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Behavioral and electrophysiological indices of inhibitory control in maltreated adolescents and nonmaltreated adolescents

Published online by Cambridge University Press:  22 December 2020

Jacqueline Bruce*
Affiliation:
Oregon Social Learning Center, Eugene, OR, USA
Hyoun K. Kim
Affiliation:
Department of Child and Family Studies, Yonsei University, Seoul, South Korea
*
Author for Correspondence: Dr. Jacqueline Bruce, Oregon Social Learning Center, 10 Shelton McMurphey Boulevard, Eugene, OR97401; E-mail: [email protected]

Abstract

Early adverse experiences are believed to have a profound effect on inhibitory control and the underlying neural regions. In the current study, behavioral and event-related potential (ERP) data were collected during a go/no-go task from adolescents who were involved with the child welfare system due to child maltreatment (n = 129) and low-income, nonmaltreated adolescents (n = 102). The nonmaltreated adolescents were more accurate than the maltreated adolescents on the go/no-go task, particularly on the no-go trials. Paralleling the results with typically developing populations, the nonmaltreated adolescents displayed a more pronounced amplitude of the N2 during the no-go trials than during the go trials. However, the maltreated adolescents demonstrated a more pronounced amplitude of the N2 during the go trials than during the no-go trials. Furthermore, while the groups did not differ during the go trials, the nonmaltreated adolescents displayed a more negative amplitude of the N2 than the maltreated adolescents during no-go trials. In contrast, there was not a significant group difference in amplitude of the P3. Taken together, these results provide evidence that the early adverse experiences encountered by maltreated populations impact inhibitory control and the underlying neural activity in early adolescence.

Type
Regular Article
Copyright
© The Author(s), 2020. Published by Cambridge University Press

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References

Aarons, G. A., Brown, S. A., Hough, R. L., Garland, A. F., & Wood, P. A. (2001). Prevalence of adolescent substance use disorders across five sectors of care. Journal of the American Academy of Child and Adolescent Psychiatry, 40, 419426. doi:10.1097/00004583-200104000-00010CrossRefGoogle Scholar
Arnsten, A. F. T. (2009). Stress signalling pathways that impair prefrontal cortex structure and function. Nature Reviews Neuroscience, 10, 410422. doi:10.1038/nrn2648CrossRefGoogle ScholarPubMed
Aron, A. R., Behrens, T. E., Smith, S., Frank, M. J., & Poldrack, R. A. (2007). Triangulating a cognitive control network using diffusion-weighted magnetic resonance imaging (MRI) and functional MRI. Journal of Neuroscience, 27, 37433752. doi:10.1523/jneurosci.0519-07.2007CrossRefGoogle ScholarPubMed
Black, J. E. (1998). How a child builds its brain: Some lessons from animal studies of neural plasticity. Preventive Medicine, 27, 168171. doi:10.1006/pmed.1998.0271CrossRefGoogle ScholarPubMed
Blair, C., & Razza, R. P. (2007). Relating effortful control, executive function, and false belief understanding to emerging math and literacy ability in kindergarten. Child Development, 78, 647663. doi:10.1111/j.1467-8624.2007.01019.xCrossRefGoogle ScholarPubMed
Booth, J. R., Burman, D. D., Meyer, J. R., Lei, Z., Trommer, B. L., Davenport, N. D., … Mesulam, M. M. (2005). Larger deficits in brain networks for response inhibition than visual selective attention in attention deficit hyperactivity disorder (ADHD). Journal of Child Psychology and Psychiatry, 46, 94111. doi:10.1111/j.1469-7610.2004.00337.xCrossRefGoogle Scholar
