The DOI matches its Crossref record; 89 of the 89 references it cites were found in a registry or an index.
Reduced anxiety-like behavior and central neurochemical change in germ-free mice: Behavior in germ-free mice
Abstract
BACKGROUND: There is increasing interest in the gut-brain axis and the role intestinal microbiota may play in communication between these two systems. Acquisition of intestinal microbiota in the immediate postnatal period has a defining impact on the development and function of the gastrointestinal, immune, neuroendocrine and metabolic systems. For example, the presence of gut microbiota regulates the set point for hypothalamic-pituitary-adrenal (HPA) axis activity. METHODS: We investigated basal behavior of adult germ-free (GF), Swiss Webster female mice in the elevated plus maze (EPM) and compared this to conventionally reared specific pathogen free (SPF) mice. Additionally, we measured brain mRNA expression of genes implicated in anxiety and stress-reactivity. KEY RESULTS: Germ-free mice, compared to SPF mice, exhibited basal behavior in the EPM that can be interpreted as anxiolytic. Altered GF behavior was accompanied by a decrease in the N-methyl-D-aspartate receptor subunit NR2B mRNA expression in the central amygdala, increased brain-derived neurotrophic factor expression and decreased serotonin receptor 1A (5HT1A) expression in the dentate granule layer of the hippocampus. CONCLUSIONS & INFERENCES: We conclude that the presence or absence of conventional intestinal microbiota influences the development of behavior, and is accompanied by neurochemical changes in the brain.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“For example, some studies involving GF Swiss Webster mice show a decreased anxiety-like behavior (Arentsen et al., 2018;Clarke et al., 2013;Neufeld et al., 2011) whereas the opposite has been found in male GF BALB/c mice (Chen et al., 2017b;Nishino et al., 2013).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Neufeld et al., 2011
In the citing paper
“Due to the lack of commensal microbes, GF animals have impaired immune systems, dysregulated hormone signaling, altered metabolism, and differences in neurotransmission from conventional counterparts (Kawase et al., 2017;Neufeld et al., 2011;Pan et al., 2018;Sudo et al., 2004;Weger et al., 2019).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Neufeld et al., 2011
In the citing paper
“GF studies also show that microbes can also regulate NMDA receptors (NMDAR) (Neufeld et al., 2011)”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Neufeld et al., 2011
In the citing paper
“In addition, expression of NMDAR and BDNF is significantly reduced in GF mice [572, 581, 582]”
From Molecular and cellular mechanisms underlying the pathogenesis of Alzheimer’s disease (2020) · cites this paper as [581]
In the citing paper
“Preliminary studies have demonstrated that alterations in the GI microbiota can lead to long-term increased anxiety (69, 115, 116) and altered exploratory behavior in mice (18, 19).”
From Intestinal microbiota and immune function in the pathogenesis of irritable bowel syndrome (2013) · cites this paper as [116]
In the citing paper
“microbial abundance has been shown to alter the expression of neurotransmitter receptors in the brain (51, 189, 191).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [189]
In the citing paper
“These findings have subsequently been reproduced, with both male and female mice demonstrating enhanced stress reactivity to a novel environmental stressors (189, 350, 351).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [189]
In the citing paper
“Indeed, germ-free animals show widespread neurodevelopmental changes, associated with alterations in monoaminergic neurotransmission in the CNS (189).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [189]
In the citing paper
“These changes include increased hippocampal dopamine D1 receptor mRNA levels and decreased dopamine D1 receptor in the striatum and nucleus accumbens, as well as increased serotonin in the blood and hippocampus, with decreased serotonin receptor expression, respectively.”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [189]
In the citing paper
“Behavioral differences in germ-free mice include their anxiolytic-like manner when compared to SPF controls, although some studies report increased anxiety-like behavior in different species (124, 189, 351, 376).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [189]
In the citing paper
“Several metabolomic studies show alterations in the dopamine and serotonin systems (124, 189, 350, 378–380).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [189]
In the citing paper
“Interestingly, these cognitive deficits in rodents can be corrected through the colonization of the intestine via a fecal transplant from the control group, but only if it occurs early in life.”
