Hostname: page-component-6bf8c574d5-qdpjg Total loading time: 0 Render date: 2025-02-16T16:17:46.811Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  11 December 2017

Sarah J. Heany ,
Nynke A. Groenewold ,
Anne Uhlmann ,
Shareefa Dalvie ,
Dan J. Stein  and
Samantha J. Brooks
Sarah J. Heany*
Affiliation:
University of Cape Town
Nynke A. Groenewold
Affiliation:
University of Cape Town
Anne Uhlmann
Affiliation:
University of Cape Town Stellenbosch University
Shareefa Dalvie
Affiliation:
University of Cape Town
Dan J. Stein
Affiliation:
University of Cape Town
Samantha J. Brooks
Affiliation:
University of Cape Town
*
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: [email protected].
Get access Rights & Permissions [Opens in a new window]

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.

Type
Regular Articles
Information
Development and Psychopathology , Volume 30 , Issue 4 , October 2018 , pp. 1475 - 1485
Copyright
Copyright © Cambridge University Press 2017 

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.)

Footnotes

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.

References

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, 14120–14125. doi:10.1073/pnas.0903183106Google Scholar
Arnsten, A. F. T. (2009). Stress signalling pathways that impair prefrontal cortex structure and function. Nature Reviews Neuroscience, 10, 410–422. doi:10.1038/nrn2648Google Scholar
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, 1038–1045. doi:10.1093/scan/nst078Google Scholar
Bale, T. L., & Epperson, C. N. (2015). Sex differences and stress across the lifespan. Nature Neuroscience, 18, 1413–1420. doi:10.1038/nn.4112Google Scholar
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, 497–499. doi:10.1016/j.jaac.2014.01.012Google Scholar
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, 327–343. doi:10.1017/S0033291715001981Google 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. doi:10.1097/00004583-199703000-00012Google Scholar
Bernstein, D. P., & Fink, L. (1998). Childhood Trauma Questionnaire: A retrospective self-report: Manual. San Antonio, TX: Psychological Corporation.Google Scholar
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, 169–190. doi:10.1016/S0145-2134(02)00541-0Google Scholar
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, 5116–5126. doi:10.1002/hbm.22537Google Scholar
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, 261–279.Google Scholar
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, 2981–2990. doi:10.1093/cercor/bht154Google Scholar
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, 23–45. doi:10.1016/j.pneurobio.2015.03.001Google Scholar
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.0009362Google Scholar
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, 2899–2909. doi:10.1002/hbm.22112Google Scholar
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, 286–293. doi:10.1016/j.biopsych.2011.10.021Google Scholar
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.2014.00112Google Scholar
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, 36–42. doi:10.1016/j.pscychresns.2012.11.009Google Scholar
Eickhoff, S. B., Bzdok, D., Laird, A. R., Kurth, F., & Fox, P. T. (2012). Activation likelihood estimation meta-analysis revisited. NeuroImage, 59, 2349–2361. doi:10.1016/j.neuroimage.2011.09.017Google Scholar
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, 820–831. doi:10.1111/adb.12162Google Scholar
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, 1476–1488. doi:10.1176/appi.ajp.2007.07030504Google Scholar
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, 93–103. doi:10.1016/j.pscychresns.2012.08.006Google Scholar
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, 10573–10581. doi:10.1523/jneurosci.5063-13.2014Google Scholar
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, 68–81. doi:10.1016/S0140-6736(08)61706-7Google Scholar
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, 1242–1247. doi:10.1038/nn958Google Scholar
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, 886–895. doi:10.1016/j.jpsychires.2010.12.004Google Scholar
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, 1828–1835. doi:10.1093/scan/nsu020Google Scholar
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, 69–79. doi:10.3758/s13415-014-0316-5Google Scholar
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, 301–308. doi:10.1016/j.biopsych.2010.09.034Google Scholar
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.2014.31Google Scholar
Hart, H., & Rubia, K. (2012). Neuroimaging of child abuse: A critical review. Frontiers in Human Neuroscience, 6, 52. doi:10.3389/fnhum.2012.00052Google Scholar
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, 168–174. doi:10.1097/TA.0b013e31824d67c3Google Scholar
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, 1533–1542. doi:10.1017/S0033291712002310Google Scholar
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.2014.00103Google Scholar
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, 1355–1368. doi:10.1007/s00429-014-0729-5Google Scholar
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, 202–208. doi:10.1016/j.pscychresns.2009.12.002Google Scholar
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, 3253–3260. doi:10.1523/jneurosci.5533-11.2012Google Scholar
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, 418–430. doi:10.1080/10538712.2014.896840Google Scholar
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, 376–381. doi:10.4314/ajpsy.v13i5.63103Google Scholar
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, 434–445. doi:10.1038/nrn2639Google Scholar
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, 1233–1239. doi:10.1016/S1053-8119(03)00169-1Google 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. doi:10.1017/S0954579415000115Google Scholar
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, 578–591. doi:10.1016/j.neubiorev.2014.10.012Google Scholar
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, 1045–1053. doi:10.1001/jamapsychiatry.2015.1376Google Scholar
Murray, C. J., & Lopez, A. D. (2013). Measuring the global burden of disease. New England Journal of Medicine, 369, 448–457. doi:10.1056/NEJMra1201534Google Scholar
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, 915–922. doi:10.1093/scan/nsw025Google Scholar
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, 6–16. doi:10.1177/1077559596001001002Google Scholar
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.2015.53Google Scholar
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, 157–163. doi:10.1016/j.biopsych.2012.03.014Google Scholar
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, 483–487. doi:10.1016/j.jpsychores.2010.01.020Google Scholar
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, 52–73. doi:10.1037/0033-2909.129.1.52Google Scholar
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, 512–526. doi:10.1080/17470919.2015.1087426Google Scholar
Sander, D., Grafman, J., & Zalla, T. (2003). The human amygdala: An evolved system for relevance detection. Reviews in the Neurosciences, 14, 303–316. doi:10.1515/revneuro.2003.14.4.303Google Scholar
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, 167–180. doi:10.1016/j.chiabu.2003.09.012Google Scholar
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, 843–857. doi:10.1023/A:1013058625719Google Scholar
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, 9–34. doi:10.1016/j.neubiorev.2014.01.009Google Scholar
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, 513–520. doi:10.3109/15622975.2015.1048723Google Scholar
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, 88–97. doi:10.1093/scan/nss105Google 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. doi:10.1016/j.neuron.2014.12.055Google Scholar
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.2015.170Google Scholar
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, 935–946. doi:10.1016/j.neubiorev.2009.12.004Google Scholar
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, 1774–1785. doi:10.1016/j.neubiorev.2013.07.008Google Scholar
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.0085107Google Scholar
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, 332–339. doi:10.1016/S0002-9343(99)00235-1Google Scholar
Wegman, H. L., & Stetler, C. (2009). A meta-analytic review of the effects of childhood abuse on medical outcomes in adulthood. Psychosomatic Medicine, 71, 805–812. doi:10.1097/PSY.0b013e3181bb2b46Google Scholar
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, 804–814. doi:10.1016/j.neuroimage.2009.05.009Google Scholar
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, 233–242. doi:10.1016/j.biopsycho.2011.08.007Google Scholar
Supplementary material: File

Heany et al supplementary material

Figure S1

Download Heany et al supplementary material(File)
File 37.9 KB