Maternal care modulates the relationship between prenatal risk and hippocampal volume in women but not in men
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Smaller hippocampal volume is associated with psychiatric disorders. Variations in hippocampal volume are discussed as both a consequence of the neurotoxic effects of stress and as a pre-existing condition leading to increased vulnerability for cognitive and emotional impairments. To investigate whether early experience can account for variability in hippocampal volume in adulthood (vulnerability hypothesis), we assessed the relationship between birth weight and hippocampal volume in 44 subjects. The reported quality of maternal care in early childhood, as evaluated by the Parental Bonding Inventory, was used as index of the quality of the postnatal environment. Hippocampal volume was assessed from magnetic resonance images using a manual segmentation protocol. We show that birth weight significantly predicts hippocampal volume in adulthood only in female subjects reporting low maternal care. The results suggest that the postnatal environment modulates the neurodevelopmental consequences of prenatal risk and that this effect is sex-specific.
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Limbic structures, especially hippocampus, are prominent targets for early life stress.
“Limbic structures, especially the hippocampus, have been shown to be prominent targets for early life stress (e.g. Coe et al., 2003; Buss et al., 2007).”
From High pregnancy anxiety during mid-gestation is associated with decreased gray matter density in 6-9-year-old children. (2010) · cites this paper as Buss et al., 2007
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Cites
da Luz, A. C. D. D. S., Dias, G. P., Bevilaqua, M. C. D. N., Cocks, G. D., Gardino, P. F., Thuret, S., & Nardi, A. E. (2013) · Neuropsychobiology · doi:10.1159/000353269 · Cited by 4,012 · see citing works
A parental bonding instrument.
Parker, G., Tupling, H., & Brown, L. B. (1979) · British Journal of Medical Psychology · doi:10.1111/j.2044-8341.1979.tb02487.x · Cited by 3,788 · see citing works
Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space
Collins, D. L., Neelin, P., Peters, T. M., & Evans, A. C. (1994) · Journal of Computer Assisted Tomography · doi:10.1097/00004728-199403000-00005 · Cited by 3,431 · cited 1× · see citing works
“This procedure includes the removal of all extracranial tissue and the cerebellum and has been validated before (Collins et al., 1994).”
MethodThe Neuroendocrinology of Stress and Aging: The Glucocorticoid Cascade Hypothesis
Sapolsky, R. M., Krey, L. C., & McEwen, B. S. (1986) · Science of Aging Knowledge Environment · doi:10.1126/sageke.2002.38.cp21 · Cited by 2,287 · see citing works
Smaller hippocampal volume predicts pathologic vulnerability to psychological trauma
Gilbertson, M. W., Shenton, M. E., Ciszewski, A., Kasai, K., Lasko, N. B., Orr, S. P., & Pitman, R. K. (2002) · Nature Neuroscience · doi:10.1038/nn958 · Cited by 1,635 · see citing works
A New and Improved Population-Based Canadian Reference for Birth Weight for Gestational Age
Kramer, M. S., Platt, R. W., Wen, S. W., Joseph, K. S., Allen, A. C., Abrahamowicz, M., Blondel, B., Bréart, G., & Bréart, G. (2001) · PEDIATRICS · doi:10.1542/peds.108.2.e35 · Cited by 1,526 · see citing works
The neurobiological consequences of early stress and childhood maltreatment
Teicher, M. H., Andersen, S. L., Polcari, A., Anderson, C. M., Navalta, C. P., & Kim, D. M. (2003) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(03)00007-1 · Cited by 1,465 · see citing works
Owens, P. C., Smith, R., Brinsmead, M. W., Hall, C., Foureur, M. J., Hurt, D., Lovelock, M., Chan, E.-C., Cubis, J., & Lewin, T. J. (1987) · Life Sciences · doi:10.1016/0024-3205(87)90603-5 · Cited by 958 · see citing works
