Abstract
Childhood maltreatment is associated with an increased risk for psychiatric and substance use disorders. However, some maltreated individuals appear resilient to these consequences while manifesting the same array of brain changes as maltreated individuals with psychopathology. Hence, a critical issue has been to identify compensatory brain alterations in these resilient individuals. We recently reported that maltreatment is associated with a more vulnerable structural brain network architecture. Resilient individuals have this same vulnerability but appeared to be able to effectively compensate due to reduced nodal efficiency (ability of a node to influence the global network) in 9 specific brain regions that moderate the relationship between maltreatment and psychopathology. Following up, we now report that network vulnerability increases progressively during late adolescence to plateau at about 21 years of age, which may help to explain age of onset of psychopathology. Further, we found that network vulnerability was most significantly affected by parental verbal abuse between 16 and 18 years of age and number of types of maltreatment during childhood. Asymptomatic individuals with no history of psychopathology had more prominent alterations in nodal efficiency than asymptomatic individuals with prior history, who specifically showed reduced nodal efficiency in the right amygdala and right subcallosal gyrus. Experiencing inadequate financial sufficiency during childhood increased the risk of susceptibility versus resilience by 2.98-fold (95% CI 1.49–5.97, p = 0.002) after adjusting for differences in exposure to maltreatment. Interestingly, adequate-to-higher financial sufficiency appeared to be protective and was associated with reduced nodal efficiency in the right postcentral gyrus and subcallosal gyrus “resilience” nodes.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Afifi, T. O., Mather, A., Boman, J., Fleisher, W., Enns, M. W., MacMillan, H., et al. 45 (2011) Childhood adversity and personality disorders: results from a nationally representative population-based study. J Psychiatr Res. Jun. pp. 814–822 6. Available at: http://linkinghub.elsevier.com/retrieve/pii/S0022395610003262, DOI: https://doi.org/10.1016/j.jpsychires.2010.11.008.
Anda, R. F., Whitfield, C. L., Felitti, V. J., Chapman, D., Edwards, V. J., Dube, S. R., et al. 53 (2002) 'Adverse childhood experiences, alcoholic parents, and later risk of alcoholism and depression.' Psychiatr Serv. Aug. pp. 1001–1009 8. Available at: http://eutils.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&id=12161676&retmode=ref&cmd=prlinks, DOI: https://doi.org/10.1176/appi.ps.53.8.1001.
Andersen, S. L., Tomoda, 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. The Journal of Neuropsychiatry and Clinical Neurosciences, 20(3), 292–301. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=18806232. https://doi.org/10.1176/jnp.2008.20.3.292.
Andersen, S. B., Karstoft, K. I., Bertelsen, M., & Madsen, T. (2014). Latent trajectories of trauma symptoms and resilience: the 3-year longitudinal prospective USPER study of Danish veterans deployed in Afghanistan. The Journal of Clinical Psychiatry, 75(9), 1001–1008. https://doi.org/10.4088/JCP.13m08914.
Anderson, A., & Cohen, M. S. 7 (2013) 'Decreased small-world functional network connectivity and clustering across resting state networks in schizophrenia: an fMRI classification tutorial.' Front Hum Neurosci. Frontiers, p. 520. Available at: https://doi.org/10.3389/fnhum.2013.00520/abstract.
Arseneault, L., Cannon, M., Fisher, H. L., Polanczyk, G., Moffitt, T. E., & Caspi, A. (2011). Childhood trauma and children's emerging psychotic symptoms: a genetically sensitive longitudinal cohort study. The American Journal of Psychiatry, 168(1), 65–72. https://doi.org/10.1176/appi.ajp.2010.10040567.
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(2), 196–203. https://doi.org/10.1007/s11682-012-9215-y.
Baker, S. T., Lubman, D. I., Yucel, M., Allen, N. B., Whittle, S., Fulcher, B. D., et al. (2015). Developmental changes in brain network hub connectivity in late adolescence. The Journal of Neuroscience, 35(24), 9078–9087. https://doi.org/10.1523/JNEUROSCI.5043-14.2015.
Bassett, D. S., & Bullmore, E. 12 (2006) 'Small-world brain networks' Neuroscientist. Dec 01. SAGE Publications, pp. 512–523 6. Available at: http://nro.sagepub.com.ezp-prod1.hul.harvard.edu/content/12/6/512.abstract.
Bebbington, P., Jonas, S., Kuipers, E., King, M., Cooper, C., Brugha, T., et al. 199 (2011) 'Childhood sexual abuse and psychosis: data from a cross-sectional national psychiatric survey in England.' Br J Psychiatry. Jul. The Royal College of Psychiatrists, pp. 29–37 1. Available at: https://doi.org/10.1192/bjp.bp.110.083642.
Bendall, S., Jackson, H. J., Hulbert, C. A., & McGorry, P. D. 34 (2008) 'Childhood trauma and psychotic disorders: a systematic, critical review of the evidence.' Schizophr Bull. May. Oxford University Press, pp. 568–579 3. Available at: http://schizophreniabulletin.oxfordjournals.org/cgi/doi/10.1093/schbul/sbm121.
