Prenatal stress disrupts social behavior, cortical neurobiology and commensal microbes in adult male offspring
Open accessAbstract
In utero and early neonatal exposure to maternal stress is linked with psychiatric disorders, and the underlying mechanisms are currently being elucidated. We used a prenatal stressor in pregnant mice to examine novel relationships between prenatal stress exposure, changes in the gut microbiome, and social behavior. Here, we show that males exposed to prenatal stress had a significant reduction in social behavior in adulthood, with increased corticosterone release following social interaction. Male offspring exposed to prenatal stress also had neuroinflammation, decreased oxytocin receptor, and decreased serotonin metabolism in their cortex in adulthood, which are linked to decreased social behavior. Finally, we found a significant difference in commensal microbes, including decreases in Bacteroides and Parabacteroides, in adult male offspring exposed to prenatal stress when compared to non-stressed controls. Our findings indicate that gestation is a critical window where maternal stress contributes to the development of aberrant social behaviors and alterations in cortical neurobiology, and that prenatal stress is sufficient to disrupt the male gut-brain axis into adulthood.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
The microbiota and HPA axis develop rapidly and profoundly in the first years of life.
“The microbiota and HPA axis develop rapidly and profoundly in the first years of life, and environmental stressors can affect both (146–148).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [146]
Environmental stressors can affect both the microbiota and the HPA axis.
“The microbiota and HPA axis develop rapidly and profoundly in the first years of life, and environmental stressors can affect both (146–148).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [146]
Male offspring presented with deficits in social cognition only, without disturbances in the other behavior or cognitive parameters measured.
“In contrast, male offspring presented with deficits in social cognition only, without disturbances in the other behavior or cognitive parameters measured (146).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [146]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing
Benjamini, Y., & Hochberg, Y. (1995) · Journal of the Royal Statistical Society Series B: Statistical Methodology · doi:10.1111/j.2517-6161.1995.tb02031.x · Cited by 109,482 · see citing works
Kessler, R. C., Berglund, P., Demler, O., Jin, R., Merikangas, K. R., & Walters, E. E. (2005) · Archives of General Psychiatry · doi:10.1001/archpsyc.62.6.593 · Cited by 20,391 · see citing works
The Mouse Brain in Stereotaxic Coordinates
Paxinos, G. (2001) · Cited by 12,859 · see citing works
Indigenous bacteria from the gut microbiota regulate host serotonin biosynthesis
Yano, J. M., Yu, K., Donaldson, G. P., Shastri, G. G., Ann, P., Ma, L., Nagler, C. R., Ismagilov, R. F., Mazmanian, S. K., & Hsiao, E. Y. (2015) · Cell · doi:10.1016/j.cell.2015.02.047 · Cited by 3,614 · see citing works
Hsiao, E. Y., McBride, S. W., Hsien, S., Sharon, G., Hyde, E. R., McCue, T., Codelli, J. A., Chow, J., Reisman, S. E., Petrosino, J. F., et al. (2013) · Cell · doi:10.1016/j.cell.2013.11.024 · Cited by 3,283 · 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
Sex differences in autism spectrum disorders
Werling, D. M., & Geschwind, D. H. (2013) · Current Opinion in Neurology · doi:10.1097/wco.0b013e32835ee548 · Cited by 1,245 · see citing works
Bailey, M. T., Dowd, S. E., Galley, J. D., Hufnagle, A. R., Allen, R. G., & Lyte, M. (2011) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2010.10.023 · Cited by 1,123 · see citing works
Calcia, M., Bonsall, D. R., Bloomfield, P. S., Selvaraj, S., Barichello, T., & Howes, O. D. (2016) · Psychopharmacology · doi:10.1007/s00213-016-4218-9 · Cited by 710 · see citing works
Frith, C. D. (2007) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2006.2003 · Cited by 690 · see citing works
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 · see citing works
Genomic and epigenetic evidence for oxytocin receptor deficiency in autism
Gregory, S. G., Connelly, J. J., Towers, A. J., Johnson, J., Biscocho, D., Markunas, C. A., Lintas, C., Abramson, R. K., Wright, H. H., Ellis, P., et al. (2009) · BMC Medicine · doi:10.1186/1741-7015-7-62 · Cited by 576 · see citing works
Prefrontal Cortex and Social Cognition in Mouse and Man
