Maternal obese-type gut microbiota differentially impact cognition, anxiety and compulsive behavior in male and female offspring in mice
Open accessAbstract
Maternal obesity is known to predispose offspring to metabolic and neurodevelopmental abnormalities. While the mechanisms underlying these phenomena are unclear, high fat diets dramatically alter intestinal microbiota, and gut microbiota can impact physiological function. To determine if maternal diet-induced gut dysbiosis can disrupt offspring neurobehavioral function, we transplanted high fat diet- (HFD) or control low fat diet-associated (CD) gut microbiota to conventionally-housed female mice. Recipient mice were then bred and the behavioral phenotype of male and female offspring was tracked. While maternal behavior was unaffected, neonatal offspring from HFD dams vocalized less upon maternal separation than pups from CD dams. Furthermore, weaned male offspring from HFD dams had significant and selective disruptions in exploratory, cognitive, and stereotypical/compulsive behavior compared to male offspring from CD dams; while female offspring from HFD dams had increases in body weight and adiposity. 16S metagenomic analyses confirmed establishment of divergent microbiota in CD and HFD dams, with alterations in diversity and taxonomic distribution throughout pregnancy and lactation. Likewise, significant alterations in gut microbial diversity and distribution were noted in offspring from HFD dams compared to CD dams, and in males compared to females. Regression analyses of behavioral performance against differentially represented taxa suggest that decreased representation of specific members of the Firmicutes phylum predict behavioral decline in male offspring. Collectively, these data establish that high fat diet-induced maternal dysbiosis is sufficient to disrupt behavioral function in murine offspring in a sex-specific manner. Thus these data reinforce the essential link between maternal diet and neurologic programming in offspring and suggest that intestinal dysbiosis could link unhealthy modern diets to the increased prevalence of neurodevelopmental and childhood disorders.
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Another study showed that HFD-exposed offspring expressed less vocalizations during maternal separation experiments than control diet offspring.
“Another study showed similar results; HFD-exposed offspring expressed less vocalizations during maternal separation experiments, a measure of early life stress in the offspring, than control diet offspring.”
From Gastrointestinal Issues and Autism Spectrum Disorder (2020) · cites this paper as [61]
Members of the Firmicutes phyla were implicated in the gut microbiome dysbiosis and behavioral correlates.
“In these experiments, members of the Firmicutes phyla were implicated in the gut microbiome dysbiosis and behavioral correlates 61.”
From Gastrointestinal Issues and Autism Spectrum Disorder (2020) · cites this paper as [61]
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Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
Love, M. I., Huber, W., & Anders, S. (2014) · Genome Biology · doi:10.1186/s13059-014-0550-8 · Cited by 95,106 · see citing works
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools
Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., & Glöckner, F. O. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks1219 · Cited by 33,055 · see citing works
UPARSE: highly accurate OTU sequences from microbial amplicon reads
Edgar, R. C. (2013) · Nature Methods · doi:10.1038/nmeth.2604 · Cited by 16,587 · see citing works
An obesity-associated gut microbiome with increased capacity for energy harvest
Turnbaugh, P. J., Ley, R. E., Mahowald, M. A., Magrini, V., Mardis, E. R., & Gordon, J. I. (2006) · Nature · doi:10.1038/nature05414 · Cited by 12,444 · see citing works
Kozich, J. J., Westcott, S. L., Baxter, N. T., Highlander, S. K., & Schloss, P. D. (2013) · Applied and Environmental Microbiology · doi:10.1128/aem.01043-13 · Cited by 7,004 · see citing works
Everard, A., Belzer, C., Geurts, L., Ouwerkerk, J. P., Druart, C., Bindels, L. B., Guiot, Y., Derrien, M., Muccioli, G. G., Delzenne, N. M., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1219451110 · Cited by 4,511 · 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
Turnbaugh, P. J., Bäckhed, F., Fulton, L., & Gordon, J. I. (2008) · Cell Host & Microbe · doi:10.1016/j.chom.2008.02.015 · Cited by 2,915 · see citing works
Peng, L., Li, Z.-R., Green, R. S., Holzmanr, I. R., & Lin, J. (2009) · The Journal of Nutrition · doi:10.3945/jn.109.104638 · Cited by 2,130 · see citing works
Prevalence of obesity in the United States, 2009-2010.
