Commensal microbiota modulate murine behaviors in a strictly contamination-free environment confirmed by culture-based methods
Open accessAbstract
BACKGROUND: There is increasing evidence suggesting the existence of an interaction between commensal microbiota, the gut and the brain. The aim of this study was to examine the influence of commensal microbiota on the host behaviors in a contamination-free environment, which was verified by culture-based methods. METHODS: Open-field and marble-burying tests were used to analyze anxiety-like behaviors and locomotor activity in gnotobiotic BALB/c mice with a common genetic background in a sterile isolator. The monoamine levels in several regions of the brain were measured in germfree (GF) mice and commensal fecal microbiota-associated mice (EX-GF). KEY RESULTS: A 24-h exposure to the environment outside the sterile isolators rendered GF mice less anxious than those not contaminated, while there was no change in the locomotion. EX-GF mice, the gnotobiotic mice with normal specific pathogen-free microbiota, were less anxious and active than GF mice using open-field and marble-burying tests. The norepinephrine, dopamine, and serotonin turnover rates were higher in the EX-GF mice than in the GF mice in most regions of the brain, suggesting that monoaminergic neurotransmission might increase in the EX-GF mice comparing the GF mice. Monoassociation with Brautia coccoides reduced the anxiety level, but it did not affect the locomotor activity. In contrast, colonization with Bifidobacterium infantis decreased the locomotor activity, while having little effect on the anxiety level. CONCLUSIONS & INFERENCES: These results strongly support the current view that gut microorganisms modulate brain development and behavior.
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Gut colonization by commensal microflora in germ-free mice immediately after birth contributed to an increase in striatal monoaminergic neurotransmission, which resulted in normalization of anxiety-like behavior.
“Nishino et al. [69] showed that gut colonization by commensal microflora in GF mice immediately after birth contributed to an increase in the striatal monoaminergic neurotransmission, which resulted in normalization of the anxiety-like behavior.”
From The Role of Microbiota-Gut-Brain Axis in Neuropsychiatric and Neurological Disorders (2021) · cites this paper as [69]
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Physiology and neurobiology of stress and adaptation: central role of the brain
McEwen, B. S. (2007) · Physiological Reviews · doi:10.1152/physrev.00041.2006 · Cited by 4,981 · see citing works
Bravo, J. A., Forsythe, P., Chew, M. V., Escaravage, E., Savignac, H. M., Dinan, T. G., Bienenstock, J., & Cryan, J. F. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1102999108 · Cited by 3,888 · see citing works
Normal gut microbiota modulates brain development and behavior
Heijtz, R. D., Wang, S., Anuar, F., Qian, Y., Björkholm, B., Samuelsson, A., Hibberd, M. L., Forssberg, H., & Pettersson, S. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1010529108 · Cited by 3,228 · see citing works
Development of the Human Infant Intestinal Microbiota
Palmer, C., Bik, E. M., DiGiulio, D. B., Relman, D. A., & Brown, P. O. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050177 · Cited by 2,877 · see citing works