Berntsen, D., Johannessen, K. B., Thomsen, Y. D., Bertelsen, M., Hoyle, R. H., & Rubin, D. C. (2012). Peace and war: trajectories of posttraumatic stress disorder symptoms before, during, and after military deployment in Afghanistan. Psychological Science, 23(12), 1557–1565. https://doi.org/10.1177/0956797612457389.
Bierer, L. M., Yehuda, R., Schmeidler, J., Mitropoulou, V., New, A. S., Silverman, J. M., et al. 8 (2003) 'Abuse and neglect in childhood: relationship to personality disorder diagnoses.' CNS Spectrums. Oct. pp. 737–754 10. Available at: http://eutils.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&id=14712172&retmode=ref&cmd=prlinks, DOI: https://doi.org/10.1017/S1092852900019118.
Boecker, R., Holz, N. E., Buchmann, A. F., Blomeyer, D., Plichta, M. M., Wolf, I., et al. (2014). Impact of early life adversity on reward processing in young adults: EEG-fMRI results from a prospective study over 25 years. PLoS One, 9(8), e104185. https://doi.org/10.1371/journal.pone.0104185 PONE-D-14-12503 [pii].
Bonanno, G. A. (2012). Uses and abuses of the resilience construct: loss, trauma, and health-related adversities. Social Science & Medicine, 74(5), 753–756. https://doi.org/10.1016/j.socscimed.2011.11.022.
Bonanno, G. A., & Diminich, E. D. (2013). Annual Research Review: positive adjustment to adversity--trajectories of minimal-impact resilience and emergent resilience. Journal of Child Psychology and Psychiatry, 54(4), 378–401. https://doi.org/10.1111/jcpp.12021.
Bonanno, G. A., Wortman, C. B., & Nesse, R. M. (2004). Prospective patterns of resilience and maladjustment during widowhood. Psychology and Aging, 19(2), 260–271. https://doi.org/10.1037/0882-7974.19.2.260.
Bonanno, G. A., Kennedy, P., Galatzer-Levy, I. R., Lude, P., & Elfstrom, M. L. (2012a). Trajectories of resilience, depression, and anxiety following spinal cord injury. Rehabilitation Psychology, 57(3), 236–247. https://doi.org/10.1037/a0029256.
Bonanno, G. A., Mancini, A. D., Horton, J. L., Powell, T. M., Leardmann, C. A., Boyko, E. J., et al. (2012b). Trajectories of trauma symptoms and resilience in deployed U.S. military service members: prospective cohort study. The British Journal of Psychiatry, 200(4), 317–323. https://doi.org/10.1192/bjp.bp.111.096552.
Bonanno, G. A., Romero, S. A., & Klein, S. I. (2015). The temporal elements of psychological resilience: an integrative framework for the study of individuals, families, and communities. Psychological Inquiry, 26(2). https://doi.org/10.1080/1047840X.2015.992677.
Brambilla, P., Soloff, P. H., Sala, M., Nicoletti, M. A., Keshavan, M. S., & Soares, J. C. (2004). Anatomical MRI study of borderline personality disorder patients. Psychiatry Research, 131(2), 125–133. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=15313519. https://doi.org/10.1016/j.pscychresns.2004.04.003.
Breiman, L. (2001). Random forests. Machine Learning, 45, 5–32. https://doi.org/10.1023/A:1010933404324.
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(1), 23–32. https://doi.org/10.1016/S0006-3223(96)00162-X.
Bremner, J. D., Vythilingam, M., Vermetten, E., Southwick, S. M., McGlashan, T., Staib, L. H., et al. (2003). Neural correlates of declarative memory for emotionally valenced words in women with posttraumatic stress disorder related to early childhood sexual abuse. Biological Psychiatry, 53(10), 879–889. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=12742675. https://doi.org/10.1016/S0006-3223(02)01891-7.
Bullmore, E., & Sporns, O. 10 (2009) 'Complex brain networks: graph theoretical analysis of structural and functional systems.' Nat. Rev. Neurosci. Mar 01. Nature Publishing Group, pp. 186–198 3. Available at: https://doi.org/10.1038/nrn2575.
Bullmore, E., Barnes, A., Bassett, D. S., Fornito, A., Kitzbichler, M., Meunier, D., et al. 47 (2009) 'Generic aspects of complexity in brain imaging data and other biological systems.' Neuroimage. Sep. pp. 1125-1134 3. Available at: http://linkinghub.elsevier.com/retrieve/pii/S1053811909005242.
Burton, C. L., Galatzer-Levy, I. R., & Bonanno, G. A. (2015). Treatment type and demographic characteristics as predictors for cancer adjustment: prospective trajectories of depressive symptoms in a population sample. Health Psychology, 34(6), 602–609. https://doi.org/10.1037/hea0000145.
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. The World Journal of Biological Psychiatry, 13(8), 569–578. https://doi.org/10.3109/15622975.2012.661079.
Carrion, V. G., Weems, C. F., & Reiss, A. L. (2007). Stress predicts brain changes in children: a pilot longitudinal study on youth stress, posttraumatic stress disorder, and the hippocampus. Pediatrics, 119(3), 509–516. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=17332204. https://doi.org/10.1542/peds.2006-2028.
