Prenatal stress and limbic-prefrontal white matter microstructure in children aged 6–9 years: a preliminary diffusion tensor imaging study
Abstract
OBJECTIVES: Maternal prenatal stress is associated with elevated risk of adverse behavioural outcomes in offspring. This association may involve developmental disruption to limbic-prefrontal white matter circuitry, of which the uncinate fasciculus is the major tract. One potential candidate for modulating brain development is maternal prenatal stress. We provide the first prospective study of prenatal stress and white matter microstructure in children. METHODS: A total of 22 healthy children (mean age 7 years) of mothers recruited in pregnancy underwent diffusion tensor magnetic resonance imaging. We examined correlations between prenatal stressful life events and white matter microstructural organisation indices (fractional anisotropy (FA) and perpendicular diffusivity (Dperp)) of the uncinate fasciculus and a "control" tract. RESULTS: Maternal prenatal stressful life events were correlated positively with right uncinate fasciculus FA, and negatively with right uncinate fasciculus Dperp in their child, with a similar trend with left uncinate fasciculus Dperp. Prenatal stress was not associated with control tract properties; sociodemographic/obstetric variables were not associated with FA/Dperp of either tract. CONCLUSIONS: Variation in maternal prenatal stress may be associated with differences in the development of white matter within brain networks underlying child social behaviour.
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Exposure to prenatal maternal stress has enduring and wide-ranging consequences on brain development in the offspring, including altered regional brain volumetric growth, cortical folding, metabolism, microstructure, and functional connectivity.
“Importantly, exposure to prenatal maternal stress is shown to have enduring and wide-ranging consequences on brain development in the offspring, including altered regional brain volumetric growth, cortical folding, metabolism, microstructure, and functional connectivity [4, 15, 19, 23–27, 35–39].”
From Brain structural and functional outcomes in the offspring of women experiencing psychological distress during pregnancy (2024) · cites this paper as [27]
Prenatal maternal stressful life events are positively correlated with right uncinate fasciculus FA, and negatively with right uncinate fasciculus perpendicular diffusivity in children.
“Moreover, prenatal maternal stressful life events are positively correlated with right uncinate fasciculus FA, and negatively with right uncinate fasciculus perpendicular diffusivity in children [27].”
From Brain structural and functional outcomes in the offspring of women experiencing psychological distress during pregnancy (2024) · cites this paper as [27]
Cites
Detection of Postnatal Depression: Development of the 10-item Edinburgh Postnatal Depression Scale
Cox, J. L., Holden, J. M., & Sagovsky, R. (1987) · British Journal of Psychiatry · doi:10.1192/bjp.150.6.782 · Cited by 14,183 · see citing works
A diffusion tensor imaging tractography atlas for virtual in vivo dissections.
CATANI, M., & THIEBAUTDESCHOTTEN, M. (2008) · Cortex · doi:10.1016/j.cortex.2008.05.004 · Cited by 1,642 · see citing works
Self-citationVirtual in vivo interactive dissection of white matter fasciculi in the human brain
Catani, M., Howard, R. J., Pajevic, S., & Jones, D. K. (2002) · NeuroImage · doi:10.1006/nimg.2002.1136 · Cited by 1,637 · see citing works
Self-citationMicrostructural maturation of the human brain from childhood to adulthood
Lebel, C., Walker, L., Leemans, A., Phillips, L., & Beaulieu, C. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2007.12.053 · Cited by 1,398 · see citing works
