Hostname: page-component-8448b6f56d-sxzjt Total loading time: 0 Render date: 2024-04-19T00:35:58.965Z Has data issue: false hasContentIssue false
  • English
  • Français

Lower structural integrity of the uncinate fasciculus is associated with a history of child maltreatment and future psychological vulnerability to stress

Published online by Cambridge University Press:  04 November 2015

Jamie L. Hanson ,
Annchen R. Knodt ,
Bartholomew D. Brigidi  and
Ahmad R. Hariri
Jamie L. Hanson*
Affiliation:
Duke University University of North Carolinaat Chapel Hill
Annchen R. Knodt
Affiliation:
Duke University
Bartholomew D. Brigidi
Affiliation:
Duke University
Ahmad R. Hariri
Affiliation:
Duke University
*
Address correspondence and reprint requests to: Jamie Hanson, Laboratory of NeuroGenetics, Duke University, 417 Chapel Drive, Duke West Campus, Sociology–Psychology Building, Room 07A, Durham, NC 27710; E-mail: jlh125@duke.edu.
Get access Rights & Permissions [Opens in a new window]

Abstract

The experience of child maltreatment is a significant risk factor for the development of later internalizing disorders such as depression and anxiety. This risk is particularly heightened after exposure to additional, more contemporaneous stress. While behavioral evidence exists for such “stress sensitization,” little is known about the mechanisms mediating such relationships, particularly within the brain. Here we report that the experience of child maltreatment independent of recent life stress, gender, and age is associated with reduced structural integrity of the uncinate fasciculus, a major white matter pathway between the amygdala and ventromedial prefrontal cortex, in young adults. We further demonstrate that individuals with lower uncinate fasciculus integrity at baseline who subsequently experience stressful life events report higher levels of internalizing symptomatology at follow-up. Our findings suggest a novel neurobiological mechanism linking child maltreatment with later internalizing symptoms, specifically altered structural connectivity within the brain's threat-detection and emotion-regulation circuitry.

Type
Regular Articles
Information
Development and Psychopathology , Volume 27 , Special Issue 4pt2: Multilevel Developmental Perspectives on Child Maltreatment , November 2015 , pp. 1611 - 1619
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

Amaral, D. G., & Price, J. L. (1984). Amygdalo-cortical projections in the monkey (Macaca fascicularis). Journal of Comparative Neurology, 230, 465–496.CrossRefGoogle ScholarPubMed
Barbas, H., & De Olmos, J. (1990). Projections from the amygdala to basoventral and mediodorsal prefrontal regions in the rhesus monkey. Journal of Comparative Neurology, 300, 549–571.CrossRefGoogle ScholarPubMed
Barnett, D., Manly, J. T., & Cicchetti, D. (1993). Defining child maltreatment: The interface between policy and research. In Cicchetti, D. & Toth, S. L. (Eds.), Child abuse, child development, and social policy (pp. 7–73). Norwood, NJ: Ablex.Google Scholar
Bernstein, D. P., Ahluvalia, T., Pogge, D., & Handelsman, L. (1997). Validity of the Childhood Trauma Questionnaire in an adolescent psychiatric population. Journal of the American Academy of Child & Adolescent Psychiatry, 36, 340–348.Google Scholar
Bishop, S. J. (2007). Neurocognitive mechanisms of anxiety: An integrative account. Trends in Cognitive Sciences, 11, 307–316.Google Scholar
Bogdan, R., Perlis, R. H., Fagerness, J., & Pizzagalli, D. A. (2010). The impact of mineralocorticoid receptor ISO/VAL genotype (rs5522) and stress on reward learning. Genes, Brain and Behavior, 9, 658–667.Google Scholar