Chaney, A., Carballedo, A., Amico, F., Fagan, A., Skokauskas, N., Meaney, J., et al. (2014). Effect of childhood maltreatment on brain structure in adult patients with major depressive disorder and healthy participants. Journal of Psychiatry & Neuroscience, 39(1), 50–59. https://doi.org/10.1503/jpn.120208.
Choi, J., Jeong, B., Rohan, M. L., Polcari, A. M., & Teicher, M. H. (2009). Preliminary evidence for white matter tract abnormalities in young adults exposed to parental verbal abuse. Biological Psychiatry, 65(3), 227–234. doi:S0006-3223(08)00792-0 [pii]. https://doi.org/10.1016/j.biopsych.2008.06.022.
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(10), 975–982. doi:S0006-3223(06)00140-5 [pii]. https://doi.org/10.1016/j.biopsych.2005.12.016.
Cressman, V. L., Balaban, J., Steinfeld, S., Shemyakin, A., Graham, P., Parisot, N., et al. (2010). Prefrontal cortical inputs to the basal amygdala undergo pruning during late adolescence in the rat. The Journal of Comparative Neurology, 518(14), 2693–2709. https://doi.org/10.1002/cne.22359.
Cutajar, M. C., Mullen, P. E., Ogloff, J. R. P., Thomas, S. D., Wells, D. L., & Spataro, J. 34 (2010) 'Psychopathology in a large cohort of sexually abused children followed up to 43 years.' Child Abuse Negl. Nov. pp. 813-822 11. Available at: http://linkinghub.elsevier.com/retrieve/pii/S0145213410002267, DOI: https://doi.org/10.1016/j.chiabu.2010.04.004.
Daly, M. 199 (2011) 'Childhood psychotic symptoms: link between non-consensual sex and later psychosis.' Br J Psychiatry. Sep. The Royal College of Psychiatrists, pp. 251–2- author reply 252 3. Available at: https://doi.org/10.1192/bjp.199.3.251a.
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(4), 286–293. https://doi.org/10.1016/j.biopsych.2011.10.021.
Dannlowski, U., Kugel, H., Huber, F., Stuhrmann, A., Redlich, R., Grotegerd, D., et al. (2013). Childhood maltreatment is associated with an automatic negative emotion processing bias in the amygdala. Human Brain Mapping, 34(11), 2899–2909. https://doi.org/10.1002/hbm.22112.
De Bellis, M. D., Keshavan, M. S., Clark, D. B., Casey, B. J., Giedd, J. N., Boring, A. M., et al. (1999). Developmental traumatology. Part II: Brain development. Biological Psychiatry, 45(10), 1271–1284. https://doi.org/10.1016/S0006-3223(99)00045-1.
De Bellis, M. D., Keshavan, M. S., Spencer, S., & Hall, J. (2000). N-Acetylaspartate concentration in the anterior cingulate of maltreated children and adolescents with PTSD. The American Journal of Psychiatry, 157(7), 1175–1177. http://www.ncbi.nlm.nih.gov/cgi-bin/Entrez/referer?http://ajp.psychiatryonline.org/cgi/content/abstract/157/7/1175. https://doi.org/10.1176/appi.ajp.157.7.1175.
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(11), 1066–1078. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=12460690. https://doi.org/10.1016/S0006-3223(02)01459-2.
Deshields, T., Tibbs, T., Fan, M. Y., & Taylor, M. (2006). Differences in patterns of depression after treatment for breast cancer. Psychooncology, 15(5), 398–406. https://doi.org/10.1002/pon.962.
Dillon, D. G., Holmes, A. J., Birk, J. L., Brooks, N., Lyons-Ruth, K., & Pizzagalli, D. A. (2009). Childhood adversity is associated with left basal ganglia dysfunction during reward anticipation in adulthood. Biological Psychiatry, 66(3), 206–213. doi:S0006-3223(09)00232-7 [pii]. https://doi.org/10.1016/j.biopsych.2009.02.019.
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(12), 1115–1122. https://doi.org/10.1001/archpsyc.57.12.1115.
Dube, S. R., Anda, R. F., Felitti, V. J., Chapman, D. P., Williamson, D. F., & Giles, W. H. 286 (2001) 'Childhood abuse, household dysfunction, and the risk of attempted suicide throughout the life span: findings from the Adverse Childhood Experiences Study.' JAMA. Dec 26. pp. 3089–3096 24. Available at: http://eutils.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&id=11754674&retmode=ref&cmd=prlinks, DOI: https://doi.org/10.1001/jama.286.24.3089.
Dube, S. R., Felitti, V. J., Dong, M., Chapman, D. P., Giles, W. H., & Anda, R. F. 111 (2003) 'Childhood abuse, neglect, and household dysfunction and the risk of illicit drug use: the adverse childhood experiences study.' Pediatrics. Mar 01. American Academy of Pediatrics, pp. 564–572 3. Available at: http://pediatrics.aappublications.org/content/111/3/564.full, DOI: https://doi.org/10.1542/peds.111.3.564.
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 & Adolescent Medicine, 165(12), 1069. https://doi.org/10.1001/archpediatrics.2011.565.
Everaerd, D., Gerritsen, L., Rijpkema, M., Frodl, T., van Oostrom, I., Franke, B., et al. (2012). Sex modulates the interactive effect of the serotonin transporter gene polymorphism and childhood adversity on hippocampal volume. Neuropsychopharmacology, 37(8), 1848–1855. doi:npp201232 [pii]. https://doi.org/10.1038/npp.2012.32.