Maternal antenatal anxiety and children's behavioural/emotional problems at 4 years
O'Connor, T. G., Heron, J., Golding, J., Beveridge, M., & Glover, V. (2002) · British Journal of Psychiatry · doi:10.1192/bjp.180.6.502 · Cited by 1,070 · see citing works
Self-citationExploreDTI: a graphical toolbox for processing, analyzing, and visualizing diffusion MR data
Leemans, A., Jeurissen, B., Sijbers, J., & Jones, D. K. (2009) · Cited by 874 · see citing works
Diffusion MRI : from quantitative measurement to in vivo neuroanatomy
Johansen‐Berg, H., & Behrens, T. E. J. (2014) · doi:10.1016/b978-0-12-374709-9.x0001-6 · Cited by 703 · see citing works
O’Connor, T. G., Heron, J., Golding, J., Glover, V. A. S., & the AL SPAC Study Team (2003) · Journal of Child Psychology and Psychiatry · doi:10.1111/1469-7610.00187 · Cited by 703 · see citing works
Self-citationWolff, J. J., Gu, H., Gerig, G., Elison, J. T., Styner, M., Gouttard, S., Botteron, K. N., Dager, S. R., Dawson, G., Estes, A. M., et al. (2012) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2011.11091447 · Cited by 671 · see citing works
Buss, C., Davis, E. P., Shahbaba, B., Pruessner, J. C., Head, K., & Sandman, C. A. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1201295109 · Cited by 652 · see citing works
den Bergh, B. R. H. V., & Marcoen, A. (2004) · Child Development · doi:10.1111/j.1467-8624.2004.00727.x · Cited by 636 · see citing works
RESTORE: Robust estimation of tensors by outlier rejection
Chang, L., Jones, D. K., & Pierpaoli, C. M. (2005) · Magnetic Resonance in Medicine · doi:10.1002/mrm.20426 · Cited by 611 · see citing works
Neurotoxicity of Glucocorticoids in the Primate Brain
Uno, H., Eisele, S., Sakai, A., Shelton, S. E., Baker, E. H., DeJesus, O. T., & Holden, J. E. (1994) · Hormones and Behavior · doi:10.1006/hbeh.1994.1030 · Cited by 511 · see citing works
Mapping Infant Brain Myelination with Magnetic Resonance Imaging
Deoni, S. C. L., Mercure, E., Blasi, A., Gasston, D., Thomson, A., Johnson, M., Williams, S. C. R., & Murphy, D. G. M. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.2106-10.2011 · Cited by 497 · see citing works
Self-citationBuss, C., Davis, E. P., Muftuler, L. T., Head, K., & Sandman, C. A. (2010) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.07.010 · Cited by 435 · see citing works
Van den Bergh, B. R. H., Van Calster, B., Smits, T., Van Huffel, S., & Lagae, L. (2008) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301450 · Cited by 434 · see citing works
Maternal Stress During Pregnancy Predicts Cognitive Ability and Fearfulness in Infancy
Bergman, K., Sarkar, P., O’Connor, T. G., Modi, N., & Glover, V. A. S. (2007) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1097/chi.0b013e31814a62f6 · Cited by 430 · see citing works
Self-citationPsychological measures of prenatal stress as predictors of infant temperament
HUIZINK, A. C., ROBLES DE MEDINA, P. G., MULDER, E. J. H., VISSER, G. H. A., & BUITELAAR, J. K. (2002) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1097/00004583-200209000-00008 · Cited by 409 · cited 2× · see citing works
“These include conduct and temperament problems (Huizink et al. 2002; O ’ Connor et al. 2002, 2003; Gutteling et al. 2005; Barker and Maughan 2009; Hay et al. 2010; Rice et al. 2010), Autistic Spectrum Disorders (Beversdorf et al. 2005; Kinney et al. 2008), Attention Defi cit Hyperactivity Disorder…”
BackgroundRice, F. J., Harold, G. T., Boivin, J., van den Bree, M. B. M., Hay, D. F., & Thapar, A. (2009) · Psychological Medicine · doi:10.1017/s0033291709005911 · Cited by 377 · 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
Are maternal smoking and stress during pregnancy related to ADHD symptoms in children?
