Advertisement

Childhood Maltreatment and Pediatric PTSD: Abnormalities in Threat Neural Circuitry

Chapter
Part of the Child Maltreatment Solutions Network book series (CMSN)

Abstract

This chapter will detail my laboratory’s work highlighting the effects of childhood maltreatment and post-traumatic stress disorder (PTSD) on the brain’s processing of threat. This review will focus on functional brain abnormalities associated with childhood maltreatment and PTSD and give consideration to which of these changes may be adaptive or maladaptive in the context of a stressful childhood environment. This chapter will begin with a brief overview of the neural circuitry involved in threat processing and regulation, followed by a summary of functional brain MRI studies my lab has conducted across adult and youth samples. In this work, I propose a model in which childhood maltreatment is associated with heightened reactivity in brain regions responsible for the detection of threat, such as the amygdala, which may aid a child in staying safe in a dangerous environment. However, recruitment and connectivity of threat-detecting regions with prefrontal regulatory regions may play a key role in determining adaptive and maladaptive emotional outcomes following childhood maltreatment. Delineating adaptive and maladaptive neurodevelopment following maltreatment is crucial if we are to advance our prevention and intervention strategies for the many harmful emotional effects of maltreatment.

Keywords

Child maltreatment Pediatric PTSD Functional MRI Neurodevelopment Threat 

Notes

Acknowledgments

This work was supported by the American Academy of Child and Adolescent Psychiatry, the Brain and Behavior Research Foundation, the University of Wisconsin School of Medicine and Institute for Clinical and Translational Research, and the National Institute of Mental Health. I am grateful for these sources of support, and for all of the staff, trainees, and participating families who have made this work possible.

