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Alterations in neural circuits underlying emotion regulation following child maltreatment: a mechanism underlying trauma-related psychopathology

Published online by Cambridge University Press:  07 April 2020

Jessica L. Jenness Open the ORCID record for Jessica L. Jenness [Opens in a new window] ,
Matthew Peverill Open the ORCID record for Matthew Peverill [Opens in a new window] ,
Adam Bryant Miller Open the ORCID record for Adam Bryant Miller [Opens in a new window] ,
Charlotte Heleniak Open the ORCID record for Charlotte Heleniak [Opens in a new window] ,
Madeline M. Robertson Open the ORCID record for Madeline M. Robertson [Opens in a new window] ,
Kelly A. Sambrook Open the ORCID record for Kelly A. Sambrook [Opens in a new window] ,
Margaret A. Sheridan Open the ORCID record for Margaret A. Sheridan [Opens in a new window]  and
Katie A. McLaughlin Open the ORCID record for Katie A. McLaughlin [Opens in a new window]
Jessica L. Jenness*
Affiliation:
Department of Psychiatry and Behavioral Sciences, University of Washington, Seattle, WA, USA
Matthew Peverill
Affiliation:
Department of Psychology, University of Washington, Seattle, WA, USA
Adam Bryant Miller
Affiliation:
Department of Psychology and Neuroscience, University of North Carolina, Chapel Hill, NC, USA
Charlotte Heleniak
Affiliation:
Department of Psychology, Columbia University, New York, NY, USA
Madeline M. Robertson
Affiliation:
Department of Psychology and Neuroscience, University of North Carolina, Chapel Hill, NC, USA
Kelly A. Sambrook
Affiliation:
Department of Radiology, University of Washington, Seattle, WA, USA
Margaret A. Sheridan
Affiliation:
Department of Psychology and Neuroscience, University of North Carolina, Chapel Hill, NC, USA
Katie A. McLaughlin
Affiliation:
Department of Psychology, Harvard University, Boston, MA, USA
*
Author for correspondence: Jessica Jenness, E-mail: [email protected]
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Abstract

Background

Disruptions in neural circuits underlying emotion regulation (ER) may be a mechanism linking child maltreatment with psychopathology. We examined the associations of maltreatment with neural responses during passive viewing of negative emotional stimuli and attempts to modulate emotional responses. We investigated whether the influence of maltreatment on neural activation during ER differed across development and whether alterations in brain function mediated the association between maltreatment and a latent general psychopathology (‘p’) factor.

Methods

Youth aged 8–16 years with (n = 79) and without (n = 72) exposure to maltreatment completed an ER task assessing neural responses during passive viewing of negative and neutral images and effortful attempts to regulate emotional responses to negative stimuli. P-factor scores were defined by a bi-factor model encompassing internalizing and externalizing psychopathology.

Results

Maltreated youth had greater activation in left amygdala and salience processing regions and reduced activation in multiple regions involved in cognitive control (bilateral superior frontal gyrus, middle frontal gyrus, and dorsal anterior cingulate cortex) when viewing negative v. neutral images than youth without maltreatment exposure. Reduced neural recruitment in cognitive control regions mediated the association of maltreatment with p-factor in whole-brain analysis. Maltreated youth exhibited increasing recruitment with age in ventrolateral prefrontal cortex during reappraisal while control participants exhibited decreasing recruitment with age. Findings were similar after adjusting for co-occurring neglect.

Conclusions

Child maltreatment influences the development of regions associated with salience processing and cognitive control during ER in ways that contribute to psychopathology.

Keywords

Child maltreatmentcognitive control networkemotion regulationfMRIP-factorsalience network
Type
Original Article
Information
Psychological Medicine , Volume 51 , Issue 11 , August 2021 , pp. 1880 - 1889
Copyright
© The Author(s) 2020. Published by Cambridge University Press