Ogden, C. L., Carroll, M. D., Kit, B. K., & Flegal, K. M. (2012) · PubMed · Cited by 2,070 · see citing works
Regulation of short-chain fatty acid production
Macfarlane, S., & Macfarlane, G. T. (2003) · Proceedings of the Nutrition Society · doi:10.1079/pns2002207 · Cited by 1,939 · see citing works
Clarke, G., Grenham, S., Scully, P., Fitzgerald, P., Moloney, R. D., Shanahan, F., Dinan, T. G., & Cryan, J. F. (2013) · Molecular Psychiatry · doi:10.1038/mp.2012.77 · Cited by 1,893 · see citing works
Human gut microbiota in obesity and after gastric bypass
Zhang, H., DiBaise, J. K., Zuccolo, A., Kudrna, D., Braidotti, M., Yu, Y., Parameswaran, P., Crowell, M. D., Wing, R., Rittmann, B. E., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0812600106 · Cited by 1,880 · see citing works
Neuroligins and neurexins link synaptic function to cognitive disease
Südhof, T. C. (2008) · Nature · doi:10.1038/nature07456 · Cited by 1,849 · see citing works
Trends in the prevalence of developmental disabilities in US children, 1997-2008
Boyle, C. A., Boulet, S., Schieve, L. A., Cohen, R. A., Blumberg, S. J., Yeargin-Allsopp, M., Visser, S., & Kogan, M. D. (2011) · Pediatrics · doi:10.1542/peds.2010-2989 · Cited by 1,732 · see citing works
Schwabe, R. F., & Jobin, C. (2013) · Nature Reviews Cancer · doi:10.1038/nrc3610 · Cited by 1,689 · see citing works
Behavioural phenotyping assays for mouse models of autism
Silverman, J. L., Yang, M., Lord, C., & Crawley, J. N. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2851 · Cited by 1,462 · see citing works
UniFrac – An online tool for comparing microbial community diversity in a phylogenetic context
Lozupone, C., Hamady, M., & Knight, R. D. (2006) · BMC Bioinformatics · doi:10.1186/1471-2105-7-371 · Cited by 1,454 · see citing works
Potential beneficial effects of butyrate in intestinal and extraintestinal diseases
Canani, R. B. (2011) · World Journal of Gastroenterology · doi:10.3748/wjg.v17.i12.1519 · Cited by 1,381 · see citing works
Kim, K., Gu, W., Lee, I., Joh, E., & Kim, D. (2012) · PLoS ONE · doi:10.1371/journal.pone.0047713 · Cited by 1,184 · see citing works
Microbial reconstitution reverses maternal diet-induced social and synaptic deficits in offspring
Buffington, S. A., Di Prisco, G. V., Auchtung, T. A., Ajami, N. J., Petrosino, J. F., & Costa-Mattioli, M. (2016) · Cell · doi:10.1016/j.cell.2016.06.001 · Cited by 1,163 · see citing works
The indigenous gastrointestinal microflora
Berg, R. (1996) · Trends in Microbiology · doi:10.1016/0966-842x(96)10057-3 · Cited by 1,153 · see citing works
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 · see citing works
Yu, Z., Han, S., Zhu, J., Sun, X., Ji, C., & Guo, X. (2013) · PLoS ONE · doi:10.1371/journal.pone.0061627 · Cited by 851 · see citing works
Choleris, E. (2001) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(01)00011-2 · Cited by 761 · see citing works
Obese-type gut microbiota induce neurobehavioral changes in the absence of obesity
Bruce-Keller, A. J., Salbaum, J. M., Luo, M., Blanchard, E., Taylor, C. M., Welsh, D. A., & Berthoud, H.-R. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.07.012 · Cited by 563 · see citing works
Self-citationLinkage of gut microbiome with cognition in hepatic encephalopathy
Bajaj, J. S., Ridlon, J. M., Hylemon, P. B., Thacker, L. R., Heuman, D. M., Smith, S., Sikaroodi, M., & Gillevet, P. M. (2012) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00190.2011 · Cited by 547 · see citing works
Depletion of Murine Intestinal Microbiota: Effects on Gut Mucosa and Epithelial Gene Expression
Reikvam, D. H., Erofeev, A. S., Sandvik, A., Grcic, V., Jahnsen, F. L., Gaustad, P., McCoy, K. D., Macpherson, A. J., Meza‐Zepeda, L. A., & Johansen, F. (2011) · PLoS ONE · doi:10.1371/journal.pone.0017996 · Cited by 531 · see citing works
Evaluation of Methods for the Extraction and Purification of DNA from the Human Microbiome
Yuan, S., Cohen, D. B., Ravel, J., Abdo, Z., & Forney, L. J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0033865 · Cited by 511 · see citing works
Prevalence of obesity among adults: United States, 2011-2012.
