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The neural correlates of Childhood Trauma Questionnaire scores in adults: A meta-analysis and review of functional magnetic resonance imaging studies

  • Sarah J. Heany (a1), Nynke A. Groenewold (a1), Anne Uhlmann (a1) (a2), Shareefa Dalvie (a1), Dan J. Stein (a1) and Samantha J. Brooks (a1)...
Abstract

Childhood maltreatment, including abuse and neglect, may have sustained effects on the integrity and functioning of the brain, alter neurophysiological responsivity later in life, and predispose individuals toward psychiatric conditions involving socioaffective disturbances. This meta-analysis aims to quantify associations between self-reported childhood maltreatment and brain function in response to socioaffective cues in adults. Seventeen functional magnetic resonance imaging studies reporting on data from 848 individuals examined with the Childhood Trauma Questionnaire were included in a meta-analysis of whole-brain findings, or a review of region of interest findings. The spatial consistency of peak activations associated with maltreatment exposure was tested using activation likelihood estimation, using a threshold of p < .05 corrected for multiple comparisons. Adults exposed to childhood maltreatment showed significantly increased activation in the left superior frontal gyrus and left middle temporal gyrus, and decreased activation in the left superior parietal lobule and the left hippocampus. Although hyperresponsivity to socioaffective cues in the amygdala and ventral anterior cingulate cortex in correlation with maltreatment severity is a replicated finding in region of interest studies, null results are reported as well. The findings suggest that childhood maltreatment has sustained effects on brain function into adulthood, and highlight potential mechanisms for conveying vulnerability to development of psychopathology.

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Corresponding author
Address correspondence and reprint requests to: Sarah Heany, Department of Psychiatry and Mental Health, University of Cape Town, Groote Schuur Hospital, J2 Block, Anzio Road, Observatory, Cape Town, South Africa; E-mail: sarah.heany@uct.ac.za.
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The first two authors contributed equally to this article. Dan J. Stein is supported by the Medical Research Council of South Africa; Samantha J. Brooks and Nynke A. Groenewold were supported by the Claude Leon Foundation, South Africa; Samantha J. Brooks was also supported by NIH Grant NIDA R21 DA040492; Sarah J. Heany was supported by the National Research Foundation of South Africa and the Oppenheimer Memorial Trust; and Anne Uhlmann was supported by a Stellenbosch University Subcommittee C postdoctoral fellowship.

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Admon, R., Lubin, G., Stern, O., Rosenberg, K., Sela, L., Ben-Ami, H., & Hendler, T. (2009). Human vulnerability to stress depends on amygdala's predisposition and hippocampal plasticity. Proceedings of the National Academy of Sciences, 106, 1412014125. doi:10.1073/pnas.0903183106
Arnsten, A. F. T. (2009). Stress signalling pathways that impair prefrontal cortex structure and function. Nature Reviews Neuroscience, 10, 410422. doi:10.1038/nrn2648
Aust, S., Alkan Hartwig, E., Koelsch, S., Heekeren, H. R., Heuser, I., & Bajbouj, M. (2014). How emotional abilities modulate the influence of early life stress on hippocampal functioning. Social Cognitive and Affective Neuroscience, 9, 10381045. doi:10.1093/scan/nst078
Bale, T. L., & Epperson, C. N. (2015). Sex differences and stress across the lifespan. Nature Neuroscience, 18, 14131420. doi:10.1038/nn.4112
Barch, D. M. (2014). Risk for mood pathology: Neural and psychological markers of abnormal negative information processing. Journal of the American Academy of Child & Adolescent Psychiatry, 53, 497499. doi:10.1016/j.jaac.2014.01.012
Benjet, C., Bromet, E., Karam, E. G., Kessler, R. C., McLaughlin, K. A., Ruscio, A. M., … Koenen, K. C. (2016). The epidemiology of traumatic event exposure worldwide: Results from the World Mental Health Survey Consortium. Psychological Medicine, 46, 327343. doi:10.1017/S0033291715001981
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, 340348. doi:10.1097/00004583-199703000-00012
Bernstein, D. P., & Fink, L. (1998). Childhood Trauma Questionnaire: A retrospective self-report: Manual. San Antonio, TX: Psychological Corporation.
