Cited by 326Gut microbiota and healthGastrointestinal motility and disordersRegulation of Appetite and Obesity

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The Neuroendocrinology of the Microbiota-Gut-Brain Axis: A Behavioural Perspective

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Cussotto, Sofia, Sandhu, Kiran V., Dinan, Timothy G., Cryan, John F.·2018·Frontiers in Neuroendocrinology

DOI 10.1016/j.yfrne.2018.04.002

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Abstract

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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Background
Short chain fatty acids in the human colon.
Cummings, J. H. (1981) · Gut · doi:10.1136/gut.22.9.763 · Cited by 1,049 · cited 1×
“Butyric, propionic and acetic acids are the main short chain fatty acids (SCFAs) produced by 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 (Cummings, 1981).”
Background
Microbial community profiling for human microbiome projects: Tools, techniques, and challengesPreprint
Hamady, M., & Knight, R. D. (2009) · Genome Research · doi:10.1101/gr.085464.108 · Cited by 1,031
The anxiolytic effect of Bifidobacterium longum NCC3001 involves vagal pathways for gut-brain communication
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
Effects 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 · cited 1×
“basal noradrenaline levels in the brainstem, however, there were no differences in corticosterone concentrations between groups (Desbonnet et al., 2008; Desbonnet et al., 2010).”
Background
The Warburg Effect Dictates the Mechanism of Butyrate-Mediated Histone Acetylation and Cell Proliferation
Donohoe, D. R., Collins, L. B., Wali, A., Bigler, R., Sun, W., & Bultman, S. J. (2012) · Molecular Cell · doi:10.1016/j.molcel.2012.08.033 · Cited by 993 · cited 1×
“directly influence neurotransmitters’ synthesis and to inhibit the histone deacetylases may be responsible for their behavioural effects (Donohoe et al., 2012; Matis et al., 2013).”
Background
The microbiome-gut-brain axis: from bowel to behavior
Cryan, J. F., & O’Mahony, S. M. (2011) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2010.01664.x · Cited by 990 · cited 1×
“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).”
Background
Sex-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
Pyrosequencing study of fecal microflora of autistic and control children
Finegold, S. M., Dowd, S. E., Gontcharova, V., Liu, C., Henley, K. E., Wolcott, R. D., Youn, E., Summanen, P. H., Granpeesheh, D., Dixon, D., et al. (2010) · Anaerobe · doi:10.1016/j.anaerobe.2010.06.008 · Cited by 977
Reduced incidence of Prevotella and other fermenters in intestinal microflora of autistic children
Kang, D.-W., Park, J. G., Ilhan, Z. E., Wallstrom, G., LaBaer, J., Adams, J. B., & Krajmalnik-Brown, R. (2013) · PLoS ONE · doi:10.1371/journal.pone.0068322 · Cited by 976 · cited 1×
“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).”
Background
Intestinal permeability, gut-bacterial dysbiosis, and behavioral markers of alcohol-dependence severity
Leclercq, S., Matamoros, S., Cani, P. D., Neyrinck, A. M., Jamar, F., Stärkel, P., Windey, K., Tremaroli, V., Bäckhed, F., Verbeke, K., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1415174111 · Cited by 972
Bacteria, Colonic Fermentation, and Gastrointestinal Health
Macfarlane, G. T., & Macfarlane, S. (2012) · Journal of AOAC INTERNATIONAL · doi:10.5740/jaoacint.sge_macfarlane · Cited by 970 · cited 2×
“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”
Background
The probiotic Bifidobacteria infantis: an assessment of potential antidepressant properties in the rat
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 · cited 2×
“basal noradrenaline levels in the brainstem, however, there were no differences in corticosterone concentrations between groups (Desbonnet et al., 2008; Desbonnet et al., 2010).”
