and Bercik, 2009; Diaz Heijtz et al., 2011; Clarke et al., 2013; Selkrig et al., 2014; Cussotto et…”
BackgroundSun, Y., Zeng, X., Liu, Y., Zhan, S., Wu, Z., Zheng, X., & Zhang, X. (2022) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2022.07.090 · Cited by 68 · see citing works
Neuroinflammation, Microbiota-Gut-Brain Axis, and Depression: The Vicious Circle
Reyes-Martínez, S., Segura-Real, L., Gómez-García, A. P., Tesoro-Cruz, E., Constantino-Jonapa, L. A., Amedei, A., & Aguirre‐García, M. M. (2023) · Journal of Integrative Neuroscience · doi:10.31083/j.jin2203065 · Cited by 76 · see citing works
Traina, G. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00345 · Cited by 69 · see citing works
Flux, M. C., & Lowry, C. A. (2019) · Neurobiology of Disease · doi:10.1016/j.nbd.2019.104578 · Cited by 68 · see citing works
Zyoud, S. H., Smale, S., Waring, W. S., Sweileh, W. M., & Al‐Jabi, S. W. (2019) · BMC Gastroenterology · doi:10.1186/s12876-019-1076-z · Cited by 68 · see citing works
The Role of the Gut-Brain Axis in Attention-Deficit/Hyperactivity Disorder
Dam, S. A., Mostert, J. C., Szopinska-Tokov, J., Bloemendaal, M., Amato, M. P., & Vásquez, A. A. (2019) · Gastroenterology Clinics of North America · doi:10.1016/j.gtc.2019.05.001 · Cited by 63 · see citing works
Tomizawa, Y., Kurokawa, S., Ishii, D., Miyaho, K., Ishii, C., Sanada, K., Fukuda, S., Mimura, M., & Kishimoto, T. (2020) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyaa070 · Cited by 62 · see citing works
“A previous animal study reported a significant difference in specific species composition between rats treated with escitalopram and those receiving vehicle, while the beta diversity in principal coordinate analysis did not differ significantly (Cussotto et al., 2018).”
ResultGut microbiota and neuropsychiatric disorders: Implications for neuroendocrine-immune regulation
Ge, T., Yao, X., Zhao, H., Yang, W., Zou, X., Peng, F., Li, B., & Cui, R. (2021) · Pharmacological Research · doi:10.1016/j.phrs.2021.105909 · Cited by 62 · see citing works
Mood‐related central and peripheral clocks
Ketchesin, K. D., Becker‐Krail, D. D., & McClung, C. A. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.14253 · Cited by 60 · see citing works
“Short- chain fatty acids, such as butyrate, acetate, and propionate, are common metabolic byproducts released by gut microbiota and have been shown to alter host immune responses, metabolism, and neurotransmitter synthesis (Cussotto et al., 2018; Rogers et al., 2016).”
BackgroundInfluentialThe contribution of age-related changes in the gut-brain axis to neurological disorders
Khan, R., Gesù, C. M. D., Lee, J., & McCullough, L. D. (2024) · Gut Microbes · doi:10.1080/19490976.2024.2302801 · Cited by 60 · see citing works
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Chemogenetics defines a short-chain fatty acid receptor gut–brain axis
Barki, N., Bolognini, D., Börjesson, U., Jenkins, L., Riddell, J. S., Hughes, D. I., Ulven, T., Hudson, B. D., Ulven, E. R., Dekker, N., et al. (2022) · eLife · doi:10.7554/elife.73777 · Cited by 57 · see citing works
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“Gut microbes can bidirectionally interact with the brain through autonomic neurotransmitters and metabolites; thus, the concept of the “microbiota-gut-brain” axis has been widely accepted in recent years [13].”
BackgroundChiu, L., & Gilbert, S. F. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-817996-3.00015-3 · Cited by 55 · see citing works
The gut–brain axis in vertebrates: implications for food intake regulation
Blanco, A. M., Calo, J., & Soengas, J. L. (2021) · Journal of Experimental Biology · doi:10.1242/jeb.231571 · Cited by 55 · see citing works
Wang, J., Qin, Y., Wu, Q., Zeng, D., Gao, X., Wang, Q., Li, Z., Ni, Y., Li, H., Zhang, P., et al. (2025) · Nature Medicine · doi:10.1038/s41591-025-03724-5 · Cited by 56 · see citing works
The gut microbiome, immune modulation, and cognitive decline: insights on the gut-brain axis
Zhang, R., Ding, N., Feng, X., & Liao, W. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1529958 · Cited by 56 · see citing works
Zhao, Q., Chen, J., Wu, M., Yin, X., Jiang, Q., Gao, H., & Zheng, H. (2023) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2023.110638 · Cited by 49 · see citing works
Leung, R., & Covașă, M. (2021) · Nutrients · doi:10.3390/nu13082581 · Cited by 50 · see citing works
“Increasing evidence suggests that these gut microbes affect endocrine functions through two pathways: directly through the production of bioactive metabolites like SCFAs, and indirectly, as modulators of inflammatory responses, immune responses and hormonal secretion [85].”