Bicks, L. K., Koike, H., Akbarian, S., & Morishita, H. (2015) · Frontiers in Psychology · doi:10.3389/fpsyg.2015.01805 · Cited by 491 · see citing works
The Gut Microbiota and Autism Spectrum Disorders
Li, Q., Han, Y., Dy, A. B. C., & Hagerman, R. J. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00120 · Cited by 462 · see citing works
Neumann, Wigger, Torner, Holsboer, & Landgraf (2000) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2000.00442.x · Cited by 452 · see citing works
Leclercq, S., Mian, F. M., Stanisz, A. M., Bindels, L. B., Cambier, E., Ben-Amram, H., Koren, O., Forsythe, P., & Bienenstock, J. (2017) · Nature Communications · doi:10.1038/ncomms15062 · Cited by 434 · see citing works
Eisenberger, N. I., Inagaki, T. K., Mashal, N. M., & Irwin, M. R. (2010) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2009.12.009 · Cited by 413 · see citing works
Morley‐Fletcher, S., Rea, M., Maccari, S., & Laviola, G. (2003) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2003.03070.x · Cited by 373 · see citing works
McKim, D. B., Weber, M. D., Niraula, A., Sawicki, C. M., Liu, X., Jarrett, B. L., Ramirez-Chan, K., Wang, Y., Roeth, R. M., Sucaldito, A. D., et al. (2018) · Molecular Psychiatry · doi:10.1038/mp.2017.64 · Cited by 365 · see citing works
Timing of Prenatal Stressors and Autism
Beversdorf, D. Q., Manning, S. E., Hillier, A. J., Anderson, S. L., Nordgren, R. E., Walters, S., Nagaraja, H. N., Cooley, W. C., Gaelic, S. E., & Bauman, M. L. (2005) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-005-5037-8 · Cited by 359 · see citing works
Blood serotonin levels in autism spectrum disorder: A systematic review and meta-analysis
Gabriele, S., Sacco, R., & Persico, A. M. (2014) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2014.02.004 · Cited by 346 · see citing works
Jašarević, E., Howerton, C. L., Howard, C. D., & Bale, T. L. (2015) · Endocrinology · doi:10.1210/en.2015-1177 · Cited by 329 · see citing works
Bilbo, S. D., Block, C. L., Bolton, J. L., Hanamsagar, R., & Tran, P. K. (2017) · Experimental Neurology · doi:10.1016/j.expneurol.2017.07.002 · Cited by 323 · see citing works
Anxiety in early pregnancy: prevalence and contributing factors
Rubertsson, C., Hellström, J., Cross, M., & Sydsjö, G. (2014) · Archives of Women s Mental Health · doi:10.1007/s00737-013-0409-0 · Cited by 318 · see citing works
The social deficits of the oxytocin knockout mouse
Winslow, J. T., & Insel, T. R. (2002) · Neuropeptides · doi:10.1054/npep.2002.0909 · Cited by 307 · see citing works
Wohleb, E. S., McKim, D. B., Shea, D. T., Powell, N. D., Tarr, A. J., Sheridan, J. F., & Godbout, J. P. (2014) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.11.029 · Cited by 300 · see citing works
The contributions of oxytocin and vasopressin pathway genes to human behavior
Ebstein, R. P., Knafo, A., Mankuta, D., Chew, S. H., & Lai, P. S. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.12.014 · Cited by 283 · see citing works
Golubeva, A. V., Crampton, S., Desbonnet, L., Edge, D., O'Sullivan, O., Lomasney, K. W., Zhdanov, A. V., Crispie, F., Moloney, R. D., Borre, Y. E., et al. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.06.002 · Cited by 283 · see citing works
Prenatal stress generates deficits in rat social behavior: Reversal by oxytocin
Lee, P. R., Brady, D. L., Shapiro, R. A., Dorsa, D. M., & Koenig, J. I. (2007) · Brain Research · doi:10.1016/j.brainres.2007.04.042 · Cited by 270 · see citing works
Sankoorikal, G. M. V., Kaercher, K. A., Boon, C. J., Lee, J. K., & Brodkin, E. S. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.07.026 · Cited by 231 · see citing works
Atopic diseases and inflammation of the brain in the pathogenesis of autism spectrum disorders
Theoharides, T. C., Tsilioni, I., Patel, A., & Doyle, R. (2016) · Translational Psychiatry · doi:10.1038/tp.2016.77 · Cited by 231 · see citing works
Gur, T. L., Shay, L., Palkar, A. V., Fisher, S., Varaljay, V. A., Dowd, S., & Bailey, M. T. (2017) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2016.12.021 · Cited by 213 · see citing works
Ko, J. (2017) · Frontiers in Neural Circuits · doi:10.3389/fncir.2017.00041 · Cited by 212 · see citing works
Neuroinflammatory Dynamics Underlie Memory Impairments after Repeated Social Defeat
McKim, D. B., Niraula, A., Tarr, A. J., Wohleb, E. S., Sheridan, J. F., & Godbout, J. P. (2016) · The Journal of Neuroscience · doi:10.1523/jneurosci.2394-15.2016 · Cited by 204 · see citing works
Early-life adversity and brain development: Is the microbiome a missing piece of the puzzle?