From The relation between cesarean birth and child cognitive development (2017) · cites this paper as [30]
In the citing paper
“These studies show that rodents lacking all gut bacteria from birth (germ-free animals) have memory deficits28 and behavioral abnormalities29, 30 when compared to animals with normal gut microbiota.”
From The relation between cesarean birth and child cognitive development (2017) · cites this paper as [30]
In the citing paper
“Early experiments using germ-free (GF) or specific pathogen-free (SPF) mice treated with antibiotics, to reduce the microbial diversity within the intestine, showed that several neurological problems occur in mice with reduced or lack of proper mature gut microbiota (7, 10, 14, 15, 34, 80, 81).”
From The gut-brain axis: how microbiota and host inflammasome influence brain physiology and pathology (2020) · cites this paper as [81]
In the citing paper
“In details, compared to colonized mice, GF mice showed exaggerated hypothalamic–pituitary–adrenal (HPA) restrain stress reaction (10), impared social behaviors (12, 15, 82), reduced anxiety-like behavior (7, 81–83) and increased motor and rearing activity (80, 84).”
From The gut-brain axis: how microbiota and host inflammasome influence brain physiology and pathology (2020) · cites this paper as [81]
In the citing paper
“The developmental abnormalities found in GF mice are totally reversible by colonization with intestinal bacteria early in life but not in adulthood, suggesting that the microbiome influences brain development.9,10”
From The Gut Microbiome and the Brain (2014) · cites this paper as [9]
In the citing paper
“Some investigations have shown neurochemical changes as a result of gut microbiome dysfunction, such as altered levels of brain-derived neurotropic factor (BDNF), reduced serotonin receptor expression, reduced synaptic plasticity gene expression, and increased striatal monoamine turnover [10–12].”
From Effect of fecal microbiota transplant on symptoms of psychiatric disorders: a systematic review (2020) · cites this paper as [12]
In the citing paper
“GF mouse models have shown that the serotonergic system in the brain is also influenced by the microbiota [24, 26], whereby excess peripheral Trp may cross the BBB to influence the rate serotonin synthesis in the brain [108].”
From The Gut Microbiota and Dysbiosis in Autism Spectrum Disorders (2018) · cites this paper as [24]
In the citing paper
“These findings suggest that gut microbes not only regulate gene expression in the mouse brain (Hoban et al., 2016; Neufeld et al., 2011; Stilling et al., 2015), but also affect alternative splicing (Stilling et al., 2018), and can regulate the production of specific isoforms of genes that have been implicated in ASD.”
From Human Gut Microbiota from Autism Spectrum Disorder Promote Behavioral Symptoms in Mice (2019) · cites this paper as Neufeld et al., 2011
In the citing paper
“In particular, studies using GF animals that demonstrated aberrant behavior and neurochemical profile were critical in establishing the link between the gut microbiota and brain development and processes (211-217).”
From Diet and the Microbiota–Gut–Brain Axis: Sowing the Seeds of Good Mental Health (2021) · cites this paper as [213]
In the citing paper
“Animal studies have demonstrated that the gut microbiota plays a crucial role in anxiety (Neufeld et al., 2011), cognitive performance (Desbonnet et al., 2015), repetitive behaviors (Desbonnet et al., 2014) and social communications (Buffington et al., 2016; Sherwin et al., 2017).”