Fienberg, S. E. (2012). A brief history of statistical models for network analysis and open challenges. Journal of Computational and Graphical Statistics, 21(4), 825–839. https://doi.org/10.1080/10618600.2012.738106.
First, M. B., Spitzer, R. L., Gibbon, M., & Williams, J. B. W. (1997). Structured clinical interview for DSM-IV axis I disorders - clinician version (SCID-CV). Washington, DC: American Psychiatric Press.
Fisher, H. L., Jones, P. B., Fearon, P., Craig, T. K., Dazzan, P., Morgan, K., et al. 40 (2010) 'The varying impact of type, timing and frequency of exposure to childhood adversity on its association with adult psychotic disorder.' Psychological Medicine. Dec. Cambridge University Press, pp. 1967–1978 12. Available at: http://www.journals.cambridge.org/abstract_S0033291710000231, DOI: https://doi.org/10.1017/S0033291710000231.
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(13), 799–807. https://doi.org/10.1016/j.jpsychires.2010.01.006.
Frodl, T., Carballedo, A., Fagan, A. J., Lisiecka, D., Ferguson, Y., & Meaney, J. F. (2012). Effects of early-life adversity on white matter diffusivity changes in patients at risk for major depression. Journal of Psychiatry & Neuroscience, 37(1), 37–45. https://doi.org/10.1503/jpn.110028.
Gaudiano, B. A., & Zimmerman, M. 121 (2010) 'The relationship between childhood trauma history and the psychotic subtype of major depression.' Acta Psychiatrica Scandinavica. Jun. Blackwell Publishing Ltd, pp. 462–470 6. Available at: https://doi.org/10.1111/j.1600-0447.2009.01477.x.
Gerritsen, L., Tendolkar, I., Franke, B., Vasquez, A. A., Kooijman, S., Buitelaar, J., et al. (2012). BDNF Val66Met genotype modulates the effect of childhood adversity on subgenual anterior cingulate cortex volume in healthy subjects. Molecular Psychiatry, 17(6), 597–603. https://doi.org/10.1038/mp.2011.51.
Green, J. G., McLaughlin, K. A., Berglund, P. A., Gruber, M. J., Sampson, N. A., Zaslavsky, A. M., et al. 67 (2010) 'Childhood adversities and adult psychiatric disorders in the national comorbidity survey replication I: associations with first onset of DSM-IV disorders.' Arch. Gen. Psychiatry. Feb. American Medical Association, pp. 113–123 2. Available at: https://doi.org/10.1001/archgenpsychiatry.2009.186.
Hanson, J. L., Chung, M. K., Avants, B. B., Shirtcliff, E. A., Gee, J. C., Davidson, R. J., et al. (2010). Early stress is associated with alterations in the orbitofrontal cortex: a tensor-based morphometry investigation of brain structure and behavioral risk. The Journal of Neuroscience, 30(22), 7466–7472. https://doi.org/10.1523/JNEUROSCI.0859-10.2010.
Hanson, J. L., Hariri, A. R., & Williamson, D. E. (2015). Blunted ventral striatum development in adolescence reflects emotional neglect and predicts depressive symptoms. Biological Psychiatry, 78(9), 598–605. doi:S0006-3223(15)00431-X [pii]. https://doi.org/10.1016/j.biopsych.2015.05.010.
Hart, H., & Rubia, K. (2012). Neuroimaging of child abuse: a critical review. Frontiers in Human Neuroscience, 6, 52. https://doi.org/10.3389/fnhum.2012.00052.
Heim, C. M., Mayberg, H. S., Mletzko, T., Nemeroff, C. B., & Pruessner, J. C. (2013). Decreased cortical representation of genital somatosensory field after childhood sexual abuse. The American Journal of Psychiatry, 170(6), 616–623. doi:1694221 [pii]. https://doi.org/10.1176/appi.ajp.2013.12070950.
Helgeson, V. S., Snyder, P., & Seltman, H. (2004). Psychological and physical adjustment to breast cancer over 4 years: identifying distinct trajectories of change. Health Psychology, 23(1), 3–15. https://doi.org/10.1037/0278-6133.23.1.3.
Herman, J. L., Perry, J. C., & van der Kolk, B. A. 146 (1989) 'Childhood trauma in borderline personality disorder.' Am J Psychiatry. Apr. American Psychiatric Publishing, pp. 490–495 4. Available at: https://doi.org/10.1176/ajp.146.4.490.
Huang, H., Gundapuneedi, T., & Rao, U. (2012). White matter disruptions in adolescents exposed to childhood maltreatment and vulnerability to psychopathology. Neuropsychopharmacology, 37(12), 2693–2701. https://doi.org/10.1038/npp.2012.133.
Jackowski, A. P., Douglas-Palumberi, H., Jackowski, M., Win, L., Schultz, R. T., Staib, L. W., et al. (2008). Corpus callosum in maltreated children with posttraumatic stress disorder: a diffusion tensor imaging study. Psychiatry Research, 162(3), 256–261. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=18296031. https://doi.org/10.1016/j.pscychresns.2007.08.006.