Sudo, N., Chida, Y., Aiba, Y., Sonoda, J., Oyama, N., Yu, X., Kubo, C., & Koga, Y. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.063388 · Cited by 2,735 · see citing works
Self-citationMechanisms underlying the resistance to diet-induced obesity in germ-free mice
Bäckhed, F., Manchester, J. K., Semenkovich, C. F., & Gordon, J. I. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0605374104 · Cited by 2,615 · see citing works
Molecular Analysis of Commensal Host-Microbial Relationships in the Intestine
Hooper, L. V., Wong, M. H., Thelin, A., Hansson, L., Falk, P. G., & Gordon, J. I. (2001) · Science · doi:10.1126/science.291.5505.881 · Cited by 2,202 · see citing works
Bercik, P., Denou, E., Collins, J., Jackson, W., Lu, J., Jury, J., Deng, Y., Blennerhassett, P., Macri, J., McCoy, K. D., et al. (2011) · Gastroenterology · doi:10.1053/j.gastro.2011.04.052 · Cited by 1,748 · see citing works
Gut feelings: the emerging biology of gut-brain communication
Mayer, E. A. (2011) · Nature Reviews Neuroscience · doi:10.1038/nrn3071 · Cited by 1,726 · see citing works
Neufeld, K. M., Kang, N., Bienenstock, J., & Foster, J. A. (2011) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2010.01620.x · Cited by 1,392 · see citing works
Sudo, N., Sawamura, S., Tanaka, K., Aiba, Y., Kubo, C., & Koga, Y. (1997) · The Journal of Immunology · doi:10.4049/jimmunol.159.4.1739 · Cited by 1,070 · see citing works
Self-citationNeurobiology of Executive Functions: Catecholamine Influences on Prefrontal Cortical Functions
Arnsten, A. F. T., & Li, B.-M. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2004.08.019 · Cited by 948 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Gastrointestinal Microflora Studies in Late‐Onset Autism
Finegold, S. M., Molitoris, D., Song, Y., Liu, C., Vaisanen, M., Bolte, E., McTeague, M., Sandler, R., Wexler, H., Marlowe, E. M., et al. (2002) · Clinical Infectious Diseases · doi:10.1086/341914 · Cited by 742 · see citing works
del Campo, N., Chamberlain, S. R., Sahakian, B. J., & Robbins, T. W. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.02.036 · Cited by 685 · see citing works
Bercik, P., Verdu, E. F., Foster, J. A., Macri, J., Potter, M., Huang, X., Malinowski, P., Jackson, W., Blennerhassett, P., Neufeld, K. A., et al. (2010) · Gastroenterology · doi:10.1053/j.gastro.2010.06.063 · Cited by 674 · see citing works
Matsuki, T., Watanabe, K., Fujimoto, J., Miyamoto, Y., Takada, T., Matsumoto, K., Oyaizu, H., & Tanaka, R. (2002) · Applied and Environmental Microbiology · doi:10.1128/aem.68.11.5445-5451.2002 · Cited by 656 · see citing works
Stark, P. L., & Lee, A. (1982) · Journal of Medical Microbiology · doi:10.1099/00222615-15-2-189 · Cited by 616 · see citing works
Short-Term Benefit From Oral Vancomycin Treatment of Regressive-Onset Autism
Sandler, R. H., Finegold, S. M., Bolte, E. R., Buchanan, C. P., Maxwell, A. P., Väisänen, M.-L., Nelson, M. N., & Wexler, H. M. (2000) · Journal of Child Neurology · doi:10.1177/088307380001500701 · Cited by 614 · see citing works
Collins, S. M., & Bercik, P. (2009) · Gastroenterology · doi:10.1053/j.gastro.2009.01.075 · Cited by 612 · see citing works
Benno, Y., Sawada, K., & MITSUOKA, T. (1984) · Microbiology and Immunology · doi:10.1111/j.1348-0421.1984.tb00754.x · Cited by 432 · see citing works
Forsythe, P., Sudo, N., Dinan, T., Taylor, V. H., & Bienenstock, J. (2010) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2009.05.058 · Cited by 429 · see citing works
Self-citationAnimal models of anxiety: do I need multiple tests?
