Hostname: page-component-78c5997874-fbnjt Total loading time: 0 Render date: 2024-11-06T01:05:43.250Z Has data issue: false hasContentIssue false
  • English
  • Français

Beating the brain about abuse: Empirical and meta-analytic studies of the association between maltreatment and hippocampal volume across childhood and adolescence

Published online by Cambridge University Press:  06 May 2015

Madelon M. E. Riem ,
Lenneke R. A. Alink ,
Dorothée Out ,
Marinus H. Van Ijzendoorn  and
Marian J. Bakermans-Kranenburg
Madelon M. E. Riem
Affiliation:
Leiden University
Lenneke R. A. Alink
Affiliation:
Leiden University
Dorothée Out
Affiliation:
Leiden University
Marinus H. Van Ijzendoorn*
Affiliation:
Leiden University
Marian J. Bakermans-Kranenburg*
Affiliation:
Leiden University
*
Address correspondence and reprint requests to: Marian J. Bakermans-Kranenburg or Marinus van IJzendoorn, Centre for Child and Family Studies, Leiden University, PO Box 9555, 2300 RB Leiden, the Netherlands; E-mail: [email protected] or [email protected].
Address correspondence and reprint requests to: Marian J. Bakermans-Kranenburg or Marinus van IJzendoorn, Centre for Child and Family Studies, Leiden University, PO Box 9555, 2300 RB Leiden, the Netherlands; E-mail: [email protected] or [email protected].
Get access Rights & Permissions [Opens in a new window]

Abstract

We present new empirical data and meta-analytic evidence for the association of childhood maltreatment with reduced hippocampal volume. In Study 1, we examined the effects of maltreatment experiences reported during the Adult Attachment Interview on hippocampal volume in female twin pairs. We found that reduced hippocampal volume was related to childhood maltreatment. In addition, individuals who reported having experienced maltreatment at older ages had larger reductions in hippocampal volume compared to individuals who reported maltreatment in early childhood. In Study 2, we present the results of a meta-analysis of 49 studies (including 2,720 participants) examining hippocampal volume in relation to experiences of child maltreatment, and test the moderating role of the timing of the maltreatment, the severity of maltreatment, and the time after exposure to maltreatment. The results of the meta-analysis confirmed that experiences of childhood maltreatment are associated with a reduction in hippocampal volume and that the effects of maltreatment are more pronounced when the maltreatment occurs in middle childhood compared to early childhood or adolescence.

Type
Regular Articles
Information
Development and Psychopathology , Volume 27 , Special Issue 2: Neural Plasticity, Sensitive Periods, and Psychopathology , May 2015 , pp. 507 - 520
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alink, L. R., Cicchetti, D., Kim, J., & Rogosch, F. A. (2012). Longitudinal associations among child maltreatment, social functioning, and cortisol regulation. Developmental Psychology, 48, 224–236.CrossRefGoogle ScholarPubMed
Anda, R. F., Whitfield, C. L., Felitti, V. J., Chapman, D., Edwards, V. J., Dube, S. R., et al. (2002). Adverse childhood experiences, alcoholic parents, and later risk of alcoholism and depression. Psychiatric Services, 53, 1001–1009.CrossRefGoogle ScholarPubMed
Andersen, S. L., & Teicher, M. H. (2004). Delayed effects of early stress on hippocampal development. Neuropsychopharmacology, 29, 1988–1993.CrossRefGoogle ScholarPubMed
Andersen, S. L., & Teicher, M. H. (2008). Stress, sensitive periods and maturational events in adolescent depression. Trends in Neuroscience, 31, 183–191.CrossRefGoogle ScholarPubMed
Andersen, S. L., Tomada, A., Vincow, E. S., Valente, E., Polcari, A., & Teicher, M. H. (2008). Preliminary evidence for sensitive periods in the effect of childhood sexual abuse on regional brain development. Journal of Neuropsychiatry and Clinical Neurosciences, 20, 292–301.CrossRefGoogle ScholarPubMed