Jackson, Y., Gabrielli, J., Fleming, K., Tunno, A. M., & Makanui, P. K. (2014). Untangling the relative contribution of maltreatment severity and frequency to type of behavioral outcome in foster youth. Child Abuse & Neglect, 38(7), 1147–1159. https://doi.org/10.1016/j.chiabu.2014.01.008.
Kellner, R. (1987). A symptom questionnaire. The Journal of Clinical Psychiatry, 48(7), 268–274 http://www.ncbi.nlm.nih.gov/pubmed/3597327.
Khan, A., McCormack, H. C., Bolger, E. A., McGreenery, C. E., Vitaliano, G., Polcari, A., et al. 6 (2015) 'Childhood maltreatment, depression, and suicidal ideation: critical importance of parental and peer emotional abuse during developmental sensitive periods in males and females.' 3rd ed Front Psychiatry. p. 42 10. Available at: https://doi.org/10.3389/fpsyt.2015.00042/abstract.
Lam, W. W., Shing, Y. T., Bonanno, G. A., Mancini, A. D., & Fielding, R. (2012). Distress trajectories at the first year diagnosis of breast cancer in relation to 6 years survivorship. Psychooncology, 21(1), 90–99. https://doi.org/10.1002/pon.1876.
Latora, V., & Marchiori, M. 87 (2001) 'Efficient behavior of small-world networks.' Phys. Rev. Lett. Nov 05. p. 198701 19. Available at: https://doi.org/10.1103/PhysRevLett.87.198701.
Liaw, A., & Wiener, M. (2002). Classification and regression by random forest. R News, 2(3), 18–22.
Lyons-Ruth, K., Bureau, J.-F., Holmes, B., Easterbrooks, A., & Brooks, N. H. 206 (2013) 'Borderline symptoms and suicidality/self-injury in late adolescence: prospectively observed relationship correlates in infancy and childhood.' Psychiatry Res. Apr 30. pp. 273–281 2–3. Available at: http://linkinghub.elsevier.com/retrieve/pii/S0165178112005318, DOI: https://doi.org/10.1016/j.psychres.2012.09.030.
Mehta, M. A., Gore-Langton, E., Golembo, N., Colvert, E., Williams, S. C., & Sonuga-Barke, E. (2010). Hyporesponsive reward anticipation in the basal ganglia following severe institutional deprivation early in life. Journal of Cognitive Neuroscience, 22(10), 2316–2325. https://doi.org/10.1162/jocn.2009.21394.
Nemeroff, C. B. (2016). Paradise lost: the neurobiological and clinical consequences of child abuse and neglect. Neuron, 89(5), 892–909. https://doi.org/10.1016/j.neuron.2016.01.019.
Ohashi, K., Anderson, C. M., Bolger, E. A., Khan, A., McGreenery, C. E., & Teicher, M. H. (2017a) 'Childhood maltreatment is associated with alteration in global network fiber-tract architecture independent of history of depression and anxiety.' Neuroimage. Feb. Available at: http://linkinghub.elsevier.com/retrieve/pii/S1053811917301489.
Ohashi, K., Anderson, C. M., Bolger, E. A., Khan, A., McGreenery, C. E., & Teicher, M. H. (2017b). Childhood maltreatment is associated with alteration in global network fiber-tract architecture independent of history of depression and anxiety. Neuroimage, 150, 50–59. https://doi.org/10.1016/j.neuroimage.2017.02.037.
Ohashi, K., Anderson, C. M., Bolger, E. A., Khan, A., McGreenery, C. E., & Teicher, M. H. (2019). Susceptibility or resilience to maltreatment can be explained by specific differences in brain network architecture. Biological Psychiatry, 85(8), 690–702. https://doi.org/10.1016/j.biopsych.2018.10.016.
Opel, N., Redlich, R., Zwanzger, P., Grotegerd, D., Arolt, V., Heindel, W., et al. (2014). Hippocampal atrophy in major depression: a function of childhood maltreatment rather than diagnosis? Neuropsychopharmacology, 39(12), 2723–2731. https://doi.org/10.1038/npp.2014.145.
Palacios-Barrios, E. E., & Hanson, J. L. (2019). Poverty and self-regulation: connecting psychosocial processes, neurobiology, and the risk for psychopathology. Comprehensive Psychiatry, 90, 52–64. https://doi.org/10.1016/j.comppsych.2018.12.012.
Paul, R., Henry, L., Grieve, S. M., Guilmette, T. J., Niaura, R., Bryant, R., et al. (2008). The relationship between early life stress and microstructural integrity of the corpus callosum in a non-clinical population. Neuropsychiatric Disease and Treatment, 4(1), 193–201. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=18728817. https://doi.org/10.2147/ndt.s1549.
Pechtel, P., Lyons-Ruth, K., Anderson, C. M., & Teicher, M. H. (2014). Sensitive periods of amygdala development: the role of maltreatment in preadolescence. Neuroimage, 97, 236–244. https://doi.org/10.1016/j.neuroimage.2014.04.025.