Rodriguez, A., & Bohlin, G. (2004) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2004.00359.x · Cited by 333 · see citing works
Altered connections on the road to psychopathy
Craig, M., Catani, M., Deeley, Q., Latham, R., Daly, E., Kanaan, R., Picchioni, M., McGuire, P. K., Fahy, T. A., & Murphy, D. (2009) · Molecular Psychiatry · doi:10.1038/mp.2009.40 · Cited by 313 · see citing works
Self-citationAutism Prevalence Following Prenatal Exposure to Hurricanes and Tropical Storms in Louisiana
Kinney, D. K., Miller, A. M., Crowley, D. J., Huang, E., & Gerber, E. (2008) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-007-0414-0 · Cited by 295 · see citing works
Marsh, R., Gerber, A. J., & Peterson, B. S. (2008) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1097/chi.0b013e318185e703 · Cited by 267 · see citing works
The Biological Basis of Diffusion Anisotropy
Beaulieu, C. (2009) · Elsevier eBooks · doi:10.1016/b978-0-12-374709-9.00006-7 · Cited by 231 · see citing works
The effects of prenatal stress on temperament and problem behavior of 27-month-old toddlers
Gutteling, B. M., de Weerth, C., Willemsen-Swinkels, S. H. N., Huizink, A. C., Mulder, E. J. H., Visser, G. H. A., & Buitelaar, J. K. (2005) · European Child & Adolescent Psychiatry · doi:10.1007/s00787-005-0435-1 · Cited by 230 · see citing works
Jones, D. K., Williams, S. C. R., Gasston, D., Horsfield, M., Simmons, A., & Howard, R. (2002) · Human Brain Mapping · doi:10.1002/hbm.10018 · Cited by 203 · see citing works
Differentiating Early-Onset Persistent Versus Childhood-Limited Conduct Problem Youth
Barker, E. D., & Maughan, B. (2009) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2009.08121770 · Cited by 200 · see citing works
Not fade away: the HPA axis and depression
Cowen, P. J. (2010) · Psychological Medicine · doi:10.1017/s0033291709005558 · Cited by 191 · see citing works
Mothers’ Antenatal Depression and Their Children’s Antisocial Outcomes
Hay, D. F., Pawlby, S. J., Waters, C. S., Perra, O., & Sharp, D. (2010) · Child Development · doi:10.1111/j.1467-8624.2009.01386.x · Cited by 161 · see citing works
Quality of child–parent attachment moderates the impact of antenatal stress on child fearfulness
Bergman, K., Sarkar, P., Glover, V. A. S., & O’Connor, T. G. (2008) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2008.01987.x · Cited by 130 · see citing works
Self-citationLateral amygdaloid nucleus expansion in adult rats is associated with exposure to prenatal stress
Salm, A. K., Pavelko, M., Krouse, E. M., Webster, W., Kraszpulski, M., & Birkle, D. L. (2004) · Developmental Brain Research · doi:10.1016/j.devbrainres.2003.11.005 · Cited by 125 · cited 2× · see citing works
“In particular, compared to controls, animals exposed to prenatal stress exhibited initially reduced, and subsequently increased, amygdala volume (Salm et al. 2004; Kraszpulski et al. 2006).”
BackgroundLife event scales for obstetric groups
Barnett, B. E. W., Hanna, B. A., & Parker, G. B. (1983) · Journal of Psychosomatic Research · doi:10.1016/0022-3999(83)90054-5 · Cited by 122 · see citing works
Sarkar, S., Craig, M., Catani, M., Dell’Acqua, F., Fahy, T. A., Deeley, Q., & Murphy, D. (2012) · Psychological Medicine · doi:10.1017/s003329171200116x · Cited by 109 · see citing works
Self-citationChernobyl exposure as stressor during pregnancy and behaviour in adolescent offspring
Huizink, A. C., Dick, D. M., Sihvola, E., Pulkkinen, L., Rose, R. J., & Kaprio, J. A. (2007) · Acta Psychiatrica Scandinavica · doi:10.1111/j.1600-0447.2007.01050.x · Cited by 86 · see citing works
Prenatal stress affects the developmental trajectory of the rat amygdala
Kraszpulski, M., Dickerson, P. A., & Salm, A. K. (2006) · Stress · doi:10.1080/10253890600798109 · Cited by 85 · see citing works