Baker, L. M., Williams, L. M., Korgaonkar, M. S., Cohen, R. A., Heaps, J. M., & Paul, R. H. (2013). Impact of early vs. late childhood early life stress on brain morphometrics. Brain Imaging and Behavior, 7, 196–203.CrossRefGoogle ScholarPubMed
Bakermans-Kranenburg, M. J., & van IJzendoorn, M. H. (1993). A psychometric study of the Adult Attachment Interview: Reliability and discriminant validity. Developmental Psychology, 29, 870.Google Scholar
Barnett, D., Manly, J. T., & Cicchetti, D., (1993). Defining child maltreatment: The interface between policy and research. In Cicchetti, D. & Toth, S. L. (Eds.), Advances in applied developmental psychology: Child abuse, child development and social policy (pp. 7–73). Norwood, NJ: Ablex Publishing.Google Scholar
Bauer, P. J., Burch, M. M., Scholin, S. E., & Guler, O. E. (2007). Using cue words to investigate the distribution of autobiographical memories in childhood. Psychological Science, 18, 910–916.CrossRefGoogle ScholarPubMed
Benoit, D., & Parker, K. C. (1994). Stability and transmission of attachment across three generations. Child Development, 65, 1444–1456.CrossRefGoogle ScholarPubMed
Bernard, K., Lind, T., & Dozier, M. (2014). Neurobiological consequences of neglect and abuse. In Korbin, J. E., & Krugman, K. D. (Eds.), Handbook of child maltreatment: Contemporary issues in research and policy (pp. 205–223). Dordrecht: Springer.CrossRefGoogle Scholar
Bernstein, D. P., Stein, J. A., Newcomb, M. D., Walker, E., Pogge, D., Ahluvalia, T., et al. (2003). Development and validation of a brief screening version of the Childhood Trauma Questionnaire. Child Abuse and Neglect, 27, 169–190.CrossRefGoogle ScholarPubMed
Bifulco, A., Brown, G. W., & Harris, T. O. (1994). Childhood Experience of Care and Abuse (CECA): A retrospective interview measure. Journal of Child Psychology and Psychiatry, 35, 1419–1435.Google ScholarPubMed
Bonne, O., Vythilingam, M., Inagaki, M., Wood, S., Neumeister, A., Nugent, A. C., et al. (2008). Reduced posterior hippocampal volume in posttraumatic stress disorder. Journal of Clinical Psychiatry, 69, 1087.CrossRefGoogle ScholarPubMed
Borenstein, M., Hedges, L. V., Higgins, J. P. T., & Rothstein, H. R. (2009). Fixed-effect versus random-effects models. In Introduction to meta-analysis (pp. 77–86). Hoboken, NJ: Wiley.CrossRefGoogle Scholar
Bremner, J. D., Mletzko, T., Welter, S., Quinn, S., Williams, C., Brummer, M., et al. (2005). Effects of phenytoin on memory, cognition and brain structure in post-traumatic stress disorder: A pilot study. Journal of Psychopharmacology, 19, 159–165.CrossRefGoogle ScholarPubMed
Bremner, J. D., Randall, P., Vermetten, E., Staib, L., Bronen, R. A., Mazure, C., et al. (1997). Magnetic resonance imaging-based measurement of hippocampal volume in posttraumatic stress disorder related to childhood physical and sexual abuse—A preliminary report. Biological Psychiatry, 41, 23–32.CrossRefGoogle ScholarPubMed
Bremner, J. D., Vythilingam, M., Vermetten, E., Southwick, S. M., McGlashan, T., Nazeer, A., et al. (2003). MRI and PET study of deficits in hippocampal structure and function in women with childhood sexual abuse and posttraumatic stress disorder. American Journal of Psychiatry, 160, 924–932.CrossRefGoogle ScholarPubMed
Carballedo, A., Lisiecka, D., Fagan, A., Saleh, K., Ferguson, Y., Connolly, G., et al. (2012). Early life adversity is associated with brain changes in subjects at family risk for depression. World Journal of Biological Psychiatry, 13, 569–578.CrossRefGoogle ScholarPubMed
Carpenter, L. L., Shattuck, T. T., Tyrka, A. R., Geracioti, T. D., & Price, L. H. (2011). Effect of childhood physical abuse on cortisol stress response. Psychopharmacology (Berlin), 214, 367–375.CrossRefGoogle ScholarPubMed