Prenatal glucocorticoids and long-term programming
Seckl (2004) · European Journal of Endocrinology · doi:10.1530/eje.0.151u049 · Cited by 825 · see citing works
Childhood trauma associated with smaller hippocampal volume in women with major depression
Vythilingam, M., Heim, C., Newport, J., Miller, A. H., Anderson, E., Bronen, R., Brummer, M., Staib, L., Vermetten, E., Charney, D. S., et al. (2002) · American Journal of Psychiatry · doi:10.1176/appi.ajp.159.12.2072 · Cited by 812 · see citing works
Wadhwa, P. D., Sandman, C. A., Porto, M., Dunkel-Schetter, C., & Garite, T. J. (1993) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(93)90016-c · Cited by 794 · see citing works
Weinstock, M. (2005) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2004.09.006 · Cited by 706 · see citing works
Pruessner, J. C. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.4.433 · Cited by 706 · see citing works
Self-citationMR-based in vivo hippocampal volumetrics: 2. Findings in neuropsychiatric disorders
Geuze, E., Vermetten, E., & Bremner, J. D. (2005) · Molecular Psychiatry · doi:10.1038/sj.mp.4001579 · Cited by 412 · see citing works
Parental 'Affectionless Control' as an Antecedent to Adult Depression: A Risk Factor Delineated
Parker, G. (1983) · Archives of General Psychiatry · doi:10.1001/archpsyc.1983.01790080038005 · Cited by 408 · see citing works
The stability of the Parental Bonding Instrument over a 20-year period
Wilhelm, K. A., Niven, H., Parker, G. B., & Hadži-Pavlović, D. (2004) · Psychological Medicine · doi:10.1017/s0033291704003538 · Cited by 369 · see citing works
The parental bonding instrument
Parker, G. B. (1990) · Social Psychiatry and Psychiatric Epidemiology · doi:10.1007/bf00782881 · Cited by 362 · see citing works
Pruessner, J. C., Baldwin, M. W., Dedovic, K., Renwick, R., Mahani, N. K., Lord, C., Meaney, M., & Lupien, S. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2005.06.014 · Cited by 336 · see citing works
Self-citationReynolds, R. M., Walker, B. R., Syddall, H. E., Andrew, R., Wood, P. J., Whorwood, C. B., & Phillips, D. I. W. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.86.1.7145 · Cited by 328 · see citing works
Age and gender predict volume decline in the anterior and posterior hippocampus in early adulthood
Pruessner, J. C., Collins, D. L., Pruessner, M., & Evans, A. C. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-01-00194.2001 · Cited by 292 · see citing works
Self-citationMaternal Asthma Is Associated with Reduced Female Fetal Growth
Murphy, V. E., Gibson, P. G., Giles, W. B., Zakár, T., Smith, R., Bisits, A. M., Kessell, C. G., & Clifton, V. L. (2003) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.200303-374oc · Cited by 290 · see citing works
Reynolds, R. M. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.86.1.245 · Cited by 242 · see citing works
Lemaire, V., Lamarque, S., Le Moal, M., Piazza, P.-V., & Abrous, D. N. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.11.009 · Cited by 211 · see citing works
Growth and living conditions in childhood and hypertension in adult life: a longitudinal study
Barker, D. J. P., Forsén, T., Eriksson, J. G., & Osmond, C. (2002) · Journal of Hypertension · doi:10.1097/00004872-200210000-00013 · Cited by 180 · see citing works
Quantitative magnetic resonance imaging of the brain in survivors of very low birth weight
Abernethy, L. J. (2002) · Archives of Disease in Childhood · doi:10.1136/adc.87.4.279 · Cited by 157 · see citing works
Parental representations of depressed outpatients from a U.S.A. sample
Plantes, M. M., Prusoff, B. A., Brennan, J., & Parker, G. B. (1988) · Journal of Affective Disorders · doi:10.1016/0165-0327(88)90083-3 · Cited by 141 · see citing works
Birth weight and the future development of diabetes. A review of the evidence.