BackgroundA brief period of sleep deprivation leads to subtle changes in mouse gut microbiota
Aidy, S. E., Bolsius, Y. G., Raven, F., & Havekes, R. (2019) · Journal of Sleep Research · doi:10.1111/jsr.12920 · Cited by 50 · see citing works
Qu, Y., Zhang, K., Pu, Y., Chang, L., Wang, S., Tan, Y., Wang, X., Zhang, J., Ohnishi, T., Yoshikawa, T., et al. (2020) · Journal of Affective Disorders · doi:10.1016/j.jad.2020.03.095 · Cited by 50 · see citing works
The human microbiome in sickness and in health
Requena, T., & Velasco, M. (2020) · Revista Clínica Española (English Edition) · doi:10.1016/j.rceng.2019.07.018 · Cited by 51 · see citing works
Human Gut Microbiota for Diagnosis and Treatment of Depression
Averina, O. V., Poluektova, E. U., Zorkina, Y., Kovtun, A. S., & Даниленко, В. Н. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25115782 · Cited by 53 · see citing works
“The HPA axis is one of the main axes of the endocrine system [75], which regulates the effectiveness and release of monoamine neurotransmitters, changes the content of the brain-derived neurotrophic factor (BDNF) and activates immune responses and systemic inflammation.”
BackgroundKumar, A., Mehan, S., Tiwari, A., Khan, Z., Gupta, G. D., Narula, A. S., & Samant, R. (2024) · Current Pharmaceutical Design · doi:10.2174/0113816128321466240816075041 · Cited by 52 · see citing works
Microglia and gut microbiota: A double-edged sword in Alzheimer's disease
Bano, N., Khan, S., Ahamad, S., Kanshana, J. S., Dar, N. J., Khan, S. J., Nazir, A., & Bhat, S. A. (2024) · Ageing Research Reviews · doi:10.1016/j.arr.2024.102515 · Cited by 49 · see citing works
Birth signalling hormones and the developmental consequences of caesarean delivery
Kenkel, W. M. (2020) · Journal of Neuroendocrinology · doi:10.1111/jne.12912 · Cited by 45 · see citing works
MacKay, M., Yang, B. H., Dursun, S. M., & Baker, G. B. (2023) · Current Neuropharmacology · doi:10.2174/1570159x21666230222092029 · Cited by 44 · see citing works
“Much still remains to be known about how metabolites formed by the gut microbiota that do not cross the BBB affect the brain, although studies on interactions with the vagus nerve are providing important information [20, 34, 107].”
BackgroundLee, K., Kim, J.-K., & Kim, D. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.564271 · Cited by 44 · see citing works
Thomann, A., Mak, J. W. Y., Zhang, J., Wüstenberg, T., Ebert, M. P., Sung, J. J. �., Bernstein, C. N., Reindl, W., & Ng, S. C. (2020) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.15787 · Cited by 44 · see citing works
Microbioma humano en la salud y la enfermedad
Requena, T., & Velasco, M. (2019) · Revista Clínica Española · doi:10.1016/j.rce.2019.07.004 · Cited by 42 · see citing works
Short Bowel Syndrome: A Paradigm for Intestinal Adaptation to Nutrition?
Beyec, J. L., Billiauws, L., Bado, A., Joly, F., & Gall, M. L. (2020) · Annual Review of Nutrition · doi:10.1146/annurev-nutr-011720-122203 · Cited by 42 · see citing works
Biyong, E. F., Alfos, S., Dumetz, F., Helbling, J., Aubert, A., Brossaud, J., Foury, A., Moisan, M., Layé, S., Richard, E., et al. (2020) · International Journal of Obesity · doi:10.1038/s41366-020-00723-z · Cited by 42 · see citing works
A Biopsychosocial Overview of the Opioid Crisis: Considering Nutrition and Gastrointestinal Health
Wiss, D. A. (2019) · Frontiers in Public Health · doi:10.3389/fpubh.2019.00193 · Cited by 41 · see citing works
“The question is: how is the microbiome linked to AUD or SUD? This emerging topic considers neuroendocrine pathways that are involved in addiction, where gut microbiota may play a causal role (139).”
BackgroundKeady, M., Prado, N. A., Lim, H. C., Brown, J. L., Paris, S., & Muletz‐Wolz, C. R. (2021) · Animal Microbiome · doi:10.1186/s42523-021-00146-9 · Cited by 41 · see citing works
Scheepers, I. M., Cryan, J. F., Bastiaanssen, T. F. S., Rea, K., Clarke, G. A., Jaspan, H. B., Harvey, B. H., Hemmings, S. M. J., Santana, L., van der Sluis, R., et al. (2019) · European Journal of Neuroscience · doi:10.1111/ejn.14610 · Cited by 41 · see citing works
Inflammation in Mental Disorders: Is the Microbiota the Missing Link?
