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Impact of childhood maltreatment and resilience on behavioral and neural patterns of inhibitory control during emotional distraction

Published online by Cambridge University Press:  08 April 2021

Lauren A. Demers*
Affiliation:
Institute of Child Development, University of Minnesota, Minneapolis, MN, USA
Ruskin H. Hunt
Affiliation:
Institute of Child Development, University of Minnesota, Minneapolis, MN, USA
Dante Cicchetti
Affiliation:
Institute of Child Development, University of Minnesota, Minneapolis, MN, USA Mt Hope Family Center, University of Rochester, Rochester, New York, USA
Julia E. Cohen-Gilbert
Affiliation:
McLean Hospital, Belmont, MA, USA
Fred A. Rogosch
Affiliation:
Mt Hope Family Center, University of Rochester, Rochester, New York, USA
Sheree L. Toth
Affiliation:
Mt Hope Family Center, University of Rochester, Rochester, New York, USA
Kathleen M. Thomas
Affiliation:
Institute of Child Development, University of Minnesota, Minneapolis, MN, USA
*
Author for Correspondence: Lauren A. Demers, Institute of Child Development, University of Minnesota, Minneapolis, MN, USA; E-mail: [email protected].

Abstract

Exposure to childhood maltreatment (CM) may disrupt typical development of neural systems underlying impulse control and emotion regulation. Yet resilient outcomes are observed in some individuals exposed to CM. Individual differences in adult functioning may result from variation in inhibitory control in the context of emotional distractions, underpinned by cognitive–affective brain circuits. Thirty-eight healthy adults with a history of substantiated CM and 34 nonmaltreated adults from the same longitudinal sample performed a Go/No-Go task in which task-relevant stimuli (letters) were presented at the center of task-irrelevant, negative, or neutral images, while undergoing functional magnetic resonance imaging. The comparison group, but not the maltreated group, made increased inhibitory control errors in the context of negative, but not neutral, distractor images. In addition, the comparison group had greater right inferior frontal gyrus and bilateral frontal pole activation during inhibitory control blocks with negative compared to neutral background images relative to the CM group. Across the full sample, greater adaptive functioning in everyday contexts was associated with superior inhibitory control and greater right frontal pole activation. Results suggest that resilience following early adversity is associated with enhanced attention and behavioral regulation in the context of task-irrelevant negative emotional stimuli in a laboratory setting.

Type
Regular Article
Copyright
© The Author(s), 2021. Published by Cambridge University Press

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References

Achenbach, T. M., & Rescorla, L. A. (2003). Manual for the ASEBA adult forms & profiles. Burlington, VT: University of Vermont. Research Center for Children, Youth, & Families.Google Scholar
Aldao, A., Nolen-Hoeksema, S., & Schweizer, S. (2010). Emotion-regulation strategies across psychopathology: A meta-analytic review. Clinical Psychology Review, 30, 217237. doi:10.1016/j.cpr.2009.11.004CrossRefGoogle ScholarPubMed
Andersen, S. L., Tomada, A., Vincow, E. S., Valente, E., Polcari, A., & Teicher, M. H. (2008). Preliminary evidence for sensitive periods in the effect of childhood sexual abuse on regional brain development. The Journal of Neuropsychiatry and Clinical Neurosciences, 20, 292301. doi:10.1176/jnp.2008.20.3.292CrossRefGoogle ScholarPubMed
Arnsten, A. F., & Rubia, K. (2012). Neurobiological circuits regulating attention, cognitive control, motivation, and emotion: Disruptions in neurodevelopmental psychiatric disorders. Journal of the American Academy of Child & Adolescent Psychiatry, 51, 356367. doi:10.1016/j.jaac.2012.01.008CrossRefGoogle ScholarPubMed
Aron, A. R., Robbins, T. W., & Poldrack, R. A. (2004). Inhibition and the right inferior frontal cortex. Trends in Cognitive Science, 8, 170177. doi:10.1016/j.tics.2004.02.010CrossRefGoogle ScholarPubMed