Background
Targeting the microbiota-gut-brain axis: prebiotics have anxiolytic and antidepressant-like effects and reverse the impact of chronic stress in mice
Burokas, A., Arboleya, S., Moloney, R. D., Peterson, V. L., Murphy, K., Clarke, G., Stanton, C., Dinan, T. G., & Cryan, J. F. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.12.031 · Cited by 952 · cited 3×
“In addition, the prebiotic combination was able to normalise the effects of chronic psychological stress on the microbiota (Burokas et al., 2017).”
BackgroundInfluential
Role 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 932 · cited 1×
“One of the main neurotransmitters involved in depression is serotonin (Nemeroff, 2002; Owens and Nemeroff, 1994) and it is recognised that 90% of the body serotonin is”
Background
Diet 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×
“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).”
Background
Effects of Diurnal Variation of Gut Microbes and High-Fat Feeding on Host Circadian Clock Function and Metabolism
Leone, V., Gibbons, S. M., Martinez, K., Hutchison, A. L., Huang, E. Y., Cham, C. M., Pierre, J. F., Heneghan, A. F., Nadimpalli, A., Hubert, N., et al. (2015) · Cell Host & Microbe · doi:10.1016/j.chom.2015.03.006 · Cited by 921 · cited 1×
“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).”
Background
Towards 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×
“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).”
Background
Enterochromaffin 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
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 · cited 2×
“rodentium in conventionally colonised mice was able to generate stress-induced memory dysfunction (Gareau et al., 2011).”
Background
Monitoring Bacterial Community of Human Gut Microbiota Reveals an Increase in Lactobacillus in Obese Patients and Methanogens in Anorexic Patients
Armougom, F., Henry, M., Vialettes, B., Raccah, D., & Raoult, D. (2009) · PLoS ONE · doi:10.1371/journal.pone.0007125 · Cited by 905
The neuropharmacology of butyrate: the bread and butter of the microbiota-gut-brain axis
Stilling, R. M., van de Wouw, M., Clarke, G., Stanton, C., Dinan, T. G., & Cryan, J. F. (2016) · Neurochemistry International · doi:10.1016/j.neuint.2016.06.011 · Cited by 891
Comparative metagenomics revealed commonly enriched gene sets in human gut microbiomes
Kurokawa, K., Itoh, T., Kuwahara, T., Oshima, K., Toh, H., Toyoda, A., Takami, H., Morita, H., Sharma, V. K., Srivastava, T. P., et al. (2007) · DNA Research · doi:10.1093/dnares/dsm018 · Cited by 869 · cited 2×
“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).”
Background
Microbiota 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×
“, 2011) and demonstrated that germfree animals suffer a social impairment, which is reversed by re-colonisation with a normal microbiota (Desbonnet et al., 2014).”
Background
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 852 · cited 8×
“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.”
BackgroundInfluential
HPA axis responses to laboratory psychosocial stress in healthy elderly adults, younger adults, and children: impact of age and gender
Kudielka, B. M., Buske-Kirschbaum, A., Hellhammer, D. H., & Kirschbaum, C. (2004) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(02)00146-4 · Cited by 851
New insights into symptoms and neurocircuit function of anorexia nervosa
Kaye, W. H., Fudge, J. L., & Paulus, M. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2682 · Cited by 843
Socially transmitted gut microbiota protect bumble bees against an intestinal parasite
Koch, H., & Schmid‐Hempel, P. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1110474108 · Cited by 828 · cited 1×
“, 2014), bumblebees (Koch and Schmid-Hempel, 2011), hyenas (Theis et al.”
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 · cited 1×
“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).”
BackgroundSelf-citation
Autism‐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
Intranasal Oxytocin Increases Positive Communication and Reduces Cortisol Levels During Couple Conflict
Ditzen, B., Schaer, M., Gabriel, B., Bodenmann, G., Ehlert, U., & Heinrichs, M. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.10.011 · Cited by 805
Targeting 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 805 · cited 1×
“eating behaviour, as well as playing a role in obesity (Arora et al., 2013; Belguesmia et al., 2016; Delzenne et al., 2011; Forssten et al., 2013).”