From Microbiota-related Changes in Bile Acid & Tryptophan Metabolism are Associated with Gastrointestinal Dysfunction in a Mouse Model of Autism (2017) · cites this paper as Neufeld et al., 2011
Citations
Cites
Basic local alignment search tool
Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990) · Journal of Molecular Biology · doi:10.1006/jmbi.1990.9999 · Cited by 98,669
Primer3 on the WWW for General Users and for Biologist Programmers
Rozen, S., & Skaletsky, H. (2003) · Humana Press eBooks · doi:10.1385/1-59259-192-2:365 · Cited by 15,068
The Mouse Brain in Stereotaxic Coordinates
Paxinos, G. (2001) · Cited by 12,859
Genome-wide atlas of gene expression in the adult mouse brain
Lein, E. S., Hawrylycz, M. J., Ao, N., Ayres, M., Bensinger, A., Bernard, A., Boe, A. F., Boguski, M. S., Brockway, K. S., Byrnes, E. J., et al. (2007) · Nature · doi:10.1038/nature05453 · Cited by 5,572
Host-Bacterial Mutualism in the Human Intestine
Bäckhed, F., Ley, R. E., Sonnenburg, J. L., Peterson, D. A., & Gordon, J. I. (2005) · Science · doi:10.1126/science.1104816 · Cited by 5,277
The gut flora as a forgotten organ
O'Hara, A. M., & Shanahan, F. (2006) · The EMBO Reports · doi:10.1038/sj.embor.7400731 · Cited by 2,791
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
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
Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress
Berton, O., McClung, C. A., DiLeone, R. J., Krishnan, V., Renthal, W., Russo, S. J., Graham, D., Tsankova, N. M., Bolanos, C. A., Rios, M., et al. (2006) · Science · doi:10.1126/science.1120972 · Cited by 2,129
Sensitive periods in the development of the brain and behavior
Knudsen, E. I. (2004) · Journal of Cognitive Neuroscience · doi:10.1162/0898929042304796 · Cited by 1,842
NMDA receptor subunits: diversity, development and disease
Cull-Candy, S., Brickley, S., & Farrant, M. (2001) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(00)00215-4 · Cited by 1,694
Interactions between commensal intestinal bacteria and the immune system
Macpherson, A. J., & Harris, N. L. (2004) · Nature reviews. Immunology · doi:10.1038/nri1373 · Cited by 1,683
H OW H OST -M ICROBIAL I NTERACTIONS S HAPE THE N UTRIENT E NVIRONMENT OF THE M AMMALIAN I NTESTINE
Hooper, L. V., Midtvedt, T., & Gordon, J. I. (2002) · Annual Review of Nutrition · doi:10.1146/annurev.nutr.22.011602.092259 · Cited by 1,623
Pellow, S., & File, S. E. (1986) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(86)90552-6 · Cited by 1,534
Smith, M., Makino, S., Květňanský, R., & Post, R. M. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-03-01768.1995 · Cited by 1,449
Principles and clinical implications of the brain-gut-enteric microbiota axis
Rhee, S. H., Pothoulakis, C., & Mayer, E. A. (2009) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2009.35 · Cited by 1,342
Genetic variant BDNF (Val66Met) polymorphism alters anxiety-related behavior
Chen, Z.-Y., Jing, D., Bath, K. G., Ieraci, A., Khan, T., Siao, C.-J., Herrera, D. G., Toth, M., Yang, C., McEwen, B. S., et al. (2006) · Science · doi:10.1126/science.1129663 · Cited by 1,340
Hensch, T. K. (2004) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.27.070203.144327 · Cited by 1,300
The ascent of mouse: advances in modelling human depression and anxiety
Cryan, J. F., & Holmes, A. (2005) · Nature Reviews Drug Discovery · doi:10.1038/nrd1825 · Cited by 1,198
Whitehead, W. E., Palsson, O., & Jones, K. R. (2002) · Gastroenterology · doi:10.1053/gast.2002.32392 · Cited by 1,116
Anxiety, defence and the elevated plus-maze.
Rodgers, R., & Dalvi, A. (1997) · Neuroscience and Biobehavioral Reviews · doi:10.1016/s0149-7634(96)00058-9 · Cited by 1,028
Ethological and temporal analyses of anxiety-like behavior: The elevated plus-maze model 20 years on
Carobrez, A. P., & Bertoglio, L. J. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.04.017 · Cited by 993
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
Self-citationSerotonin receptor 1A knockout: An animal model of anxiety-related disorder
Ramboz, S., Oosting, R. S., Amara, D. A., Kung, H. F., Blier, P., Mendelsohn, M. M., Mann, J. J., Brunner, D., & Hen, R. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.24.14476 · Cited by 831
Influences of microbiota on intestinal immune system development.