Ramos, A. (2008) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2008.07.005 · Cited by 413 · see citing works
Gastrointestinal microbiology enters the metagenomics era
Frank, D. N., & Pace, N. R. (2008) · Current Opinion in Gastroenterology · doi:10.1097/mog.0b013e3282f2b0e8 · Cited by 405 · see citing works
LYTE, M., LI, W., OPITZ, N., GAYKEMA, R., & GOEHLER, L. (2006) · Physiology & Behavior · doi:10.1016/j.physbeh.2006.06.019 · Cited by 334 · see citing works
Broekkamp, C. L., Rijk, H. W., Joly-Gelouin, D., & Lloyd, K. L. (1986) · European Journal of Pharmacology · doi:10.1016/0014-2999(86)90051-8 · Cited by 286 · see citing works
Effects of Estrogen on Activity and Fear-Related Behaviors in Mice
Morgan, M., & Pfaff, D. W. (2001) · Hormones and Behavior · doi:10.1006/hbeh.2001.1716 · Cited by 271 · see citing works
Lehmann, M. L., & Herkenham, M. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.0577-11.2011 · Cited by 234 · see citing works
Njung'e, K., & Handley, S. L. (1991) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.1991.tb12392.x · Cited by 183 · see citing works
Raison, C. L., Lowry, C. A., & Rook, G. A. W. (2010) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2010.161 · Cited by 169 · see citing works
Maukonen, J., Satokari, R., Mättö, J., Söderlund, H., Mattila-Sandholm, T., & Saarela, M. (2006) · Journal of Medical Microbiology · doi:10.1099/jmm.0.46134-0 · Cited by 156 · see citing works
Animal Models for Anxiety and Response to Serotonergic Drugs
Broekkamp, C. L. E., Berendsen, H. H. G., Jenck, F., & VanDelft, A. M. L. (2010) · Psychopathology · doi:10.1159/000284620 · Cited by 134 · see citing works
Shanks, N. M., Zalcman, S., Zacharko, R. M., & Anisman, H. (1991) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(91)90591-o · Cited by 97 · see citing works
Mikami, K., Takahashi, H., Kimura, M., Isozaki, M., Izuchi, K., Shibata, R., Sudo, N., Matsumoto, H., & Koga, Y. (2009) · Pediatric Research · doi:10.1203/pdr.0b013e31819ed7a8 · Cited by 71 · see citing works
Self-citationEcological Succession of Bacterial Communities during Conventionalization of Germ-Free Mice
Gillilland, M. G., Erb‐Downward, J. R., Bassis, C. M., Shen, M. C., Toews, G. B., Young, V. B., & Huffnagle, G. B. (2012) · Applied and Environmental Microbiology · doi:10.1128/aem.05239-11 · Cited by 63 · see citing works
Cell adhesion and invasion mechanisms in microbial pathogenesis
Finlay, B. B. (1990) · Current Opinion in Cell Biology · doi:10.1016/0955-0674(90)90078-s · Cited by 52 · see citing works
Dietary nucleic acids promote a shift in Th1/Th2 balance toward Th1‐dominant immunity
Sudo, N., Aiba, Takaki, Tanaka, Yu, Oyama, Koga, & Kubo (2000) · Clinical & Experimental Allergy · doi:10.1046/j.1365-2222.2000.00811.x · Cited by 46 · see citing works
Self-citationDietary l-tyrosine alleviates the behavioral alterations induced by social isolation stress in mice
Kabuki, Y., Mizobe, Y., Yamada, S., & Furuse, M. (2009) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2009.08.014 · Cited by 24 · see citing works
Self-citationGastrointestinal microbiology in autistic spectrum disorder: a review
Gondalia, S. V., Palombo, E. A., Knowles, S. R., & Austin, D. (2010) · Reviews in Medical Microbiology · doi:10.1097/mrm.0b013e32833a3dc9 · Cited by 8 · see citing works
Nakayama, K., Katsu, H., Ando, T., & Nakajo, R. (2002) · Brain Research Bulletin · doi:10.1016/s0361-9230(02)00886-9 · Cited by 7 · see citing works
Flagged first, then by citations
Research works printed but not linked: 2
- Finlay BB. Cell adhesion and inva- sion mechanisms in microbial path- ogenesis. Curr Opin Cell Biol 1990; 2: 815-20.
- Mayer EA. Gut feelings: the emerg- ing biology of gut-brain communica- tion. Nat Rev Neurosci 2011; 12: 453 -66.