O’Mahony, S. M., Clarke, G., Dinan, T. G., & Cryan, J. F. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2015.09.068 · Cited by 203 · see citing works
Diz-Chaves, Y., Astiz, M., Bellini, M. J., & García‐Segura, L. M. (2012) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2012.11.013 · Cited by 178 · see citing works
Coretti, L., Cristiano, C., Florio, E., Scala, G., Lama, A., Keller, S., Cuomo, M., Russo, R., Pero, R., Paciello, O., et al. (2017) · Scientific Reports · doi:10.1038/srep45356 · Cited by 175 · see citing works
Association of autism severity with a monoamine oxidase A functional polymorphism
Cohen, I., Liu, X., Schutz, C. K., White, B., Jenkins, E., Brown, W., & Holden, J. (2003) · Clinical Genetics · doi:10.1034/j.1399-0004.2003.00115.x · Cited by 152 · see citing works
Lukas, M., & Neumann, I. D. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.08.011 · Cited by 136 · see citing works
Bailey, M. T., Engler, H., & Sheridan, J. F. (2006) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2005.09.008 · Cited by 133 · see citing works
<scp>O</scp>xytocin modulation of neural circuits for social behavior
Marlin, B. J., & Froemke, R. C. (2017) · Developmental Neurobiology · doi:10.1002/dneu.22452 · Cited by 130 · see citing works
O’Connor, T. G., Monk, C. E., & Fitelson, E. M. (2013) · Journal of Child Psychology and Psychiatry · doi:10.1111/jcpp.12153 · Cited by 129 · see citing works
Nelson, L. H., & Lenz, K. M. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.09.006 · Cited by 120 · see citing works
(2005) · Archives of General Psychiatry · doi:10.1001/archpsyc.62.7.768 · Cited by 100 · see citing works
Autism Spectrum Disorders: Translating human deficits into mouse behavior
Pasciuto, E., Borrie, S. C., Kanellopoulos, A. K., Santos, A. R. S., Cappuyns, E., D’Andrea, L., Pacini, L., & Bagni, C. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.07.013 · Cited by 92 · see citing works
Long‐Term Impact of Early Life Events on Physiology and Behaviour
Boersma, G. J., Bale, T. L., Casanello, P. C., Lara, H. E., Lucion, A. B., Suchecki, D., & Tamashiro, K. L. (2014) · Journal of Neuroendocrinology · doi:10.1111/jne.12153 · Cited by 74 · see citing works
Brunson, K. L., Grigoriadis, D. E., Lorang, M. T., & Baram, T. Z. (2002) · Experimental Neurology · doi:10.1006/exnr.2002.7937 · Cited by 74 · see citing works
Stress and the Commensal Microbiota: Importance in Parturition and Infant Neurodevelopment
Gur, T., Worly, B. L., & Bailey, M. T. (2015) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2015.00005 · Cited by 69 · see citing works
Neuroendocrine and Immune Influences on the CNS: It's a Matter of Sex
Bale, T. L. (2009) · Neuron · doi:10.1016/j.neuron.2009.09.036 · Cited by 62 · see citing works
Ehrlich, D., & Rainnie, D. G. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.55 · Cited by 48 · see citing works
Wooddell, L. J., Hamel, A. F., Murphy, A. M., Byers, K. L., Kaburu, S., Meyer, J. S., Suomi, S. J., & Dettmer, A. M. (2017) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2017.06.018 · Cited by 48 · see citing works
Wilson, C., & Terry, A. V. (2012) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2012.12.015 · Cited by 32 · see citing works
Gu, F., Chauhan, V. P. S., & Chauhan, A. (2017) · Journal of Neuroscience Research · doi:10.1002/jnr.24027 · Cited by 29 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis
Rusch, J. A., Layden, B. T., & Dugas, L. R. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1130689 · Cited by 415 · see citing works
Frankiensztajn, L. M., Elliott, E., & Koren, O. (2020) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2019.12.003 · Cited by 248 · see citing works
Leigh, S., Uhlig, F., Wilmes, L., Sánchez-Díaz, P., Gheorghe, C. E., Goodson, M. S., Kelley‐Loughnane, N., Hyland, N. P., Cryan, J. F., & Clarke, G. A. (2023) · The Journal of Physiology · doi:10.1113/jp281951 · Cited by 193 · see citing works
Galley, J. D., Mashburn‐Warren, L., Blalock, L. C., Lauber, C. L., Carroll, J., Ross, K. M., Hobel, C. J., Coussons‐Read, M. E., Schetter, C. D., & Gur, T. (2022) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2022.10.005 · Cited by 120 · see citing works
Jabarin, R., Netser, S., & Wagner, S. (2022) · Molecular Autism · doi:10.1186/s13229-022-00521-6 · Cited by 113 · see citing works