Burke, K. C., Burke, J. D., Regier, D. A., & Rae, D. S. (1990). Age at onset of selected mental disorders in five community populations. Archives of General Psychiatry, 47, 511–518.Google Scholar
Chapman, D. P., Whitfield, C. L., Felitti, V. J., Dube, S. R., Edwards, V. J., & Anda, R. F. (2004). Adverse childhood experiences and the risk of depressive disorders in adulthood. Journal of Affective Disorders, 82, 217–225.Google Scholar
Choi, J., Jeong, B., Polcari, A., Rohan, M. L., & Teicher, M. H. (2012). Reduced fractional anisotropy in the visual limbic pathway of young adults witnessing domestic violence in childhood. NeuroImage, 59, 1071–1079.Google Scholar
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, 227–234.Google Scholar
Cicchetti, D., & Gunnar, M. R. (2008). Integrating biological measures into the design and evaluation of preventive interventions. Development and Psychopathology, 20, 737–743.CrossRefGoogle ScholarPubMed
Cicchetti, D., & Tucker, D. (1994). Development and self-regulatory structures of the mind. Development and Psychopathology, 6, 533–549.Google Scholar
Clark, L. A., & Watson, D. (1991). Tripartite model of anxiety and depression: Psychometric evidence and taxonomic implications. Journal of Abnormal Psychology, 100, 316–336.Google Scholar
Clements, K., & Turpin, G. (1996). The life events scale for students: Validation for use with British samples. Personality and Individual Differences, 20, 747–751.Google Scholar
Covault, J., Tennen, H., Armeli, S., Conner, T. S., Herman, A. I., Cillessen, A. H. N., et al. (2007). Interactive effects of the serotonin transporter 5-HTTLPR polymorphism and stressful life events on college student drinking and drug use. Biological Psychiatry, 61, 609–616.Google Scholar
Danese, A., Moffitt, T. E., Harrington, H., Milne, B. J., Polanczyk, G., Pariante, C. M., et al. (2009). Adverse childhood experiences and adult risk factors for age-related disease: Depression, inflammation, and clustering of metabolic risk markers. Archives of Pediatrics & Adolescent Medicine, 163, 1135–1143.Google Scholar
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.Google Scholar
Davidson, R. J., Putnam, K. M., & Larson, C. L. (2000). Dysfunction in the neural circuitry of emotion regulation—A possible prelude to violence. Science, 289, 591–594.Google Scholar
Davis, M., & Whalen, P. J. (2001). The amygdala: Vigilance and emotion. Molecular Psychiatry, 6, 13–34.Google Scholar
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.Google Scholar
Eluvathingal, T. J., Chugani, H. T., Behen, M. E., Juhász, C., Muzik, O., Maqbool, M., et al. (2006). Abnormal brain connectivity in children after early severe socioemotional deprivation: A diffusion tensor imaging study. Pediatrics, 117, 2093–2100.CrossRefGoogle ScholarPubMed
Espejo, E. P., Hammen, C. L., Connolly, N. P., Brennan, P. A., Najman, J. M., & Bor, W. (2007). Stress sensitization and adolescent depressive severity as a function of childhood adversity: A link to anxiety disorders. Journal of Abnormal Child Psychology, 35, 287–299.Google Scholar
Etkin, A., Prater, K. E., Hoeft, F., Menon, V., & Schatzberg, A. F. (2010). Failure of anterior cingulate activation and connectivity with the amygdala during implicit regulation of emotional processing in generalized anxiety disorder. American Journal of Psychiatry, 167, 545–554.CrossRefGoogle ScholarPubMed