Bruce, J., Fisher, P. A., Graham, A. M., Moore, W. E., Peake, S. J., & Mannering, A. M. (2013). Patterns of brain activation in foster children and nonmaltreated children during an inhibitory control task. Development and Psychopathology, 25, 931941. doi:10.1017/s095457941300028xCrossRefGoogle ScholarPubMed
Bruce, J., Tarullo, A. R., & Gunnar, M. R. (2009). Disinhibited social behavior among internationally adopted children. Development and Psychopathology, 21, 157171. doi:10.1017/s0954579409000108CrossRefGoogle ScholarPubMed
Bryck, R. L., & Fisher, P. A. (2012). Training the brain: Practical applications of neural plasticity from the intersection of cognitive neuroscience, developmental psychology, and prevention science. American Psychologist, 67, 87100. doi:10.1037/a0024657CrossRefGoogle ScholarPubMed
Bunge, S. A., Dudukovic, N. M., Thomason, M. E., Vaidya, C. J., & Gabrieli, J. D. E. (2002). Immature frontal lobe contributions to cognitive control in children: Evidence from fMRI. Neuron, 33, 301311. doi:10.1016/s0896-6273(01)00583-9CrossRefGoogle ScholarPubMed
Burden, M. J., Andrew, C., Saint-Amour, D., Meintjes, E. M., Molteno, C. D., Hoyme, H. E., … Jacobson, S. W. (2009). The effects of fetal alcohol syndrome on response execution and inhibition: An event-related potential study. Alcoholism: Clinical and Experimental Research, 33, 19942004. doi:10.1111/j.1530-0277.2009.01038.xCrossRefGoogle Scholar
Casey, B. J., Castellanos, F. X., Giedd, J. N., Marsh, W. L., Hamburger, S. D., Schubert, A. B., … Rapoport, J. L. (1997). Implication of right frontostriatal circuitry in response inhibition and Attention-Deficit/Hyperactivity Disorder. Journal of the American Academy of Child and Adolescent Psychiatry, 36, 374383. doi:10.1097/00004583-199703000-00016CrossRefGoogle ScholarPubMed
Casey, B. J., Tottenham, N., & Fossella, J. (2002). Clinical, imaging, lesion, and genetic approaches toward a model of cognitive control. Developmental Psychobiology, 40, 237254. doi:10.1002/dev.10030CrossRefGoogle Scholar
Casey, B. J., Trainor, R. J., Orendi, J. L., Schubert, A. B., Nystrom, L. E., Giedd, J. N., … Rapoport, J. L. (1997). A developmental functional MRI study of prefrontal activation during performance of a Go-No-Go task. Journal of Cognitive Neuroscience, 9, 835847. doi:10.1162/jocn.1997.9.6.835CrossRefGoogle ScholarPubMed
Clausen, J. M., Landsverk, J., Ganger, W., Chadwick, D., & Litrownik, A. (1998). Mental health problems of children in foster care. Journal of Child and Family Studies, 7, 283296. doi:10.1023/a:1022989411119CrossRefGoogle Scholar
Crozier, J. C., & Barth, R. P. (2005). Cognitive and academic functioning in maltreated children. Children and Schools, 27, 197206. doi:10.1093/cs/27.4.197CrossRefGoogle Scholar
Davis, E. P., Bruce, J., Snyder, K., & Nelson, C. A. (2003). The X-trials: Neural correlates of an inhibitory control task in children and adults. Journal of Cognitive Neuroscience, 15, 432443. doi:10.1162/089892903321593144CrossRefGoogle ScholarPubMed
De Bellis, M. D. (2001). Developmental traumatology: The psychobiological development of maltreated children and its implications for research, treatment, and policy. Development and Psychopathology, 13, 539564. doi:10.1017/s0954579401003078CrossRefGoogle Scholar
Durston, S., Davidson, M. C., Tottenham, N., Galvan, A., Spicer, J., Fossella, J. A., & Casey, B. J. (2006). A shift from diffuse to focal cortical activity with development. Developmental Science, 9, 18. doi:10.1111/j.1467-7687.2005.00454.xCrossRefGoogle ScholarPubMed