Yang, H., Li, M., Zhou, M., Xu, H., Huan, F., Liu, N., Gao, R., Wang, J., Zhang, N., & Jiang, L. (2021) · Inflammation · doi:10.1007/s10753-021-01514-y · Cited by 101 · see citing works
Stress gets into the belly: Early life stress and the gut microbiome
Hantsoo, L. V., & Zemel, B. S. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113474 · Cited by 91 · see citing works
Chen, H. J., Antonson, A. M., Rajasekera, T. A., Patterson, J. M., Bailey, M. T., & Gur, T. (2020) · Translational Psychiatry · doi:10.1038/s41398-020-00876-5 · Cited by 89 · see citing works
Oliphant, K., Ali, M., D’Souza, M., Hughes, P. D., Sulakhe, D., Wang, A. Z., Xie, B., Yeasin, R., Msall, M. E., Andrews, B., et al. (2021) · Gut Microbes · doi:10.1080/19490976.2021.1997560 · Cited by 90 · see citing works
Gestational Factors throughout Fetal Neurodevelopment: The Serotonin Link
Hanswijk, S. I., Spoelder, M., Shan, L., Verheij, M. M. M., Muilwijk, O. G., Li, W., Liu, C., Kolk, S. M., & Homberg, J. R. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21165850 · Cited by 86 · see citing works
Aatsinki, A., Keskitalo, A., Laitinen, V., Munukka, E., Uusitupa, H., Lahti, L., Kortesluoma, S., Mustonen, P., Rodrigues, A. J., Coimbra, B., et al. (2020) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2020.104754 · Cited by 81 · see citing works
Audet, M. (2019) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2019.100772 · Cited by 79 · see citing works
Creutzberg, K. C., Sanson, A., Viola, T. W., Marchisella, F., Begni, V., Grassi‐Oliveira, R., & Riva, M. A. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.04.032 · Cited by 65 · see citing works
Madison, A. A., & Bailey, M. T. (2023) · Biological Psychiatry · doi:10.1016/j.biopsych.2023.10.014 · Cited by 67 · see citing works
The microbiome and gut endocannabinoid system in the regulation of stress responses and metabolism
Srivastava, R. K., Lutz, B., & Ruiz de Azua, I. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.867267 · Cited by 56 · see citing works
Ortega, V. A., Mercer, E. M., Giesbrecht, G. F., & Arrieta, M. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.634539 · Cited by 51 · see citing works
Prenatal pregnancy-related anxiety predicts boys’ ADHD symptoms via placental C-reactive protein
Shao, S., Wang, J., Huang, K., Wang, S., Liu, H., Wan, S., Yan, S., Hao, J., Zhu, P., & Tao, F. (2020) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2020.104797 · Cited by 50 · see citing works
Champagne-Jorgensen, K., Mian, M. F., Kay, S., Hanani, H., Oren, Z., Neufeld, K. M., Koren, O., & Bienenstock, J. (2019) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2019.11.020 · Cited by 49 · see citing works
Prenatal stress impacts foetal neurodevelopment: Temporal windows of gestational vulnerability
Collins, J. M., Keane, J. M., Deady, C., Khashan, A. S., McCarthy, F. P., O’Keeffe, G. W., Clarke, G. A., Cryan, J. F., Caputi, V., & O’Mahony, S. M. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105793 · Cited by 50 · see citing works
Maternal effects in mammals: Broadening our understanding of offspring programming
Edwards, P. D., Lavergne, S. G., McCaw, L. K., Wijenayake, S., Boonstra, R., McGowan, P. O., & Holmes, M. M. (2021) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2021.100924 · Cited by 47 · see citing works
Jiang, J., Fu, Y., Tang, A., Gao, X., Zhang, D., Shen, Y., Mou, T., Hu, S., Gao, J., & Lai, J. (2023) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.14091 · Cited by 46 · see citing works
Unique maternal immune and functional microbial profiles during prenatal stress
Antonson, A. M., Evans, M. V., Galley, J. D., Chen, H. J., Rajasekera, T. A., Lammers, S. M., Hale, V. L., Bailey, M. T., & Gur, T. (2020) · Scientific Reports · doi:10.1038/s41598-020-77265-x · Cited by 47 · see citing works
Birth signalling hormones and the developmental consequences of caesarean delivery
Kenkel, W. M. (2020) · Journal of Neuroendocrinology · doi:10.1111/jne.12912 · Cited by 45 · see citing works
Naudé, P. J. W., Claassen-Weitz, S., Gardner‐Lubbe, S., Botha, G., Kaba, M., Zar, H. J., Nicol, M. P., & Stein, D. J. (2019) · Acta Neuropsychiatrica · doi:10.1017/neu.2019.43 · Cited by 44 · see citing works
Morel, C., Sánchez, I. M., Cherifi, Y., Chartrel, N., & Heijtz, R. D. (2023) · Neuropharmacology · doi:10.1016/j.neuropharm.2023.109479 · Cited by 42 · see citing works
Inflammation in Mental Disorders: Is the Microbiota the Missing Link?