Cebra, J. (1999) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/69.5.1046s · Cited by 819
Lactobacillus acidophilus modulates intestinal pain and induces opioid and cannabinoid receptors
Rousseaux, C., Thuru, X., Gelot, A., Barnich, N., Neut, C., Dubuquoy, L., Dubuquoy, C., Merour, E., Geboes, K., Chamaillard, M., et al. (2007) · Nature Medicine · doi:10.1038/nm1521 · Cited by 793
Interaction between BDNF and Serotonin: Role in Mood Disorders
Martinowich, K., & Lu, B. (2008) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301571 · Cited by 793
Increased anxiety of mice lacking the serotonin 1A receptor
Parks, C. L., Robinson, P. S., Sibille, E. L., Shenk, T. E., & Tóth, M. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.18.10734 · Cited by 691
Collins, S. M., & Bercik, P. (2009) · Gastroenterology · doi:10.1053/j.gastro.2009.01.075 · Cited by 612
The gut microbiota modulates host energy and lipid metabolism in mice
Velagapudi, V. R., Hezaveh, R., Reigstad, C. S., Gopalacharyulu, P., Yetukuri, L., Islam, S., Felin, J., Perkins, R., Borén, J., Orešič, M., et al. (2010) · Journal of Lipid Research · doi:10.1194/jlr.m002774 · Cited by 589
Roceri, M., Hendriks, W. J. A. J., Racagni, G., Ellenbroek, B. A., & Riva, M. A. (2002) · Molecular Psychiatry · doi:10.1038/sj.mp.4001036 · Cited by 474
Specific probiotic therapy attenuates antibiotic induced visceral hypersensitivity in mice
Verdú, E. F., Bercik, P., Verma-Gandhu, M., Huang, X.-X., Blennerhassett, P., Jackson, W., Mao, Y., Wang, L., Rochat, F., & Collins, S. M. (2006) · Gut · doi:10.1136/gut.2005.066100 · Cited by 448
Walker, J. R., Ediger, J. P., Graff, L. A., Greenfeld, J. M., Clara, I., Lix, L., Rawsthorne, P., Miller, N., Rogala, L., McPhail, C. M., et al. (2008) · The American Journal of Gastroenterology · doi:10.1111/j.1572-0241.2008.01980.x · Cited by 437
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
Self-citationBergami, M., Rimondini, R., Santi, S., Blum, R., Götz, M., & Canossa, M. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0803702105 · Cited by 415
Gastrointestinal microbiology enters the metagenomics era
Frank, D. N., & Pace, N. R. (2008) · Current Opinion in Gastroenterology · doi:10.1097/mog.0b013e3282f2b0e8 · Cited by 410
Rodrigues, S. M., Schafe, G. E., & LeDoux, J. E. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-17-06889.2001 · Cited by 350
LYTE, M., LI, W., OPITZ, N., GAYKEMA, R., & GOEHLER, L. (2006) · Physiology & Behavior · doi:10.1016/j.physbeh.2006.06.019 · Cited by 334
Sprouse, J. S., & Aghajanian, G. K. (1988) · Neuropharmacology · doi:10.1016/0028-3908(88)90079-2 · Cited by 333
Kunze, W. A., Mao, Y., Wang, B., Huizinga, J. D., Ma, X., Forsythe, P., & Bienenstock, J. (2009) · Journal of Cellular and Molecular Medicine · doi:10.1111/j.1582-4934.2009.00686.x · Cited by 328
Self-citationRoceri, M., Cirulli, F., Pessina, C., Peretto, P., Racagni, G., & Riva, M. A. (2004) · Biological Psychiatry · doi:10.1016/j.biopsych.2003.12.011 · Cited by 317
Holmes, A., Yang, R. J., Lesch, K., Crawley, J. N., & Murphy, D. L. (2003) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300266 · Cited by 316
Vagal and hormonal gut-brain communication: from satiation to satisfaction