Durston, S., Thomas, K. M., Yang, Y., Ulug, A. M., Zimmerman, R. D., & Casey, B. J. (2002). A neural basis for the development of inhibitory control. Developmental Science, 5, F9F16. doi:10.1111/1467-7687.00235CrossRefGoogle Scholar
Eigsti, I.-M., Zayas, V., Mischel, W., Shoda, Y., Ayduk, O., Dadlani, M. B., … Casey, B. J. (2006). Predicting cognitive control from preschool to late adolescence and young adulthood. Psychological Science, 17, 478484. doi:10.1111/j.1467-9280.2006.01732.xCrossRefGoogle ScholarPubMed
Fishbein, D. (2000). The importance of neurobiological research to the prevention of psychopathology. Prevention Science, 1, 89106. doi:10.1023/a:1010090114858CrossRefGoogle Scholar
Folstein, J. R., & Van Petten, C. (2008). Influence of cognitive control and mismatch on the N2 component of the ERP: A review. Psychophysiology, 45, 152170. doi:10.1111/j.1469-8986.2007.00602.xGoogle ScholarPubMed
Ghashghaei, H. T., & Barbas, H. (2002). Pathways for emotion: Interactions of prefrontal and anterior temporal pathways in the amygdala of the rhesus monkey. Neuroscience, 115, 12611279. doi:10.1016/S0306-4522(02)00446-3CrossRefGoogle ScholarPubMed
Gogtay, N., Giedd, J. N., Lusk, L., Hayashi, K. M., Greenstein, D., Vaituzis, A. C., … Thompson, P. M. (2004). Dynamic mapping of human cortical development during childhood through early adulthood. Proceedings of the National Academy of Sciences, 101, 81748179. doi:10.1073/pnas.0402680101CrossRefGoogle ScholarPubMed
Gunnar, M. R., Fisher, P. A., & The Early Experience Stress and Prevention Network. (2006). Bringing basic research on early experience and stress neurobiology to bear on preventive interventions for neglected and maltreated children. Development and Psychopathology, 18, 651677. doi:10.10170s0954579406060330CrossRefGoogle ScholarPubMed
Gunnar, M. R., & Quevedo, K. (2007). The neurobiology of stress and development. Annual Review of Psychology, 58, 145173. doi:10.1146/annurev.psych.58.110405.085605CrossRefGoogle ScholarPubMed
Helmeke, C., Seidel, K., Poeggel, G., Bredy, T. W., Abraham, A., & Braun, K. (2009). Paternal deprivation during infancy results in dendrite- and time-specific changes of dendritic development and spine formation in the orbitofrontal cortex of the biparental rodent Octodon degus. Neuroscience, 163, 790798. doi:10.1016/j.neuroscience.2009.07.008CrossRefGoogle ScholarPubMed
Herman, J. P., Ostrander, M. M., Mueller, N. K., & Figueiredo, H. (2005). Limbic system mechanisms of stress regulation: Hypothalamo–pituitary–adrenocortical axis. Progress in Neuropsychopharmacology and Biological Psychiatry, 29, 12011213. doi:10.1016/j.pnpbp.2005.08.006CrossRefGoogle ScholarPubMed
Holmes, A., & Wellman, C. L. (2009). Stress-induced prefrontal reorganization and executive dysfunction in rodents. Neuroscience and Biobehavioral Reviews, 33, 773783. doi:10.1016/j.neubiorev.2008.11.005CrossRefGoogle ScholarPubMed
Jasper, H. H. (1958). The ten-twenty electrode system of the International Federation. Electroencephalography and Clinical Neurophysiology, 10, 371375.Google Scholar
Keller, T. E., Salazar, A. M., & Courtney, M. E. (2010). Prevalence and timing of diagnosable mental health, alcohol, and substance use problems among older adolescents in the child welfare system. Children and Youth Services Review, 32, 626634. doi:10.1016/j.childyouth.2009.12.010CrossRefGoogle ScholarPubMed
Kim, H., Wildeman, C., Jonson-Reid, M., & Drake, B. (2017). Lifetime prevalence of investigating child maltreatment among US children. American Journal of Public Health, 107, 274280. doi:10.2105/ajph.2016.303545CrossRefGoogle ScholarPubMed