Bari, A., & Robbins, T. W. (2013). Inhibition and impulsivity: Behavioral and neural basis of response control. Progress in Neurobiology, 108, 4479. doi:10.1016/j.pneurobio.2013.06.005CrossRefGoogle ScholarPubMed
Barnett, D., Manly, J. T., Cicchetti, D., & Toth, S. L. (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. 774). Norwood, NJ: Ablex.Google Scholar
Belsky, J., Schlomer, G. L., & Ellis, B. J. (2012). Beyond cumulative risk: Distinguishing harshness and unpredictability as determinants of parenting and early life history strategy. Developmental Psychology, 48, 662673. doi:10.1037/a0024454CrossRefGoogle ScholarPubMed
Bremner, J. D., Vermetten, E., Vythilingam, M., Afzal, N., Schmahl, C., Elzinga, B., & Charney, D. S. (2004). Neural correlates of the classic color and emotional Stroop in women with abuse-related posttraumatic stress disorder. Biological Psychiatry, 55, 612620. doi:10.1016/j.biopsych.2003.10.001CrossRefGoogle ScholarPubMed
Caldwell, J. G., Krug, M. K., Carter, C. S., & Minzenberg, M. J. (2014). Cognitive control in the face of fear: Reduced cognitive-emotional flexibility in women with a history of child abuse. Journal of Aggression, Maltreatment & Trauma, 23, 454472. doi:10.1080/10926771.2014.904466CrossRefGoogle Scholar
Chester, D. S., Lynam, D. R., Milich, R., Powell, D. K., Andersen, A. H., & DeWall, C. N. (2016). How do negative emotions impair self-control? A neural model of negative urgency. NeuroImage, 132, 4350. doi:10.1016/j.neuroimage.2016.02.024CrossRefGoogle ScholarPubMed
Chikazoe, J., Konishi, S., Asari, T., Jimura, K., & Miyashita, Y. (2007). Activation of right inferior frontal gyrus during response inhibition across response modalities. Journal of Cognitive Neuroscience, 19, 6980. doi:10.1162/jocn.2007.19.1.69CrossRefGoogle ScholarPubMed
Cicchetti, D., & Lynch, M. (1993). Toward an ecological/transactional model of community violence and child maltreatment: Consequences for children's development. Psychiatry, 56, 96118. doi:10.1080/00332747.1993.11024624Google ScholarPubMed
Cicchetti, D., & Lynch, M. (1995). Failures in the expectable environment and their impact on individual development: The case of child maltreatment. In Cicchetti, D. & Cohen, D. J. (Eds.), Developmental psychopathology: Risk, disorder, and adaptation (Vol. 2, pp. 3271). New York: Wiley.Google Scholar
Cicchetti, D., Rogosch, F. A., Lynch, M., & Holt, K. D. (1993). Resilience in maltreated children: Processes leading to adaptive outcome. Development and Psychopathology, 5, 629647. doi:10.1017/S0954579400006209CrossRefGoogle Scholar
Cicchetti, D., & Toth, S. L. (2005). Child maltreatment. Annual Review of Clinical Psychology, 1, 409438. doi:10.1146/annurev.clinpsy.1.102803.144029CrossRefGoogle ScholarPubMed
Cicchetti, D., Toth, S. L., & Manly, J. T. (2003). Maternal maltreatment classification interview. Rochester, NY: Unpublished manuscript, Mt. Hope Family Center.Google Scholar
Cohen-Gilbert, J. E., Nickerson, L. D., Sneider, J. T., Oot, E. N., Seraikas, A. M., Rohan, M. L., & Silveri, M. M. (2017). College binge drinking associated with decreased frontal activation to negative emotional distractors during inhibitory control. Frontiers in Psychology, 8, 1650. doi:10.3389/fpsyg.2017.01650CrossRefGoogle ScholarPubMed
Cohen-Gilbert, J. E., & Thomas, K. M. (2013). Inhibitory control during emotional distraction across adolescence and early adulthood. Child Development, 84, 19541966. doi:10.1111/cdev.12085CrossRefGoogle ScholarPubMed
Cowell, R. A., Cicchetti, D., Rogosch, F. A., & Toth, S. L. (2015). Childhood maltreatment and its effect on neurocognitive functioning: Chronicity and timing matter. Development and Psychopathology, 27, 521533. doi:10.1017/s0954579415000139CrossRefGoogle ScholarPubMed
Daly, B. P., Hildenbrand, A. K., Turner, E., Berkowitz, S., & Tarazi, R. A. (2017). Executive functioning among college students with and without history of childhood maltreatment. Journal of Aggression, Maltreatment & Trauma, 26, 717735. doi:10.1080/10926771.2017.1317685CrossRefGoogle Scholar
de Graaf-Peters, V. B., & Hadders-Algra, M. (2006). Ontogeny of the human central nervous system: What is happening when? Early Human Development, 82, 257266. doi:10.1016/j.earlhumdev.2005.10.013CrossRefGoogle Scholar