Carrion, V. G., Weems, C. F., Eliez, S., Patwardhan, A., Brown, W., Ray, R. D., et al. (2001). Attenuation of frontal asymmetry in pediatric posttraumatic stress disorder. Biological Psychiatry, 50, 943–951.CrossRefGoogle ScholarPubMed
Cicchetti, D., & Rogosch, F. A. (2001a). Diverse patterns of neuroendocrine activity in maltreated children. Development and Psychopathology, 13, 677–693.CrossRefGoogle ScholarPubMed
Cicchetti, D., & Rogosch, F. A. (2001b). The impact of child maltreatment and psychopathology on neuroendocrine functioning. Development and Psychopathology, 13, 783–804.CrossRefGoogle ScholarPubMed
Cohen, R. A., Grieve, S., Hoth, K. F., Paul, R. H., Sweet, L., Tate, D., et al. (2006). Early life stress and morphometry of the adult anterior cingulate cortex and caudate nuclei. Biological Psychiatry, 59, 975–982.CrossRefGoogle ScholarPubMed
Crowell, J. A., Treboux, D., & Waters, E. (2002). Stability of attachment representations: The transition to marriage. Developmental Psychology, 38, 467–479.CrossRefGoogle ScholarPubMed
Crowell, J. A., Waters, E., Treboux, D., O'Connor, E., Colon-Downs, C., Feider, O., et al. (1996). Discriminant validity of the Adult Attachment Interview. Child Development, 67, 2584–2599.CrossRefGoogle ScholarPubMed
Dannlowski, U., Stuhrmann, A., Beutelmann, V., Zwanzger, P., Lenzen, T., Grotegerd, D., et al. (2012). Limbic scars: Long-term consequences of childhood maltreatment revealed by functional and structural magnetic resonance imaging. Biological Psychiatry, 71, 286–293.CrossRefGoogle ScholarPubMed
De Bellis, M. D., Hall, J., Boring, A. M., Frustaci, K., & Moritz, G. (2001 ). A pilot longitudinal study of hippocampal volumes in pediatric maltreatment-related posttraumatic stress disorder. Biological Psychiatry, 50, 305–309.CrossRefGoogle ScholarPubMed
De Bellis, M. D., Keshavan, M. S., Clark, D. B., Casey, B. J., Giedd, J. N., Boring, A. M., et al. (1999). A.E. Bennett Research Award: Developmental traumatology: Part II. Brain development. Biological Psychiatry, 45, 1271–1284.CrossRefGoogle ScholarPubMed
De Bellis, M. D., Keshavan, M. S., Shifflett, H., Iyengar, S., Beers, S. R., Hall, J., et al. (2002). Brain structures in pediatric maltreatment-related posttraumatic stress disorder: A sociodemographically matched study. Biological Psychiatry, 52, 1066–1078.CrossRefGoogle ScholarPubMed
De Brito, S. A., Viding, E., Sebastian, C. L., Kelly, P. A., Mechelli, A., Maris, H., et al. (2013). Reduced orbitofrontal and temporal grey matter in a community sample of maltreated children. Journal of Child Psychology and Psychiatry, 54, 105–112.CrossRefGoogle Scholar
De Kloet, E. R., Rosenfeld, P., Van Eekelen, J. A., Sutanto, W., & Levine, S. (1988). Stress, glucocorticoids and development. Progress in Brain Research, 73, 101–120.CrossRefGoogle ScholarPubMed
De Weerth, C., & van Geert, P. (2002). A longitudinal study of basal cortisol in infants: Intra-individual variability, circadian rhythm and developmental trends. Infant Behavior and Development, 25, 375–398.CrossRefGoogle Scholar
Driessen, M., Herrmann, J., Stahl, K., Zwaan, M., Meier, S., Hill, A., et al. (2000). Magnetic resonance imaging volumes of the hippocampus and the amygdala in women with borderline personality disorder and early traumatization. Archives of General Psychiatry, 57, 1115–1122.CrossRefGoogle ScholarPubMed
Duval, S., & Tweedie, R. (2000). Trim and fill: A simple funnel plot–based method of testing and adjusting for publication bias in meta-analysis. Biometrics, 56, 455–463.CrossRefGoogle ScholarPubMed
Edmiston, E. E., Wang, F., Mazure, C. M., Guiney, J., Sinha, R., Mayes, L. C., et al. (2011). Corticostriatal–limbic gray matter morphology in adolescents with self-reported exposure to childhood maltreatment. Archives of Pediatrics and Adolescent Medicine, 165, 1069–1077.CrossRefGoogle ScholarPubMed