References

  1. Bernstein, D. P., Stein, J. A., Newcomb, M. D., Walker, E., Pogge, D., Ahluvalia, T., … Zule, W. (2003). Development and validation of a brief screening version of the Childhood Trauma Questionnaire. Child Abuse & Neglect, 27(2), 169–190.CrossRefGoogle Scholar
  2. Birn, R. M., Patriat, R., Phillips, M. L., Germain, A., & Herringa, R. J. (2014). Childhood maltreatment and combat posttraumatic stress differentially predict fear-related fronto-subcortical connectivity. Depression and Anxiety, 31(10), 880–892.  https://doi.org/10.1002/da.22291CrossRefPubMedPubMedCentralGoogle Scholar
  3. Cohen, J. A., & Mannarino, A. P. (2015). Trauma-focused cognitive behavior therapy for traumatized children and families. Child and Adolescent Psychiatric Clinics of North America, 24(3), 557–570.  https://doi.org/10.1016/j.chc.2015.02.005CrossRefPubMedPubMedCentralGoogle Scholar
  4. Crozier, J. C., Wang, L., Huettel, S. A., & De Bellis, M. D. (2014). Neural correlates of cognitive and affective processing in maltreated youth with posttraumatic stress symptoms: Does gender matter? Development and Psychopathology, 26(2), 491–513.  https://doi.org/10.1017/S095457941400008XCrossRefPubMedPubMedCentralGoogle Scholar
  5. Dannlowski, U., Kugel, H., Huber, F., Stuhrmann, A., Redlich, R., Grotegerd, D., … Suslow, T. (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.22112CrossRefPubMedGoogle Scholar
  6. Dannlowski, U., Stuhrmann, A., Beutelmann, V., Zwanzger, P., Lenzen, T., Grotegerd, D., … Kugel, H. (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.2011.10.021CrossRefPubMedGoogle Scholar
  7. Daskalakis, N. P., Bagot, R. C., Parker, K. J., Vinkers, C. H., & de Kloet, E. R. (2013). The three-hit concept of vulnerability and resilience: Toward understanding adaptation to early-life adversity outcome. Psychoneuroendocrinology, 38(9), 1858–1873.  https://doi.org/10.1016/j.psyneuen.2013.06.008CrossRefPubMedPubMedCentralGoogle Scholar
  8. Diehle, J., Opmeer, B. C., Boer, F., Mannarino, A. P., & Lindauer, R. J. L. (2014). Trauma-focused cognitive behavioral therapy or eye movement desensitization and reprocessing: What works in children with posttraumatic stress symptoms? A randomized controlled trial. European Child & Adolescent Psychiatry, 24(2), 227–236.  https://doi.org/10.1007/s00787-014-0572-5CrossRefGoogle Scholar
  9. DuMont, K. A., Widom, C. S., & Czaja, S. J. (2007). Predictors of resilience in abused and neglected children grown-up: The role of individual and neighborhood characteristics. Child Abuse & Neglect, 31(3), 255–274.  https://doi.org/10.1016/j.chiabu.2005.11.015CrossRefGoogle Scholar
  10. Finkelhor, D., Turner, H. A., Shattuck, A., & Hamby, S. L. (2013). Violence, crime, and abuse exposure in a national sample of children and youth: An update. JAMA Pediatrics, 167(7), 614–621.  https://doi.org/10.1001/jamapediatrics.2013.42CrossRefPubMedGoogle Scholar
  11. Fonzo, G. A., Huemer, J., & Etkin, A. (2016). History of childhood maltreatment augments dorsolateral prefrontal processing of emotional valence in PTSD. Journal of Psychiatric Research, 74, 45–54.  https://doi.org/10.1016/j.jpsychires.2015.12.015CrossRefPubMedGoogle Scholar
  12. Fox, M. D., & Raichle, M. E. (2007). Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nature Reviews Neuroscience, 8(9), 700–711.  https://doi.org/10.1038/nrn2201CrossRefPubMedGoogle Scholar
  13. Garrett, A. S., Carrion, V., Kletter, H., Karchemskiy, A., Weems, C. F., & Reiss, A. (2012). Brain activation to facial expressions in youth with PTSD symptoms. Depression and Anxiety, 29(5), 449–459.  https://doi.org/10.1002/da.21892CrossRefPubMedGoogle Scholar
  14. Gee, D. G., Gabard-Durnam, L. J., Flannery, J., Goff, B., Humphreys, K. L., Telzer, E. H., … Tottenham, N. (2013). Early developmental emergence of human amygdala-prefrontal connectivity after maternal deprivation. Proceedings of the National Academy of Sciences of the United States of America, 110(39), 15638–15643.  https://doi.org/10.1073/pnas.1307893110CrossRefPubMedPubMedCentralGoogle Scholar
  15. Gee, D. G., Humphreys, K. L., Flannery, J., Goff, B., Telzer, E. H., Shapiro, M., … Tottenham, N. (2013). A developmental shift from positive to negative connectivity in human amygdala-prefrontal circuitry. The Journal of Neuroscience, 33(10), 4584–4593.  https://doi.org/10.1523/JNEUROSCI.3446-12.2013CrossRefPubMedPubMedCentralGoogle Scholar