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 and Neglect, 27, 169190. doi:10.1016/S0145-2134(02)00541-0
Bos, P. A, Montoya, E. R., Terburg, D., & van Honk, J. (2014). Cortisol administration increases hippocampal activation to infant crying in males depending on childhood neglect. Human Brain Mapping, 35, 51165126. doi:10.1002/hbm.22537
Brooks, S. J., & Stein, D. J. (2015). Systematic review of the neural bases of psychotherapy for anxiety and related disorders. Dialogues in Clinical Neuroscience, 17, 261279.
Buhle, J. T., Silvers, J. A., Wager, T. D., Lopez, R., Onyemekwu, C., Kober, H., … Ochsner, K. N. (2014). Cognitive reappraisal of emotion: A meta-analysis of human neuroimaging studies. Cerebral Cortex, 24, 29812990. doi:10.1093/cercor/bht154
Clauss, J. A., Avery, S. N., & Blackford, J. U. (2015). The nature of individual differences in inhibited temperament and risk for psychiatric disease: A review and meta-analysis. Progress in Neurobiology, 127, 2345. doi:10.1016/j.pneurobio.2015.03.001
Croy, I., Schellong, J., Gerber, J., Joraschky, P., Iannilli, E., & Hummel, T. (2010). Women with a history of childhood maltreatment exhibit more activation in association areas following non-traumatic olfactory stimuli: A fMRI study. PLOS ONE, 5, e9362. doi:10.1371/journal.pone.0009362
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, 28992909. doi:10.1002/hbm.22112
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, 286293. doi:10.1016/j.biopsych.2011.10.021
DeBello, W. M., McBride, T. J., Nichols, G. S., Pannoni, K. E., Sanculi, D., & Totten, D. J. (2014). Input clustering and the microscale structure of local circuits. Frontiers in Neural Circuits, 8. doi:10.3389/fncir.2014.00112
Edmiston, E. K., & Blackford, J. U. (2013). Childhood maltreatment and response to novel face stimuli presented during functional magnetic resonance imaging in adults. Psychiatry Research: Neuroimaging, 212, 3642. doi:10.1016/j.pscychresns.2012.11.009
Eickhoff, S. B., Bzdok, D., Laird, A. R., Kurth, F., & Fox, P. T. (2012). Activation likelihood estimation meta-analysis revisited. NeuroImage, 59, 23492361. doi:10.1016/j.neuroimage.2011.09.017
Elton, A., Smitherman, S., Young, J., & Kilts, C. D. (2015). Effects of childhood maltreatment on the neural correlates of stress- and drug cue-induced cocaine craving. Addiction Biology, 20, 820831. doi:10.1111/adb.12162
Etkin, A., & Wager, T. D. (2007). Functional neuroimaging of anxiety: A meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. American Journal of Psychiatry, 164, 14761488. doi:10.1176/appi.ajp.2007.07030504
Fonzo, G. A, Flagan, T. M., Sullivan, S., Allard, C. B., Grimes, E. M., Simmons, A. N., … Stein, M. B. (2013). Neural functional and structural correlates of childhood maltreatment in women with intimate-partner violence-related posttraumatic stress disorder. Psychiatry Research: Neuroimaging, 211, 93103. doi:10.1016/j.pscychresns.2012.08.006
Freeman, J. B., Stolier, R. M., Ingbretsen, Z. A., & Hehman, E. A. (2014). Amygdala responsivity to high-level social information from unseen faces. Journal of Neuroscience, 34, 1057310581. doi:10.1523/jneurosci.5063-13.2014
Gilbert, R., Widom, C. S., Browne, K., Fergusson, D., Webb, E., & Janson, S. (2009). Burden and consequences of child maltreatment in high-income countries. Lancet, 373, 6881. doi:10.1016/S0140-6736(08)61706-7