Elzinga, B. M., Roelofs, K., Tollenaar, M. S., Bakvis, P., van Pelt, J., & Spinhoven, P. (2008). Diminished cortisol responses to psychosocial stress associated with lifetime adverse events a study among healthy young subjects. Psychoneuroendocrinology, 33, 227–237.CrossRefGoogle ScholarPubMed
English, D. J., Bangdiwala, S. I., & Runyan, D. K. (2005). The dimensions of maltreatment: Introduction. Child Abuse and Neglect, 29, 441–460.CrossRefGoogle Scholar
English, D. J., & the LONGSCAN Investigators. (1997). Modified Maltreatment Classification System (MMCS). Unpublished manuscript.Google Scholar
Felitti, V. J. (2002). The relationship of adverse childhood experiences to adult health: Turning gold into lead. Zeitschrift für Psychosomatische Medizin und Psychotherapie, 48, 359–369.CrossRefGoogle ScholarPubMed
Fergusson, D. M., Horwood, L. J., & Woodward, L. J. (2000). The stability of child abuse reports: A longitudinal study of the reporting behaviour of young adults. Psychological Medicine, 30, 529–544.CrossRefGoogle ScholarPubMed
Foa, E. B. (1995). Posttraumatic Stress Diagnostic Scale. Bloomington, IN: NCS Pearson.Google Scholar
Frodl, T., Reinhold, E., Koutsouleris, N., Reiser, M., & Meisenzahl, E. M. (2010). Interaction of childhood stress with hippocampus and prefrontal cortex volume reduction in major depression. Journal of Psychiatric Research, 44, 799–807.CrossRefGoogle ScholarPubMed
Gilbody, S. M., Song, F., Eastwood, A. J., & Sutton, A. (2000). The causes, consequences and detection of publication bias in psychiatry. Acta Psychiatrica Scandinavica, 102, 241–249.CrossRefGoogle ScholarPubMed
Gunnar, M. R., & Fisher, P. A. (2006). Bringing basic research on early experience and stress neurobiology to bear on preventive interventions for neglected and maltreated children. Development and Psychopathology, 18, 651–677.CrossRefGoogle ScholarPubMed
Gunnar, M. R., & Vazquez, D. M. (2001). Low cortisol and a flattening of expected daytime rhythm: Potential indices of risk in human development. Development and Psychopathology, 13, 515–538.CrossRefGoogle Scholar
Heim, C., Newport, D. J., Wagner, D., Wilcox, M. M., Miller, A. H., & Nemeroff, C. B. (2002). The role of early adverse experience and adulthood stress in the prediction of neuroendocrine stress reactivity in women: A multiple regression analysis. Depression and Anxiety, 15, 117–125.CrossRefGoogle ScholarPubMed
Hernaus, D., van Winkel, R., Gronenschild, E., Habets, P., Kenis, G., Marcelis, M., et al. (2014). Brain-derived neurotrophic factor/FK506-binding protein 5 genotype by childhood trauma interactions do not impact on hippocampal volume and cognitive performance. PLOS ONE, 9, e92722.CrossRefGoogle Scholar
Hesse, E. (2008). The Adult Attachment Interview: Protocol, method of analysis, and empirical studies. In Cassidy, J. & Shaver, P. R. (Eds.), Handbook of attachment: Theory, research, and clinical applications (2nd ed., pp. 552–598). New York: Guilford Press.Google Scholar
Hoy, K., Barrett, S., Shannon, C., Campbell, C., Watson, D., Rushe, T., et al. (2012). Childhood trauma and hippocampal and amygdalar volumes in first-episode psychosis. Schizophrenia Bulletin, 38, 1162–1169.CrossRefGoogle ScholarPubMed
Jenkinson, M., Bannister, P., Brady, M., & Smith, S. (2002). Improved optimization for the robust and accurate linear registration and motion correction of brain images. NeuroImage, 17, 825–841.CrossRefGoogle ScholarPubMed
Jenkinson, M., & Smith, S. (2001). A global optimisation method for robust affine registration of brain images. Medical Image Analysis, 5, 143–156.CrossRefGoogle ScholarPubMed