Ogden, C. L., Carroll, M. D., Kit, B. K., & Flegal, K. M. (2013) · PubMed · Cited by 502 · see citing works
Enduring consequences of maternal obesity for brain inflammation and behavior of offspring
Bilbo, S. D., & Tsang, V. (2010) · The FASEB Journal · doi:10.1096/fj.09-144014 · Cited by 489 · see citing works
Evaluation of marble-burying behavior as a model of anxiety
Njung'e, K., & Handley, S. L. (1991) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(91)90590-x · Cited by 487 · see citing works
Scattoni, M. L., Crawley, J. N., & Ricceri, L. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.08.003 · Cited by 473 · see citing works
Gene expression patterns in human placenta
Sood, R., Zehnder, J. L., Druzin, M. L., & Brown, P. O. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0508035103 · Cited by 454 · see citing works
Olfson, M., Blanco, C., Wang, S., Laje, G., & Correll, C. U. (2014) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2013.3074 · Cited by 449 · see citing works
Wang, L., Christophersen, C. T., Sorich, M. J., Gerber, J. P., Angley, M. T., & Conlon, M. A. (2013) · Molecular Autism · doi:10.1186/2040-2392-4-42 · Cited by 418 · see citing works
Lyte, M. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003726 · Cited by 399 · see citing works
Marble Burying and Nestlet Shredding as Tests of Repetitive, Compulsive-like Behaviors in Mice
Angoa‐Pérez, M., Kane, M. J., Briggs, D. I., Francescutti, D. M., & Kuhn, D. M. (2013) · Journal of Visualized Experiments · doi:10.3791/50978 · Cited by 391 · see citing works
Microbiome and metabolic disease: revisiting the bacterial phylum Bacteroidetes
Johnson, E. L., Heaver, S. L., Walters, W. A., & Ley, R. E. (2017) · Journal of Molecular Medicine · doi:10.1007/s00109-016-1492-2 · Cited by 389 · see citing works
An overview of links between obesity and mental health
Avila, C., Holloway, A. C., Hahn, M. K., Morrison, K. M., Restivo, M., Anglin, R., & Taylor, V. H. (2015) · Current Obesity Reports · doi:10.1007/s13679-015-0164-9 · Cited by 366 · see citing works
Shih, R. A., Belmonte, P. L., & Zandi, P. P. (2004) · International Review of Psychiatry · doi:10.1080/09540260400014401 · Cited by 341 · see citing works
Sex differences in developmental programming models
Aiken, C., & Ozanne, S. E. (2012) · Reproduction · doi:10.1530/rep-11-0489 · Cited by 340 · see citing works
Linking the gut microbiota to human health
Robles, V., & Guarner, F. (2013) · British Journal Of Nutrition · doi:10.1017/s0007114512005235 · Cited by 307 · see citing works
Gut microbiota and gastrointestinal health: current concepts and future directions
Aziz, Q., Doré, J., Emmanuel, A., Guarner, F., & Quigley, E. M. M. (2013) · Neurogastroenterology & Motility · doi:10.1111/nmo.12046 · Cited by 280 · see citing works
Ohland, C. L., Kish, L., Bell, H., Thiesen, A., Hotte, N., Pankiv, E., & Madsen, K. L. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.02.008 · Cited by 273 · see citing works
Murphy, E. F., Cotter, P. D., Hogan, A., O’Sullivan, Ó., Joyce, A., Fouhy, F., Clarke, S. F., Marques, T. M., O’Toole, P. W., Stanton, C., et al. (2012) · Gut · doi:10.1136/gutjnl-2011-300705 · Cited by 273 · see citing works
Mao, J., Zhang, X., Sieli, P. T., Falduto, M. T., Torres, K. E., & Rosenfeld, C. S. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1000440107 · Cited by 261 · see citing works
Understanding the interactions between bacteria in the human gut through metabolic modeling
Shoaie, S., Karlsson, F. H., Mardinoğlu, A., Nookaew, I., Bordel, S., & Nielsen, J. (2013) · Scientific Reports · doi:10.1038/srep02532 · Cited by 260 · see citing works
Sweeney, T. E., & Morton, J. M. (2013) · JAMA Surgery · doi:10.1001/jamasurg.2013.5 · Cited by 250 · see citing works
