Abstract
The deleterious outcomes associated with exposure to childhood maltreatment (CM) are well known and may be at least partially mediated by self-harm behaviors. It has been suggested that these self-harm behaviors serve as a means of decreasing negative mood states but the effects of CM on health outcomes may be much more sinister. A wealth of data suggest that CM may lead to experience-dependent changes in neural circuits underlying reward processes; processes associated with many harmful behaviors. The present study examined the relationship between a history of CM and the microstructure of a white matter tract that may be central to reward processes. Healthy adults (N = 122) were assessed with a diffusion tensor imaging (DTI) exam and the Childhood Trauma Questionnaire (CTQ). Probabilistic tractography was used to delineate the accumbofrontal “reward” tract, connecting the orbitofrontal cortex and nucleus accumbens, and measures of white matter microstructure were extracted. We then examined whether variation in CTQ scores were associated with variation in the microstructure of this tract as measured by fractional anisotropy (FA). After accounting for the effects of age and sex, the CTQ total score accounted for approximately 6% of the variance of FA in the accumbofrontal tract (F(3, 121) = 5.74; p = .001). Post hoc analyses indicated that the overall severity of CM, rather than a specific type of maltreatment, drove this result. These findings indicate that CM influences white matter microstructure in a fiber tract that is likely central to reward processes and adds to a growing literature implicating CM in long-term health-related outcomes.
References
Anda, R. F., Felitti, V. J., Bremner, J. D., Walker, J. D., Whitfield, C., Perry, B. D., Dube, S. R., & Giles, W. H. (2006). The enduring effects of abuse and related adverse experiences in childhood. A convergence of evidence from neurobiology and epidemiology. European Archives of Psychiatry and Clinical Neuroscience, 256(3), 174–186.
Assaf, Y., & Pasternak, O. (2008). Diffusion tensor imaging (DTI)-based white matter map** in brain research: A review. Journal of Molecular Neuroscience, 34(1), 51–61.
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.
Behrens, T. E., Johansen-Berg, H., Woolrich, M., Smith, S., Wheeler-Kingshott, C., Boulby, P., Barker, G., Sillery, E., Sheehan, K., & Ciccarelli, O. (2003). Non-invasive map** of connections between human thalamus and cortex using diffusion imaging. Nature Neuroscience, 6(7), 750–757.
Bernstein, D. P., Stein, J. A., Newcomb, M. D., Walker, E., Pogge, D., Ahluvalia, T., Stokes, J., Handelsman, L., Medrano, M., & Desmond, D. (2003). Development and validation of a brief screening version of the childhood trauma questionnaire. Child Abuse & Neglect, 27(2), 169–190.
Birn, R.M., Roeber, B.J., Pollak, S.D. (2017). Early childhood stress exposure, reward pathways, and adult decision making. Proceedings of the National Academy of Sciences, 201708791.
Bjornebekk, A., Westlye, L. T., Fjell, A. M., Grydeland, H., & Walhovd, K. B. (2012). Social reward dependence and brain white matter microstructure. Cerebral cortex (New York, N.Y. : 1991), 22(11), 2672–2679.
Boecker, R., Holz, N. E., Buchmann, A. F., Blomeyer, D., Plichta, M. M., Wolf, I., Baumeister, S., Meyer-Lindenberg, A., Banaschewski, T., & Brandeis, D. (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.
Chaney, A., Carballedo, A., Amico, F., Fagan, A., Skokauskas, N., Meaney, J., & Frodl, T. (2014). Effect of childhood maltreatment on brain structure in adult patients with major depressive disorder and healthy participants. Journal of psychiatry & neuroscience : JPN, 39(1), 50–59.
Clark, L., Manes, F., Antoun, N., Sahakian, B. J., & Robbins, T. W. (2003). The contributions of lesion laterality and lesion volume to decision-making impairment following frontal lobe damage. Neuropsychologia, 41(11), 1474–1483.
Dannlowski, U., Stuhrmann, A., Beutelmann, V., Zwanzger, P., Lenzen, T., Grotegerd, D., Domschke, K., Hohoff, C., Ohrmann, P., Bauer, J., Lindner, C., Postert, C., Konrad, C., Arolt, V., Heindel, W., Suslow, T., & 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.