Korgaonkar, M. S., Antees, C., Williams, L. M., Gatt, J. M., Bryant, R. A., Cohen, R., et al. (2013). Early exposure to traumatic stressors impairs emotional brain circuitry. PLOS ONE, 8, e75524.CrossRefGoogle ScholarPubMed
Labudda, K., Kreisel, S., Beblo, T., Mertens, M., Kurlandchikov, O., Bien, C. G., et al. (2013). Mesiotemporal volume loss associated with disorder severity: A VBM study in borderline personality disorder. PLOS ONE, 8, e83677.CrossRefGoogle ScholarPubMed
Landre, L., Destrieux, C., Baudry, M., Barantin, L., Cottier, J. P., Martineau, J., et al. (2010). Preserved subcortical volumes and cortical thickness in women with sexual abuse-related PTSD. Psychiatry Research: Neuroimaging, 183, 181–186.CrossRefGoogle ScholarPubMed
Larson, M. C., White, B. P., Cochran, A., Donzella, B., & Gunnar, M. (1998). Dampening of the cortisol response to handling at 3 months in human infants and its relation to sleep, circadian cortisol activity, and behavioral distress. Developmental Psychobiology, 33, 327–337.3.0.CO;2-S>CrossRefGoogle ScholarPubMed
Lenze, S. N., Xiong, C., & Sheline, Y. I. (2008). Childhood adversity predicts earlier onset of major depression but not reduced hippocampal volume. Psychiatry Research: Neuroimaging, 162, 39–49.CrossRefGoogle Scholar
Lindauer, R. J., Vlieger, E. J., Jalink, M., Olff, M., Carlier, I. V., Majoie, C. B., et al. (2005). Effects of psychotherapy on hippocampal volume in out-patients with post-traumatic stress disorder: A MRI investigation. Psychological Medicine, 35, 1421–1431.CrossRefGoogle ScholarPubMed
Magnus, P., Berg, K., & Nance, W. E. (1983). Predicting zygosity in Norwegian twin pairs born 1915–1960. Clinical Genetics, 24, 103–112.CrossRefGoogle ScholarPubMed
Main, M., Hesse, E., & Goldwyn, R. (2008). Studying differences in language usage in recounting attachment history: An introduction to the AAI. New York: Guilford Press.Google Scholar
McCrory, E., De Brito, S. A., & Viding, E. (2010). Research review: The neurobiology and genetics of maltreatment and adversity. Journal of Child Psychology and Psychiatry and Allied Disciplines, 51, 1079–1095.CrossRefGoogle ScholarPubMed
McCrory, E., De Brito, S. A., & Viding, E. (2011). The impact of childhood maltreatment: A review of neurobiological and genetic factors. Frontiers in Psychiatry, 2, 48.CrossRefGoogle ScholarPubMed
McGowan, P. O., Sasaki, A., D'Alessio, A. C., Dymov, S., Labonte, B., Szyf, M., et al. (2009). Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nature Neuroscience, 12, 342–348.CrossRefGoogle ScholarPubMed
Mehta, M. A., Golembo, N. I., Nosarti, C., Colvert, E., Mota, A., Williams, S. C., et al. (2009). Amygdala, hippocampal and corpus callosum size following severe early institutional deprivation: The English and Romanian Adoptees study pilot. Journal of Child Psychology and Psychiatry, 50, 943–951.CrossRefGoogle ScholarPubMed
Mullen, B. (1989). Advanced BASIC meta-analysis. Hillsdale, NJ: Erlbaum.Google Scholar
Murphy, A., Steele, M., Dube, S. R., Bate, J., Bonuck, K., Meissner, P., et al. (2014). Adverse Childhood Experiences (ACEs) Questionnaire and Adult Attachment Interview (AAI): Implications for parent–child relationships. Child Abuse and Neglect, 38, 224–233.CrossRefGoogle ScholarPubMed
Nanni, V., Uher, R., & Danese, A. (2012). Childhood maltreatment predicts unfavorable course of illness and treatment outcome in depression: A meta-analysis. American Journal of Psychiatry, 169, 141–151.CrossRefGoogle ScholarPubMed
Nijenhuis, E. R., Van der Hart, O., & Kruger, K. (2002). The psychometric characteristics of the Traumatic Experiences Checklist (TEC): First findings among psychiatric outpatients. Clinical Psychology & Psychotherapy, 9, 200–210.CrossRefGoogle Scholar
Norman, R. E., Byambaa, M., De, R., Butchart, A., Scott, J., & Vos, T. (2012). The long-term health consequences of child physical abuse, emotional abuse, and neglect: A systematic review and meta-analysis. PLOS Medicine, 9, e1001349.CrossRefGoogle ScholarPubMed