Background
Effects of sodium butyrate, a new pharmacological agent, on cells in culture
Kruh, J. (1981) · Molecular and Cellular Biochemistry · doi:10.1007/bf00222695 · Cited by 803 · cited 1×
“In fact, one of the most recognised cellular mechanism of action of butyrate is its ability to inhibit the histone deacetylases (Kruh, 1982).”
Background
Oxytocin, 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
Enteric dysbiosis associated with a mouse model of alcoholic liver disease
Yan, A. W., Fouts, D. E., Brandl, J., Stärkel, P., Torralba, M., Schott, E., Tsukamoto, H., Nelson, K. E., Brenner, D. A., & Schnabl, B. (2011) · Hepatology · doi:10.1002/hep.24018 · Cited by 791
Gut microbiota fermentation of prebiotics increases satietogenic and incretin gut peptide production with consequences for appetite sensation and glucose response after a meal
Cani, P. D., Lecourt, E., Dewulf, E. M., Sohet, F. M., Pachikian, B. D., Naslain, D., Backer, F. D., Neyrinck, A. M., & Delzenne, N. M. (2009) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.2009.28095 · Cited by 788 · cited 1×
“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).”
Background
Evidence for a Neuroendocrinological Foundation of Human Affiliation: Plasma Oxytocin Levels Across Pregnancy and the Postpartum Period Predict Mother-Infant Bonding
Feldman, R., Weller, A., Zagoory-Sharon, O., & Levine, A. (2007) · Psychological Science · doi:10.1111/j.1467-9280.2007.02010.x · Cited by 787 · cited 1×
“endogenous oxytocin levels peri-partum are associated with increased mother-infant bonding (Feldman et al., 2007).”
Background
Differences between the gut microflora of children with autistic spectrum disorders and that of healthy children
Parracho, H. M., Bingham, M. O., Gibson, G. R., & McCartney, A. L. (2005) · Journal of Medical Microbiology · doi:10.1099/jmm.0.46101-0 · Cited by 784 · cited 1×
“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).”
Background
Colonic 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
Gut 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×
“compared to non-treated mice, suggesting that gut microbes are able to modulate the activity of these hormones (Desbonnet et al., 2015).”
BackgroundResultInfluential
Glucocorticoid-sensitive hippocampal neurons are involved in terminating the adrenocortical stress response.
Sapolsky, R. M., Krey, L. C., & McEwen, B. S. (1984) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.81.19.6174 · Cited by 758 · cited 1×
“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).”
Background
Why 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×
“prone to develop ASD than females (Baron-Cohen et al., 2011; Pfaff et al., 2011).”
Weight loss during oligofructose supplementation is associated with decreased ghrelin and increased peptide YY in overweight and obese adults
Parnell, J. A., & Reimer, R. A. (2009) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.2009.27465 · Cited by 749
Functional Cross‐Talk Between the Hypothalamic‐Pituitary‐Gonadal and ‐Adrenal Axes
Viau, V. (2002) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2002.00798.x · Cited by 744 · cited 4×
“1, the HPG is also connected and influenced by the HPA axis (Viau, 2002).”
BackgroundInfluential
Stress, Glucocorticoids, and Damage to the Nervous System: The Current State of Confusion
Sapolsky, R. M. (1996) · Stress · doi:10.3109/10253899609001092 · Cited by 738 · cited 1×
“When a threat is perceived, the HPA axis mounts a defensive response and restores the homeostatic balance in the organism (de Kloet et al., 2005; Frodl and O'Keane, 2013; McEwen, 2007; Sapolsky, 1996).”
Background
Central 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×
“evoke in the host the so-called fight-or-flight response (Jansen et al., 1995).”