De Brito, S. A., Viding, E., Sebastian, C. L., Kelly, P. A., Mechelli, A., Maris, H., & McCrory, E. J. (2013). Reduced orbitofrontal and temporal grey matter in a community sample of maltreated children. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 54(1), 105–112.
Dembo, R., Williams, L., Wothke, W., Schmeidler, J., & Brown, C. H. (1992). The role of family factors, physical abuse, and sexual victimization experiences in high-risk youths' alcohol and other drug use and delinquency: A longitudinal model. Violence and Victims, 7(3), 245–266.
DeRosse, P., Ikuta, T., Peters, B. D., Karlsgodt, K. H., Szeszko, P. R., & Malhotra, A. K. (2014). Adding insult to injury: Childhood and adolescent risk factors for psychosis predict lower fractional anisotropy in the superior longitudinal fasciculus in healthy adults. Psychiatry Research, 224(3), 296–302.
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.
Douglas, K. R., Chan, G., Gelernter, J., Arias, A. J., Anton, R. F., Weiss, R. D., Brady, K., Poling, J., Farrer, L., & Kranzler, H. R. (2010). Adverse childhood events as risk factors for substance dependence: Partial mediation by mood and anxiety disorders. Addictive Behaviors, 35(1), 7–13.
Edmiston, E. E., Wang, F., Mazure, C. M., Guiney, J., Sinha, R., Mayes, L. C., & Blumberg, H. P. (2011). Corticostriatal-limbic gray matter morphology in adolescents with self-reported exposure to childhood maltreatment. Archives of Pediatrics & Adolescent Medicine, 165(12), 1069–1077.
Felitti, V. J., Anda, R. F., Nordenberg, D., Williamson, D. F., Spitz, A. M., Edwards, V., Koss, M. P., & Marks, J. S. (1998). Relationship of childhood abuse and household dysfunction to many of the leading causes of death in adults. The adverse childhood experiences (ACE) study. American Journal of Preventive Medicine, 14(4), 245–258.
First, M., Spitzer, R., Williams, J., & Gibbon, M. (1995). Structured clinical interview for DSM-IV-non-patient edition. New York: New York State Psychiatric Institute.
Galvan, A., Hare, T. A., Parra, C. E., Penn, J., Voss, H., Glover, G., & Casey, B. (2006). Earlier development of the accumbens relative to orbitofrontal cortex might underlie risk-taking behavior in adolescents. Journal of Neuroscience, 26(25), 6885–6892.
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.
Hanson, J. L., Chung, M. K., Avants, B. B., Shirtcliff, E. A., Gee, J. C., Davidson, R. J., & Pollak, S. D. (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(22), 7466–7472.
Hanson, J. L., Albert, D., Iselin, A.-M. R., Carre, J. M., Dodge, K. A., & Hariri, A. R. (2015a). Cumulative stress in childhood is associated with blunted reward-related brain activity in adulthood. Social Cognitive and Affective Neuroscience, 11(3), 405–412.
Hanson, J. L., Hariri, A. R., & Williamson, D. E. (2015b). Blunted ventral striatum development in adolescence reflects emotional neglect and predicts depressive symptoms. Biological Psychiatry, 78(9), 598–605.
Hanson, J. L., Knodt, A. R., Brigidi, B. D., & Hariri, A. R. (2015c). Lower structural integrity of the uncinate fasciculus is associated with a history of child maltreatment and future psychological vulnerability to stress. Development and Psychopathology, 27(4 Pt 2), 1611–1619.
Hollingshead, A.B., 1975. Four factor index of social status.
Huckins, J. F., Adeyemo, B., Miezin, F. M., Power, J. D., Gordon, E. M., Laumann, T. O., Heatherton, T. F., Petersen, S. E., & Kelley, W. M. (2019). Reward-related regions form a preferentially coupled system at rest. Human Brain Map**, 40(2), 361–376.
Hussey, J. M., Chang, J. J., & Kotch, J. B. (2006). Child maltreatment in the United States: Prevalence, risk factors, and adolescent health consequences. Pediatrics, 118(3), 933–942.
Jenkinson, M., & Smith, S. (2001). A global optimisation method for robust affine registration of brain images. Medical Image Analysis, 5(2), 143–156.