Fink, L. A., Bernstein, D., Handelsman, L., Foote, J., & Lovejoy, M. (1995). Initial reliability and validity of the childhood trauma interview: A new multidimensional measure of childhood interpersonal trauma. American Journal of Psychiatry, 152, 1329–1335.Google ScholarPubMed
First, M. B., Spitzer, R. L., Gibbon, M., & Williams, J. (1996). Structured Clinical Interview for DSM-IV Axis I disorders: Research version, non-patient edition (pp. 1–2). New York: New York State Psychiatric Institute.Google Scholar
Ghashghaei, H. T., & Barbas, H. (2002). Pathways for emotion: Interactions of prefrontal and anterior temporal pathways in the amygdala of the rhesus monkey. Neuroscience, 115, 1261–1279.Google Scholar
Glaser, J.-P., van Os, J., Portegijs, P. J. M., & Myin-Germeys, I. (2006). Childhood trauma and emotional reactivity to daily life stress in adult frequent attenders of general practitioners. Journal of Psychosomatic Research, 61, 229–236.Google Scholar
Gooding, H. C., Milliren, C. E., Austin, S. B., Sheridan, M. A., & McLaughlin, K. A. (2015). Child abuse, resting blood pressure, and blood pressure reactivity to psychosocial stress. Journal of Pediatric Psychology. Advance online publication. doi:10.1093/jpepsy/jsv040 Google ScholarPubMed
Gorka, A. X., Hanson, J. L., Radtke, S. R., & Hariri, A. R. (2014). Reduced hippocampal and medial prefrontal gray matter mediate the association between reported childhood maltreatment and trait anxiety in adulthood and predict sensitivity to future life stress. Biology of Mood & Anxiety Disorders, 4, 12.Google Scholar
Govindan, R. M., Behen, M. E., Helder, E., Makki, M. I., & Chugani, H. T. (2010). Altered water diffusivity in cortical association tracts in children with early deprivation identified with tract-based spatial statistics (TBSS). Cerebral Cortex, 20, 561–569.Google Scholar
Green, J. G., McLaughlin, K. A., Berglund, P. A., Gruber, M. J., Sampson, N. A., Zaslavsky, A. M., et al. (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, 113–123.Google Scholar
Hammen, C. (2005). Stress and depression. Annual Review of Clinical Psychology, 1, 293–319.CrossRefGoogle ScholarPubMed
Hammen, C., Henry, R., & Daley, S. E. (2000). Depression and sensitization to stressors among young women as a function of childhood adversity. Journal of Consulting and Clinical Psychology, 68, 782–787.CrossRefGoogle ScholarPubMed
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. Journal of Neuroscience, 30, 7466–7472.CrossRefGoogle ScholarPubMed
Hanson, J. L., Nacewicz, B. M., Sutterer, M. J., Cayo, A. A., Schaefer, S. M., Rudolph, K. D., et al. (2015). Behavioral problems after early life stress: Contributions of the hippocampus and amygdala. Biological Psychiatry, 77, 314–323.Google Scholar
Hariri, A. R. (2009). The neurobiology of individual differences in complex behavioral traits. Annual Review of Neuroscience, 32, 225–247.CrossRefGoogle ScholarPubMed
Harkness, K. L., Bruce, A. E., & Lumley, M. N. (2006). The role of childhood abuse and neglect in the sensitization to stressful life events in adolescent depression. Journal of Abnormal Psychology, 115, 730–741.CrossRefGoogle ScholarPubMed
Heim, C., Newport, D. J., Mletzko, T., Miller, A. H., & Nemeroff, C. B. (2008). The link between childhood trauma and depression: Insights from HPA axis studies in humans. Psychoneuroendocrinology, 33, 693–710.CrossRefGoogle ScholarPubMed
Herringa, R. J., Birn, R. M., Ruttle, P. L., Burghy, C. A., Stodola, D. E., Davidson, R. J., et al. (2013). Childhood maltreatment is associated with altered fear circuitry and increased internalizing symptoms by late adolescence. Proceedings of the National Academy of Sciences, 110, 19119–19124.Google Scholar
