Hostname: page-component-8448b6f56d-42gr6 Total loading time: 0 Render date: 2024-04-17T20:36:21.829Z Has data issue: false hasContentIssue false
  • English
  • Français

Patterns of brain activation in foster children and nonmaltreated children during an inhibitory control task

Published online by Cambridge University Press:  08 November 2013

Jacqueline Bruce ,
Philip A. Fisher ,
Alice M. Graham ,
William E. Moore III ,
Shannon J. Peake  and
Anne M. Mannering
Jacqueline Bruce*
Affiliation:
Oregon Social Learning Center
Philip A. Fisher
Affiliation:
Oregon Social Learning Center University of Oregon
Alice M. Graham
Affiliation:
University of Oregon
William E. Moore III
Affiliation:
University of Oregon
Shannon J. Peake
Affiliation:
University of Oregon
Anne M. Mannering
Affiliation:
Oregon State University
*
Address correspondence and reprint requests to: Jacqueline Bruce, Oregon Social Learning Center, 10 Shelton McMurphey Boulevard, Eugene, OR 97401; E-mail: jackieb@oslc.org.
Get access Rights & Permissions [Opens in a new window]

Abstract

Children in foster care have often encountered a range of adverse experiences, including neglectful and/or abusive care and multiple caregiver transitions. Prior research findings suggest that such experiences negatively affect inhibitory control and the underlying neural circuitry. In the current study, event-related functional magnetic resonance imaging was employed during a go/no go task that assesses inhibitory control to compare the behavioral performance and brain activation of foster children and nonmaltreated children. The sample included two groups of 9- to 12-year-old children: 11 maltreated foster children and 11 nonmaltreated children living with their biological parents. There were no significant group differences on behavioral performance on the task. In contrast, patterns of brain activation differed by group. The nonmaltreated children demonstrated stronger activation than did the foster children across several regions, including the right anterior cingulate cortex, the middle frontal gyrus, and the right lingual gyrus, during correct no go trials, whereas the foster children displayed stronger activation than the nonmaltreated children in the left inferior parietal lobule and the right superior occipital cortex, including the lingual gyrus and cuneus, during incorrect no go trials. These results provide preliminary evidence that the early adversity experienced by foster children impacts the neural substrates of inhibitory control.

Type
Regular Articles
Information
Development and Psychopathology , Volume 25 , Issue 4pt1 , November 2013 , pp. 931 - 941
Copyright
Copyright © Cambridge University Press 2013 

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.)