Gilbertson, M. W., Shenton, M. E., Ciszewski, A., Kasai, K., Lasko, N. B., Orr, S. P., & Pitman, R. K. (2002). Smaller hippocampal volume predicts pathologic vulnerability to psychological trauma. Nature Neuroscience, 5, 12421247. doi:10.1038/nn958
Grant, M. M., Cannistraci, C., Hollon, S. D., Gore, J., & Shelton, R. (2011). Childhood trauma history differentiates amygdala response to sad faces within MDD. Journal of Psychiatric Research, 45, 886895. doi:10.1016/j.jpsychires.2010.12.004
Grimm, S., Pestke, K., Feeser, M., Aust, S., Weigand, A., Wang, J., … Bajbouj, M. (2014). Early life stress modulates oxytocin effects on limbic system during acute psychosocial stress. Social Cognitive and Affective Neuroscience, 9, 18281835. doi:10.1093/scan/nsu020
Groenewold, N. A., Roest, A. M., Renken, R. J., Opmeer, E. M., Veltman, D. J., van der Wee, N. J. A., … Harmer, C. J. (2015). Cognitive vulnerability and implicit emotional processing: Imbalance in frontolimbic brain areas? Cognitive, Affective & Behavioral Neuroscience, 15, 6979. doi:10.3758/s13415-014-0316-5
Hamani, C., Mayberg, H., Stone, S., Laxton, A., Haber, S., & Lozano, A. M. (2011). The subcallosal cingulate gyrus in the context of major depression. Biological Psychiatry, 69, 301308. doi:10.1016/j.biopsych.2010.09.034
Harrison, E. L., & Baune, B. T. (2014). Modulation of early stress-induced neurobiological changes: A review of behavioural and pharmacological interventions in animal models. Translational Psychiatry, 4, e390. doi:10.1038/tp.2014.31
Hart, H., & Rubia, K. (2012). Neuroimaging of child abuse: A critical review. Frontiers in Human Neuroscience, 6, 52. doi:10.3389/fnhum.2012.00052
Herbert, H. K., van As, A. B., Bachani, A. M., Mtambeka, P., Stevens, K. A., Millar, A. J. W., & Hyder, A. A. (2012). Patterns of pediatric injury in South Africa: An analysis of hospital data between 1997 and 2006. Journal of Trauma and Acute Care Surgery, 73, 168174. doi:10.1097/TA.0b013e31824d67c3
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, 15331542. doi:10.1017/S0033291712002310
Hoeijmakers, L., Lucassen, P. J., & Korosi, A. (2014). The interplay of early-life stress, nutrition, and immune activation programs adult hippocampal structure and function. Frontiers in Molecular Neuroscience, 7, 103. doi:10.3389/fnmol.2014.00103
Holz, N. E., Buchmann, A. F., Boecker, R., Blomeyer, D., Baumeister, S., Wolf, I., … Laucht, M. (2015). Role of FKBP5 in emotion processing: Results on amygdala activity, connectivity and volume. Brain Structure & Function, 220, 13551368. doi:10.1007/s00429-014-0729-5
Hsu, D. T., Langenecker, S. A., Kennedy, S. E., Zubieta, J. K., & Heitzeg, M. M. (2010). fMRI BOLD responses to negative stimuli in the prefrontal cortex are dependent on levels of recent negative life stress in major depressive disorder. Psychiatry Research: Neuroimaging, 183, 202208. doi:10.1016/j.pscychresns.2009.12.002
Hsu, D. T., Mickey, B. J., Langenecker, S. A., Heitzeg, M. M., Love, T. M., Wang, H., … Enoch, M. A. (2012). Variation in the corticotropin-releasing hormone receptor 1 (CRHR1) gene influences fMRI signal responses during emotional stimulus processing. Journal of Neuroscience, 32, 32533260. doi:10.1523/jneurosci.5533-11.2012
Karos, K., Niederstrasser, N., Abidi, L., Bernstein, D. P., & Bader, K. (2014). Factor structure, reliability, and known groups validity of the German version of the Childhood Trauma Questionnaire (Short-Form) in Swiss patients and nonpatients. Journal of Child Sexual Abuse, 23, 418430. doi:10.1080/10538712.2014.896840