  16. Giedd, J. N., Lalonde, F. M., Celano, M. J., White, S. L., Wallace, G. L., Lee, N. R., & Lenroot, R. K. (2009). Anatomical brain magnetic resonance imaging of typically developing children and adolescents. Journal of the American Academy of Child and Adolescent Psychiatry, 48(5), 465–470.CrossRefGoogle Scholar
  17. Green, J. G., McLaughlin, K. A., Berglund, P. A., Gruber, M. J., Sampson, N. A., Zaslavsky, A. M., & Kessler, R. C. (2010). Childhood adversities and adult psychiatric disorders in the national comorbidity survey replication I: Associations with first onset of DSM-IV disorders. Archives of General Psychiatry, 67(2), 113–123.  https://doi.org/10.1001/archgenpsychiatry.2009.186CrossRefPubMedPubMedCentralGoogle Scholar
  18. Hartley, C. A., & Phelps, E. A. (2010). Changing fear: The neurocircuitry of emotion regulation. Neuropsychopharmacology, 35(1), 136–146.  https://doi.org/10.1038/npp.2009.121CrossRefPubMedGoogle Scholar
  19. Herringa, R. J., Birn, R. M., Ruttle, P. L., Burghy, C. A., Stodola, D. E., Davidson, R. J., & Essex, M. J. (2013). Childhood maltreatment is associated with altered fear circuitry and increased internalizing symptoms by late adolescence. Proceedings of the National Academy of Sciences of the United States of America, 110(47), 19119–19124.  https://doi.org/10.1073/pnas.1310766110CrossRefPubMedPubMedCentralGoogle Scholar
  20. Herringa, R. J., Burghy, C. A., Stodola, D. E., Fox, M. E., Davidson, R. J., & Essex, M. J. (2016). Enhanced prefrontal-amygdala connectivity following childhood adversity as a protective mechanism against internalizing in adolescence. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 1(4), 326–334.  https://doi.org/10.1016/j.bpsc.2016.03.003CrossRefGoogle Scholar
  21. Herringa, R. J., Phillips, M. L., Fournier, J. C., Kronhaus, D. M., & Germain, A. (2013). Childhood and adult trauma both correlate with dorsal anterior cingulate activation to threat in combat veterans. Psychological Medicine, 43(7), 1533–1542.  https://doi.org/10.1017/S0033291712002310CrossRefPubMedGoogle Scholar
  22. Hillis, S., Mercy, J., Saul, J., Gleckel, J., Abad, N., & Kress, H. (2016). THRIVES: Using the best evidence to prevent violence against children. Journal of Public Health Policy, 37(Suppl 1), 51–65.  https://doi.org/10.1057/s41271-016-0003-6CrossRefPubMedGoogle Scholar
  23. Kalisch, R., & Gerlicher, A. M. V. (2014). Making a mountain out of a molehill: On the role of the rostral dorsal anterior cingulate and dorsomedial prefrontal cortex in conscious threat appraisal, catastrophizing, and worrying. Neuroscience & Biobehavioral Reviews, 42, 1–8.  https://doi.org/10.1016/j.neubiorev.2014.02.002CrossRefGoogle Scholar
  24. Keding, T. J., & Herringa, R. J. (2016). Paradoxical prefrontal-amygdala recruitment to angry and happy expressions in pediatric posttraumatic stress disorder. Neuropsychopharmacology, 41(12), 2903–2912.  https://doi.org/10.1038/npp.2016.104CrossRefPubMedPubMedCentralGoogle Scholar
  25. Kim, M. J., Gee, D. G., Loucks, R. A., Davis, F. C., & Whalen, P. J. (2011). Anxiety dissociates dorsal and ventral medial prefrontal cortex functional connectivity with the amygdala at rest. Cerebral Cortex (New York, N.Y.: 1991), 21(7), 1667–1673.  https://doi.org/10.1093/cercor/bhq237CrossRefGoogle Scholar
  26. Kim, P., Evans, G. W., Angstadt, M., Ho, S. S., Sripada, C. S., Swain, J. E., … Phan, K. L. (2013). Effects of childhood poverty and chronic stress on emotion regulatory brain function in adulthood. Proceedings of the National Academy of Sciences of the United States of America, 110(46), 18442–18447.  https://doi.org/10.1073/pnas.1308240110CrossRefPubMedPubMedCentralGoogle Scholar
  27. Lee, H., Heller, A. S., van Reekum, C. M., Nelson, B., & Davidson, R. J. (2012). Amygdala-prefrontal coupling underlies individual differences in emotion regulation. NeuroImage, 62(3), 1575–1581.  https://doi.org/10.1016/j.neuroimage.2012.05.044CrossRefPubMedPubMedCentralGoogle Scholar
  28. Maheu, F. S., Dozier, M., Guyer, A. E., Mandell, D., Peloso, E., Poeth, K., … Ernst, M. (2010). A preliminary study of medial temporal lobe function in youths with a history of caregiver deprivation and emotional neglect. Cognitive, Affective & Behavioral Neuroscience, 10(1), 34–49.  https://doi.org/10.3758/CABN.10.1.34CrossRefGoogle Scholar
  29. Malter Cohen, M., Jing, D., Yang, R. R., Tottenham, N., Lee, F. S., & Casey, B. J. (2013). Early-life stress has persistent effects on amygdala function and development in mice and humans. Proceedings of the National Academy of Sciences of the United States of America, 110(45), 18274–18278.  https://doi.org/10.1073/pnas.1310163110CrossRefPubMedPubMedCentralGoogle Scholar