Herts, K. L., McLaughlin, K. A., & Hatzenbuehler, M. L. (2012). Emotion dysregulation as a mechanism linking stress exposure to adolescent aggressive behavior. Journal of Abnormal Child Psychology, 40, 1111–1122.Google Scholar
Huang, H., Gundapuneedi, T., & Rao, U. (2012). White matter disruptions in adolescents exposed to childhood maltreatment and vulnerability to psychopathology. Neuropsychopharmacology, 37, 2693–2701.Google Scholar
Jahanshad, N., Kochunov, P. V., Sprooten, E., Mandl, R. C., Nichols, T. E., Almasy, L., et al. (2013). Multi-site genetic analysis of diffusion images and voxelwise heritability analysis: A pilot project of the ENIGMA-DTI working group. NeuroImage, 81, 455–469.Google Scholar
Kessler, R. C. (1997). The effects of stressful life events on depression. Annual Review of Psychology, 48, 191–214.Google Scholar
Kessler, R. C., Berglund, P., Demler, O., Jin, R., Merikangas, K. R., & Walters, E. E. (2005). Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication. Archives of General Psychiatry, 62, 593–602.Google Scholar
Kim, J., & Cicchetti, D. (2010). Longitudinal pathways linking child maltreatment, emotion regulation, peer relations, and psychopathology. Journal of Child Psychology and Psychiatry, 51, 706–716.CrossRefGoogle ScholarPubMed
Ledoux, J. E. (2000). Emotion circuits in the brain. Annual Review of Neuroscience, 23, 155–184.CrossRefGoogle ScholarPubMed
Leitzke, B. T., Hilt, L. M., & Pollak, S. D. (2015). Maltreated youth display a blunted blood pressure response to an acute interpersonal stressor. Journal of Clinical Child and Adolescent Psychology, 44, 305–313.Google Scholar
Manly, J. T., Kim, J. E., Rogosch, F. A., & Cicchetti, D. (2001). Dimensions of child maltreatment and children's adjustment: Contributions of developmental timing and subtype. Development and Psychopathology, 13, 759–782.Google Scholar
McCrory, E. J., & Viding, E. (2015). The theory of latent vulnerability: Reconceptualizing the link between childhood maltreatment and psychiatric disorder. Development and Psychopathology, 27, 493–505.Google Scholar
McGrath, C. L., Kelley, M. E., Holtzheimer, P. E., Dunlop, B. W., Craighead, W. E., Franco, A. R., et al. (2013). Toward a neuroimaging treatment selection biomarker for major depressive disorder. JAMA Psychiatry, 70, 821–829.Google Scholar
McLaughlin, K. A., Conron, K. J., Koenen, K. C., & Gilman, S. E. (2010). Childhood adversity, adult stressful life events, and risk of past-year psychiatric disorder: A test of the stress sensitization hypothesis in a population-based sample of adults. Psychological Medicine, 40, 1647–1658.Google Scholar
McLaughlin, K. A., Koenen, K. C., Hill, E. D., Petukhova, M., Sampson, N. A., Zaslavsky, A. M., et al. (2013). Trauma exposure and posttraumatic stress disorder in a national sample of adolescents. Journal of the American Academy of Child & Adolescent Psychiatry, 52, 815–830.Google Scholar
McLaughlin, K. A., Sheridan, M. A., Alves, S., & Mendes, W. B. (2014). Child maltreatment and autonomic nervous system reactivity: Identifying dysregulated stress reactivity patterns by using the biopsychosocial model of challenge and threat. Psychosomatic Medicine, 76, 538–546.CrossRefGoogle ScholarPubMed
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.Google Scholar
Monroe, S., & Reid, M. (2008). Gene-environment interactions in depression research. Psychological Science, 19, 947.Google Scholar
Morecraft, R. J., Geula, C., & Mesulam, M. M. (1992). Cytoarchitecture and neural afferents of orbitofrontal cortex in the brain of the monkey. Journal of Comparative Neurology, 323, 341–358.CrossRefGoogle ScholarPubMed