Marin, S., Hé, Y., Butler, K., & Tsuang, M. T. (2020) · Neuroscience Bulletin · doi:10.1007/s12264-020-00535-1 · Cited by 41 · see citing works
Sensitive phases in the development of rodent social behavior
Sachser, N., Zimmermann, T. D., Hennessy, M. B., & Kaiser, S. (2020) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2020.07.014 · Cited by 40 · see citing works
Fitzgerald, E., Parent, C. I., Kee, M. Z. L., & Meaney, M. J. (2021) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2021.635304 · Cited by 39 · see citing works
Prenatal stress-induced disruptions in microbial and host tryptophan metabolism and transport
Galley, J. D., Chen, H. J., Antonson, A. M., & Gur, T. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113471 · Cited by 42 · see citing works
Critical Review of the Cross-Links Between Dietary Components, the Gut Microbiome, and Depression
Randeni, N., & Xu, B. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26020614 · Cited by 42 · see citing works
A Review of the Impact of Maternal Prenatal Stress on Offspring Microbiota and Metabolites
Yeramilli, V. A., Cheddadi, R., Shah, J., Brawner, K. M., & Martin, C. A. (2023) · Metabolites · doi:10.3390/metabo13040535 · Cited by 35 · see citing works
Cattaneo, A., Suderman, M., Cattane, N., Mazzelli, M., Begni, V., Maj, C., D'Aprile, I., Pariante, C., Luoni, A., Berry, A., et al. (2020) · Neurobiology of Stress · doi:10.1016/j.ynstr.2020.100271 · Cited by 31 · see citing works
Antonson, A. M., Kenney, A. D., Chen, H. J., Corps, K. N., Yount, J. S., & Gur, T. (2021) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2021.05.004 · Cited by 32 · see citing works
Identifying a biological signature of prenatal maternal stress
Keane, J. M., Khashan, A. S., McCarthy, F. P., Kenny, L. C., Collins, J. M., O’Donovan, S. M., Brown, J. R.-M., Cryan, J. F., Dinan, T. G., Clarke, G. A., et al. (2020) · JCI Insight · doi:10.1172/jci.insight.143007 · Cited by 31 · see citing works
Geng, X., Wu, H., Li, Z., Li, C., Chen, D., Zong, J., Liu, Z., Wei, S., & Peng, W. (2021) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2021/1703981 · Cited by 30 · see citing works
Allen, J. M., Jaggers, R. M., Solden, L., Loman, B. R., Davies, R. H., Mackos, A. R., Ladaika, C. A., Berg, B. M., Chichlowski, M., & Bailey, M. T. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01774 · Cited by 27 · see citing works
Kimmel, M., Verosky, B. G., Chen, H. J., Davis, O., & Gur, T. (2023) · Biological Psychiatry · doi:10.1016/j.biopsych.2023.11.014 · Cited by 28 · see citing works
Lynch, C. M. K., Nagpal, J. K., Clarke, G. A., & Cryan, J. F. (2021) · Current Opinion in Physiology · doi:10.1016/j.cophys.2021.100468 · Cited by 23 · see citing works
The microbiome as a modulator of neurological health across the maternal-offspring interface
Orchanian, S. B., & Hsiao, E. Y. (2025) · Journal of Clinical Investigation · doi:10.1172/jci184314 · Cited by 22 · see citing works
Exploring the role of gut microbiota in depression: Pathogenesis and therapeutic insights
Zhang, J., He, J., Hu, J., Ji, Y., & Lou, Z. (2025) · Asian Journal of Psychiatry · doi:10.1016/j.ajp.2025.104411 · Cited by 19 · see citing works
GPCR signaling: role in mediating the effects of early adversity in psychiatric disorders
Tiwari, P., Fanibunda, S. E., Kapri, D., Vasaya, S., Pati, S., & Vaidya, V. A. (2021) · FEBS Journal · doi:10.1111/febs.15738 · Cited by 19 · see citing works
Maternal stress during the third trimester of pregnancy and the neonatal microbiome
Weiss, S. J., & Hamidi, M. (2023) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.1080/14767058.2023.2214835 · Cited by 18 · see citing works
Fetal CCL2 signaling mediates offspring social behavior and recapitulates effects of prenatal stress
Chen, H. J., Galley, J. D., Verosky, B. G., Yang, F. T., Rajasekera, T. A., Bailey, M. T., & Gur, T. (2023) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2023.10.032 · Cited by 18 · see citing works
More than just a number: the gut microbiota and brain function across the extremes of life
Nuzum, N. D., Deady, C., Kittel‐Schneider, S., Cryan, J. F., O’Mahony, S. M., & Clarke, G. A. (2024) · Gut Microbes · doi:10.1080/19490976.2024.2418988 · Cited by 20 · see citing works
Galley, J. D., Rajasekera, T. A., Bennouna, D., Batabyal, A., Verosky, B. G., Woodke, S. T., Stokes, J., Brown, A. K., Murthy, S., Kopec, R. E., et al. (2024) · Beneficial Microbes · doi:10.1163/18762891-bja00047 · Cited by 17 · see citing works
Mañas-Ojeda, A., Ros‐Bernal, F., Olucha-Bordonau, F. E., & Castillo-Gómez, E. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21165819 · Cited by 16 · see citing works
Cusick, J. A., Wellman, C. L., & Demas, G. E. (2022) · Hormones and Behavior · doi:10.1016/j.yhbeh.2022.105146 · Cited by 16 · see citing works
Pawluski, J. L., Murail, P., Grudet, F., Bys, L., Golubeva, A. V., Bastiaanssen, T. F. S., Oberlander, T. F., Cryan, J. F., O’Mahony, S. M., & Charlier, T. D. (2023) · Journal of Neuroendocrinology · doi:10.1111/jne.13261 · Cited by 17 · see citing works
Stress and depression-associated shifts in gut microbiota: A pilot study of human pregnancy
Rajasekera, T. A., Galley, J. D., Mackos, A. R., Chen, H. J., Mitchell, J. G., Kleinman, J. J., Cappelucci, P., Mashburn‐Warren, L., Lauber, C. L., Bailey, M. T., et al. (2024) · Brain Behavior & Immunity - Health · doi:10.1016/j.bbih.2024.100730 · Cited by 18 · see citing works
Discrete role for maternal stress and gut microbes in shaping maternal and offspring immunity
Chen, H. J., Bischoff, A., Galley, J. D., Peck, L., Bailey, M. T., & Gur, T. (2022) · Neurobiology of Stress · doi:10.1016/j.ynstr.2022.100480 · Cited by 16 · see citing works
Glucocorticosteroids Effects on Brain Development in the Preterm Infant: A Role for Microglia?