Background
Interactions between the Hypothalamic-Pituitary-Adrenal Axis and the Female Reproductive System: Clinical Implications
Chrousos, G. P., Torpy, D. J., & Gold, P. W. (1998) · Annals of Internal Medicine · doi:10.7326/0003-4819-129-3-199808010-00012 · Cited by 711
Beneficial metabolic effects of a probiotic via butyrate-induced GLP-1 hormone secretion
Yadav, H., Lee, J.-H., Lloyd, J., Walter, P., & Rane, S. G. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.452516 · Cited by 709
Maternal gut bacteria promote neurodevelopmental abnormalities in mouse offspring
Kim, S., Kim, H., Yim, Y. S., Ha, S., Atarashi, K., Tan, T. G., Longman, R. S., Honda, K., Littman, D. R., Choi, G. B., et al. (2017) · Nature · doi:10.1038/nature23910 · Cited by 678 · cited 2×
“Indeed, pre-treatment of MIA mothers with the antibiotic vancomycin prevents the development of behavioural deficits in the offspring (Kim et al., 2017).”
Background
Influence of a high-fat diet on gut microbiota, intestinal permeability and metabolic endotoxaemia
Moreira, A. P. B., Teixeira, T. F. S., Machado, A. B. F., Pelúzio, M. D. C. G., & Alfenas, R. D. C. G. (2012) · British Journal Of Nutrition · doi:10.1017/s0007114512001213 · Cited by 675
Critical role of gut microbiota in the production of biologically active, free catecholamines in the gut lumen of mice
Asano, Y., Hiramoto, T., Nishino, R., Aiba, Y., Kimura, T., Yoshihara, K., Koga, Y., & Sudo, N. (2012) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00341.2012 · Cited by 659
Antibiotic-induced perturbations in gut microbial diversity influences neuro-inflammation and amyloidosis in a murine model of Alzheimer’s disease
Minter, M. R., Zhang, C., Leone, V., Ringus, D. L., Zhang, X., Oyler-Castrillo, P., Musch, M. W., Liao, F., Ward, J. F., Holtzman, D. M., et al. (2016) · Scientific Reports · doi:10.1038/srep30028 · Cited by 655
Social behavior functions and related anatomical characteristics of vasotocin/vasopressin systems in vertebrates
Goodson, J. L., & Bass, A. H. (2001) · Brain Research Reviews · doi:10.1016/s0165-0173(01)00043-1 · Cited by 645 · cited 1×
“pair-bond formation, and in stress response (Goodson and Bass, 2001).”
The role of testosterone in social interaction
Eisenegger, C., Haushofer, J., & Fehr, E. (2011) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2011.04.008 · Cited by 630
The GABA system in anxiety and depression and its therapeutic potential
Möhler, H. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.08.040 · Cited by 627 · cited 1×
“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).”
Background
The microbiota–gut–brain axis in obesity
Torres‐Fuentes, C., Schellekens, H., Dinan, T. G., & Cryan, J. F. (2017) · The Lancet. Gastroenterology & hepatology · doi:10.1016/s2468-1253(17)30147-4 · Cited by 623
Stress as a Common Risk Factor for Obesity and Addiction
Sinha, R., & Jastreboff, A. M. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.01.032 · Cited by 611 · cited 1×
“For instance, it is well established that stress is one of the most significant risk factors for addiction (Sinha and Jastreboff, 2013) and, as”
Background
The gut-brain barrier in major depression: intestinal mucosal dysfunction with an increased translocation of LPS from gram negative enterobacteria (leaky gut) plays a role in the inflammatory pathophysiology of depression.
Maes, M. H. J., Kubera, M., & Leunis, J. (2008) · PubMed · Cited by 609
Automated Three‐Chambered Social Approach Task for Mice
Yang, M., Silverman, J. L., & Crawley, J. N. (2011) · Current Protocols in Neuroscience · doi:10.1002/0471142301.ns0826s56 · Cited by 598 · cited 2×
“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.”