Philip, N. S., Sweet, L. H., Tyrka, A. R., Price, L. H., Carpenter, L. L., Kuras, Y. I., et al. (2013). Early life stress is associated with greater default network deactivation during working memory in healthy controls: a preliminary report. Brain Imaging and Behavior, 7(2), 204–212. https://doi.org/10.1007/s11682-012-9216-x.
Polcari, A., Rabi, K., Bolger, E., & Teicher, M. H. (2014). Parental verbal affection and verbal aggression in childhood differentially influence psychiatric symptoms and wellbeing in young adulthood. Child Abuse & Neglect, 38(1), 91–102. https://doi.org/10.1016/j.chiabu.2013.10.003.
Porter, B., Bonanno, G. A., Frasco, M. A., Dursa, E. K., & Boyko, E. J. (2017). Prospective post-traumatic stress disorder symptom trajectories in active duty and separated military personnel. Journal of Psychiatric Research, 89, 55–64. https://doi.org/10.1016/j.jpsychires.2017.01.016.
Rubinov, M., & Sporns, O. 52 (2010) 'Complex network measures of brain connectivity: uses and interpretations.' Neuroimage. Sep. pp. 1059–1069 3. Available at: http://linkinghub.elsevier.com/retrieve/pii/S105381190901074X, DOI: https://doi.org/10.1016/j.neuroimage.2009.10.003.
Samplin, E., Ikuta, T., Malhotra, A. K., Szeszko, P. R., & 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(9), 1174–1179. https://doi.org/10.1016/j.jpsychires.2013.05.008.
Schalinski, I., Teicher, M. H., Nischk, D., Hinderer, E., Muller, O., & Rockstroh, B. (2016). Type and timing of adverse childhood experiences differentially affect severity of PTSD, dissociative and depressive symptoms in adult inpatients. BMC Psychiatry, 16, 295. https://doi.org/10.1186/s12888-016-1004-5.
Schalinski, I., Breinlinger, S., Hirt, V., Teicher, M. H., Odenwald, M., & Rockstroh, B. (2017). Environmental adversities and psychotic symptoms: the impact of timing of trauma, abuse, and neglect. Schizophrenia Research. https://doi.org/10.1016/j.schres.2017.10.034.
Schalinski, I., Teicher, M. H., Carolus, A. M., & Rockstroh, B. (2018). Defining the impact of childhood adversities on cognitive deficits in psychosis: an exploratory analysis. Schizophrenia Research, 192, 351–356. https://doi.org/10.1016/j.schres.2017.05.014.
Schmahl, C. G., Vermetten, E., Elzinga, B. M., & Bremner, J. D. (2003). Magnetic resonance imaging of hippocampal and amygdala volume in women with childhood abuse and borderline personality disorder. Psychiatry Research: Neuroimaging, 122(3), 193–198. https://doi.org/10.1016/s0925-4927(03)00023-4.
Seckfort, D. L., Paul, R., Grieve, S. M., Vandenberg, B., Bryant, R. A., Williams, L. M., et al. (2008). Early life stress on brain structure and function across the lifespan: a preliminary study. Brain Imaging and Behavior, 2, 49–58. https://doi.org/10.1007/s11682-007-9015-y.
Sheu, Y. S., Polcari, A., Anderson, C. M., & Teicher, M. H. (2010). Harsh corporal punishment is associated with increased T2 relaxation time in dopamine-rich regions. Neuroimage, 53(2), 412–419. doi:S1053-8119(10)00887-6 [pii]. https://doi.org/10.1016/j.neuroimage.2010.06.043.
Shin, L. M., McNally, R. J., Kosslyn, S. M., Thompson, W. L., Rauch, S. L., Alpert, N. M., et al. (1999). Regional cerebral blood flow during script-driven imagery in childhood sexual abuse-related PTSD: a PET investigation. The American Journal of Psychiatry, 156(4), 575–584.
Shin, S. H., Miller, D. P., & Teicher, M. H. (2013). Exposure to childhood neglect and physical abuse and developmental trajectories of heavy episodic drinking from early adolescence into young adulthood. Drug and Alcohol Dependence, 127(1–3), 31–38. doi:S0376-8716(12)00222-0 [pii]. https://doi.org/10.1016/j.drugalcdep.2012.06.005.
Stam, C. J., & Reijneveld, J. C. 1 (2007) 'Graph theoretical analysis of complex networks in the brain.' Nonlinear Biomedical Physics. Jul 05. BioMed Central Ltd, p. 3 1. Available at: http://www.nonlinearbiomedphys.com/content/1/1/3, DOI: https://doi.org/10.1186/1753-4631-1-3.
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(4), 951–959. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=9234472. https://doi.org/10.1017/S0033291797005242.
Strobl, C., Boulesteix, A. L., Zeileis, A., & Hothorn, T. (2007). Bias in random forest variable importance measures: illustrations, sources and a solution. BMC Bioinformatics, 8, 25. doi:1471-2105-8-25 [pii]. https://doi.org/10.1186/1471-2105-8-25.
Teicher, M. H., & Parigger, A. 10 (2015) 'The ‘Maltreatment and Abuse Chronology of Exposure’ (MACE) scale for the retrospective assessment of abuse and neglect during development.' PLoS ONE. Public Library of Science, p. e0117423 2. Available at: https://doi.org/10.1371/journal.pone.0117423.