Out, D., Pieper, S., Bakermans-Kranenburg, M. J., & van IJzendoorn, M. H. (2010). Physiological reactivity to infant crying: A behavioral genetic study. Genes, Brain, and Behavior, 9, 868–876.CrossRefGoogle ScholarPubMed
Pederson, C. L., Maurer, S. H., Kaminski, P. L., Zander, K. A., Peters, C. M., Stokes-Crowe, L. A., et al. (2004). Hippocampal volume and memory performance in a community-based sample of women with posttraumatic stress disorder secondary to child abuse. Journal of Traumatic Stress, 17, 37–40.CrossRefGoogle Scholar
Peterson, C., Warren, K. L., & Short, M. M. (2011). Infantile amnesia across the years: A 2-year follow-up of children's earliest memories. Child Development, 82, 1092–1105.CrossRefGoogle Scholar
Rao, H., Betancourt, L., Giannetta, J. M., Brodsky, N. L., Korczykowski, M., Avants, B. B., et al. (2010). Early parental care is important for hippocampal maturation: Evidence from brain morphology in humans. NeuroImage, 49, 1144–1150.CrossRefGoogle ScholarPubMed
Rasbash, J., Charlton, C., Browne, W. J., Healy, M., & Cameron, B. (2005). MLwiN. Bristol: University of Bristol, Centre for Multilevel Modeling.Google Scholar
Read, J., van Os, J., Morrison, A. P., & Ross, C. A. (2005). Childhood trauma, psychosis and schizophrenia: A literature review with theoretical and clinical implications. Acta Psychiatrica Scandinavica, 112, 330–350.CrossRefGoogle ScholarPubMed
Riem, M. M. E., Bakermans-Kranenburg, M. J., Pieper, S., Tops, M., Boksem, M. A. S., Vermeiren, R. R. J. M., et al. (2011). Oxytocin modulates amygdala, insula, and inferior frontal gyrus responses to infant crying: A randomized controlled trial. Biological Psychiatry, 70, 291–297.CrossRefGoogle ScholarPubMed
Riem, M. M. E., van IJzendoorn, M. H., Tops, M., Boksem, M. A. S., Rombouts, S. A. R. B., & Bakermans-Kranenburg, M. J. (2012). No laughing matter: Intranasaloxytocin administration changes functional brain connectivity during exposure to infant laughter. Neuropsychopharmacology, 37, 1257–1266.CrossRefGoogle Scholar
Rubin, D. C. (2000). The distribution of early childhood memories. Memory, 8, 265–269.CrossRefGoogle ScholarPubMed
Sagi, A., van IJzendoorn, M. H., Scharf, M., Koren-Karie, N., Joels, T., & Mayseless, O. (1994). Stability and discriminant validity of the Adult Attachment Interview: A psychometric study in young Israeli adults. Developmental Psychology, 30, 771.CrossRefGoogle Scholar
Sala, M., Caverzasi, E., Lazzaretti, M., Morandotti, N., De Vidovich, G., Marraffini, E., et al. (2011). Dorsolateral prefrontal cortex and hippocampus sustain impulsivity and aggressiveness in borderline personality disorder. Journal of Affective Disorders, 131, 417–421.CrossRefGoogle ScholarPubMed
Samplin, E., Ikuta, T., Malhotra, A. K., Szeszko, P. R. S., & Derosse, P. (2013). Sex differences in resilience to childhood maltreatment: Effects of trauma history on hippocampal volume, general cognition and subclinical psychosis in healthy adults. Journal of Psychiatric Research, 47, 1174–1179.CrossRefGoogle ScholarPubMed
Sapolsky, R. M., Krey, L. C., & McEwen, B. S. (1985). Prolonged glucocorticoid exposure reduces hippocampal neuron number: Implications for aging. Journal of Neuroscience, 5, 1222–1227.CrossRefGoogle ScholarPubMed
Sapolsky, R. M., & Meaney, M. J. (1986). Maturation of the adrenocortical stress response: Neuroendocrine control mechanisms and the stress hyporesponsive period. Brain Research Reviews, 11, 65–76.CrossRefGoogle Scholar
Sapolsky, R. M., Uno, H., Rebert, C. S., & Finch, C. E. (1990). Hippocampal damage associated with prolonged glucocorticoid exposure in primates. Journal of Neuroscience, 10, 2897–2902.CrossRefGoogle ScholarPubMed