Phillips, D. I. W. (1998) · PubMed · Cited by 138 · see citing works
Prenatal stress causes gender‐dependent neuronal loss and oxidative stress in rat hippocampus
Zhu, Z., Li, X., Chen, W., Zhao, Y., Li, H., Qing, C., Jia, N., Bai, Z., & Liu, J. (2004) · Journal of Neuroscience Research · doi:10.1002/jnr.20338 · Cited by 122 · see citing works
Kajantie, E., Phillips, D. I. W., Andersson, S., Barker, D. J., Dunkel, L., Forsén, T., Osmond, C., Tuominen, J. A., Wood, P. J., & Eriksson, J. G. (2002) · Clinical Endocrinology · doi:10.1046/j.1365-2265.2002.01659.x · Cited by 116 · see citing works
Montano, M. M., Wang, M.-H., & Saal, F. S. V. (1993) · Reproduction · doi:10.1530/jrf.0.0990283 · Cited by 95 · see citing works
Manassis, K., Owens, M., Adam, K. S., West, M., & Sheldon-Keller, A. (1999) · Australian & New Zealand Journal of Psychiatry · doi:10.1080/j.1440-1614.1999.00560.x · Cited by 91 · see citing works
Brabham, T., Phelka, A., Zimmer, C. A., Nash, A., López, J. F., & Vázquez, D. M. (2000) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.2000.279.5.r1899 · Cited by 73 · see citing works
Lizardi, H., & Klein, D. N. (2005) · The Journal of Nervous and Mental Disease · doi:10.1097/01.nmd.0000154838.16100.36 · Cited by 70 · see citing works
Parental Characteristics of Jews and Greeks in Australia
Parker, G. B., & Lipscombe, P. (1979) · Australian & New Zealand Journal of Psychiatry · doi:10.3109/00048677909159140 · Cited by 35 · see citing works
Phillips, D. I. W. (2004) · Endocrine Research · doi:10.1081/erc-200044086 · Cited by 33 · see citing works
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Lupien, S. J., McEwen, B. S., Gunnar, M. R., & Heim, C. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2639 · Cited by 6,256 · see citing works
Self-citationMcEwen, B. S., & Gianaros, P. J. (2010) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.05331.x · Cited by 1,715 · see citing works
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Hackman, D. A., Farah, M. J., & Meaney, M. J. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2897 · Cited by 1,409 · see citing works
Self-citationHeim, C., & Binder, E. B. (2012) · Experimental Neurology · doi:10.1016/j.expneurol.2011.10.032 · Cited by 986 · see citing works
Social influences on neuroplasticity: stress and interventions to promote well-being
Davidson, R. J., & McEwen, B. S. (2012) · Nature Neuroscience · doi:10.1038/nn.3093 · Cited by 892 · see citing works
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Harris, A., & Seckl, J. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.06.007 · Cited by 871 · see citing works
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Nemeroff, C. B. (2016) · Neuron · doi:10.1016/j.neuron.2016.01.019 · Cited by 768 · see citing works
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Dedovic, K., Duchesne, A., Andrews, J., Engert, V., & Pruessner, J. C. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2009.05.074 · Cited by 699 · see citing works
Self-citationChampagne, D. L., Bagot, R. C., van Hasselt, F., Ramakers, G., Meaney, M. J., de Kloet, E. R., Joels, M., & Krugers, H. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0526-08.2008 · Cited by 661 · see citing works
Self-citationBuss, 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
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O’Donnell, K. J., & Meaney, M. J. (2017) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2016.16020138 · Cited by 608 · see citing works
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Noble, K. G., Houston, S. M., Kan, E., & Sowell, E. R. (2012) · Developmental Science · doi:10.1111/j.1467-7687.2012.01147.x · Cited by 542 · see citing works
Frodl, T., & O'Keane, V. (2013) · Neurobiology of Disease · doi:10.1016/j.nbd.2012.03.012 · Cited by 555 · see citing works