Berthoud, H. ‐. (2008) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2008.01104.x · Cited by 307
The Mouse Defense Test Battery: pharmacological and behavioral assays for anxiety and panic
Blanchard, D. C., Griebel, G., & Blanchard, R. J. (2003) · European Journal of Pharmacology · doi:10.1016/s0014-2999(03)01276-7 · Cited by 295
Chun, J. J. M., Schatz, D. G., Oettinger, M. A., Jaenisch, R., & Baltimore, D. (1991) · Cell · doi:10.1016/0092-8674(91)90220-s · Cited by 287
Effects of centrally administered anxiolytic compounds in animal models of anxiety
Menard, J. L., & Treit, D. (1999) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(98)00056-6 · Cited by 280
IgA responses in the intestinal mucosa against pathogenic and non-pathogenic microorganisms
Macpherson, A. J., Hunziker, L., McCoy, K. D., & Lamarre, A. (2001) · Microbes and Infection · doi:10.1016/s1286-4579(01)01460-5 · Cited by 275
Rasmusson, A. M. (2002) · Neuropsychopharmacology · doi:10.1016/s0893-133x(02)00286-5 · Cited by 265
Corticosterone response to the plus-mazeHigh correlation with risk assessment in rats and mice
Rodgers, R. J., Haller, J., Holmes, A., Halász, J., WALTON, T., & Brain, P. F. (1999) · Physiology & Behavior · doi:10.1016/s0031-9384(99)00140-7 · Cited by 261
Li, W., Dowd, S. E., Scurlock, B., Acosta-Martinez, V., & Lyte, M. (2009) · Physiology & Behavior · doi:10.1016/j.physbeh.2008.12.004 · Cited by 246
Kamiya, T., Wang, L., Forsythe, P., Goettsche, G., Mao, Y., Wang, Y., Tougas, G., & Bienenstock, J. (2006) · Gut · doi:10.1136/gut.2005.070987 · Cited by 242
Self-citationWhitfield, H. J., Brady, L. S., Smith, M. A., Mamalaki, E., Fox, R. J., & Herkenham, M. A. (1990) · Cellular and Molecular Neurobiology · doi:10.1007/bf00733641 · Cited by 187
Alfonso, J., Frick, L. R., Silberman, D. M., Palumbo, M. L., Genaro, A. M., & Frasch, A. C. C. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.06.036 · Cited by 179
Influence of differential housing on emotional behaviour and neurotrophin levels in mice
Zhu, S., Yee, B. K., Nyffeler, M., Winblad, B. G., Feldon, J., & Mohammed, A. H. S. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.11.024 · Cited by 174
Kennett, G. A., Marcou, M., Dourish, C. T., & Curzon, G. (1987) · European Journal of Pharmacology · doi:10.1016/0014-2999(87)90336-0 · Cited by 172
Psychological factors in the irritable bowel syndrome.
Creed, F. H., & Guthrie, E. (1987) · Gut · doi:10.1136/gut.28.10.1307 · Cited by 160
Walf, A., Koonce, C. J., Manley, K., & Frye, C. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.09.016 · Cited by 153
Reyes, T. M., Walker, J. R., DeCino, C., Hogenesch, J. B., & Sawchenko, P. E. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-13-05607.2003 · Cited by 149
Adamec, R., Head, D., Blundell, J., Burton, P., & Berton, O. (2006) · Physiology & Behavior · doi:10.1016/j.physbeh.2006.03.005 · Cited by 145
David, D. J. P., Klemenhagen, K. C., Holick, K. A., Saxe, M., Mendez‐David, I., Santarelli, L., Craig, D. A., Zhong, H., Swanson, C. J., Hegde, L. G., et al. (2007) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.106.109678 · Cited by 142
de Armentia, M. L., & Sah, P. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-17-06876.2003 · Cited by 134