Scheeringa, M. S., Myers, L., Putnam, F. W., & Zeanah, C. H. (2012). Diagnosing PTSD in early childhood: An empirical assessment of four approaches. Journal of Traumatic Stress, 25, 359–367.CrossRefGoogle ScholarPubMed
Scott, K. M., Smith, D. R., & Ellis, P. M. (2010). Prospectively ascertained child maltreatment and its association with DSM-IV mental disorders in young adults. Archives of General Psychiatry, 67, 712–719.CrossRefGoogle ScholarPubMed
Shaffer, A., Huston, L., & Egeland, B. (2008). Identification of child maltreatment using prospective and self-report methodologies: A comparison of maltreatment incidence and relation to later psychopathology. Child Abuse and Neglect, 32, 682–692.CrossRefGoogle ScholarPubMed
Sheffield, J. M., Williams, L. E., Woodward, N. D., & Heckers, S. (2013). Reduced gray matter volume in psychotic disorder patients with a history of childhood sexual abuse. Schizophrenia Research, 143, 185–191.CrossRefGoogle ScholarPubMed
Smith, S. M. (2002). Fast robust automated brain extraction. Human Brain Mapping, 17, 143–155.CrossRefGoogle ScholarPubMed
Smith, S. M., De Stefano, N., Jenkinson, M., & Matthews, P. M. (2001). Normalized accurate measurement of longitudinal brain change. Journal of Computer Assisted Tomography, 25, 466–475.CrossRefGoogle ScholarPubMed
Smith, S. M., Jenkinson, M., Woolrich, M. W., Beckmann, C. F., Behrens, T. E., Johansen-Berg, H., et al. (2004). Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage, 23(Suppl. 1), S208–S219.CrossRefGoogle ScholarPubMed
Smith, S. M., Zhang, Y., Jenkinson, M., Chen, J., Matthews, P. M., Federico, A., et al. (2002). Accurate, robust, and automated longitudinal and cross-sectional brain change analysis. NeuroImage, 17, 479–489.CrossRefGoogle ScholarPubMed
Soloff, P., Nutche, J., Goradia, D., & Diwadkar, V. (2008). Structural brain abnormalities in borderline personality disorder: A voxel-based morphometry study. Psychiatry Research: Neuroimaging, 164, 223–236.CrossRefGoogle ScholarPubMed
Soloff, P. H., Lynch, K. G., & Kelly, T. M. (2002). Childhood abuse as a risk factor for suicidal behavior in borderline personality disorder. Journal of Personality Disorders, 16, 201–214.CrossRefGoogle ScholarPubMed
Stein, M. B., Koverola, C., Hanna, C., Torchia, M. G., & McClarty, B. (1997). Hippocampal volume in women victimized by childhood sexual abuse. Psychological Medicine, 27, 951–959.CrossRefGoogle ScholarPubMed
Sullivan, R. M. (2004). Hemispheric asymmetry in stress processing in rat prefrontal cortex and the role of mesocortical dopamine. Stress, 7, 131–143.CrossRefGoogle ScholarPubMed
Sutton, A. J., Duval, S., Tweedie, R., Abrams, K. R., & Jones, D. R. (2000). Empirical assessment of effect of publication bias on meta-analyses. British Medical Journal, 320, 1574–1577.CrossRefGoogle ScholarPubMed
Teicher, M. H., Anderson, C. M., & Polcari, A. (2012). Childhood maltreatment is associated with reduced volume in the hippocampal subfields CA3, dentate gyrus, and subiculum. Proceedings of the National Academy of Sciences, 109, E563–E572.CrossRefGoogle ScholarPubMed
Teicher, M. H., & Samson, J. A. (2013). Childhood maltreatment and psychopathology: A case for ecophenotypic variants as clinically and neurobiologically distinct subtypes. American Journal of Psychiatry, 170, 1114–1133.CrossRefGoogle ScholarPubMed
Teicher, M. H., Tomoda, A., & Andersen, S. L. (2006). Neurobiological consequences of early stress and childhood maltreatment: Are results from human and animal studies comparable? Annals of the New York Academy of Sciences, 1071, 313–323.CrossRefGoogle ScholarPubMed
Thomaes, K., Dorrepaal, E., Draijer, N., de Ruiter, M. B., van Balkom, A. J., Smit, J. H., et al. (2010). Reduced anterior cingulate and orbitofrontal volumes in child abuse-related complex PTSD. Journal of Clinical Psychiatry, 71, 1636–1644.CrossRefGoogle ScholarPubMed