Method
GPR41/FFAR3 and GPR43/FFAR2 as Cosensors for Short-Chain Fatty Acids in Enteroendocrine Cells vs FFAR3 in Enteric Neurons and FFAR2 in Enteric Leukocytes
Nøhr, 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 597
Absence of the gut microbiota enhances anxiety-like behavior and neuroendocrine response to acute stress in rats
Crumeyrolle-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×
“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).”
Background
Rhythmicity 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×
“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).”
Background
Anxiety, depression, and the microbiome: A role for gut peptides
Lach, G., Schellekens, H., Dinan, T. G., & Cryan, J. F. (2018) · Neurotherapeutics · doi:10.1007/s13311-017-0585-0 · Cited by 573 · cited 1×
“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).”
Background
Stress 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×
“adrenal cortex produces glucocorticoid hormones: cortisol in humans and corticosterone in rodents (Stephens and Wand, 2012).”
Background
Collective 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×
“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.”
Background
Homeostasis in intestinal epithelium is orchestrated by the circadian clock and microbiota cues transduced by TLRs
Mukherji, A., Kobiita, A., Ye, T., & Chambon, P. (2013) · Cell · doi:10.1016/j.cell.2013.04.020 · Cited by 560
How does the brain deal with cumulative stress? A review with focus on developmental stress, HPA axis function and hippocampal structure in humans
Frodl, T., & O'Keane, V. (2013) · Neurobiology of Disease · doi:10.1016/j.nbd.2012.03.012 · Cited by 555
Interactions between Gut Microbiota, Host Genetics and Diet Modulate the Predisposition to Obesity and Metabolic Syndrome
Ussar, S., Griffin, N. W., Bézy, O., Fujisaka, S., Vienberg, S. G., Softic, S., Deng, L., Bry, L., Gordon, J. I., & Kahn, C. R. (2015) · Cell Metabolism · doi:10.1016/j.cmet.2015.07.007 · Cited by 545
Antidepressant-Like Effects of the Histone Deacetylase Inhibitor, Sodium Butyrate, in the Mouse
Schroeder, F. A., Lin, C. L., Crusio, W. E., & Akbarian, S. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.06.036 · Cited by 541 · cited 1×
“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).”
Background
Infant 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
Childhood overweight after establishment of the gut microbiota: the role of delivery mode, pre-pregnancy weight and early administration of antibiotics
Ajslev, T. A., Andersen, C. S., Gamborg, M., Sørensen, T. I. A., & Jess, T. (2011) · International Journal of Obesity · doi:10.1038/ijo.2011.27 · Cited by 534
Social 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 530 · cited 2×
“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.”
Background
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×
“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).”
Background
Vagal 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×
“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).”
Background
Long term consequences of neonatal rearing on central corticotropin-releasing factor systems in adult male rat offspring
Plotsky, P. M., Thrivikraman, K. V., Nemeroff, C. B., Caldji, C., Sharma, S., & Meaney, M. J. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300769 · Cited by 522
Prebiotic intake reduces the waking cortisol response and alters emotional bias in healthy volunteers
Schmidt, K., Cowen, P. J., Harmer, C. J., Tzortzis, G., Errington, S., & Burnet, P. W. J. (2015) · Psychopharmacology · doi:10.1007/s00213-014-3810-0 · Cited by 522
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×
“Tryptophan is an essential amino acid and is a precursor to many biologically active agents, such as serotonin (Ruddick et al., 2006).”
Background
Microbiota 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
Infant 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 514 · cited 1×
“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).”
Background
Bifidobacterium longum 1714 as a translational psychobiotic: modulation of stress, electrophysiology and neurocognition in healthy volunteers
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
Metabolism and Circadian Rhythms—Implications for Obesity
Froy, O. (2010) · Endocrine Reviews · doi:10.1210/er.2009-0014 · Cited by 505 · cited 1×
“Circadian rhythms regulate several aspects of physiology including metabolism and play a critical role in obesity (Bray and Young, 2007; Froy, 2010).”
Background
Neuropeptide, 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×
“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).”