Karlsgodt, K. H., Bato, A. A., Blair, M. A., DeRosse, P., Szeszko, P. R., & Malhotra, A. K. (2015a). White matter microstructure in the executive network associated with aggression in healthy adolescents and young adults. Social Cognitive and Affective Neuroscience, 10(9), 1251–1256.
Karlsgodt, K. H., John, M., Ikuta, T., Rigoard, P., Peters, B. D., Derosse, P., Malhotra, A. K., & Szeszko, P. R. (2015b). The accumbofrontal tract: Diffusion tensor imaging characterization and developmental change from childhood to adulthood. Human Brain Map**, 36(12), 4954–4963.
Kelly, P. A., Viding, E., Wallace, G. L., Schaer, M., De Brito, S. A., Robustelli, B., & McCrory, E. J. (2013). Cortical thickness, surface area, and gyrification abnormalities in children exposed to maltreatment: Neural markers of vulnerability? Biological Psychiatry, 74(11), 845–852.
Kessler, R. C., McLaughlin, K. A., Green, J. G., Gruber, M. J., Sampson, N. A., Zaslavsky, A. M., Aguilar-Gaxiola, S., Alhamzawi, A. O., Alonso, J., & Angermeyer, M. (2010). Childhood adversities and adult psychopathology in the WHO world mental health surveys. The British Journal of Psychiatry, 197(5), 378–385.
Kring, A. M., & Barch, D. M. (2014). The motivation and pleasure dimension of negative symptoms: Neural substrates and behavioral outputs. European Neuropsychopharmacology, 24(5), 725–736.
Lim, L., Hart, H., Mehta, M., Worker, A., Simmons, A., Mirza, K., & Rubia, K. (2018). Grey matter volume and thickness abnormalities in young people with a history of childhood abuse. Psychological Medicine, 48(6), 1034–1046.
MacDonald, K., Thomas, M. L., Sciolla, A. F., Schneider, B., Pappas, K., Bleijenberg, G., Bohus, M., Bekh, B., Carpenter, L., Carr, A., Dannlowski, U., Dorahy, M., Fahlke, C., Finzi-Dottan, R., Karu, T., Gerdner, A., Glaesmer, H., Grabe, H. J., Heins, M., Kenny, D. T., Kim, D., Knoop, H., Lobbestael, J., Lochner, C., Lauritzen, G., Ravndal, E., Riggs, S., Sar, V., Schäfer, I., Schlosser, N., Schwandt, M. L., Stein, M. B., Subic-Wrana, C., Vogel, M., & Wingenfeld, K. (2016). Minimization of childhood maltreatment is common and consequential: Results from a large, multinational sample using the childhood trauma questionnaire. PLoS One, 11(1), e0146058–e0146058.
McLaughlin, K. A., Green, J., 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 ii: Associations with persistence of dsm-iv disorders. Archives of General Psychiatry, 67(2), 124–132.
McLaughlin, K. A., Green, J. G., Gruber, M. J., Sampson, N. A., Zaslavsky, A. M., & Kessler, R. C. (2012). Childhood adversities and first onset of psychiatric disorders in a national sample of US adolescents. Archives of General Psychiatry, 69(11), 1151–1160.
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.
Merrick, M. T., Ports, K. A., Ford, D. C., Afifi, T. O., Gershoff, E. T., & Grogan-Kaylor, A. (2017). Unpacking the impact of adverse childhood experiences on adult mental health. Child Abuse & Neglect, 69, 10–19.
Mori, S., & Zhang, J. (2006). Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron, 51(5), 527–539.
Peters, B. D., Szeszko, P. R., Radua, J., Ikuta, T., Gruner, P., DeRosse, P., Zhang, J. P., Giorgio, A., Qiu, D., Tapert, S. F., Brauer, J., Asato, M. R., Khong, P. L., James, A. C., Gallego, J. A., & Malhotra, A. K. (2012). White matter development in adolescence: Diffusion tensor imaging and meta-analytic results. Schizophrenia Bulletin, 38(6), 1308–1317.
Reuben, A., Moffitt, T. E., Caspi, A., Belsky, D. W., Harrington, H., Schroeder, F., Hogan, S., Ramrakha, S., Poulton, R., & Danese, A. (2016). Lest we forget: Comparing retrospective and prospective assessments of adverse childhood experiences in the prediction of adult health. Journal of Child Psychology and Psychiatry, 57(10), 1103–1112.