Thomaes, K., Dorrepaal, E., Draijer, N., Jansma, E. P., Veltman, D. J., & van Balkom, A. J. (2014). Can pharmacological and psychological treatment change brain structure and function in PTSD? A systematic review. Journal of Psychiatric Research, 50, 1–15.CrossRefGoogle ScholarPubMed
Tottenham, N., Hare, T. A., Quinn, B. T., McCarry, T. W., Nurse, M., Gilhooly, T., et al. (2010). Prolonged institutional rearing is associated with atypically large amygdala volume and difficulties in emotion regulation. Developmental Science, 13, 46–61.CrossRefGoogle ScholarPubMed
Vermetten, E., Vythilingam, M., Southwick, S. M., Charney, D. S., & Bremner, J. D. (2003). Long-term treatment with paroxetine increases verbal declarative memory and hippocampal volume in posttraumatic stress disorder. Biological Psychiatry, 54, 693–702.CrossRefGoogle ScholarPubMed
Vythilingam, M., Heim, C., Newport, J., Miller, A. H., Anderson, E., Bronen, R., et al. (2002). Childhood trauma associated with smaller hippocampal volume in women with major depression. American Journal of Psychiatry, 159, 2072–2080.CrossRefGoogle ScholarPubMed
Waters, E., Hamilton, C. E., & Weinfield, N. S. (2000). The stability of attachment security from infancy to adolescence and early adulthood: General introduction. Child Development, 71, 678–683.CrossRefGoogle ScholarPubMed
Waters, E., Merrick, S., Treboux, D., Crowell, J., & Albersheim, L. (2000). Attachment security in infancy and early adulthood: A twenty-year longitudinal study. Child Development, 71, 684–689.CrossRefGoogle ScholarPubMed
Weaver, I. C., Cervoni, N., Champagne, F. A., D'Alessio, A. C., Sharma, S., Seckl, J. R., et al. (2004). Epigenetic programming by maternal behavior. Nature Neuroscience, 7, 847–854.CrossRefGoogle ScholarPubMed
Weinfield, N. S., Sroufe, L. A., & Egeland, B. (2000). Attachment from infancy to early adulthood in a high-risk sample: Continuity, discontinuity, and their correlates. Child Development, 71, 695–702.CrossRefGoogle Scholar
Weniger, G., Lange, C., Sachsse, U., & Irle, E. (2009). Reduced amygdala and hippocampus size in trauma-exposed women with borderline personality disorder and without posttraumatic stress disorder. Journal of Psychiatry and Neuroscience, 34, 383–388.Google ScholarPubMed
Whittle, S., Dennison, M., Vijayakumar, N., Simmons, J. G., Yucel, M., Lubman, D. I., et al. (2013). Childhood maltreatment and psychopathology affect brain development during adolescence. Journal of the American Academy of Child & Adolescent Psychiatry, 52, 940–952.CrossRefGoogle ScholarPubMed
Woon, F. L., & Hedges, D. W. (2008). Hippocampal and amygdala volumes in children and adults with childhood maltreatment-related posttraumatic stress disorder: A meta-analysis. Hippocampus, 18, 729–736.CrossRefGoogle ScholarPubMed
Zach, P., Mrzilkova, J., Rezacova, L., Stuchlik, A., & Vales, K. (2010). Delayed effects of elevated corticosterone level on volume of hippocampal formation in laboratory rat. Physiological Research, 59, 985–996.CrossRefGoogle ScholarPubMed
Zanarini, M. C., Frankenburg, F. R., Reich, D. B., Marino, M. F., Lewis, R. E., Williams, A. A., et al. (2000). Biparental failure in the childhood experiences of borderline patients. Journal of Personality Disorders, 14, 264–273.CrossRefGoogle ScholarPubMed
Zetzsche, T., Preuss, U. W., Frodl, T., Schmitt, G., Seifert, D., Münchhausen, E., et al. (2007). Hippocampal volume reduction and history of aggressive behaviour in patients with borderline personality disorder. Psychiatry Research: Neuroimaging, 154, 157–170.CrossRefGoogle ScholarPubMed
Zhang, Y., Brady, M., & Smith, S. (2001). Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Transactions on Medical Imaging, 20, 45–57.CrossRefGoogle ScholarPubMed