Kochanska, G., Murray, K. T., & Harlan, E. T. (2000). Effortful control in early childhood: Continuity and change, antecedents, and implications for social development. Developmental Psychology, 36, 220232. doi:10.1037/0012-1649.36.2.220CrossRefGoogle ScholarPubMed
Lamm, C., Zelazo, P. D., & Lewis, M. D. (2006). Neural correlates of cognitive control in childhood and adolescence: Disentangling the contributions of age and executive function. Neuropsychologia, 44, 21392148. doi:10.1016/j.neuropsychologia.2005.10.013CrossRefGoogle ScholarPubMed
Lewis, E., Dozier, M., Ackerman, J., & Sepulveda-Kozakowski, S. (2007). The effect of caregiving instability on adopted children's inhibitory control abilities and oppositional behavior. Developmental Psychology, 43, 14151427. doi:10.1037/0012-1649.43.6.1415CrossRefGoogle Scholar
Liddle, P. F., Kiehl, K. A., & Smith, A. M. (2001). Event-related fMRI study of response inhibition. Human Brain Mapping, 12, 100109. doi:10.1002/1097-0193(200102)12:2 < 100::aid-hbm1007 > 3.0.co;2-63.0.CO;2-6>CrossRefGoogle ScholarPubMed
Loman, M. M., Johnson, A. E., Westerlund, A., Pollak, S. D., Nelson, C. A., & Gunnar, M. R. (2013). The effect of early deprivation on executive attention in middle childhood. Journal of Child Psychology and Psychiatry, 54, 3745. doi:10.1111/j.1469-7610.2012.02602.xCrossRefGoogle ScholarPubMed
Luck, S. J. (2005). An introduction to the event-related potential technique. Cambridge, MA: MIT Press.Google Scholar
McClelland, M. M., Cameron, C. E., Connor, C. M., Farris, C. L., Jewkes, A. M., & Morrison, F. J. (2007). Links between behavioral regulation and preschoolers’ literacy, vocabulary, and math skills. Developmental Psychology, 43, 947959. doi:10.1037/0012-1649.43.4.947CrossRefGoogle ScholarPubMed
McDermott, J. M., Westerlund, A., Zeanah, C. H., Nelson, C. A., & Fox, N. A. (2012). Early adversity and neural correlates of executive function: Implications for academic adjustment. Developmental Cognitive Neuroscience, 2, S59S66. doi:10.1016/j.dcn.2011.09.008CrossRefGoogle ScholarPubMed
Mueller, S. C., Maheu, F. S., Dozier, M., Peloso, E., Mandell, D., Leibenluft, E., … Ernst, M. (2010). Early-life stress is associated with impairment in cognitive control in adolescence: An fMRI study. Neuropsychologia, 48, 30373044. doi:10.1016/j.neuropsychologia.2010.06.013CrossRefGoogle ScholarPubMed
Nieuwenhuis, S., Aston-Jones, G., & Cohen, J. D. (2005). Decision making, the P3, and the locus coeruleus–norepinephrine system. Psychological Bulletin, 131, 510532. doi:10.1037/0033-2909.131.4.510CrossRefGoogle ScholarPubMed
Nieuwenhuis, S., Yeung, N., Van Den Wildenberg, W., & Ridderinkhof, K. R. (2003). Electrophysiological correlates of anterior cingulate function in a go/no-go task: Effects of response conflict and trial type frequency. Cognitive, Affective and Behavioral Neuroscience, 3, 1726. doi:10.3758/cabn.3.1.17CrossRefGoogle Scholar
Pears, K. C., Bruce, J., Fisher, P. A., & Kim, H. K. (2010). Indiscriminate friendliness in maltreated foster children. Child Maltreatment, 15, 6475. doi:10.1177/1077559509337891CrossRefGoogle ScholarPubMed
Pears, K. C., Capaldi, D. M., & Owen, L. D. (2007). Substance use risk across three generations: The roles of parent discipline practices and inhibitory control. Psychology of Addictive Behaviors, 21, 373386. doi:10.1037/0893-164x.21.3.373CrossRefGoogle ScholarPubMed
Pechtel, P., & Pizzagalli, D. A. (2014). 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 Scholar
Pilowsky, D. J., & Wu, L.-T. (2006). Psychiatric symptoms and substance use disorders in a nationally representative sample of American adolescents involved with foster care. Journal of Adolescent Health, 38, 351358. doi:10.1016/j.jadohealth.2005.06.014CrossRefGoogle Scholar