Zinni, M., Pansiot, J., Billion, E., Baud, O., & Mairesse, J. (2021) · Current Neuropharmacology · doi:10.2174/1570159x19666210517112913 · Cited by 15 · see citing works
Yang, J., Deng, Y., Cai, Y., Liu, Y., Peng, L., Luo, Z., & Li, D. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.1048565 · Cited by 15 · see citing works
Interactions of the maternal microbiome with diet, stress, and infection influence fetal development
Puglisi, C. H., Kim, M. J., Aldhafeeri, M., Lewandowski, M., & Vuong, H. E. (2025) · FEBS Journal · doi:10.1111/febs.70031 · Cited by 16 · see citing works
Intestinal dysbiosis during pregnancy and microbiota-associated impairments in offspring
Abu, Y. F., & Roy, S. (2025) · Frontiers in Microbiomes · doi:10.3389/frmbi.2025.1548650 · Cited by 18 · see citing works
The Neurobiology of Infant Attachment-Trauma and Disruption of Parent–Infant Interactions
Naeem, N., Zanca, R. M., Weinstein, S., Urquieta, A., Sosa, A., Yu, B., & Sullivan, R. M. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.882464 · Cited by 19 · see citing works
Lopizzo, N., Mazzelli, M., Zonca, V., Begni, V., D’Aprile, I., Cattane, N., Pariante, C. M., Riva, M. A., & Cattaneo, A. (2020) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2020.104794 · Cited by 15 · see citing works
Anzà, S., Schneider, D., Daniel, R., Heistermann, M., Sangmaneedet, S., Ostner, J., & Schülke, O. (2023) · Microbiome · doi:10.1186/s40168-023-01596-w · Cited by 13 · see citing works
Luft, C., da Costa, M. S., Antunes, G. L., de Oliveira, J. R., & Donadio, M. V. F. (2022) · Neurochemistry International · doi:10.1016/j.neuint.2022.105384 · Cited by 12 · see citing works
Larsen, A., Pintye, J. C., Abuna, F., Bhat, A. S., Dettinger, J. C., Gómez, L., Marwa, M. M., Ngumbau, N. M., Odhiambo, B. O., Phipps, A. I., et al. (2023) · Paediatric and Perinatal Epidemiology · doi:10.1111/ppe.12978 · Cited by 12 · see citing works
Maternal Prenatal Stress and the Offspring Gut Microbiome: A Cross‐Species Systematic Review
Graf, M. D., Murgueitio, N., Vogel, S. C., Hicks, L., Carlson, A. L., Propper, C. B., & Kimmel, M. (2024) · Developmental Psychobiology · doi:10.1002/dev.70005 · Cited by 12 · see citing works
The Impact of Stress, Microbial Dysbiosis, and Inflammation on Necrotizing Enterocolitis
Yeramilli, V. A., Cheddadi, R., Benjamin, H., & Martin, C. A. (2023) · Microorganisms · doi:10.3390/microorganisms11092206 · Cited by 13 · see citing works
Császár-Nagy, N., Bob, P., & Bókkon, I. (2024) · Current Neuropharmacology · doi:10.2174/1570159x22666240507095700 · Cited by 13 · see citing works
Galley, J. D., King, M. K., Rajasekera, T. A., Batabyal, A., Woodke, S. T., & Gur, T. (2024) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2024.08.006 · Cited by 11 · see citing works
Arzuaga, A. L., Edmison, D. D., Mroczek, J., Larson, J., & Ragozzino, M. E. (2022) · Behavioural Brain Research · doi:10.1016/j.bbr.2022.114114 · Cited by 11 · see citing works
I "Gut" Rhythm: the microbiota as a modulator of the stress response and circadian rhythms
Tofani, G. S. S., Clarke, G. A., & Cryan, J. F. (2025) · FEBS Journal · doi:10.1111/febs.17400 · Cited by 10 · see citing works
Rubinstein, M. R., Burgueño, A. L., Quiroga, S., Wald, M. R., & Genaro, A. M. (2023) · Cells · doi:10.3390/cells12131735 · Cited by 10 · see citing works
Rotem‐Kohavi, N., Keane, J., Clarke, G. A., Dinan, T. G., Cryan, J. F., McCarthy, F. P., Oberlander, T. F., & O’Mahony, S. M. (2021) · Springer eBooks · doi:10.1007/978-3-030-60159-1_8 · Cited by 9 · see citing works
Melnikova, V. I., Лифанцева, Н. В., Voronova, S. N., & Bondarenko, N. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms252413565 · Cited by 9 · see citing works
Sabatini, G., Boccadoro, I., Prete, R., Battista, N., & Corsetti, A. (2025) · Nutrients · doi:10.3390/nu17152470 · Cited by 8 · see citing works
Ryan, N., O’Mahony, S. M., Leahy‐Warren, P., Philpott, L. F., & Mulcahy, H. (2025) · PLoS ONE · doi:10.1371/journal.pone.0318237 · Cited by 8 · see citing works