Samanez-Larkin, G. R., Levens, S. M., Perry, L. M., Dougherty, R. F., & Knutson, B. (2012). Frontostriatal white matter integrity mediates adult age differences in probabilistic reward learning. Journal of Neuroscience, 32(15), 5333–5337.
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.
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 & Neglect, 32(7), 682–692.
Stevens, J. S., van Rooij, S. J. H., & Jovanovic, T. (2018). Developmental contributors to trauma response: The importance of sensitive periods, early environment, and sex differences. Current Topics in Behavioral Neurosciences, 38, 1–22.
Takiguchi, S., Fujisawa, T. X., Mizushima, S., Saito, D. N., Okamoto, Y., Shimada, K., Koizumi, M., Kumazaki, H., Jung, M., Kosaka, H., Hiratani, M., Ohshima, Y., Teicher, M. H., & Tomoda, A. (2015). Ventral striatum dysfunction in children and adolescents with reactive attachment disorder: Functional MRI study. BJPsych open, 1(2), 121–128.
Teicher, M. H., & Parigger, A. (2015). The ‘maltreatment and abuse chronology of exposure’(MACE) scale for the retrospective assessment of abuse and neglect during development. PLoS One, 10(2), e0117423.
Teicher, M. H., Samson, J. A., Anderson, C. M., & Ohashi, K. (2016a). The effects of childhood maltreatment on brain structure, function and connectivity. Nature Reviews Neuroscience, 17(10), 652–666.
Teicher, M. H., Samson, J. A., Anderson, C. M., & Ohashi, K. (2016b). The effects of childhood maltreatment on brain structure, function and connectivity. Nature reviews. Neuroscience, 17(10), 652–666.
Thomaes, K., Dorrepaal, E., Draijer, N., de Ruiter, M. B., van Balkom, A. J., Smit, J. H., & Veltman, D. J. (2010). Reduced anterior cingulate and orbitofrontal volumes in child abuse-related complex PTSD. Journal of Clinical Psychiatry, 71(12), 1636–1644.
Whittle, S., Vijayakumar, N., Dennison, M., Schwartz, O., Simmons, J. G., Sheeber, L., & Allen, N. B. (2016). Observed measures of negative parenting predict brain development during adolescence. PLoS One, 11(1), e0147774.
WHO, T.I.S.f.P.o.A.N.a. (2006). Preventing child maltreatment: A guide to taking action and generating evidence. WHO Press, France.
Williams, L. M. (1994). Recall of childhood trauma: A prospective study of women's memories of child sexual abuse. Journal of Consulting and Clinical Psychology, 62(6), 1167–1176.
Zlotnick, C., Johnson, J., Kohn, R., Vicente, B., Rioseco, P., & Saldivia, S. (2008). Childhood trauma, trauma in adulthood, and psychiatric diagnoses: Results from a community sample. Comprehensive Psychiatry, 49(2), 163–169.
Acknowledgements
This work was supported in part by grants from the National Institute of Mental Health to Dr. DeRosse (MH086756) and Dr. Karlsgodt (MH101506) and the NSLIJ Research Institute General Clinical Research Center (M01 RR018535).
Funding
This study was funded by grants from the National Institute of Mental Health to Dr. DeRosse (MH086756) and Dr. Karlsgodt (MH101506) and the NSLIJ Research Institute General Clinical Research Center (M01 RR018535).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
Dr.’s DeRosse, Ikuta, Karlsgodt and Szeszko report no competing interests. Dr. Malhotra has served as consultant or speaker for Bristol-Myers Squibb, Astra Zeneca, Vanda Pharmaceuticals and Clinical Data, Inc., and has received research support from Pfizer, Janssen Pharmaceuticals, Bristol-Myers Squibb, and Eli Lilly.
Ethical approval
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
Informed consent
Informed consent was obtained from all individual participants included in the study.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
DeRosse, P., Ikuta, T., Karlsgodt, K.H. et al. History of childhood maltreatment is associated with reduced fractional anisotropy of the accumbofrontal ‘reward’ tract in healthy adults. Brain Imaging and Behavior 14, 353–361 (2020). https://doi.org/10.1007/s11682-020-00265-y
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11682-020-00265-y