Cited by
Sorted by citations
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
Gut/brain axis and the microbiota
Mayer, E. A., Tillisch, K., & Gupta, A. (2015) · Journal of Clinical Investigation · doi:10.1172/jci76304 · Cited by 1,503 · see citing works
Gut microbes and the brain: paradigm shift in neuroscience
Mayer, E. A., Knight, R., Mazmanian, S. K., Cryan, J. F., & Tillisch, K. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.3299-14.2014 · Cited by 1,033 · see citing works
The Role of Microbiota-Gut-Brain Axis in Neuropsychiatric and Neurological Disorders
Socała, K., Doboszewska, U., Szopa, A., Serefko, A., Włodarczyk, M., Zielińska, A., Poleszak, E., Fichna, J., & Wlaź, P. (2021) · Pharmacological Research · doi:10.1016/j.phrs.2021.105840 · Cited by 857 · see citing works
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 · see citing works
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 · see citing works
The microbiome and host behavior
Vuong, H. E., Yano, J. M., Fung, T. C., & Hsiao, E. Y. (2017) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-072116-031347 · Cited by 537 · see citing works
The microbiome: a key regulator of stress and neuroinflammation
Rea, K., Dinan, T. G., & Cryan, J. F. (2016) · Neurobiology of Stress · doi:10.1016/j.ynstr.2016.03.001 · Cited by 508 · see citing works
Gut microbiota and the neuroendocrine system
Farzi, A., Fröhlich, E. E., & Holzer, P. (2018) · Neurotherapeutics · doi:10.1007/s13311-017-0600-5 · Cited by 478 · see citing works
The effects of probiotics on depressive symptoms in humans: a systematic review
Wallace, C. J. K., & Milev, R. (2017) · Annals of General Psychiatry · doi:10.1186/s12991-017-0138-2 · Cited by 471 · see citing works
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
Microbiota alteration is associated with the development of stress-induced despair behavior
Marin, I. A., Goertz, J. E., Ren, T., Rich, S. S., Onengut-Gumuscu, S., Farber, E., Wu, M., Overall, C. C., Kipnis, J., & Gaultier, A. (2017) · Scientific Reports · doi:10.1038/srep43859 · Cited by 369 · see citing works
Gut microbiota, enteroendocrine functions and metabolism
Cani, P. D., Everard, A., & Duparc, T. (2013) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2013.09.008 · Cited by 378 · see citing works
Pokusaeva, K., Johnson, C., Luk, B., Uribe, G., Fu, Y., Oezguen, N., Matsunami, R. K., Lugo, M., Major, A., Mori‐Akiyama, Y., et al. (2017) · Neurogastroenterology & Motility · doi:10.1111/nmo.12904 · Cited by 337 · see citing works
Effect of probiotics on central nervous system functions in animals and humans: a systematic review
Wang, H., Lee, I.-S., Braun, C., & Enck, P. (2016) · Journal of Neurogastroenterology and Motility · doi:10.5056/jnm16018 · Cited by 334 · see citing works
The Impact of Microbiota on Brain and Behavior: Mechanisms & Therapeutic Potential
Borre, Y. E., Moloney, R. D., Clarke, G., Dinan, T. G., & Cryan, J. F. (2014) · Advances in Experimental Medicine and Biology · doi:10.1007/978-1-4939-0897-4_17 · Cited by 329 · see citing works
Luna, R. A., & Foster, J. A. (2015) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2014.10.007 · Cited by 325 · see citing works
The neuroendocrinology of the microbiota-gut-brain axis: a behavioural perspective
Cussotto, S., Sandhu, K. V., Dinan, T. G., & Cryan, J. F. (2018) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2018.04.002 · Cited by 326 · see citing works
Interplay between the gut-brain axis, obesity and cognitive function
Agustí, A., García-Pardo, M. P., López-Almela, I., Campillo, I., Maes, M., Romaní-Pérez, M., & Sanz, Y. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00155 · Cited by 294 · see citing works