An Updated Narrative Mini-Review on the Microbiota Changes in Antenatal and Post-Partum Depression
Doroftei, B., Ilie, O., Diaconu, R., Huțanu, D., Stoian, I. L., & Ilea, C. G. (2022) · Diagnostics · doi:10.3390/diagnostics12071576 · Cited by 8 · see citing works
Martin, E. M., Xue, J., & Smith, C. J. W. (2025) · Behavioural Brain Research · doi:10.1016/j.bbr.2025.115723 · Cited by 7 · see citing works
The relationship between human milk, a functional nutrient, and microbiota
Sakarya, E., Şanlıer, N. T., & Şanlıer, N. (2021) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2021.2008301 · Cited by 7 · see citing works
Dunn, J. T., Guidotti, A., & Grayson, D. R. (2024) · eNeuro · doi:10.1523/eneuro.0186-23.2024 · Cited by 7 · see citing works
Prenatal Stress and Adaptive Behavior of Offspring: The Role of Placental Serotonin
Бондаренко, Н. С., Voronova, S. N., Voronezhskaya, E. E., & Melnikova, V. I. (2022) · Doklady Biochemistry and Biophysics · doi:10.1134/s160767292202003x · Cited by 7 · see citing works
Dong, Y., Weng, J., Zhu, Y., Sun, D., He, W., Chen, Q., Cheng, J., Zhu, Y., & Jiang, Y. (2023) · BMC Genomics · doi:10.1186/s12864-023-09186-8 · Cited by 8 · see citing works
Luft, C., Haute, G. V., Wearick‐Silva, L. E., Antunes, K. H., da Costa, M. S., de Oliveira, J. R., & Donadio, M. V. F. (2021) · Neurochemistry International · doi:10.1016/j.neuint.2021.105053 · Cited by 7 · see citing works
Piscotta, F. J., Whitfield, S. T., Nakashige, T. G., Estrela, A. B., Ali, T. A., & Brady, S. F. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109746 · Cited by 7 · see citing works
Satyapal, H., Wankhede, N. L., Yadav, A., Rahangdale, S. R., Aglawe, M. M., Taksande, B. G., Koppula, S., Umekar, M. J., & Kale, M. B. (2025) · Physiology & Behavior · doi:10.1016/j.physbeh.2025.115199 · Cited by 6 · see citing works
Guez‐Barber, D., Eisch, A. J., & Cristancho, A. G. (2023) · Developmental Neuroscience · doi:10.1159/000530745 · Cited by 7 · see citing works
Cillis, F. D., Petrillo, G., D’Aprile, I., Marizzoni, M., Saleri, S., Mazzelli, M., Zonca, V., Benedetto, M. G. D., Riva, M. A., & Cattaneo, A. (2025) · Nutrients · doi:10.3390/nu17172812 · Cited by 6 · see citing works
Prenatal Stress and Ethanol Exposure: Microbiota-Induced Immune Dysregulation and Psychiatric Risks
Camarini, R., Marianno, P., Hanampa-Maquera, M., Oliveira, S. D. S., & Câmara, N. O. S. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25189776 · Cited by 5 · see citing works
Mohammadi-Mahdiabadi-Hasani, M.-H., Farahmandfar, M., Zarrindast, M., Nasehi, M., Torkaman‐Boutorabi, A., & Hassanzadeh, G. (2025) · Journal of Psychopharmacology · doi:10.1177/02698811251334034 · Cited by 5 · see citing works
Pang, J., Hao, J., Gu, X., Zhang, L., Wang, W., Qin, Z. H., Feng, Q., Liu, C., Xie, H., Yang, S., et al. (2025) · Molecular Psychiatry · doi:10.1038/s41380-025-03258-9 · Cited by 6 · see citing works
Blaine, B., Kamal, M., Roberts, M., Schickling, B., Lauffer, M. C., Zhang, Y., Bertolli, A. X., Weber, M. A., Taylor, R., Nadeem, S., et al. (2025) · Molecular Psychiatry · doi:10.1038/s41380-025-03094-x · Cited by 4 · see citing works
Neurodevelopment and the gut microbiome
Oliphant, K., & Lu, J. N. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-820602-7.00006-4 · Cited by 4 · see citing works
Ultrasound-Induced Prenatal Stress: New Possibilities for Modeling Mental Disorders
Abramova, O. V., Morozova, A. Y., Zubkov, E. A., Ushakova, V., Zorkina, Y., Proshin, A. T., Storozheva, Z. I., Gurina, O. I., & Chekhonin, V. P. (2023) · Developmental Neuroscience · doi:10.1159/000534687 · Cited by 3 · see citing works
Prenatal stress alters transcription of NMDA-type glutamate receptors in the hippocampus
Buck, T. G., Dong, E., McCarthy, M., Guidotti, A., & Sodhi, M. (2024) · Neuroscience Letters · doi:10.1016/j.neulet.2024.137886 · Cited by 4 · see citing works
Chronic Ultrasound Prenatal Stress Altered the Brain’s Neurochemical Systems in Newborn Rats