Pollak, S. D., Nelson, C. A., Schlaak, M. F., Roeber, B. J., Wewerka, S. S., Wiik, K. L., … Gunnar, M. R. (2010). Neurodevelopmental effects of early deprivation in postinstitutionalized children. Child Development, 81, 224236. doi:10.1111/j.1467-8624.2009.01391.xCrossRefGoogle ScholarPubMed
Rubia, K., Smith, A. B., Woolley, J., Nosarti, C., Heyman, I., Taylor, E., & Brammer, M. (2006). Progressive increase of frontostriatal brain activation from childhood to adulthood during event-related tasks of cognitive control. Human Brain Mapping, 27, 973993. doi:10.1002/hbm.20237CrossRefGoogle ScholarPubMed
Sheinkopf, S. J., Lester, B. M., Sanes, J. N., Eliassen, J. C., Hutchison, E. R., Seifer, R., … Casey, B. J. (2009). Functional MRI and response inhibition in children exposed to cocaine in utero. Developmental Neuroscience, 31, 159166. doi:10.1159/000207503CrossRefGoogle ScholarPubMed
Smith, A. M., Fried, P. A., Hogan, M. J., & Cameron, I. (2004). Effects of prenatal marijuana on response inhibition: An fMRI study of young adults. Neurotoxicology and Teratology, 26, 533542. doi:10.1016/j.ntt.2004.04.004CrossRefGoogle ScholarPubMed
Sowell, E. R., Thompson, P. M., Leonard, C. M., Welcome, S. E., Kan, E., & Toga, A. W. (2004). Longitudinal mapping of cortical thickness and brain growth in normal children. Journal of Neuroscience, 24, 82238231. doi:10.1523/jneurosci.1798-04.2004CrossRefGoogle ScholarPubMed
Sullivan, R. M., & Gratton, A. (2002). Prefrontal cortical regulation of hypothalamic-pituitary-adrenal function in the rat and implications for psychopathology: Side matters. Psychoneuroendocrinology, 27, 99114. doi:10.1016/s0306-4530(01)00038-5CrossRefGoogle ScholarPubMed
Thatcher, R. W., Walker, R. A., & Giudice, S. (1987). Human cerebral hemispheres develop at different rates and ages. Science, 236, 11101113. doi:10.1126/science.3576224CrossRefGoogle ScholarPubMed
Toupin, J., Déry, M., Pauzé, R., Mercier, H., & Fortin, L. (2000). Cognitive and familial contributions to conduct disorder in children. Journal of Child Psychology and Psychiatry, 41, 333344. doi:10.1111/1469-7610.00617CrossRefGoogle ScholarPubMed
Troller-Renfree, S. V., Buzzell, G. A., Bowers, M. E., Salo, V. C., Forman-Alberti, A., Smith, E., … Fox, N. A. (2019). Development of inhibitory control during childhood and its relations to early temperament and later social anxiety: Unique insights provided by latent growth modeling and signal detection theory. Journal of Child Psychology and Psychiatry, 60, 622629. doi:10.1111/jcpp.13025CrossRefGoogle ScholarPubMed
U.S. Department of Health and Human Services. (2019). Child maltreatment 2017. Retrieved from Washington, DC: https://www.acf.hhs.gov/cb/research-data-technology/statistics-research/child-maltreatmentGoogle Scholar
Wechsler, D. (2011). Wechsler abbreviated scale of intelligence – Second edition manual. Bloomington, MN: Pearson Assessment.Google Scholar
Wills, T. A., & Stoolmiller, M. (2002). The role of self-control in early escalation of substance use: A time-varying analysis. Journal of Consulting and Clinical Psychology, 70, 986997. doi:10.1037/0022-006x.70.4.986CrossRefGoogle ScholarPubMed
Zima, B. T., Bussing, R., Freeman, S., Yang, X., Belin, T. R., & Forness, S. R. (2000). Behavior problems, academic skill delays and school failure among school-aged children in foster care: Their relationship to placement characteristics. Journal of Child and Family Studies, 9, 87103. doi:10.1023/a:1009415800475CrossRefGoogle Scholar