Lochner, C., Seedat, S., Allgulander, C., Kidd, M., Stein, D., & Gerdner, A. (2010). Childhood trauma in adults with social anxiety disorder and panic disorder: A cross-national study. African Journal of Psychiatry, 13, 376381. doi:10.4314/ajpsy.v13i5.63103
Lupien, S. J., McEwen, B. S., Gunnar, M. R., & Heim, C. (2009). Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nature Reviews Neuroscience, 10, 434445. doi:10.1038/nrn2639
Maldjian, J. A., Laurienti, P. J., Burdette, J. B., & Kraft, R. A. (2003). An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. NeuroImage, 19, 12331239. doi:10.1016/S1053-8119(03)00169-1
McCrory, E. J., & Viding, E. (2015). The theory of latent vulnerability: Reconceptualizing the link between childhood maltreatment and psychiatric disorder. Development and Psychopathology, 27, 493505. doi:10.1017/S0954579415000115
McLaughlin, K. A., Sheridan, M. A., & Lambert, H. K. (2014). Childhood adversity and neural development: Deprivation and threat as distinct dimensions of early experience. Neuroscience & Biobehavioral Reviews, 47, 578591. doi:10.1016/j.neubiorev.2014.10.012
Miller, C. H., Hamilton, J. P., Sacchet, M. D., & Gotlib, I. H. (2015). Meta-analysis of functional neuroimaging of major depressive disorder in youth. JAMA Psychiatry, 2130, 10451053. doi:10.1001/jamapsychiatry.2015.1376
Murray, C. J., & Lopez, A. D. (2013). Measuring the global burden of disease. New England Journal of Medicine, 369, 448457. doi:10.1056/NEJMra1201534
Muscatell, K. A., Dedovic, K., Slavich, G. M., Jarcho, M. R., Breen, E. C., Bower, J. E., … Eisenberger, N. I. (2016). Neural mechanisms linking social status and inflammatory responses to social stress. Social Cognitive and Affective Neuroscience, 11, 915922. doi:10.1093/scan/nsw025
Neumann, D. A., Houskamp, B. M., Pollock, V. E., & Briere, J. (1996). The long-term sequelae of childhood sexual abuse in women: A meta-analytic review. Child Maltreatment, 1, 616. doi:10.1177/1077559596001001002
Nicol, K., Pope, M., Romaniuk, L., & Hall, J. (2015). Childhood trauma, midbrain activation and psychotic symptoms in borderline personality disorder. Translational Psychiatry, 5, e559. doi:10.1038/tp.2015.53
Nikolova, Y. S., Bogdan, R., Brigidi, B. D., & Hariri, A. R. (2012). Ventral striatum reactivity to reward and recent life stress interact to predict positive affect. Biological Psychiatry, 72, 157163. doi:10.1016/j.biopsych.2012.03.014
Noll-Hussong, M., Otti, A., Laeer, L., Wohlschlaeger, A., Zimmer, C., Lahmann, C., … Guendel, H. (2010). Aftermath of sexual abuse history on adult patients suffering from chronic functional pain syndromes: An fMRI pilot study. Journal of Psychosomatic Research, 68, 483487. doi:10.1016/j.jpsychores.2010.01.020
Ozer, E. J., Best, S. R., Lipsey, T. L., & Weiss, D. S. (2003). Predictors of posttraumatic stress disorder and symptoms in adults: A meta-analysis. Psychological Bulletin, 129, 5273. doi:10.1037/0033-2909.129.1.52
Sanchez, M. M., McCormack, K. M., & Howell, B. R. (2015). Social buffering of stress responses in nonhuman primates: Maternal regulation of the development of emotional regulatory brain circuits. Social Neuroscience, 10, 512526. doi:10.1080/17470919.2015.1087426
Sander, D., Grafman, J., & Zalla, T. (2003). The human amygdala: An evolved system for relevance detection. Reviews in the Neurosciences, 14, 303316. doi:10.1515/revneuro.2003.14.4.303
Scher, C. D., Forde, D. R., McQuaid, J. R., & Stein, M. B. (2004). Prevalence and demographic correlates of childhood maltreatment in an adult community sample. Child Abuse and Neglect, 28, 167180. doi:10.1016/j.chiabu.2003.09.012