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References

Askren, M. K., McAllister-Day, T. K., Koh, N., Mestre, Z., Dines, J. N., Korman, B. A., … Madhyastha, T. M. (2016). Using Make for reproducible and parallel neuroimaging workflow and quality-assurance. Frontiers in Neuroinformatics, 10, 2.CrossRefGoogle ScholarPubMed
Ball, T. M., Ramsawh, H. J., Campbell-Sills, L., Paulus, M. P., & Stein, M. B. (2013). Prefrontal dysfunction during emotion regulation in generalized anxiety and panic disorders. Psychological Medicine, 43, 1475–1486.CrossRefGoogle ScholarPubMed
Beauregard, M., Paquette, V., & Lévesque, J. (2006). Dysfunction in the neural circuitry of emotional self-regulation in major depressive disorder. Neuroreport, 17, 843–846.CrossRefGoogle ScholarPubMed
Behzadi, Y., Restom, K., Liau, J., & Liu, T. T. (2007). A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. NeuroImage, 37, 90–101.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Bifulco, A., Brown, G. W., & Harris, T. O. (1994). Childhood Experience of Care and Abuse (CECA): A retrospective interview measure. Journal of Child Psychology and Psychiatry, 35, 1419–1435.CrossRefGoogle ScholarPubMed
Caspi, A., Houts, R. M., Belsky, D. W., Goldman-Mellor, S. J., Harrington, H., Israel, S., … Moffitt, T. E. (2014). The p factor one general psychopathology factor in the structure of psychiatric disorders? Clinical Psychological Science, 2, 119–137.CrossRefGoogle Scholar
Dillon, D. G., & Pizzagalli, D. A. (2013). Evidence of successful modulation of brain activation and subjective experience during reappraisal of negative emotion in unmedicated depression. Psychiatry Research: Neuroimaging, 212, 99–107.CrossRefGoogle ScholarPubMed
Eisenberg, N., Fabes, R. A., & Murphy, B. C. (1996). Parents’ reactions to children's negative emotions: Relations to children's social competence and comforting behavior. Child Development, 67, 2227–2247.CrossRefGoogle ScholarPubMed
Eklund, A., Nichols, T. E., & Knutsson, H. (2016). Cluster failure: Why fMRI inferences for spatial extent have inflated false-positive rates. Proceedings of the National Academy of Sciences, 113, 7900–7905.CrossRefGoogle ScholarPubMed
Finkelhor, D., Hamby, S. L., Ormrod, R., & Turner, H. (2005). The Juvenile Victimization Questionnaire: Reliability, validity, and national norms. Child Abuse & Neglect, 29, 383–412.CrossRefGoogle ScholarPubMed
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, 614–621.CrossRefGoogle Scholar
Goodkind, M., Eickhoff, S. B., Oathes, D. J., Jiang, Y., Chang, A., Jones-Hagata, L. B., … Etkin, A. (2015). Identification of a common neurobiological substrate for mental illness. JAMA Psychiatry, 72, 305–315.CrossRefGoogle ScholarPubMed
Heleniak, C., Jenness, J. L., Vander Stoep, A., McCauley, E., & McLaughlin, K. A. (2016 a). Childhood maltreatment exposure and disruptions in emotion regulation: A transdiagnostic pathway to adolescent internalizing and externalizing psychopathology. Cognitive Therapy and Research, 40, 394–415.CrossRefGoogle ScholarPubMed
Heleniak, C., McLaughlin, K. A., Ormel, J., & Riese, H. (2016 b). Cardiovascular reactivity as a mechanism linking child trauma to adolescent psychopathology. Biological Psychology, 120, 108–119.CrossRefGoogle ScholarPubMed
Kelly, P. A., Viding, E., Puetz, V. B., Palmer, A. L., Mechelli, A., Pingault, J.-B., … McCrory, E. J. (2015). Sex differences in socioemotional functioning, attentional bias, and gray matter volume in maltreated children: A multilevel investigation. Development and Psychopathology, 27, 1591–1609.CrossRefGoogle ScholarPubMed
Lahey, B. B., Krueger, R. F., Rathouz, P. J., Waldman, I. D., & Zald, D. H. (2017). A hierarchical causal taxonomy of psychopathology across the life span. Psychological Bulletin, 143, 142.CrossRefGoogle ScholarPubMed
Lake, A. J., Finn, P. R., & James, T. W. (2017). Neural correlates of emotion reappraisal in individuals with externalizing psychopathology. Brain Imaging and Behavior, 11, 76–85.CrossRefGoogle ScholarPubMed
LeWinn, K. Z., Strigo, I. A., Connolly, C. G., Ho, T. C., Tymofiyeva, O., Sacchet, M. D., … Yang, T. T. (2018). An exploratory examination of reappraisal success in depressed adolescents: Preliminary evidence of functional differences in cognitive control brain regions. Journal of Affective Disorders, 240, 155–164.CrossRefGoogle ScholarPubMed
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, R947–R948.CrossRefGoogle ScholarPubMed
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, 1151–1160.CrossRefGoogle Scholar
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 & Adolescent Psychiatry, 54, 753–762.CrossRefGoogle ScholarPubMed
McLaughlin, K. A., & Sheridan, M. A. (2016). Beyond cumulative risk: A dimensional approach to childhood adversity. Current Directions in Psychological Science, 25, 239–245.CrossRefGoogle ScholarPubMed
McLaughlin, K. A., Sheridan, M. A., Alves, S., & Mendes, W. B. (2014 a). 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