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Brito, N. H., & Noble, K. G. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00276 · Cited by 525 · see citing works
Buss, 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
Self-citationLupien, S. J., Parent, S., Evans, A. C., Tremblay, R. E., Zelazo, P. D., Corbo, V., Pruessner, J. C., & Séguin, J. R. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1105371108 · Cited by 379 · see citing works
Self-citationEdmiston, E. E. (2011) · Archives of Pediatrics & Adolescent Medicine · doi:10.1001/archpediatrics.2011.565 · Cited by 341 · see citing works
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Pruessner, J. C., Dedovic, K., Pruessner, M., Lord, C., Buss, C., Collins, L., Dagher, A., & Lupien, S. J. (2010) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.02.016 · Cited by 333 · see citing works
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Self-citationJuster, R.-P., Bizik, G., Picard, M., Arsenault-Lapierre, G., Sindi, S., Trepanier, L., Marin, M.-F., Wan, N., Sekerovic, Z., Lord, C., et al. (2011) · Development and Psychopathology · doi:10.1017/s0954579411000289 · Cited by 268 · see citing works
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Quirin, M., Pruessner, J. C., & Kuhl, J. (2008) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2008.01.013 · Cited by 167 · see citing works
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Jones, S. L., Dufoix, R., Laplante, D. P., Elgbeili, G., Patel, R., Chakravarty, M. M., King, S., & Pruessner, J. C. (2019) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2019.00144 · Cited by 92 · see citing works
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Quirin, M., Gillath, O., Pruessner, J. C., & Eggert, L. D. (2010) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsp042 · Cited by 71 · see citing works
Self-citationPruessner, M., Vracotas, N., Joober, R., Pruessner, J. C., & Malla, A. K. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.06.002 · Cited by 58 · see citing works
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Schneider, S., Brassen, S., Bromberg, U., Banaschewski, T., Conrod, P., Flor, H., Gallinat, J., Garavan, H., Heinz, A., Martinot, J.-L., et al. (2012) · Translational Psychiatry · doi:10.1038/tp.2012.113 · Cited by 33 · see citing works
Den Braber, A., Van ‘t Ent, D., Stoffers, D., Linkenkaer-Hansen, K., I. Boomsma, D., & J.C. de Geus, E. (2013) · International Journal of Psychological Research · doi:10.21500/20112084.712 · Cited by 11 · see citing works
- Authors
- Buss, C., Lord, C., Wadiwalla, M., Hellhammer, D. H., Lupien, S. J., Meaney, M. J., & Pruessner, J. C.
- Affiliations
- Universität Trier (DE)
- Douglas Mental Health University Institute (CA)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2007-03-07
- Volume
- 27
- Issue
- 10
- Pages
- 2592-2595
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6672503
- OpenAlex
- W2050889951
- Cited by
- 187
- References
- 35
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 1 · 2023: 5 · 2022: 7 · 2021: 6 · 2020: 7 · 2019: 7 · 2018: 9 · 2017: 6 · 2016: 18 · 2015: 16 · 2014: 13 · 2013: 12 · 2012: 20
- FWCI
- 14.26
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Canadian Institutes of Health Research (67071)
- Natural Sciences and Engineering Research Council of Canada (249996)
- Topics
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Maternal Mental Health During Pregnancy and Postpartum
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- maternal care, hippocampal volume, birth weight, prenatal risk, sex differences, postnatal environment, brain development, vulnerability hypothesis, childhood stress
- MeSH terms
- Adult, Birth Weight, Child, Child Rearing, Female, Hippocampus, Humans, Magnetic Resonance Imaging, Male, Mothers, Prognosis, Risk Factors, Sex Factors, Stress, Physiological, Embryonic Development
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