Mori, S., Wakana, S., Van Zijl, P. C., & Nagae-Poetscher, L. M. (2005). MRI atlas of human white matter. Amsterdam: Elsevier.Google Scholar
Paykel, E. S. (2003). Life events and affective disorders. Acta Psychiatrica Scandinavica, 108(Suppl.), 61–66.CrossRefGoogle Scholar
Petrides, M., & Pandya, D. N. (1988). Association fiber pathways to the frontal-cortex from the superior temporal region in the rhesus-monkey. Journal of Comparative Neurology, 273, 52–66.Google Scholar
Porrino, L. J., Crane, A. M., & Goldman-Rakic, P. S. (1981). Direct and indirect pathways from the amygdala to the frontal lobe in rhesus monkeys. Journal of Comparative Neurology, 198, 121–136.CrossRefGoogle Scholar
Quirk, G. J., & Beer, J. S. (2006). Prefrontal involvement in the regulation of emotion: Convergence of rat and human studies. Current Opinion in Neurobiology, 16, 723–727.CrossRefGoogle ScholarPubMed
R Core Team. (2014). R: A language and environment for statistical computing [Computer software]. Vienna: R Foundation for Statistical Computing.Google Scholar
Rutter, M. (1998). Developmental catch-up, and deficit, following adoption after severe global early privation. Journal of Child Psychology and Psychiatry and Allied Disciplines, 39, 465–476.Google Scholar
Scher, C. D., Stein, M. B., Asmundson, G. J., McCreary, D. R., & Forde, D. R. (2001). The Childhood Trauma Questionnaire in a community sample: Psychometric properties and normative data. Journal of Traumatic Stress, 14, 843–857.CrossRefGoogle Scholar
Shapero, B. G., Black, S. K., Liu, R. T., Klugman, J., Bender, R. E., Abramson, L. Y., et al. (2013). Stressful life events and depression symptoms: The effect of childhood emotional abuse on stress reactivity. Journal of Clinical Psychology, 70, 209–223.Google Scholar
Sheehan, D. V., Lecrubier, Y., Sheehan, K. H., Amorim, P., Janavs, J., Weiller, E., et al. (1998). The Mini-International Neuropsychiatric Interview (M.I.N.I.): The development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. Journal of Clinical Psychiatry, 59, 22–33; quiz, 34–57.Google Scholar
Smith, S. M., Jenkinson, M., Johansen-Berg, H., Rueckert, D., Nichols, T. E., Mackay, C. E., et al. (2006). Tract-based spatial statistics: Voxelwise analysis of multi-subject diffusion data. NeuroImage, 31, 1487–1505.Google Scholar
Swartz, J. R., Knodt, A. R., Radtke, S. R., & Hariri, A. R. (2015). A neural biomarker of psychological vulnerability to future life stress. Neuron, 85, 505–511.CrossRefGoogle ScholarPubMed
Tarullo, A. R., & Gunnar, M. R. (2006). Child maltreatment and the developing HPA axis. Hormones and Behavior, 50, 632–639.Google Scholar
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.Google Scholar
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, 190–204.Google Scholar
Tromp, D. P. M., Grupe, D. W., Oathes, D. J., McFarlin, D. R., Hernandez, P. J., Kral, T. R. A., et al. (2012). Reduced structural connectivity of a major frontolimbic pathway in generalized anxiety disorder. Archives of General Psychiatry, 69, 925–934.CrossRefGoogle Scholar
Walsh, W. A., Dawson, J., & Mattingly, M. J. (2010). How are we measuring resilience following childhood maltreatment? Is the research adequate and consistent? What is the impact on research, practice, and policy? Trauma, Violence & Abuse, 11, 27–41.Google Scholar
Wildeman, C., Emanuel, N., Leventhal, J. M., Putnam-Hornstein, E., Waldfogel, J., & Lee, H. (2014). The prevalence of confirmed maltreatment among US children, 2004 to 2011. JAMA Pediatrics, 168, 706–713.Google Scholar