Background
Sex 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 500 · cited 1×
“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”
Background
Gut Microbiota Composition in Male Rat Models under Different Nutritional Status and Physical Activity and Its Association with Serum Leptin and Ghrelin Levels
Queipo-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×
“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.”
Background
Probiotics, gut microbiota and health
Butel, M. J. (2013) · Médecine et Maladies Infectieuses · doi:10.1016/j.medmal.2013.10.002 · Cited by 486 · cited 2×
“Probiotics are defined as living micro-organisms that, if administered in adequate amount, confer health benefits to the host (Butel, 2014).”
Background
Role 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 474
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×
“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).”
Background
Oxytocin 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×
“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).”
Background
FSH and testosterone signaling in Sertoli cells
Walker, W. H., & Cheng, J. (2005) · Reproduction · doi:10.1530/rep.1.00358 · Cited by 467 · cited 1×
“In males, FSH and LH stimulate the production of testosterone, a hormone required for normal spermatogenesis (Huang et al., 2001; Walker and Cheng, 2005).”
Background
Inulin-type fructans modulate gastrointestinal peptides involved in appetite regulation (glucagon-like peptide-1 and ghrelin) in rats
Cani, P. D., Dewever, C., & Delzenne, N. M. (2004) · British Journal Of Nutrition · doi:10.1079/bjn20041225 · Cited by 458 · cited 2×
“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).”
Background
Is eating behavior manipulated by the gastrointestinal microbiota? Evolutionary pressures and potential mechanisms
Alcock, J., Maley, C. C., & Aktipis, C. A. (2014) · BioEssays · doi:10.1002/bies.201400071 · Cited by 454
Microbiota profile in feces of breast- and formula-fed newborns by using fluorescence in situ hybridization (FISH)
Bezirtzoglou, E., Tsiotsias, A., & Welling, G. W. (2011) · Anaerobe · doi:10.1016/j.anaerobe.2011.03.009 · Cited by 453 · cited 1×
“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).”
Background
Activation in vagal afferents and central autonomic pathways: Early responses to intestinal infection with Campylobacter jejuni
Goehler, 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×
“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).”
Background
Maternal 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×
“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”
Result
Probiotic gut effect prevents the chronic psychological stress‐induced brain activity abnormality in mice
Ait‐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
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
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×
“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
Acute effects of steroid hormones and neuropeptides on human social-emotional behavior: A review of single administration studies
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
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×
“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).”
Background
Immune 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×
“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…”
BackgroundInfluential
Melancholic 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×
“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).”
Background
Modulation 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
General 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 422 · cited 1×
“The TSH, in turn, stimulates the thyroid to produce T3 and T4 until levels in the blood return to normal (Zoeller et al., 2007).”
Background
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×
“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.”
Background
Oxytocin and sexual behavior
Carter, C. S. (1992) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(05)80176-9 · Cited by 417 · cited 1×
“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;…”
Method
Maternal 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×
“…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).”
Background
The 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
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×
“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).”
Background
Responses 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
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×
“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).”
Background
Oligofructose 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 390 · cited 1×
“, 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
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×
“satiety, reduced hunger and reduced the desire to ingest food in humans (Cani et al., 2006).”
Background
The 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
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 373 · cited 12×
“GABA transporters are localized on the blood-brain barrier (BBB) and allow gut- derived GABA to reach the CNS (Takanaga et al., 2001).”
BackgroundInfluential
Intestinal Dysbiosis: A Possible Mechanism of Alcohol‐Induced Endotoxemia and Alcoholic Steatohepatitis in Rats
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
Neurotransmitters 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 357 · cited 1×
“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).”
Background
Interleukin-1β in Immune Cells of the Abdominal Vagus Nerve: a Link between the Immune and Nervous Systems?
Goehler, 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×
“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).”
Background
Effect of Lactobacillus rhamnosus CGMCC1.3724 supplementation on weight loss and maintenance in obese men and women
Sanchez, 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×
“reductions in circulating leptin concentrations (Sanchez et al., 2014).”