Alcohol Exposure Alters NMDAR Function in the Bed Nucleus of the Stria Terminalis
Kash, T. L., Baucum, A. J., Conrad, K. L., Colbran, R. J., & Winder, D. G. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2009.69 · Cited by 133
Hünnerkopf, R., Strobel, A., Gutknecht, L., Brocke, B., & Lesch, K. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301383 · Cited by 133
Ren‐Patterson, R. F., Cochran, L. W., Holmes, A., Sherrill, S., Huang, S., Tolliver, T. J., Lesch, K., Lu, B., & Murphy, D. L. (2005) · Journal of Neuroscience Research · doi:10.1002/jnr.20410 · Cited by 130
Examination of behavioral deficits triggered by targeting BDNF in fetal or postnatal brains of mice
Chan, J., Unger, T. J., BYRNES, J. J., & Rios, M. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.06.002 · Cited by 125
Anxiety-related traits in mice with modified genes of the serotonergic pathway
Lesch, K., Zeng, Y., Reif, A., & Gutknecht, L. (2003) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2003.08.106 · Cited by 116
Neuropathophysiology of functional gastrointestinal disorders
Wood, J. D. (2007) · World Journal of Gastroenterology · doi:10.3748/wjg.v13.i9.1313 · Cited by 111
Hypersensitivity for capsaicin in patients with functional dyspepsia
Hammer, J., Führer, M., Pipal, L., & Matiasek, J. (2007) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2007.00997.x · Cited by 107
Bhatnagar, S., Sun, L. M., Raber, J., Maren, S., Julius, D. J., & Dallman, M. F. (2004) · Physiology & Behavior · doi:10.1016/j.physbeh.2004.01.018 · Cited by 106
Wang, B., Mao, Y., Diorio, C. J., Wang, L., Huizinga, J. D., Bienenstock, J., & Kunze, W. (2009) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2009.01384.x · Cited by 106
Self-citationDwivedi, Y., Mondal, A. C., Payappagoudar, G. V., & Rizavi, H. S. (2004) · Neuropharmacology · doi:10.1016/j.neuropharm.2004.10.004 · Cited by 97
Ma, X., Mao, Y., Wang, B., Huizinga, J. D., Bienenstock, J., & Kunze, W. (2009) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.90511.2008 · Cited by 93
Self-citationButterweck, V, Winterhoff, H., & Herkenham, M. (2001) · Molecular Psychiatry · doi:10.1038/sj.mp.4000937 · Cited by 91
Itoh, K., Hashimoto, K., Kumakiri, C., Shimizu, E., & Iyo, M. (2003) · American Journal of Medical Genetics Part B Neuropsychiatric Genetics · doi:10.1002/ajmg.b.20078 · Cited by 85
Effects of gut microbiota on the brain: implications for psychiatry
Neufeld, K. M., & Foster, J. A. (2009) · Journal of Psychiatry and Neuroscience · doi:10.1139/jpn.0931 · Cited by 76
Self-citationProgesterone modulation of α5 nAChR subunits influences anxiety‐related behavior during estrus cycle
Gangitano, D., Salas, R., Teng, Y., Perez, E., & De Biasi, M. (2009) · Genes, Brain and Behavior · doi:10.1111/j.1601-183x.2009.00476.x · Cited by 76
Li, Q., Holmes, A., Ma, L., de Kar, L. D. V., García, F., & Murphy, D. L. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.3223-04.2004 · Cited by 66
Rodgers, R. J., Davies, B., & Shore, R. F. (2002) · Genes Brain & Behavior · doi:10.1034/j.1601-183x.2002.10406.x · Cited by 65
Brain-gut axis and mucosal immunity: a perspective on mucosal psychoneuroimmunology.