Anatomy and functional role of the inferior longitudinal fasciculus: a search that has just begun
Ashtari, M. (2011) · Developmental Medicine & Child Neurology · doi:10.1111/j.1469-8749.2011.04122.x · Cited by 79 · see citing works
Neurodevelopmental Outcomes of Preterm Birth
(2010) · Cambridge University Press eBooks · doi:10.1017/cbo9780511712166 · Cited by 67 · see citing works
Maternal anxiety at amniocentesis and plasma cortisol
Sarkar, P., Bergman, K., Fisk, N. M., & Glover, V. A. S. (2006) · Prenatal Diagnosis · doi:10.1002/pd.1444 · Cited by 63 · see citing works
Self-citationPrenatal Stress Inhibits Neuronal Maturation through Downregulation of Mineralocorticoid Receptors
Tamura, M., Sajo, M., Kakita, A., Matsuki, N., & Koyama, R. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.3447-10.2011 · Cited by 52 · see citing works
Restraint stress during late pregnancy in rats elicits early hypermyelination in the offspring
Wiggins, R. C., & Gottesfeld, Z. (1986) · Metabolic Brain Disease · doi:10.1007/bf01001781 · Cited by 19 · see citing works
Diffusion tensor imaging findings in preterm and low birth weight populations
Allin, M. P. G. (2010) · Cambridge University Press eBooks · doi:10.1017/cbo9780511712166.009 · Cited by 1 · see citing works
Basser (2000) · doi:10.1002/1522-2594(200010)44:4
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Van den Bergh, B. R. H., van den Heuvel, M. I., Lahti, M., Braeken, M., de Rooij, S. R., Entringer, S., Hoyer, D., Roseboom, T., Räikkönen, K., King, S., et al. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.07.003 · Cited by 1,181 · see citing works
Prenatal stress: Effects on fetal and child brain development
(2020) · International Review of Neurobiology · doi:10.1016/bs.irn.2019.11.002 · Cited by 326 · see citing works
Self-citationThe Placenta as a Mediator of Stress Effects on Neurodevelopmental Reprogramming
Bronson, S. L., & Bale, T. L. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.231 · Cited by 285 · see citing works
Callaghan, B. L., & Tottenham, N. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2015.204 · Cited by 268 · see citing works
Lebel, C., Walton, M., Letourneau, N., Giesbrecht, G. F., Kaplan, B. J., & Dewey, D. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.12.004 · Cited by 237 · see citing works
Wu, Y., Lu, Y.-C., Jacobs, M., Pradhan, S., Kapse, K., Zhao, L., Niforatos-Andescavage, N., Vezina, G., du Plessis, A. J., & Limperopoulos, C. (2020) · JAMA Network Open · doi:10.1001/jamanetworkopen.2019.19940 · Cited by 218 · see citing works
Oxidative stress, prefrontal cortex hypomyelination and cognitive symptoms in schizophrenia
Maas, D. A., Vallès, A., & Martens, G. J. M. (2017) · Translational Psychiatry · doi:10.1038/tp.2017.138 · Cited by 181 · see citing works
Prenatal stress and the developing brain: Risks for neurodevelopmental disorders
den Bergh, B. R. H. V., Dahnke, R., & Mennes, M. (2018) · Development and Psychopathology · doi:10.1017/s0954579418000342 · Cited by 160 · see citing works
Rapid infant prefrontal cortex development and sensitivity to early environmental experience
Hodel, A. S. (2018) · Developmental Review · doi:10.1016/j.dr.2018.02.003 · Cited by 160 · see citing works
Does prenatal stress alter the developing connectome?
Scheinost, D., Sinha, R., Cross, S., Kwon, S. H., Sze, G. K., Constable, R. T., & Ment, L. R. (2016) · Pediatric Research · doi:10.1038/pr.2016.197 · Cited by 143 · see citing works
Wu, Y., De Asis-Cruz, J., & Limperopoulos, C. (2024) · Molecular Psychiatry · doi:10.1038/s41380-024-02449-0 · Cited by 124 · see citing works
“Studies examining the effects of prenatal maternal stress exposure on brain development in the offspring have focused on newborns [14 – 19], children [20 – 27], adults [28 – 31], and more recently, fetuses [4, 32 – 35].”