Scher, C., Stein, M., Asmundson, G. G., McCreary, D., & Forde, D. (2001). The Childhood Trauma Questionnaire in a community sample: Psychometric properties and normative data. Journal of Traumatic Stress, 14, 843857. doi:10.1023/A:1013058625719
Schurz, M., Radua, J., Aichhorn, M., Richlan, F., & Perner, J. (2014). Fractionating theory of mind: A meta-analysis of functional brain imaging studies. Neuroscience & Biobehavioral Reviews, 42, 934. doi:10.1016/j.neubiorev.2014.01.009
Skokauskas, N., Carballedo, A., Fagan, A., & Frodl, T. (2015). The role of sexual abuse on functional neuroimaging markers associated with major depressive disorder. World Journal of Biological Psychiatry, 16, 513520. doi:10.3109/15622975.2015.1048723
Steuwe, C., Daniels, J. K., Frewen, P. A, Densmore, M., Pannasch, S., Beblo, T., … Lanius, R. A. (2014). Effect of direct eye contact in PTSD related to interpersonal trauma: An fMRI study of activation of an innate alarm system. Social Cognitive and Affective Neuroscience, 9, 8897. doi:10.1093/scan/nss105
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, 505511. doi:10.1016/j.neuron.2014.12.055
Tozzi, L., Carballedo, A., Wetterling, F., McCarthy, H., O'Keane, V., Gill, M., … Frodl, T. (2016). Single-nucleotide polymorphism of the FKBP5 gene and childhood maltreatment as predictors of structural changes in brain areas involved in emotional processing in depression. Neuropsychopharmacology, 41, 487. doi:10.1038/npp.2015.170
van der Meer, L., Costafreda, S., Aleman, A., & David, A. S. (2010). Self-reflection and the brain: A theoretical review and meta-analysis of neuroimaging studies with implications for schizophrenia. Neuroscience & Biobehavioral Reviews, 34, 935946. doi:10.1016/j.neubiorev.2009.12.004
van der Velde, J., Servaas, M. N., Goerlich, K. S., Bruggeman, R., Horton, P., Costafreda, S. G., & Aleman, A. (2013). Neural correlates of alexithymia: A meta-analysis of emotion processing studies. Neuroscience & Biobehavioral Reviews, 37, 17741785. doi:10.1016/j.neubiorev.2013.07.008
Van Harmelen, A.-L., Hauber, K., Gunther Moor, B., Spinhoven, P., Boon, A. E., Crone, E. A, & Elzinga, B. M. (2014). Childhood emotional maltreatment severity is associated with dorsal medial prefrontal cortex responsivity to social exclusion in young adults. PLOS ONE, 9, e85107. doi:10.1371/journal.pone.0085107
Walker, E. A., Gelfand, A., Katon, W. J., Koss, M. P., Von Korff, M., Bernstein, D., & Russo, J. (1999). Adult health status of women with histories of childhood abuse and neglect. American Journal of Medicine, 107, 332339. doi:10.1016/S0002-9343(99)00235-1
Wegman, H. L., & Stetler, C. (2009). A meta-analytic review of the effects of childhood abuse on medical outcomes in adulthood. Psychosomatic Medicine, 71, 805812. doi:10.1097/PSY.0b013e3181bb2b46
Williams, L. M., Gatt, J. M., Schofield, P. R., Olivieri, G., Peduto, A., & Gordon, E. (2009). “Negativity bias” in risk for depression and anxiety: Brain–body fear circuitry correlates, 5-HTT-LPR and early life stress. NeuroImage, 47, 804814. doi:10.1016/j.neuroimage.2009.05.009
Zhong, M., Wang, X., Xiao, J., Yi, J., Zhu, X., Liao, J., … Yao, S. (2011). Amygdala hyperactivation and prefrontal hypoactivation in subjects with cognitive vulnerability to depression. Biological Psychology, 88, 233242. doi:10.1016/j.biopsycho.2011.08.007
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