A gut microbial factor modulates locomotor behaviour in Drosophila
Schretter, C. E., Vielmetter, J., Bartos, I., Marka, Z., Marka, S., Argade, S., & Mazmanian, S. K. (2018) · Nature · doi:10.1038/s41586-018-0634-9 · Cited by 289 · see citing works
Cross talk: the microbiota and neurodevelopmental disorders
Kelly, J. R., Minuto, C., Cryan, J. F., Clarke, G., & Dinan, T. G. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00490 · Cited by 271 · see citing works
Liu, W.-H., Chuang, H.-L., Huang, Y.-T., Wu, C.-C., Chou, G.-T., Wang, S., & Tsai, Y.-C. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.10.046 · Cited by 269 · see citing works
Jaglin, M., Rhimi, M., Philippe, C., Pons, N., Bruneau, A., Goustard, B., Daugé, V., Maguin, E., Naudon, L., & Rabot, S. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00216 · Cited by 269 · see citing works
Gut Dysbiosis in Patients with Anorexia Nervosa
Morita, C., Tsuji, H., Hata, T., Gondo, M., Takakura, S., Kawai, K., Yoshihara, K., Ogata, K., Nomoto, K., Miyazaki, K., et al. (2015) · PLOS ONE · doi:10.1371/journal.pone.0145274 · Cited by 238 · see citing works
Self-citationThe role of the gut microbiota in dietary interventions for depression and anxiety
Bear, T. L. K., Dalziel, J. E., Coad, J., Roy, N. C., Butts, C. A., & Gopal, P. K. (2020) · Advances in Nutrition · doi:10.1093/advances/nmaa016 · Cited by 229 · see citing works
Biological aging and the human gut microbiota
Maffei, V. J., Kim, S., Blanchard, E., Luo, M., Jazwinski, S. M., Taylor, C. M., & Welsh, D. A. (2017) · The Journals of Gerontology Series A · doi:10.1093/gerona/glx042 · Cited by 219 · see citing works
The function of gut microbiota in immune-related neurological disorders: a review
Sittipo, P., Choi, J., Lee, S., & Lee, Y. K. (2022) · Journal of Neuroinflammation · doi:10.1186/s12974-022-02510-1 · Cited by 221 · see citing works
Regulation of gut luminal serotonin by commensal microbiota in mice
Hata, T., Asano, Y., Yoshihara, K., Kimura-Todani, T., Miyata, N., Zhang, X.-T., Takakura, S., Aiba, Y., Koga, Y., & Sudo, N. (2017) · PLOS ONE · doi:10.1371/journal.pone.0180745 · Cited by 211 · see citing works
Self-citationGut Microbiota: The Brain Peacekeeper
Mu, C., Yang, Y., & Zhu, W. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.00345 · Cited by 188 · see citing works
The gut microbiome and mental health: implications for anxiety- and trauma-related disorders
Malan-Muller, S., Valles-Colomer, M., Raes, J., Lowry, C. A., Seedat, S., & Hemmings, S. M. J. (2018) · OMICS: A Journal of Integrative Biology · doi:10.1089/omi.2017.0077 · Cited by 161 · see citing works
Human-Derived Bifidobacterium dentium Modulates the Mammalian Serotonergic System and Gut–Brain Axis
Engevik, M. A., Luck, B., Visuthranukul, C., Ihekweazu, F. D., Engevik, A. C., Shi, Z., Danhof, H. A., Chang-Graham, A. L., Hall, A., Endres, B. T., et al. (2021) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2020.08.002 · Cited by 164 · see citing works
Microbiota influence the development of the brain and behaviors in C57BL/6J mice
Lu, J., Synowiec, S., Lu, L., Yu, Y., Bretherick, T., Takada, S., Yarnykh, V., Caplan, J., Caplan, M., Claud, E. C., et al. (2018) · PLoS ONE · doi:10.1371/journal.pone.0201829 · Cited by 159 · see citing works
Role of the intestinal microbiome, intestinal barrier and psychobiotics in depression
Trzeciak, P., & Herbet, M. (2021) · Nutrients · doi:10.3390/nu13030927 · Cited by 139 · see citing works
The role of the microbiome in the neurobiology of social behaviour