BackgroundWu, Y., Espinosa, K. M., Barnett, S. D., Kapse, A., Quistorff, J. L., Lopez, C., Andescavage, N., Pradhan, S., Lu, Y.-C., Kapse, K., et al. (2022) · JAMA Network Open · doi:10.1001/jamanetworkopen.2022.9244 · Cited by 113 · see citing works
A Neurobiological Model of Borderline Personality Disorder: Systematic and Integrative Review
Ruocco, A. C., & Carcone, D. (2016) · Harvard Review of Psychiatry · doi:10.1097/hrp.0000000000000123 · Cited by 111 · see citing works
Association of Prenatal Maternal Anxiety With Fetal Regional Brain Connectivity
De Asis-Cruz, J., Krishnamurthy, D., Zhao, L., Kapse, K., Vezina, G., Andescavage, N., Quistorff, J., Lopez, C., & Limperopoulos, C. (2020) · JAMA Network Open · doi:10.1001/jamanetworkopen.2020.22349 · Cited by 81 · see citing works
Lautarescu, A., Pecheva, D., Nosarti, C., Sigurðardottir, J. N., Zhang, H. G., Victor, S., Craig, M., Edwards, A. D., & Counsell, S. J. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2019.08.010 · Cited by 72 · see citing works
Self-citationHumphreys, K. L., Camacho, M. C., Roth, M. C., & Estes, E. C. (2020) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2020.100877 · Cited by 67 · see citing works
Huizink, A. C., & de Rooij, S. R. (2018) · Development and Psychopathology · doi:10.1017/s0954579418000354 · Cited by 62 · see citing works
Maternal prenatal anxiety and child COMT genotype predict working memory and symptoms of ADHD
O’Donnell, K. J., Glover, V. A. S., Lahti, J. M. T., Lahti‐Pulkkinen, M., Edgar, R. D., Räikkönen, K., & O’Connor, T. G. (2017) · PLoS ONE · doi:10.1371/journal.pone.0177506 · Cited by 57 · see citing works
Self-citationRadhakrishnan, A., Aswathy, B. S., Kumar, V. M., & Gulia, K. K. (2014) · Brain Research · doi:10.1016/j.brainres.2014.11.021 · Cited by 54 · see citing works
Franke, K., den Bergh, B. R. H. V., de Rooij, S. R., Kroegel, N., Nathanielsz, P. W., Rakers, F., Roseboom, T. J., Witte, O. W., & Schwab, M. G. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.01.031 · Cited by 52 · see citing works
Manning, K. Y., Long, X., Watts, D., Tomfohr-Madsen, L., Giesbrecht, G. F., & Lebel, C. (2022) · Biological Psychiatry · doi:10.1016/j.biopsych.2022.05.011 · Cited by 51 · see citing works
Mother–infant interactions and regional brain volumes in infancy: an MRI study
Sethna, V., Pote, I., Wang, S., Gudbrandsen, M., Blasi, A., McCusker, C., Daly, E., Perry, E., Adams, K. P. H., Deprez, M., et al. (2016) · Brain Structure and Function · doi:10.1007/s00429-016-1347-1 · Cited by 50 · see citing works
Self-citationJensen, S. K. G., Pangelinan, M., Björnholm, L., Klasnja, A., Leemans, A., Drakesmith, M., Evans, C. J., Barker, E. D., & Paus, T. (2018) · NeuroImage · doi:10.1016/j.neuroimage.2017.10.033 · Cited by 44 · see citing works
Gao, Y., Huang, Y., & Li, X. (2016) · Journal of Psychopathology and Behavioral Assessment · doi:10.1007/s10862-016-9556-8 · Cited by 41 · see citing works
Exposure to prenatal maternal distress and infant white matter neurodevelopment
Demers, C. H., Bagonis, M. M., Al‐Ali, K., Garcia, S. E., Styner, M. A., Gilmore, J. H., Hoffman, M. C., Hankin, B. L., & Davis, E. P. (2021) · Development and Psychopathology · doi:10.1017/s0954579421000742 · Cited by 36 · see citing works
Maternal depressive symptoms, neonatal white matter, and toddler social-emotional development
Lautarescu, A., Bonthrone, A. F., Pietsch, M., Batalle, D., Cordero-Grande, L., Tournier, J.-D., Christiaens, D., Hajnal, J. V., Chew, A., Falconer, S., et al. (2022) · Translational Psychiatry · doi:10.1038/s41398-022-02073-y · Cited by 29 · see citing works