Shanahan, F. (1999) · PubMed · Cited by 57
Bohmaker, K., Eison, A. S., Yocca, F. D., et al. (1993) · Neuropharmacology · doi:10.1016/0028-3908(93)90048-8 · Cited by 53
Kotlinska, J. H., & Liljequist, S. (1998) · Psychopharmacology · doi:10.1007/s002130050499 · Cited by 52
Effects of NMDA antagonists on ethanol-withdrawal induced “anxiety” in the elevated plus maze
Gatch, M. B., Wallis, C. J., & Lal, H. (1999) · Alcohol · doi:10.1016/s0741-8329(99)00045-2 · Cited by 51
Neurobehavioral Changes Resulting from Recombinase Activation Gene 1 Deletion
Cushman, J. D., Lo, J., Huang, Z. L., Wasserfall, C. H., & Petitto, J. M. (2003) · Clinical and Vaccine Immunology · doi:10.1128/cdli.10.1.13-18.2003 · Cited by 51
Drossman, D. A. (2005) · Journal of Clinical Gastroenterology · doi:10.1097/01.mcg.0000156107.13247.69 · Cited by 46
Bouwknecht, J. A., van der Gugten, J., Groenink, L., Olivier, B., & Paylor, R. E. (2004) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2004.04.036 · Cited by 44
Serotonin receptor binding and mRNA expression in the hippocampus of fearful amygdala-kindled rats
Kalynchuk, L. E., Pinel, J. P. J., & Meaney, M. J. (2005) · Neuroscience Letters · doi:10.1016/j.neulet.2005.11.005 · Cited by 35
Foster, J. A., Puchowicz, M. J., McIntyre, D., & Herkenham, M. A. (2004) · The Journal of Comparative Neurology · doi:10.1002/cne.20197 · Cited by 30
Self-citationKaiyala, K. J., Vincow, E. S., Sexton, T. J., & Neumaier, J. F. (2003) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(03)00152-7 · Cited by 21
Anxiolytic-like action of intra-hippocampally administered NMDA antagonists in rats.
Jessa, M., Nazar, M., & Płaźnik, A. (1995) · PubMed · Cited by 17
Research works printed but not linked: 1
- Neufeld, 2008, Impact of intestinal microbiota on anxiety-like behaviour, Neurogastroenterol Motil, 20, 125
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
Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour
Cryan, J. F., & Dinan, T. G. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3346 · Cited by 4,572
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
Self-citationGut microbiota regulate motor deficits and neuroinflammation in a model of Parkinson's disease
Sampson, T. R., Debelius, J. W., Thron, T., Janssen, S., Shastri, G. G., Ilhan, Z. E., Challis, C., Schretter, C. E., Rocha, S., Gradinaru, V., et al. (2016) · Cell · doi:10.1016/j.cell.2016.11.018 · Cited by 3,622
The gut microbiota--masters of host development and physiology
Sommer, F., & Bäckhed, F. (2013) · Nature Reviews Microbiology · doi:10.1038/nrmicro2974 · Cited by 3,681
Metadata
- Authors
- Neufeld, K. M., Kang, N., Bienenstock, J., & Foster, J. A.
- Affiliations
- St. Joseph’s Healthcare Hamilton (CA)
- Corresponding author
- Foster, J. A.
- Venue
- Neurogastroenterology & Motility
- Publisher
- Wiley
- Published
- 2010-11-05
- Volume
- 23
- Issue
- 3
- Pages
- 255-e119
- ISSN
- 1350-1925 (ISSN-L)
- OpenAlex
- W1920510593
- Cited by
- 1,392
- References
- 89
- Citations by year
- 2026: 49 · 2025: 72 · 2024: 90 · 2023: 86 · 2022: 131 · 2021: 173 · 2020: 134 · 2019: 118 · 2018: 108 · 2017: 106 · 2016: 111 · 2015: 71 · 2014: 53 · 2013: 48 · 2012: 29
- FWCI
- 11.72
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neurogastroenterology & Motility (publishedVersion)
- PubMed (publishedVersion)
- Funders
- University of California, Irvine
- 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 › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- germ-free mice, gut microbiota, gut-brain axis, anxiety-like behavior, elevated plus maze, central amygdala, NR2B, brain-derived neurotrophic factor, serotonin receptor 1A, hippocampus, hypothalamic-pituitary-adrenal axis, stress reactivity, neurochemical changes
- MeSH terms
- Animals, Anxiety, Behavior, Animal, Brain, Brain Chemistry, Corticosterone, Female, Germ-Free Life, Humans, Hypothalamo-Hypophyseal System, Motor Activity, Pituitary-Adrenal System, Stress, Psychological, Gene Expression, Receptors, Neurotransmitter, Neurotransmitter Agents, Gastrointestinal Tract, Mice, Metagenome
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 ›
Are you an author, or do you see a problem with this page? Request a review