Demers, L. A., Handley, E. D., Hunt, R. H., Rogosch, F. A., Toth, S. L., Thomas, K. M., … Cicchetti, D. (2019). Childhood maltreatment disrupts brain-mediated pathways between adolescent maternal relationship quality and positive adult outcomes. Child Maltreatment, 24(4), 424434. doi:10.1177/1077559519847770CrossRefGoogle ScholarPubMed
Demers, L. A., McKenzie, K. J., Hunt, R. H., Cicchetti, D., Cowell, R. A., Rogosch, F. A., … Thomas, K. M. (2018). Separable effects of childhood maltreatment and adult adaptive functioning on amygdala connectivity during emotion processing. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 3, 116124. doi:10.1016/j.bpsc.2017.08.010Google ScholarPubMed
DePrince, A. P., Weinzierl, K. M., & Combs, M. D. (2009). Executive function performance and trauma exposure in a community sample of children. Child Abuse & Neglect, 33, 353361. doi:10.1016/j.chiabu.2008.08.002CrossRefGoogle Scholar
Diorio, D., Viau, V., & Meaney, M. J. (1993). The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamic-pituitary-adrenal responses to stress. Journal of Neuroscience, 13, 38393847. doi:10.1523/JNEUROSCI.13-09-03839.1993CrossRefGoogle ScholarPubMed
Fani, N., King, T. Z., Clendinen, C., Hardy, R. A., Surapaneni, S., Blair, J. R., … Ressler, K. J. (2019). Attentional control abnormalities in posttraumatic stress disorder: Functional, behavioral, and structural correlates. Journal of Affective Disorders, 253, 343. doi:10.1016/j.jad.2019.04.098CrossRefGoogle ScholarPubMed
Fay-Stammbach, T., & Hawes, D. J. (2019). Caregiver ratings and performance-based indices of executive function among preschoolers with and without maltreatment experience. Child Neuropsychology, 25, 721741. doi:10.1080/09297049.2018.1530344CrossRefGoogle ScholarPubMed
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.2012.08.006CrossRefGoogle ScholarPubMed
Frank, D. W., Dewitt, M., Hudgens-Haney, M., Schaeffer, D. J., Ball, B. H., Schwarz, N. F., … Sabatinelli, D. (2014). Emotion regulation: Quantitative meta-analysis of functional activation and deactivation. Neuroscience & Biobehavioral Reviews, 45, 202211. doi:10.1016/j.neubiorev.2014.06.010CrossRefGoogle ScholarPubMed
Gershoff, E. T. (2002). Corporal punishment by parents and associated child behaviors and experiences: A meta-analytic and theoretical review. Psychological Bulletin, 128, 539. doi:10.1037/0033-2909.128.4.539CrossRefGoogle ScholarPubMed
Gilbert, R., Widom, C. S., Browne, K., Fergusson, D., Webb, E., & Janson, S. (2009). Burden and consequences of child maltreatment in high-income countries. The Lancet, 373, 6881. doi:10.1016/S0140-6736(08)61706-7CrossRefGoogle ScholarPubMed
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.2010.12.004CrossRefGoogle ScholarPubMed
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, 74667472. doi:10.1523/JNEUROSCI.0859-10.2010CrossRefGoogle ScholarPubMed
Hart, H., & Rubia, K. (2012). Neuroimaging of child abuse: A critical review. Frontiers in Human Neuroscience, 6, 124. doi:10.3389/fnhum.2012.00052CrossRefGoogle ScholarPubMed
Havighurst, R. J. (1956). Research on the developmental-task concept. School Review, 64, 215223. doi:10.1086/442319CrossRefGoogle Scholar
Hein, T. C., & Monk, C. S. (2017). Research review: Neural response to threat in children, adolescents, and adults after child maltreatment – a quantitative meta-analysis. Journal of Child Psychology and Psychiatry, 58, 222230. doi:10.1111/jcpp.12651CrossRefGoogle ScholarPubMed
Herzog, J. I., Niedtfeld, I., Rausch, S., Thome, J., Mueller-Engelmann, M., Steil, R., … Schmahl, C. (2019). Increased recruitment of cognitive control in the presence of traumatic stimuli in complex PTSD. European Archives of Psychiatry and Clinical Neuroscience, 269, 147159. doi:10.1007/s00406-017-0822-xCrossRefGoogle ScholarPubMed
Jedd, K., Hunt, R. H., Cicchetti, D., Hunt, E., Cowell, R. A., Rogosch, F. A., … Thomas, K. M. (2015). Long-term consequences of childhood maltreatment: Altered amygdala functional connectivity. Development and Psychopathology, 27, 15771589. doi:10.1017/S0954579415000954CrossRefGoogle ScholarPubMed