Sarkar, A., Harty, S., Johnson, K. V. ‐., Moeller, A. H., Carmody, R. N., Lehto, S. M., Erdman, S. E., Dunbar, R. I. M., & Burnet, P. W. J. (2020) · Biological Reviews · doi:10.1111/brv.12603 · Cited by 135 · see citing works
Gut microbiota of mice putatively modifies amino acid metabolism in the host brain
Kawase, T., Nagasawa, M., Ikeda, H., Yasuo, S., Koga, Y., & Furuse, M. (2017) · British Journal of Nutrition · doi:10.1017/s0007114517000678 · Cited by 119 · see citing works
Self-citationHata, T., Miyata, N., Takakura, S., Yoshihara, K., Asano, Y., Kimura-Todani, T., Yamashita, M., Zhang, X.-T., Watanabe, N., Mikami, K., et al. (2019) · Endocrinology · doi:10.1210/en.2019-00408 · Cited by 116 · see citing works
Vodička, M., Ergang, P., Hrnčíř, T., Mikulecká, A., Kvapilová, P., Vagnerová, K., Šestáková, B., Fajstová, A., Hermanová, P., Hudcovic, T., et al. (2018) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2018.07.007 · Cited by 112 · see citing works
Of microbes and minds: A narrative review on the second brain aging
Calvani, R., Picca, A., Lo Monaco, M. R., Landi, F., Bernabei, R., & Marzetti, E. (2018) · Frontiers in Medicine · doi:10.3389/fmed.2018.00053 · Cited by 92 · see citing works
Luk, B., Veeraragavan, S., Engevik, M., Balderas, M., Major, A., Runge, J., Luna, R. A., & Versalovic, J. (2018) · PLOS ONE · doi:10.1371/journal.pone.0196510 · Cited by 90 · see citing works
Gut microbiota regulates key modulators of social behavior
Parashar, A., & Udayabanu, M. (2016) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2015.11.002 · Cited by 88 · see citing works
Beyond phylotyping: understanding the impact of gut microbiota on host biology
Reigstad, C. S., & Kashyap, P. C. (2013) · Neurogastroenterology & Motility · doi:10.1111/nmo.12134 · Cited by 66 · see citing works
Salami, M. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.613120 · Cited by 67 · see citing works
Destrez, A., Grimm, P., & Julliand, V. (2019) · Physiology & Behavior · doi:10.1016/j.physbeh.2019.02.003 · Cited by 42 · see citing works
- Authors
- Nishino, R., Mikami, K., Takahashi, H., Tomonaga, S., Furuse, M., Hiramoto, T., Aiba, Y., Koga, Y., & Sudo, N.
- Affiliations
- Tokai University (JP)
- Laboratory for Infectious Diseases Isehara Kanagawa Japan
- Kyushu University (JP)
- Corresponding author
- Nishino, R.
- Venue
- Neurogastroenterology & Motility
- Publisher
- Wiley
- Published
- 2013-03-11
- Volume
- 25
- Issue
- 6
- Pages
- 521
- ISSN
- 1350-1925 (ISSN-L)
- 1365-2982
- OpenAlex
- W2060139683
- Cited by
- 266
- References
- 42
- Citations by year
- 2026: 5 · 2025: 13 · 2024: 17 · 2023: 26 · 2022: 21 · 2021: 35 · 2020: 23 · 2019: 21 · 2018: 30 · 2017: 26 · 2016: 20 · 2015: 15 · 2014: 10 · 2013: 4
- FWCI
- 7.31
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Neurogastroenterology & Motility (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Japan Society for the Promotion of Science (24659350, 25293167)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Keywords
- commensal microbiota, gut-brain axis, anxiety-like behavior, locomotor activity, gnotobiotic mice, germ-free mice, sterile environment, monoamine neurotransmission, norepinephrine, dopamine, serotonin, Bifidobacterium infantis, microbial colonization, host behavior
- MeSH terms
- Animals, Anxiety, Behavior, Animal, Bifidobacterium, Brain, Dopamine, Exploratory Behavior, Feces, Germ-Free Life, Mice, Inbred BALB C, Motor Activity, Norepinephrine, Serotonin, Specific Pathogen-Free Organisms, Gastrointestinal Tract, Mice, Microbiota
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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