Teicher, M. H., & Samson, J. A. (2016). Annual Research Review: enduring neurobiological effects of childhood abuse and neglect. Journal of Child Psychology and Psychiatry, 57(3), 241–266. https://doi.org/10.1111/jcpp.12507.
Teicher, M. H., Ito, Y., Glod, C. A., Andersen, S. L., Dumont, N., & Ackerman, E. (1997). Preliminary evidence for abnormal cortical development in physically and sexually abused children using EEG coherence and MRI. Annals of the New York Academy of Sciences, 821, 160–175. https://doi.org/10.1111/j.1749-6632.1997.tb48277.x.
Teicher, M. H., Dumont, N. L., Ito, Y., Vaituzis, C., Giedd, J. N., & Andersen, S. L. (2004). Childhood neglect is associated with reduced corpus callosum area. Biological Psychiatry, 56(2), 80–85. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=15231439. https://doi.org/10.1016/j.biopsych.2004.03.016.
Teicher, M. H., Samson, J. A., Polcari, A., & McGreenery, C. E. (2006). Sticks, stones, and hurtful words: relative effects of various forms of childhood maltreatment. The American Journal of Psychiatry, 163(6), 993–1000. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=16741199. https://doi.org/10.1176/ajp.2006.163.6.993.
Teicher, M. H., Samson, J. A., Polcari, A., & Andersen, S. L. (2009). Length of time between onset of childhood sexual abuse and emergence of depression in a young adult sample: a retrospective clinical report. The Journal of Clinical Psychiatry, 70(5), 684–691. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=19358787. https://doi.org/10.4088/JCP.08m04235.
Teicher, M. H., Samson, J. A., Sheu, Y. S., Polcari, A., & McGreenery, C. E. (2010). Hurtful words: association of exposure to peer verbal abuse with elevated psychiatric symptom scores and corpus callosum abnormalities. The American Journal of Psychiatry, 167(12), 1464–1471. https://doi.org/10.1176/appi.ajp.2010.10010030.
Teicher, M. H., Anderson, C. M., & Polcari, A. (2012a). Childhood maltreatment is associated with reduced volume in the hippocampal subfields CA3, dentate gyrus, and subiculum. Proceedings of the National Academy of Sciences of the United States of America, 109(9), E563–E572. doi:1115396109 [pii]. https://doi.org/10.1073/pnas.1115396109.
Teicher, M. H., Anderson, C. M., & Polcari, A. 109 (2012b) 'Childhood maltreatment is associated with reduced volume in the hippocampal subfields CA3, dentate gyrus, and subiculum.' Proc. Natl. Acad. Sci. U.S.A. Feb 28. pp. E563–72 9. Available at: https://doi.org/10.1073/pnas.1115396109.
Teicher, M. H., Anderson, C. M., Ohashi, K., & Polcari, A. (2014a). Childhood maltreatment: altered network centrality of cingulate, precuneus, temporal pole and insula. Biological Psychiatry, 76(4), 297–305. doi:S0006-3223(13)00857-3 [pii]. https://doi.org/10.1016/j.biopsych.2013.09.016.
Teicher, M. H., Anderson, C. M., Ohashi, K., & Polcari, A. 76 (2014b) 'Childhood maltreatment: altered network centrality of cingulate, precuneus, temporal pole and insula.' Biol. Psychiatry. Aug 15. pp. 297–305 4. Available at: http://linkinghub.elsevier.com/retrieve/pii/S0006322313008573. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4258110/pdf/nihms546881.pdf, DOI: https://doi.org/10.1016/j.biopsych.2013.09.016.
Teicher, M. H., Samson, J. A., Anderson, C. M., & Ohashi, K. (2016). The effects of childhood maltreatment on brain structure, function and connectivity. Nature Reviews. Neuroscience, 17(10), 652–666. https://doi.org/10.1038/nrn.2016.111.
Teicher, M. H., Anderson, C. M., Ohashi, K., Khan, A., McGreenery, C. E., Bolger, E. A., et al. (2018). Differential effects of childhood neglect and abuse during sensitive exposure periods on male and female hippocampus. Neuroimage, 169, 443–452. https://doi.org/10.1016/j.neuroimage.2017.12.055.
Tomoda, A., Navalta, C. P., Polcari, A., Sadato, N., & Teicher, M. H. (2009a). Childhood sexual abuse is associated with reduced gray matter volume in visual cortex of young women. Biological Psychiatry, 66(7), 642–648 http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=19560122.
Tomoda, A., Suzuki, H., Rabi, K., Sheu, Y. S., Polcari, A., & Teicher, M. H. (2009b). Reduced prefrontal cortical gray matter volume in young adults exposed to harsh corporal punishment. Neuroimage, 47(Suppl 2), T66–T71 http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=19285558.
Tomoda, A., Polcari, A., Anderson, C. M., & Teicher, M. H. (2012). Reduced visual cortex gray matter volume and thickness in young adults who witnessed domestic violence during childhood. PLoS One, 7(12), e52528. https://doi.org/10.1371/journal.pone.0052528 PONE-D-12-28954 [pii].
Tupler, L. A., & De Bellis, M. D. (2006). Segmented hippocampal volume in children and adolescents with posttraumatic stress disorder. Biological Psychiatry, 59(6), 523–529. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=16199014. https://doi.org/10.1016/j.biopsych.2005.08.007.