Kensinger, E. A., & Schacter, D. L. (2006). Processing emotional pictures and words: Effects of valence and arousal. Cognitive, Affective, & Behavioral Neuroscience, 6, 110126. doi:10.3758/CABN.6.2.110CrossRefGoogle ScholarPubMed
Koechlin, E. (2011). Frontal pole function: What is specifically human? Trends in Cognitive Sciences, 15, 241. doi:10.1016/j.tics.2011.04.005CrossRefGoogle ScholarPubMed
Lang, P. J., Bradley, M. M., & Cuthbert, B. N. (2008). International affective picture system (IAPS): Affective ratings of pictures and instruction manual. Gainesville: University of Florida, Tech Rep A-8.Google Scholar
Liu, R. T. (2019). Childhood maltreatment and impulsivity: A meta-analysis and recommendations for future study. Journal of Abnormal Child Psychology, 47, 221243. doi:10.1007/s10802-018-0445-3CrossRefGoogle ScholarPubMed
Luby, J. L., Barch, D., Whalen, D., Tillman, R., & Belden, A. (2017). Association between early life adversity and risk for poor emotional and physical health in adolescence: A putative mechanistic neurodevelopmental pathway. JAMA Pediatrics, 171, 11681175. doi:10.1001/jamapediatrics.2017.3009CrossRefGoogle ScholarPubMed
Mackiewicz Seghete, K. L., DePrince, A. P., & Banich, M. T. (2018). Association between initial age of exposure to childhood abuse and cognitive control: Preliminary evidence. Journal of Traumatic Stress 31: 437447. doi:10.1002/jts.22290CrossRefGoogle ScholarPubMed
Mackiewicz Seghete, K. L., Kaiser, R. H., DePrince, A. P., & Banich, M. T. (2017). General and emotion-specific alterations to cognitive control in women with a history of childhood abuse. NeuroImage: Clinical, 16, 151164. doi:10.1016/j.nicl.2017.06.030CrossRefGoogle ScholarPubMed
Marusak, H. A., Martin, K. R., Etkin, A., & Thomason, M. E. (2015). Childhood trauma exposure disrupts the automatic regulation of emotional processing. Neuropsychopharmacology, 40, 12501258. doi:10.1038/npp.2014.311CrossRefGoogle ScholarPubMed
Mezzacappa, E., Kindlon, D., & Earls, F. (2001). Child abuse and performance task assessments of executive functions in boys. Journal of Child Psychology and Psychiatry, 42, 10411048. doi:10.1111/1469-7610.00803CrossRefGoogle ScholarPubMed
Moreno-López, L., Ioannidis, K., Askelund, A. D., Smith, A. J., Schueler, K., & Van Harmelen, A. L. (2020). The resilient emotional brain: A scoping review of the medial prefrontal cortex and limbic structure and function in resilient adults with a history of childhood maltreatment. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 5, 392402. doi:10.1016/j.bpsc.2019.12.008Google ScholarPubMed
Muehlenkamp, J. J., Kerr, P. L., Bradley, A. R., & Larsen, M. A. (2010). Abuse subtypes and nonsuicidal self-injury: Preliminary evidence of complex emotion regulation patterns. The Journal of Nervous and Mental Disease, 198, 258263. doi:10.1097/NMD.0b013e3181d612abCrossRefGoogle ScholarPubMed
Navalta, C. P., Polcari, A., Webster, D. M., Boghossian, A., & Teicher, M. H. (2006). Effects of childhood sexual abuse on neuropsychological and cognitive function in college women. The Journal of Neuropsychiatry and Clinical Neurosciences, 18, 4553. doi:10.1176/jnp.18.1.45CrossRefGoogle ScholarPubMed
Nigg, J. T. (2017). Annual research review: On the relations among self-regulation, self-control, executive functioning, effortful control, cognitive control, impulsivity, risk-taking, and inhibition for developmental psychopathology. Journal of Child Psychology and Psychiatry, 58, 361383. doi:10.1111/jcpp.12675CrossRefGoogle ScholarPubMed
Nooner, K. B., Mennes, M., Brown, S., Castellanos, F. X., Leventhal, B., Milham, M. P., & Colcombe, S. J. (2013). Relationship of trauma symptoms to amygdala-based functional brain changes in adolescents. Journal of Traumatic Stress, 26, 784787. doi:10.1002/jts.21873CrossRefGoogle ScholarPubMed
Ohashi, K., Anderson, C. M., Bolger, E. A., Khan, A., McGreenery, C. E., & Teicher, M. H. (2019). Susceptibility or resilience to maltreatment can be explained by specific differences in brain network architecture. Biological Psychiatry, 85, 690702. doi:10.1016/j.biopsych.2018.10.016CrossRefGoogle ScholarPubMed