Marin, S., Hé, Y., Butler, K., & Tsuang, M. T. (2020) · Neuroscience Bulletin · doi:10.1007/s12264-020-00535-1 · Cited by 41 · see citing works
The role of mast cells in the gut and brain
Traina, G. (2021) · Journal of Integrative Neuroscience · doi:10.31083/j.jin.2021.01.313 · Cited by 42 · see citing works
“The intestinal microbiota influences behaviors and neural functions [19].”
BackgroundGut Microbiota Profiles in Children and Adolescents with Psychiatric Disorders
Šoltýsová, M., Tomova, A., & Ostatníková, D. (2022) · Microorganisms · doi:10.3390/microorganisms10102009 · Cited by 44 · see citing works
“Gut bacteria can also produce NTs or can stimulate their production in the host organism, as summarized by several authors [1,15,16].”
BackgroundPatel, J. K., Chaudhary, H., Rajput, K. N., Parekh, B., & Joshi, R. G. (2023) · Scientific Reports · doi:10.1038/s41598-023-39168-5 · Cited by 39 · see citing works
Kumar, N., Sahoo, N. K., Mehan, S., & verma, B. (2023) · Multiple Sclerosis and Related Disorders · doi:10.1016/j.msard.2023.104547 · Cited by 40 · see citing works
Amorim, N. M. L., McGovern, E., Raposo, A. E., Khatiwada, S., Shen, S., Koentgen, S., Hold, G. L., Behary, J., El-Omar, E. M., & Zekry, A. (2022) · Frontiers in Medicine · doi:10.3389/fmed.2022.770017 · Cited by 38 · see citing works
Avolio, E., Olivito, I., Rosina, E., Romano, L., Angelone, T., Bartolo, A. D., Scimeca, M., Bellizzi, D., D’Aquila, P., Passarino, G., et al. (2022) · Neuroscience · doi:10.1016/j.neuroscience.2022.06.038 · Cited by 40 · see citing works
Gut microbiota and its roles in the pathogenesis and therapy of endocrine system diseases
Wu, Z., Tian, E., Chen, Y., Dong, Z., & Peng, Q. (2022) · Microbiological Research · doi:10.1016/j.micres.2022.127291 · Cited by 39 · see citing works
The critical role of gut-brain axis microbiome in mental disorders
Basiji, K., Sendani, A. A., Ghavami, S. B., Farmani, M., Kazemifard, N., Sadeghi, A., Lotfali, E., & Aghdaei, H. A. (2023) · Metabolic Brain Disease · doi:10.1007/s11011-023-01248-w · Cited by 36 · see citing works
“HPA is one of the main endocrine system axis (Cussotto et al. 2018 ), that regulates the effi - cacy and release of monoamine neurotransmitters, modifies the abundance of BDNF, and activates immune responses and systemic inflammation.”
BackgroundGut microbiota in obesity and related complications: Unveiling the complex interplay
Islam, M. M., Islam, M. M., Rahman, M. A., Ripon, M. A. R., & Hossain, M. S. (2023) · Life Sciences · doi:10.1016/j.lfs.2023.122211 · Cited by 36 · see citing works
- Authors
- Cussotto, S., Sandhu, K. V., Dinan, T. G., & Cryan, J. F.
- Affiliations
- University College Cork (IE)
- Corresponding author
- Cryan, John F.
- Venue
- Frontiers in Neuroendocrinology
- Publisher
- Elsevier BV
- Published
- 2018-10
- Volume
- 51
- Pages
- 80-101
- ISSN
- 0091-3022 (ISSN-L)
- OpenAlex
- W2804326576
- Cited by
- 326
- References
- 407
- Citations by year
- 2026: 17 · 2025: 43 · 2024: 53 · 2023: 43 · 2022: 54 · 2021: 36 · 2020: 43 · 2019: 32 · 2018: 5
- FWCI
- 2.84
- Type
- journal article
- Language
- en
- Open access
- green
- hdl.handle.net
- Licence
- Locations
- Frontiers in Neuroendocrinology (publishedVersion)
- PubMed (publishedVersion)
- Arrow@dit (Dublin Institute of Technology) (submittedVersion, cc-by-nc-nd)
- 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 › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
- Keywords
- gut microbiota, gut-brain axis, neuroendocrine system, behavioral responses, stress, eating behaviour, sexual behavior, social behavior, cognition, addiction, host-microbe interactions
- MeSH terms
- Gastrointestinal Microbiome, Animals, Brain, Feeding Behavior, Humans, Learning, Neurosecretory Systems, Sexual Behavior, Social Behavior, Stress, Psychological, Behavior, Addictive
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