McLaughlin, K. A., Sheridan, M. A., & Lambert, H. K. (2014 b). Childhood adversity and neural development: Deprivation and threat as distinct dimensions of early experience. Neuroscience & Biobehavioral Reviews, 47, 578–591.CrossRefGoogle ScholarPubMed
McRae, K., Gross, J. J., Weber, J., Robertson, E. R., Sokol-Hessner, P., Ray, R. D., … Ochsner, K. N. (2012). The development of emotion regulation: An fMRI study of cognitive reappraisal in children, adolescents and young adults. Social Cognitive and affective Neuroscience, 7, 11–22.CrossRefGoogle Scholar
Miller, A. B., McLaughlin, K. A., Busso, D. S., Brueck, S., Peverill, M., & Sheridan, M. A. (2018). Neural correlates of emotion regulation and adolescent suicidal ideation. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 3, 125–132.Google ScholarPubMed
Ochsner, K. N., Ray, R. D., Cooper, J. C., Robertson, E. R., Chopra, S., Gabrieli, J. D., & Gross, J. J. (2004). For better or for worse: Neural systems supporting the cognitive down-and up-regulation of negative emotion. Neuroimage, 23, 483–499.CrossRefGoogle ScholarPubMed
Perlman, G., Simmons, A. N., Wu, J., Hahn, K. S., Tapert, S. F., Max, J. E., … Yang, T. T. (2012). Amygdala response and functional connectivity during emotion regulation: A study of 14 depressed adolescents. Journal of Affective Disorders, 139, 75–84.CrossRefGoogle ScholarPubMed
Pine, D. S., Mogg, K., Bradley, B. P., Montgomery, L., Monk, C. S., McClure, E., … Kaufman, J. (2005). Attention bias to threat in maltreated children: Implications for vulnerability to stress-related psychopathology. American Journal of Psychiatry, 162, 291–296.CrossRefGoogle ScholarPubMed
Price, R. B., Siegle, G. J., Silk, J. S., Ladouceur, C. D., McFarland, A., Dahl, R. E., & Ryan, N. D. (2014). Looking under the hood of the dot-probe task: An fMRI study in anxious youth. Depression and Anxiety, 31, 178–187.CrossRefGoogle ScholarPubMed
Rodman, A. M., Jenness, J. L., Weissman, D. G., Pine, D. S., & McLaughlin, K. A. (2019). Neurobiological markers of resilience to depression following childhood maltreatment: The role of neural circuits supporting the cognitive control of emotion. Biological Psychiatry, 86(6), 464–473.CrossRefGoogle ScholarPubMed
Silvers, J. A., Insel, C., Powers, A., Franz, P., Helion, C., Martin, R., … Ochsner, K. N. (2017). The transition from childhood to adolescence is marked by a general decrease in amygdala reactivity and an affect-specific ventral-to-dorsal shift in medial prefrontal recruitment. Developmental Cognitive Neuroscience, 25, 128–137.CrossRefGoogle Scholar
Silvers, J. A., Insel, C., Powers, A., Franz, P., Helion, C., Martin, R. E., … Ochsner, K. N. (2016). vlPFC–vmPFC–amygdala interactions underlie age-related differences in cognitive regulation of emotion. Cerebral Cortex, 27, 3502–3514.Google Scholar
Silvers, J. A., McRae, K., Gabrieli, J. D., Gross, J. J., Remy, K. A., & Ochsner, K. N. (2012). Age-related differences in emotional reactivity, regulation, and rejection sensitivity in adolescence. Emotion (Washington, D.C.), 12, 1235.CrossRefGoogle ScholarPubMed
Spear, L. P. (2009). Heightened stress responsivity and emotional reactivity during pubertal maturation: Implications for psychopathology. Development and Psychopathology, 21, 87–97.CrossRefGoogle ScholarPubMed
Steinberg, A. M., Brymer, M. J., Kim, S., Briggs, E. C., Ippen, C. G., Ostrowski, S. A., … Pynoos, R. S. (2013). Psychometric properties of the UCLA PTSD reaction index: Part I. Journal of Traumatic Stress, 26, 1–9.CrossRefGoogle ScholarPubMed
Wager, T. D., Davidson, M. L., Hughes, B. L., Lindquist, M. A., & Ochsner, K. N. (2008). Prefrontal-subcortical pathways mediating successful emotion regulation. Neuron, 59, 1037–1050.CrossRefGoogle ScholarPubMed
Wager, T. D., Waugh, C. E., Lindquist, M., Noll, D. C., Fredrickson, B. L., & Taylor, S. F. (2009). Brain mediators of cardiovascular responses to social threat: Part I: Reciprocal dorsal and ventral sub-regions of the medial prefrontal cortex and heart-rate reactivity. Neuroimage, 47, 821–835.CrossRefGoogle ScholarPubMed
Walker, E. A., Unutzer, J., Rutter, C., Gelfand, A., Saunders, K., VonKorff, M., … Katon, W. (1999). Costs of health care use by women HMO members with a history of childhood abuse and neglect. Archives of General Psychiatry, 56, 609–613.CrossRefGoogle ScholarPubMed
Weissman, D. G., Bitran, D., Miller, A. B., Schaefer, J. D., Sheridan, M. A., & McLaughlin, K. A. (2019). Difficulties with emotion regulation as a transdiagnostic mechanism linking child maltreatment with the emergence of psychopathology. Development and Psychopathology, 31, 899–915.CrossRefGoogle ScholarPubMed
Yamamoto, D. J., Woo, C.-W., Wager, T. D., Regner, M. F., & Tanabe, J. (2015). Influence of dorsolateral prefrontal cortex and ventral striatum on risk avoidance in addiction: A mediation analysis. Drug and Alcohol Dependence, 149, 10–17.CrossRefGoogle ScholarPubMed
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