Pearlstein, J. G., Johnson, S. L., Modavi, K., Peckham, A. D., & Carver, C. S. (2019). Neurocognitive mechanisms of emotion-related impulsivity: The role of arousal. Psychophysiology, 56, e13293. doi:10.1111/psyp.13293CrossRefGoogle ScholarPubMed
Pechtel, P., & Pizzagalli, D. A. (2011). Effects of early life stress on cognitive and affective function: An integrated review of human literature. Psychopharmacology, 214, 5570. doi:10.1007/s00213-010-2009-2CrossRefGoogle ScholarPubMed
Phillips, M. L., Drevets, W. C., Rauch, S. L., & Lane, R. (2003). Neurobiology of emotion perception I: The neural basis of normal emotion perception. Biological Psychiatry, 54, 504514. doi:10.1016/S0006-3223(03)00168-9CrossRefGoogle ScholarPubMed
Powers, A., Etkin, A., Gyurak, A., Bradley, B., & Jovanovic, T. (2015). Associations between childhood abuse, posttraumatic stress disorder, and implicit emotion regulation deficits: Evidence from a low-income, inner-city population. Psychiatry, 78, 251264. doi:10.1080/00332747.2015.1069656CrossRefGoogle ScholarPubMed
Rieder, C., & Cicchetti, D. (1989). Organizational perspective on cognitive control functioning and cognitive-affective balance in maltreated children. Developmental Psychology, 25, 382393. doi:10.1037/0012-1649.25.3.382CrossRefGoogle Scholar
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, 464473. doi:10.1016/j.biopsych.2019.04.033CrossRefGoogle ScholarPubMed
Schulenberg, J. E., Bryant, A. L., & O'Malley, P. M. (2004). Taking hold of some kind of life: How developmental tasks relate to trajectories of well-being during the transition to adulthood. Development and Psychopathology, 16, 11191140. doi:10.1017/S0954579404040167CrossRefGoogle ScholarPubMed
Schweizer, S., Walsh, N. D., Stretton, J., Dunn, V. J., Goodyer, I. M., & Dalgleish, T. (2016). Enhanced emotion regulation capacity and its neural substrates in those exposed to moderate childhood adversity. Social Cognitive and Affective Neuroscience, 11, 272281. doi:10.1093/scan/nsv109CrossRefGoogle ScholarPubMed
Shields, G. S., Sazma, M. A., & Yonelinas, A. P. (2016). The effects of acute stress on core executive functions: A meta-analysis and comparison with cortisol. Neuroscience & Biobehavioral Reviews, 68, 651668. doi:10.1016/j.neubiorev.2016.06.038CrossRefGoogle ScholarPubMed
Sowell, E. R., Peterson, B. S., Thompson, P. M., Welcome, S. E., Henkenius, A. L., & Toga, A. W. (2003). Mapping cortical change across the human life span. Nature Neuroscience, 6, 309315. doi:10.1038/nn1008CrossRefGoogle ScholarPubMed
Sujan, A. C., Humphreys, K. L., Ray, L. A., & Lee, S. S. (2014). Differential association of child abuse with self-reported versus laboratory-based impulsivity and risk-taking in young adulthood. Child Maltreatment, 19, 145155. doi:10.1177/1077559514543827CrossRefGoogle ScholarPubMed
Sun, D., Haswell, C. C., Morey, R. A., & De Bellis, M. D. (2019). Brain structural covariance network centrality in maltreated youth with PTSD and in maltreated youth resilient to PTSD. Development and Psychopathology, 31, 557571. doi:10.1017/S0954579418000093CrossRefGoogle ScholarPubMed
Teicher, M. H., Samson, J. A., Anderson, C. M., & Ohashi, K. (2016). The effects of childhood maltreatment on brain structure, function and connectivity. Nature Reviews. Neuroscience, 17, 652666. doi:10.1038/nrn.2016.111CrossRefGoogle ScholarPubMed
van der Bij, J., den Kelder, R. O., Montagne, B., & Hagenaars, M. A. (2020). Inhibitory control in trauma-exposed youth: A systematic review. Neuroscience & Biobehavioral Reviews, 118, 451462. doi:10.1016/j.neubiorev.2020.06.001CrossRefGoogle ScholarPubMed
Weissman, D. G., Jenness, J. L., Colich, N. L., Miller, A. B., Sambrook, K. A., Sheridan, M. A., & McLaughlin, K. A. (2019). Altered neural processing of threat-related information in children and adolescents exposed to violence: A transdiagnostic mechanism contributing to the emergence of psychopathology. Journal of the American Academy of Child & Adolescent Psychiatry, 59, 12741284. doi:10.1016/j.jaac.2019.08.471CrossRefGoogle Scholar