Influences of Dietary and Environmental Stress on Microbial Populations in the Murine Gastrointestinal Tract
Tannock, G. W., & Savage, D. C. (1974) · Infection and Immunity · doi:10.1128/iai.9.3.591-598.1974 · Cited by 349 · cited 1×
“intestinal microbial populations in mice (Tannock and Savage, 1974).”
Glucocorticoids, stress, and fertility.
Whirledge, S., & Cidlowski, J. A. (2010) · PubMed · Cited by 347
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
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×
“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).”
Background
Estrogen receptors in the central nervous system and their implication for dopamine-dependent cognition in females
Almey, A., Milner, T. A., & Brake, W. G. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.06.010 · Cited by 337
Stressor Exposure Disrupts Commensal Microbial Populations in the Intestines and Leads to Increased Colonization by Citrobacter rodentium
Bailey, 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×
“29 enteric pathogen Citrobacter rodentium (Bailey et al., 2010).”
Background
Infant 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×
“…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).”
BackgroundInfluential
Programming 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 326
Thyroid 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 324
The impact of perinatal probiotic intervention on the development of overweight and obesity: follow-up study from birth to 10 years
Luoto, R., Kalliomäki, M. A., Laitinen, K., & Isolauri, E. (2010) · International Journal of Obesity · doi:10.1038/ijo.2010.50 · Cited by 323 · cited 1×
“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”
Background
Gut Commensal E. coli Proteins Activate Host Satiety Pathways following Nutrient-Induced Bacterial Growth
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×
“coli proteins was able to increase plasma PYY and GLP-1 levels enhancing satiety (Breton et al., 2016).”
Background
The 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×
“the immune system (Leonard, 2005) and the gonadal axis (Viau, 2002).”
Background
Commensal 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×
“Specifically, the gut bacteria species that suppress protein appetite are Acetobacter pomorum and Lactobacilli (Leitao-Goncalves et al., 2017).”
Background
Weight gain in anorexia nervosa does not ameliorate the faecal microbiota, branched chain fatty acid profiles and gastrointestinal complaints
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×
“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).”
Background
The role of corticotrophin-releasing factor in stress-induced relapse to alcohol-seeking behavior in rats
Lê, A. D., Harding, S. E., Juzytsch, W., Watchus, J., Shalev, U., & Shaham, Y. (2000) · Psychopharmacology · doi:10.1007/s002130000411 · Cited by 310
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×
“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”
Background
The microbiota–gut–brain axis in gastrointestinal disorders: stressed bugs, stressed brain or both?
Palma, G. D., Collins, S. M., Berčík, P., & Verdu, E. F. (2014) · The Journal of Physiology · doi:10.1113/jphysiol.2014.273995 · Cited by 309

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Research works printed but not linked: 2

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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
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 933
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 767
“A notable role of human digestive system in brain development has been proposed [15, 50].”
Background
Gut Microbiota and Energy Homeostasis in Fish
Butt, R. L., & Volkoff, H. (2019) · Frontiers in Endocrinology · doi:10.3389/fendo.2019.00009 · Cited by 637
A systematic review of gut microbiota composition in observational studies of major depressive disorder, bipolar disorder and schizophrenia
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
“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].”
Background

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Authors: Cussotto, S., Sandhu, K. V., Dinan, T. G., & Cryan, J. F.
Affiliations: University College Cork (IE)
Corresponding author: Cryan, John F.
ORCID: Cussotto, Sofia
Dinan, Timothy G.
Cryan, John F.
Venue: Frontiers in Neuroendocrinology
Publisher: Elsevier BV
Published: 2018-10
Volume: 51
Pages: 80-101
ISSN: 0091-3022 (ISSN-L)
DOI: 10.1016/j.yfrne.2018.04.002
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: cc-by-nc-nd
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
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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The Neuroendocrinology of the Microbiota-Gut-Brain Axis: A Behavioural Perspective

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