White, C. L., Pistell, P. J., Purpera, M. N., Gupta, S., Fernandez-Kim, S.-O., Hise, T. L., Keller, J. N., Ingram, D. K., Morrison, C. D., & Bruce-Keller, A. J. (2009) · Neurobiology of Disease · doi:10.1016/j.nbd.2009.04.002 · Cited by 245 · see citing works
Self-citationMicrobiome disturbances and autism spectrum disorders
Rosenfeld, C. S. (2015) · Drug Metabolism and Disposition · doi:10.1124/dmd.115.063826 · Cited by 229 · see citing works
Gallou-Kabani, C., Gabory, A., Tost, J., Karimi, M., Mayeur, S., Lesage, J., Boudadi, E., Gross, M.-S., Taurelle, J., Vigé, A., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0014398 · Cited by 229 · see citing works
Buie, T., Fuchs, G. J., Furuta, G. T., Kooros, K., Levy, J., Lewis, J. D., Wershil, B. K., & Winter, H. (2010) · Pediatrics · doi:10.1542/peds.2009-1878d · Cited by 228 · see citing works
Progress toward treatments for synaptic defects in autism
Delorme, R., Ey, E., Toro, R., Leboyer, M., Gillberg, C., & Bourgeron, T. (2013) · Nature Medicine · doi:10.1038/nm.3193 · Cited by 218 · see citing works
Maternal high fat diet consumption during the perinatal period programs offspring behavior
Sullivan, E. L., Nousen, E. K., & Chamlou, K. A. (2014) · Physiology & Behavior · doi:10.1016/j.physbeh.2012.07.014 · Cited by 217 · see citing works
Early prenatal stress impact on coping strategies and learning performance is sex dependent
Mueller, B. R., & Bale, T. L. (2007) · Physiology & Behavior · doi:10.1016/j.physbeh.2007.01.017 · Cited by 216 · see citing works
Effect of Intestinal Microbial Ecology on the Developing Brain
Douglas‐Escobar, M., Elliott, E., & Neu, J. (2013) · Archives of Pediatrics and Adolescent Medicine · doi:10.1001/jamapediatrics.2013.497 · Cited by 207 · see citing works
Collins, S. M., Kassam, Z., & Berčík, P. (2013) · Current Opinion in Microbiology · doi:10.1016/j.mib.2013.06.004 · Cited by 206 · see citing works
Gabory, A., Ferry, L., Fajardy, I., Jouneau, L., Gothié, J.-D., Vigé, A., Fleur, C., Mayeur, S., Gallou-Kabani, C., Gross, M.-S., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0047986 · Cited by 204 · see citing works
Maternal obesity is necessary for programming effect of high-fat diet on offspring
White, C. L., Purpera, M. N., & Morrison, C. D. (2009) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.91015.2008 · Cited by 198 · see citing works
Desulfovibrio species are potentially important in regressive autism
Finegold, S. M. (2011) · Medical Hypotheses · doi:10.1016/j.mehy.2011.04.032 · Cited by 197 · see citing works
Gut microbiome composition is associated with temperament during early childhood
Christian, L. M., Galley, J. D., Hade, E. M., Schoppe-Sullivan, S., Kamp Dush, C., & Bailey, M. T. (2015) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2014.10.018 · Cited by 191 · see citing works
Veena, S. R., Galé, C. R., Krishnaveni, G. V., Kehoe, S. H., Srinivasan, K., & Fall, C. H. D. (2016) · BMC Pregnancy and Childbirth · doi:10.1186/s12884-016-1011-z · Cited by 186 · see citing works
Chu, D. M., Meyer, K. M., Prince, A., & Aagaard, K. M. (2016) · Gut Microbes · doi:10.1080/19490976.2016.1241357 · Cited by 186 · see citing works
Maternal Obesity Is Associated with Alterations in the Gut Microbiome in Toddlers
Galley, J. D., Bailey, M. T., Dush, C. M. K., Schoppe‐Sullivan, S. J., & Christian, L. M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0113026 · Cited by 180 · see citing works
Parental Dietary Fat Intake Alters Offspring Microbiome and Immunity
Myles, I. A., Fontecilla, N. M., Janelsins, B., Vithayathil, P. J., Segre, J. A., & Datta, S. K. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1301057 · Cited by 174 · see citing works