Self-citationPrenatal Programming of Neurodevelopment: Structural and Functional Changes
Demers, C. H., Aran, Ö., Glynn, L. M., & Davis, E. P. (2021) · Springer eBooks · doi:10.1007/978-3-030-60159-1_9 · Cited by 25 · see citing works
LUPIEN, S. J., Ouellet‐Morin, I., Herba, C. M., Juster, R., & McEwen, B. S. (2016) · Epigenetics and human health · doi:10.1007/978-3-319-24493-8_1 · Cited by 26 · see citing works
Comprehensive Review of the Impact of Maternal Stress on Fetal Development
Tadanki, D., Kaza, P., Meisinger, E., Syed, A., Johnson, A., Bainbridge, G., Cho, M., Anigbogu, C., & Gupta, G. (2025) · Pediatric Discovery · doi:10.1002/pdi3.70004 · Cited by 33 · see citing works
Kumpulainen, V., Merisaari, H., Copeland, A., Silver, E. A., Pulli, E. P., Lewis, J. D., Saukko, E., Saunavaara, J. P., Karlsson, L., Karlsson, H., et al. (2022) · European Journal of Neuroscience · doi:10.1111/ejn.15785 · Cited by 19 · see citing works
Glover, V. A. S., Ahmed-Salim, Y., & Capron, L. (2016) · Springer eBooks · doi:10.1007/978-3-319-22023-9_12 · Cited by 20 · see citing works
Self-citationRoss, K. M., Letourneau, N. L., Climie, E. A., Giesbrecht, G. F., & Dewey, D. (2020) · Developmental Neuropsychology · doi:10.1080/87565641.2020.1838525 · Cited by 18 · see citing works
Marečková, K., Klasnja, A., Andrýsková, L., Brázdil, M., & Paus, T. (2018) · Human Brain Mapping · doi:10.1002/hbm.24435 · Cited by 18 · see citing works
McQuaid, G. A., Darcey, V. L., Avalos, M. F., Fishbein, D. H., & VanMeter, J. W. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.112145 · Cited by 21 · see citing works
Kumpulainen, V., Copeland, A., Pulli, E. P., Silver, E. A., Kataja, E., Saukko, E., Merisaari, H., Lewis, J. D., Karlsson, L., Karlsson, H., et al. (2023) · Biological Psychiatry · doi:10.1016/j.biopsych.2023.05.014 · Cited by 18 · see citing works
Jirsaraie, R. J., Palma, A. M., Small, S. L., Sandman, C. A., Davis, E. P., Baram, T. Z., Stern, H. S., Glynn, L. M., & Yassa, M. A. (2023) · Biological Psychiatry Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2023.08.002 · Cited by 16 · see citing works
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Dufford, A. J., Salzwedel, A., Gilmore, J. H., Gao, W., & Kim, P. (2021) · Developmental Psychobiology · doi:10.1002/dev.22166 · Cited by 16 · see citing works
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Franke, K., den Bergh, B. R. H. V., de Rooij, S. R., Roseboom, T. J., Nathanielsz, P. W., Witte, O. W., & Schwab, M. G. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/148916 · Cited by 15 · see citing works
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Camerota, M., & Willoughby, M. T. (2019) · Child Development · doi:10.1111/cdev.13271 · Cited by 13 · see citing works
Barda, T., Schmitz‐Koep, B., Menegaux, A., Bartmann, P., Dieter Wolke, C., Sorg, C., & Hedderich, D. M. (2025) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2025.106061 · Cited by 11 · see citing works
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Mennes, M., den Bergh, B. R. H. V., Lagae, L. G., Lagae, L., & Stiers, P. L. J. (2019) · Brain Imaging and Behavior · doi:10.1007/s11682-018-0027-6 · Cited by 14 · see citing works
Canini, M., Pecco, N., Caglioni, M., Katušić, A., Išasegi, I. Ž., Oprandi, C., Scifo, P., Pozzoni, M., Lorioli, L., Garbetta, G., et al. (2023) · Journal of Neuroscience Research · doi:10.1002/jnr.25207 · Cited by 10 · see citing works