  30. Maren, S., Phan, K. L., & Liberzon, I. (2013). The contextual brain: Implications for fear conditioning, extinction and psychopathology. Nature Reviews. Neuroscience, 14(6), 417–428.  https://doi.org/10.1038/nrn3492CrossRefPubMedPubMedCentralGoogle Scholar
  31. McCrory, E. J., De Brito, S. A., Sebastian, C. L., Mechelli, A., Bird, G., Kelly, P. A., & Viding, E. (2011). Heightened neural reactivity to threat in child victims of family violence. Current Biology, 21(23), R947–R948.  https://doi.org/10.1016/j.cub.2011.10.015CrossRefPubMedGoogle Scholar
  32. McLaughlin, K. A., Peverill, M., Gold, A. L., Alves, S., & Sheridan, M. A. (2015). Child maltreatment and neural systems underlying emotion regulation. Journal of the American Academy of Child and Adolescent Psychiatry, 54(9), 753–762.  https://doi.org/10.1016/j.jaac.2015.06.010CrossRefPubMedPubMedCentralGoogle Scholar
  33. Milad, M. R., & Quirk, G. J. (2012). Fear extinction as a model for translational neuroscience: Ten years of progress. Annual Review of Psychology, 63, 129–151.  https://doi.org/10.1146/annurev.psych.121208.131631CrossRefPubMedPubMedCentralGoogle Scholar
  34. Phillips, M. L., Ladouceur, C. D., & Drevets, W. C. (2008). A neural model of voluntary and automatic emotion regulation: implications for understanding the pathophysiology and neurodevelopment of bipolar disorder. Molecular Psychiatry, 13(9), 829–857.CrossRefGoogle Scholar
  35. Prinz, R. J., Sanders, M. R., Shapiro, C. J., Whitaker, D. J., & Lutzker, J. R. (2009). Population-based prevention of child maltreatment: The U.S. triple P system population trial. Prevention Science, 10(1), 1–12.  https://doi.org/10.1007/s11121-009-0123-3CrossRefPubMedPubMedCentralGoogle Scholar
  36. Robinson, O. J., Charney, D. R., Overstreet, C., Vytal, K., & Grillon, C. (2012). The adaptive threat bias in anxiety: Amygdala-dorsomedial prefrontal cortex coupling and aversive amplification. NeuroImage, 60(1), 523–529.  https://doi.org/10.1016/j.neuroimage.2011.11.096CrossRefPubMedGoogle Scholar
  37. Shackman, A. J., Salomons, T. V., Slagter, H. A., Fox, A. S., Winter, J. J., & Davidson, R. J. (2011). The integration of negative affect, pain and cognitive control in the cingulate cortex. Nature Reviews. Neuroscience, 12(3), 154–167.  https://doi.org/10.1038/nrn2994CrossRefPubMedPubMedCentralGoogle Scholar
  38. Suzuki, H., Luby, J. L., Botteron, K. N., Dietrich, R., McAvoy, M. P., & Barch, D. M. (2014). Early life stress and trauma and enhanced limbic activation to emotionally valenced faces in depressed and healthy children. Journal of the American Academy of Child and Adolescent Psychiatry, 53(7), 800–813.e10.  https://doi.org/10.1016/j.jaac.2014.04.013CrossRefPubMedPubMedCentralGoogle Scholar
  39. Swartz, J. R., Williamson, D. E., & Hariri, A. R. (2015). Developmental change in amygdala reactivity during adolescence: Effects of family history of depression and stressful life events. The American Journal of Psychiatry, 172(3), 276–283.  https://doi.org/10.1176/appi.ajp.2014.14020195CrossRefPubMedGoogle Scholar
  40. Tottenham, N., Hare, T. A., Millner, A., Gilhooly, T., Zevin, J. D., & Casey, B. J. (2011). Elevated amygdala response to faces following early deprivation. Developmental Science, 14(2), 190–204.  https://doi.org/10.1111/j.1467-7687.2010.00971.xCrossRefPubMedPubMedCentralGoogle Scholar
  41. Uematsu, A., Matsui, M., Tanaka, C., Takahashi, T., Noguchi, K., Suzuki, M., & Nishijo, H. (2012). Developmental trajectories of amygdala and hippocampus from infancy to early adulthood in healthy individuals. PLoS One, 7(10), e46970.  https://doi.org/10.1371/journal.pone.0046970CrossRefPubMedPubMedCentralGoogle Scholar
  42. van Wingen, G. A., Geuze, E., Vermetten, E., & Fernandez, G. (2011). The neural consequences of combat stress: Long-term follow-up. Molecular Psychiatry, 17(2), 116–118.  https://doi.org/10.1038/mp.2011.110CrossRefPubMedGoogle Scholar
  43. Vink, M., Derks, J. M., Hoogendam, J. M., Hillegers, M., & Kahn, R. S. (2014). Functional differences in emotion processing during adolescence and early adulthood. NeuroImage, 91, 70–76.  https://doi.org/10.1016/j.neuroimage.2014.01.035CrossRefPubMedGoogle Scholar
  44. Wolf, R. C., & Herringa, R. J. (2016). Prefrontal-amygdala dysregulation to threat in pediatric posttraumatic stress disorder. Neuropsychopharmacology, 41(3), 822–831.  https://doi.org/10.1038/npp.2015.209CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of PsychiatryUniversity of Wisconsin School of Medicine and Public HealthMadisonUSA

Personalised recommendations