Kang, S. S., Kurti, A., Fair, D. A., & Fryer, J. D. (2014) · Journal of Neuroinflammation · doi:10.1186/s12974-014-0156-9 · Cited by 167 · see citing works
Nahum Sacks, K., Friger, M., Shoham-Vardi, I., Abokaf, H., Spiegel, E., Sergienko, R., Landau, D., & Sheiner, E. (2016) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2016.03.030 · Cited by 165 · see citing works
Regulation of innate and adaptive immunity by the commensal microbiota
Jarchum, I., & Pamer, E. G. (2011) · Current Opinion in Immunology · doi:10.1016/j.coi.2011.03.001 · Cited by 152 · see citing works
Kim, D. W., Young, S. L., Grattan, D. R., & Jasoni, C. L. (2014) · Biology of Reproduction · doi:10.1095/biolreprod.113.117259 · Cited by 138 · see citing works
The mind-body-microbial continuum
Gonzalez, A., Stombaugh, J., Lozupone, C., Turnbaugh, P. J., Gordon, J. I., & Knight, R. D. (2011) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2011.13.1/agonzalez · Cited by 132 · see citing works
Maternal Dietary Fat Intake in Association With Autism Spectrum Disorders
Lyall, K., Munger, K. L., O'Reilly, É. J., Santangelo, S. L., & Ascherio, A. (2013) · American Journal of Epidemiology · doi:10.1093/aje/kws433 · Cited by 128 · see citing works
Gender-Dependent Effects of Maternal Immune Activation on the Behavior of Mouse Offspring
Xuan, I. C. Y., & Hampson, D. R. (2014) · PLoS ONE · doi:10.1371/journal.pone.0104433 · Cited by 127 · see citing works
Metabolic tinkering by the gut microbiome
Selkrig, J., Wong, P., Zhang, X., & Pettersson, S. (2014) · Gut Microbes · doi:10.4161/gmic.28681 · Cited by 116 · see citing works
Association Between Maternal Obesity and Autism Spectrum Disorder in Offspring: A Meta-analysis
Li, Y., Ou, J., Liu, L., Zhang, D., Zhao, J., & Tang, S. (2015) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-015-2549-8 · Cited by 104 · see citing works
Yi, P., & Li, L. (2011) · Veterinary Microbiology · doi:10.1016/j.vetmic.2011.10.024 · Cited by 94 · see citing works
Obesity increases cerebrocortical reactive oxygen species and impairs brainfunction
Freeman, L. R., Zhang, L., Nair, A. R., Dasuri, K., Francis, J., Fernandez-Kim, S.-O., Bruce‐Keller, A. J., & Keller, J. N. (2012) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2012.08.577 · Cited by 92 · see citing works
Self-citationBested, A. C., Logan, A. C., & Selhub, E. M. (2013) · Gut Pathogens · doi:10.1186/1757-4749-5-4 · Cited by 84 · see citing works
Maloney, C., Hay, S. M., Young, L. E., Sinclair, K. D., & Rees, W. D. (2010) · Journal of Nutrition · doi:10.3945/jn.109.119453 · Cited by 79 · see citing works
Rodriguez, J. S., Rodríguez‐González, G. L., Reyes‐Castro, L. A., Ibáñez, C., Ramírez, A., Chavira, R., Larrea, F., Nathanielsz, P. W., & Zambrano, E. (2012) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2011.12.012 · Cited by 77 · see citing works
Marble Burying and Nestlet Shredding as Tests of Repetitive, Compulsive-like Behaviors in Mice
Angoa‐Pérez, M., Kane, M. J., Briggs, D. I., Francescutti, D. M., & Kuhn, D. M. (2013) · Journal of Visualized Experiments · doi:10.3791/50978-v · Cited by 71 · see citing works
Microbiome to Brain: Unravelling the Multidirectional Axes of Communication
Aidy, S. E., Stilling, R. M., Dinan, T. G., & Cryan, J. F. (2016) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-20215-0_15 · Cited by 64 · see citing works
Friedman, J. E. (2015) · Diabetes Care · doi:10.2337/dc15-0628 · Cited by 59 · see citing works
Zolbanin, J. M., Doosti, M.-H., Kosari‐Nasab, M., & Salari, A. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.03.016 · Cited by 57 · see citing works
Probiotics in the Treatment of Depression: Science or Science Fiction?