Abramova, O. V., Zorkina, Y., Ka, P., Ushakova, V. M., Morozova, A. Y., Zubkov, E. A., Pavlova, O., Storozheva, Z. I., Gurina, O. I., & Chekhonin, V. P. (2024) · Neural Plasticity · doi:10.1155/2024/3829941 · Cited by 3 · see citing works
Prenatal maternal stress effects in wild Assamese macaques (Macaca assamensis)
Anzà, S. (2022) · doi:10.53846/goediss-9510 · Cited by 3 · see citing works
Schiele, J., Tsai, P.-L., Ernst, G., Blank, C., Beck, S., Schimmele, T., Burth, E., Gebauer, D., Lowry, C. A., Noschka, R., et al. (2025) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2025.106169 · Cited by 2 · see citing works
Stoehr, M. C., Martin, E. M., Babalola, J. T., Xue, J., Kern, M., Li, N. Y., Winters, M. F., Bhagwagar, S., & Smith, C. J. (2026) · Journal of Neuroendocrinology · doi:10.1111/jne.70151 · Cited by 2 · see citing works
Prenatal-induced psychopathologies: All roads lead to microglia
Lebow, M., Kuperman, Y., & Chen, A. (2023) · Elsevier eBooks · doi:10.1016/b978-0-12-817558-3.00016-0 · Cited by 2 · see citing works
Rajasekera, T. A., Galley, J. D., Mashburn‐Warren, L., Lauber, C. L., Bailey, M. T., Worly, B. L., & Gur, T. (2024) · Scientific Reports · doi:10.1038/s41598-024-77560-x · Cited by 2 · see citing works
Identifying the Role of Vasopressin and Oxytocin in the Microbiota-Gut-Brain-Behavior Axis
Peters, N. V. (2022) · Digital Archive @ GSU · doi:10.57709/14972899 · Cited by 2 · see citing works
Impact of Sex, Gonadectomy, and Repeated Restraint Stress on Gut Microbiome in Mice
Mekadim, C., Mrázek, J., Vodička, M., Ergang, P., Fliegerova, K. O., Mahayri, T. M., Chawengsaksophak, K., & Pácha, J. (2025) · Molecular Neurobiology · doi:10.1007/s12035-025-05305-6 · Cited by 1 · see citing works
Mechanisms linking sleep, innate immunity, and neuroinflammation
Opp, M. R., Rowe, R. K., & Krueger, J. M. (2026) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2026.106803 · Cited by 2 · see citing works
Кулешова, О. Н. (2023) · Neuroscience and Behavioral Physiology · doi:10.1007/s11055-023-01555-w · Cited by 1 · see citing works
Oliphant, K., Ali, M., D’Souza, M., Hughes, P. D., Sulakhe, D., Wang, A. Z., Xie, B., Yeasin, R., Msall, M. E., Andrews, B., et al. (2021) · Research Square · doi:10.21203/rs.3.rs-668952/v1 · Cited by 1 · see citing works
Prenatal maternal stress and infant gut microbiota
Viitaharju, J. (2020) · Työväentutkimus Vuosikirja
- Authors
- Gur, T. L., Palkar, A. V., Rajasekera, T., Allen, J., Niraula, A., Godbout, J., & Bailey, M. T.
- Affiliations
- The Ohio State University Wexner Medical Center (US)
- Nationwide Children's Hospital (US)
- Corresponding author
- Gur, Tamar L.
- Venue
- Behavioural Brain Research
- Publisher
- Elsevier BV
- Published
- 2019-02
- Volume
- 359
- Pages
- 886-894
- ISSN
- 0166-4328 (ISSN-L)
- PMC
- PMC6542272
- OpenAlex
- W2810891667
- Cited by
- 127
- References
- 53
- Citations by year
- 2026: 12 · 2025: 18 · 2024: 19 · 2023: 23 · 2022: 15 · 2021: 21 · 2020: 15 · 2019: 4
- FWCI
- 5.76
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- Locations
- Behavioural Brain Research (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Ohio State University
- National Alliance for Research on Schizophrenia and Depression
- Brain and Behavior Research Foundation
- March of Dimes Prematurity Research Center Ohio Collaborative
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Maternal Mental Health During Pregnancy and Postpartum
- Keywords
- prenatal stress, maternal stress, social behavior, gut microbiota, gut-brain axis, corticosterone, neuroinflammation, oxytocin receptor, serotonin metabolism, Bacteroides, Parabacteroides, mental illness, mouse model
- MeSH terms
- Gastrointestinal Microbiome, Animals, Animals, Newborn, Calcium-Binding Proteins, Cerebral Cortex, Corticosterone, Female, Hydroxyindoleacetic Acid, Interpersonal Relations, Male, Microfilament Proteins, Pregnancy, Prenatal Exposure Delayed Effects, RNA, Ribosomal, 16S, Serotonin, Social Behavior Disorders, Stress, Psychological, Cytokines, Receptors, Oxytocin, Hindlimb Suspension, Recognition, Psychology, Mice
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