Ugwu, I. D., Amico, F., Carballedo, A., Fagan, A. J., & Frodl, T. (2014). Childhood adversity, depression, age and gender effects on white matter microstructure: a DTI study. Brain Structure & Function, 220, 1997–2009. https://doi.org/10.1007/s00429-014-0769-x.
Usher, J. A., & Neisser, U. (1993). Childhood amnesia and the beginnings of memory for four early life events. Journal of Experimental Psychology. General, 122(2), 155–165. https://www.ncbi.nlm.nih.gov/pubmed/8315398. https://doi.org/10.1037/0096-3445.122.2.155.
Van Dam, N. T., Rando, K., Potenza, M. N., Tuit, K., & Sinha, R. (2014). Childhood maltreatment, altered limbic neurobiology, and substance use relapse severity via trauma-specific reductions in limbic gray matter volume. JAMA Psychiatry, 71(8), 917–925. https://doi.org/10.1001/jamapsychiatry.2014.680.
van der Werff, S. J., Pannekoek, J. N., Veer, I. M., van Tol, M. J., Aleman, A., Veltman, D. J., et al. (2013). Resting-state functional connectivity in adults with childhood emotional maltreatment. Psychological Medicine, 43(9), 1825–1836. https://doi.org/10.1017/S0033291712002942.
van Harmelen, A. L., van Tol, M. J., van der Wee, N. J., Veltman, D. J., Aleman, A., Spinhoven, P., et al. (2010). Reduced medial prefrontal cortex volume in adults reporting childhood emotional maltreatment. Biological Psychiatry, 68(9), 832–838. https://doi.org/10.1016/j.biopsych.2010.06.011.
van Harmelen, A. L., van Tol, M. J., Demenescu, L. R., van der Wee, N. J., Veltman, D. J., Aleman, A., et al. (2013). Enhanced amygdala reactivity to emotional faces in adults reporting childhood emotional maltreatment. Social Cognitive and Affective Neuroscience, 8(4), 362–369. https://doi.org/10.1093/scan/nss007.
van Harmelen, A. L., van Tol, M. J., Dalgleish, T., van der Wee, N. J., Veltman, D. J., Aleman, A., et al. (2014). Hypoactive medial prefrontal cortex functioning in adults reporting childhood emotional maltreatment. Social Cognitive and Affective Neuroscience, 9(12), 2026–2033. https://doi.org/10.1093/scan/nsu008.
Vermetten, E., Schmahl, C., Lindner, S., Loewenstein, R. J., & Bremner, J. D. (2006). Hippocampal and amygdalar volumes in dissociative identity disorder. The American Journal of Psychiatry, 163(4), 630–636. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=16585437. https://doi.org/10.1176/ajp.2006.163.4.630.
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. The American Journal of Psychiatry, 159(12), 2072–2080. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=12450959. https://doi.org/10.1176/appi.ajp.159.12.2072.
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 & Neuroscience, 34(5), 383–388 http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=19721849.
Widom, C. S., Czaja, S. J., & Paris, J. 23 (2009) 'A prospective investigation of borderline personality disorder in abused and neglected children followed up into adulthood.' J. Pers. Disord. Oct. pp. 433-446 5. Available at: https://doi.org/10.1521/pedi.2009.23.5.433.
Zanarini, M. C., Williams, A. A., Lewis, R. E., Reich, R. B., Vera, S. C., Marino, M. F., et al. 154 (1997) 'Reported pathological childhood experiences associated with the development of borderline personality disorder.' Am J Psychiatry. Aug. American Psychiatric Publishing, pp. 1101–1106 8. Available at: https://doi.org/10.1176/ajp.154.8.1101.
Zhu, J., Lowen, S. B., Anderson, C. M., Ohashi, K., Khan, A., & Teicher, M. H. (2019). Association of prepubertal and postpubertal exposure to childhood maltreatment with adult amygdala function. JAMA Psychiatry, 76(8), 843–853. https://doi.org/10.1001/jamapsychiatry.2019.0931.
Funding
This work was supported by the National Institute of Mental Health Awards MH-091391 and MH-113077, National Institute of Drug Abuse Award DA-017846, and National Institute of Child Health and Human Development Award HD-079484 to MHT.
Author information
Authors and Affiliations
Contributions
Cynthia E. McGreenery and Elizabeth Bolger, MA, Developmental Biopsychiatry Research Program, McLean Hospital, Belmont, MA, assisted with recruitment and assessment of study participants; and Michael Rohan, PhD, and Gordana Vitaliano, MD, PhD, Brain Imaging Center, McLean Hospital, Belmont, MA, provided technical and clinical support.
Corresponding author
Ethics declarations
The Partners Healthcare institutional review board approved this study and all subjects provided informed consent.
Rights and permissions
About this article
Cite this article
Teicher, M.H., Ohashi, K. & Khan, A. Additional Insights into the Relationship Between Brain Network Architecture and Susceptibility and Resilience to the Psychiatric Sequelae of Childhood Maltreatment. ADV RES SCI 1, 49–64 (2020). https://doi.org/10.1007/s42844-020-00002-w
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42844-020-00002-w