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Shah, R., Salafia, C. M., Girardi, T., Rukat, C., Brunner, J., Barrett, E. S., O’Connor, T. G., Misra, D. P., & Miller, R. K. (2024) · Journal of Affective Disorders · doi:10.1016/j.jad.2024.05.108 · Cited by 3 · see citing works
Self-citationUltrasonic Vocalizations and Behavior of Rat Pups Born From Sleep-Deprived Dams
Gulia, K. K., & Kumar, V. M. (2018) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-12-809600-0.00044-5 · Cited by 4 · see citing works
Maternal Prenatal Stress and the Developmental Origins of Mental Health
O’Donnell, K. J., & Glover, V. A. S. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-801383-0.00007-4 · Cited by 4 · see citing works
Self-citationO’Connor, T. G. (2016) · Wiley eBooks · doi:10.1002/9781119125556.devpsy105 · Cited by 4 · see citing works
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Chukwu, O. O., Iyare, C. O., Okorocha, A. E., Konyefom, N. G., Emelike, C. U., Onyeji, G. N., Igwe, N. P., & Ezimah, A. C. U. (2025) · Journal of Medicinal Plants · doi:10.61882/jmp.24.93.79 · Cited by 1 · see citing works
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Luszczewska-Sierakowska, I., & Jonak, K. (2020) · Medycyna Weterynaryjna · doi:10.21521/mw.6400
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du Plessis, A. J., & Volpe, J. J. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-10513-5.00011-5
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Niu, Y., Camacho, M. C., Wu, S., & Humphreys, K. L. (2024) · Current topics in behavioral neurosciences · doi:10.1007/7854_2024_542
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Glover, V. A. S. (2026) · Cambridge University Press eBooks · doi:10.1017/9781911623496.036
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Early Infant Subcortical Volume is Associated with Maternal Prenatal Depression
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- Authors
- Sarkar, S., Craig, M. C., Dell’Acqua, F., O’Connor, T. G., Catani, M., Deeley, Q., Glover, V., & Murphy, D. G. M.
- Affiliations
- King's College London (GB)
- University of Rochester Medicine (US)
- Imperial College London (GB)
- Corresponding author
- Craig, Michael C.
- ORCID
- Venue
- The World Journal of Biological Psychiatry
- Publisher
- Informa UK Limited
- Published
- 2014-05
- Volume
- 15
- Issue
- 4
- Pages
- 346-352
- ISSN
- 1562-2975 (ISSN-L)
- 1814-1412
- OpenAlex
- W2156508144
- Cited by
- 70
- References
- 43
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 5 · 2023: 3 · 2022: 5 · 2021: 5 · 2020: 6 · 2019: 10 · 2018: 5 · 2017: 5 · 2016: 12 · 2015: 6 · 2014: 1
- FWCI
- 7.92
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The World Journal of Biological Psychiatry (publishedVersion)
- PubMed (publishedVersion)
- Research Portal (King's College London) (submittedVersion)
- Funders
- March of Dimes Foundation
- National Institute for Health and Care Research
- Baily Thomas Charitable Fund
- Topics
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Maternal Mental Health During Pregnancy and Postpartum
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced Neuroimaging Techniques and Applications
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Keywords
- prenatal stress, uncinate fasciculus, white matter microstructure, fractional anisotropy, brain development, children
- MeSH terms
- Adult, Brain, Child, Female, Frontal Lobe, Humans, Life Change Events, Limbic System, Nerve Net, Pregnancy, Pregnancy Complications, Prenatal Exposure Delayed Effects, Stress, Psychological, Diffusion Tensor Imaging, White Matter
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