Dinan, T. G., & Quigley, E. M. M. (2011) · Australian & New Zealand Journal of Psychiatry · doi:10.3109/00048674.2011.613766 · Cited by 53 · see citing works
The microbiome and childhood diseases: Focus on brain‐gut axis
O’Mahony, S. M., Stilling, R. M., Dinan, T. G., & Cryan, J. F. (2015) · Birth Defects Research Part C Embryo Today Reviews · doi:10.1002/bdrc.21118 · Cited by 50 · see citing works
Wilcoxon, J. S., Schwartz, J., Aird, F., & Redei, E. E. (2003) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00552.2002 · Cited by 39 · see citing works
Maftei, O., Whitrow, M. J., Davies, M. J., Giles, L. C., Owens, J. A., & Moore, V. (2014) · Diabetic Medicine · doi:10.1111/dme.12637 · Cited by 34 · see citing works
Gene–environment interactions in psychopathology throughout early childhood
Pinto, R., Soares, I., Carvalho-Correia, E., & Mesquita, A. R. (2015) · Psychiatric Genetics · doi:10.1097/ypg.0000000000000106 · Cited by 24 · see citing works
Effects of Microbes on Germfree Animals
Luckey, T. D. (1965) · Advances in applied microbiology · doi:10.1016/s0065-2164(08)70387-3 · Cited by 24 · see citing works
Lerch, S., Dormann, C., Brandwein, C., Gass, P., & Chourbaji, S. (2015) · Laboratory Animals · doi:10.1177/0023677215603260 · Cited by 9 · see citing works
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Rivell, A., & Mattson, M. P. (2019) · Trends in Neurosciences · doi:10.1016/j.tins.2019.08.006 · Cited by 50 · see citing works
Probiotics in human mental health and diseases—A minireview
Sivamaruthi, B. S., Prasanth, M. I., Kesika, P., & Chaiyasut, C. (2021) · Tropical Journal of Pharmaceutical Research · doi:10.4314/tjpr.v18i4.29 · Cited by 44 · see citing works
- Authors
- Bruce-Keller, A. J., Fernandez-Kim, S.-O., Townsend, R. L., Kruger, C., Carmouche, R., Newman, S., Salbaum, J. M., & Berthoud, H.-R.
- Affiliations
- Pennington Biomedical Research Center (US)
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2017-04-25
- Volume
- 12
- Issue
- 4
- Pages
- e0175577
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC5404786
- OpenAlex
- W2610086359
- Cited by
- 76
- References
- 91
- Citations by year
- 2026: 3 · 2025: 11 · 2024: 3 · 2023: 8 · 2022: 12 · 2021: 10 · 2020: 11 · 2019: 8 · 2018: 8 · 2017: 2
- FWCI
- 3.24
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- PLoS ONE (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Funders
- Louisiana Clinical and Translational Science Center
- National Institutes of Health (NIH 2P30DK072476, 1U54-GM-104940, which funds the Louisiana Clinical, DK072476, 3P30-GM118430)
- National Institute of General Medical Sciences (P30GM118430, U54GM104940)
- National Institute of Diabetes and Digestive and Kidney Diseases (R01DK047348, P30DK072476)
- National Center for Complementary and Integrative Health (P50AT002776)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Keywords
- maternal obesity, gut microbiota, high-fat diet, gut dysbiosis, offspring neurobehavior, sex differences, anxiety, compulsive behavior, cognitive function, neonatal vocalizations, maternal separation, adiposity, Firmicutes, pregnancy and lactation, microbiota transplantation
- MeSH terms
- Gastrointestinal Microbiome, Animals, Animal Communication, Animals, Newborn, Anxiety, Cognition, Compulsive Behavior, Female, Male, Mice, Inbred C57BL, Obesity, Pregnancy, Prenatal Exposure Delayed Effects, Maternal Nutritional Physiological Phenomena, Adiposity
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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