References

Achenbach, T. M. (1991). Manual for the Child Behavior Checklist/4–18 and 1991 profile. Burlington, VT: University of Vermont, Department of Psychiatry.Google Scholar
Arnsten, A. F. T. (2009). Stress signalling pathways that impair prefrontal cortex structure and function. Nature Reviews Neuroscience, 10, 410–422.Google Scholar
Beckmann, C. F., Jenkinson, M., Woolrich, M. W., Behrens, T. E. J., Flitney, D. E., Devlin, J. T., et al. (2006). Applying FSL to the FIAC data: Model-based and model-free analysis of voice and sentence repetition priming. Human Brain Mapping, 27, 380–391.Google Scholar
Beers, S. R., & De Bellis, M. D. (2002). Neuropsychological function in children with maltreatment-related posttraumatic stress disorder. American Journal of Psychiatry, 159, 483–486.Google Scholar
Behen, M. E., Muzik, O., Saporta, A. S. D., Wilson, B. J., Pai, D., Hua, J., et al. (2009). Abnormal fronto-striatal connectivity in children with histories of early deprivation: A diffusion tensor imaging study. Brain Imaging and Behavior, 3, 292–297.Google Scholar
Black, J. E. (1998). How a child builds its brain: Some lessons from animal studies of neural plasticity. Preventive Medicine, 27, 168–171.Google Scholar
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, 647–663.Google Scholar
Botvinick, M. M., Braver, T. S., Barch, D. M., Carter, C. S., & Cohen, J. D. (2001). Conflict monitoring and cognitive control. Psychological Review, 108, 624–652.Google Scholar
Braet, W., Johnson, K. A., Tobin, C. T., Acheson, R., Bellgrove, M. A., Robertson, I. H., et al. (2009). Functional developmental changes underlying response inhibition and error-detection processes. Neuropsychologia, 47, 3143–3151.Google Scholar
Brett, M. (2011). MarsBaR documentation. Retreived November 28, 2011, from http://marsbar.sourceforge.net/marsbar.pdfGoogle Scholar
Bruce, J., McDermott, J. M., Fisher, P. A., & Fox, N. A. (2009). Using behavioral and electrophysiological measures to assess the effects of a preventive intervention: A preliminary study with preschool-aged foster children. Prevention Science, 10, 129–140.Google Scholar
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, 301–311.Google Scholar
Carrion, V. G., Weems, C. F., Eliez, S., Patwardhan, A., Brown, W., Ray, R. D., et al. (2001). Attenuation of frontal asymmetry in pediatric postraumatic stress disorder. Biological Psychiatry, 50, 943–951.Google Scholar
Casey, B. J., Castellanos, F. X., Giedd, J. N., Marsh, W. L., Hamburger, S. D., Schubert, A. B., et al. (1997). Implication of right frontostriatal circuitry in response inhibition and attention-deficit/hyperactivity disorder. Journal of the American Academy of Child & Adolescent Psychiatry, 36, 374–383.Google Scholar
Casey, B. J., Tottenham, N., & Fossella, J. (2002). Clinical, imaging, lesion, and genetic approaches toward a model of cognitive control. Developmental Psychobiology, 40, 237–254.Google Scholar
Casey, B. J., Trainor, R. J., Giedd, J. N., Vauss, Y. C., Vaituzis, A. C., Hamburger, S. D., et al. (1997). The role of the anterior cingulate in automatic and controlled processes: A developmental neuroanatomical study. Developmental Psychobiology, 3, 61–69.Google Scholar
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, 283–296.Google Scholar
Dale, A. M. (1999). Optimal experimental design for event-related fMRI. Human Brain Mapping, 8, 109–114.Google 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, 432–443.Google Scholar
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, 539–564.Google Scholar
De Bellis, M. D., Keshavan, M. S., Spencer, S., & Hall, J. (2000). N-Acetylaspartate concentration in the anterior cingulate of maltreated children and adolescents with PTSD. American Journal of Psychiatry, 157, 1175–1177.CrossRefGoogle ScholarPubMed
dosReis, S., Zito, J. M., Safer, D. J., & Soeken, K. L. (2001). Mental health services for youths in foster care and disabled youths. American Journal of Public Health, 91, 1094–1099.Google Scholar
Durston, S., Davidson, M. C., Tottenham, N., Galvan, A., Spicer, J., Fossella, J. A., et al. (2006). A shift from diffuse to focal cortical activity with development. Developmental Science, 9, 1–8.CrossRefGoogle ScholarPubMed
Durston, S., Mulder, M., Casey, B. J., Ziermans, T., & van Engeland, H. (2006). Activation in ventral prefrontal cortex is sensitive to genetic vulnerability for attention-deficit hyperactivity disorder. Biological Psychiatry, 60, 1062–1070.Google Scholar
Durston, S., Thomas, K. M., Worden, M. S., Yang, Y., & Casey, B. J. (2002). The effect of preceding context on inhibition: An event-related fMRI study. NeuroImage, 16, 449–453.Google Scholar
Durston, S., Thomas, K. M., Yang, Y., Uluğ, A. M., Zimmerman, R. D., & Casey, B. J. (2002). A neural basis for the development of inhibitory control. Developmental Science, 5, F9–F16.Google Scholar
Durston, S., Tottenham, N., Thomas, K. M., Davidson, M. C., Eigsti, I.-M., Yang, Y., et al. (2003). Differential patterns of striatal activation in young children with and without ADHD. Biological Psychiatry, 53, 871–878.Google Scholar
Eigsti, I.-M., Zayas, V., Mischel, W., Shoda, Y., Ayduk, O., Dadlani, M. B., et al. (2006). Predicting cognitive control from preschool to late adolescence and young adulthood. Psychological Science, 17, 478–484.Google Scholar
Eisenberg, N., Fabes, R. A., Shepard, S. A., Murphy, B. C., Guthrie, I. K., Jones, S., et al. (1997). Contemporaneous and longitudinal prediction of children's social functioning from regulation and emotionality. Child Development, 68, 642–664.Google Scholar
Fishbein, D. (2000). The importance of neurobiological research to the prevention of psychopathology. Prevention Science, 1, 89–106.Google Scholar
Garavan, H., Ross, T. J., Kaufman, K., & Stein, E. A. (2003). A midline dissociation between error-processing and response-conflict monitoring. NeuroImage, 20, 1132–1139.Google Scholar
Garland, A. F., Hough, R. L., McCabe, K. M., Yeh, M., Wood, P. A., & Aarons, G. A. (2001). Prevalence of psychiatric disorders in youths across five sectors of care. Journal of the American Academy of Child & Adolescent Psychiatry, 40, 409–418.Google Scholar
Gerstadt, C. L., Hong, Y. J., & Diamond, A. (1994). The relationship between cognition and action: Performance of children 31/2–7 years old on a Stroop-like day–night test. Cognition, 53, 129–153.Google Scholar
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, 1261–1279.Google Scholar
Gogtay, N., Giedd, J. N., Lusk, L., Hayashi, K. M., Greenstein, D., Vaituzis, A. C., et al. (2004). Dynamic mapping of human cortical development during childhood through early adulthood. Proceedings of the National Academy of Sciences, 101, 8174–8179.Google Scholar
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, 651–677.Google Scholar
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, 790–798.Google Scholar
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, 1201–1213.Google Scholar
Hester, R., Fassbender, C., & Garavan, H. (2004). Individual differences in error processing: A review and reanalysis of three event-related fMRI studies using the GO/NOGO task. Cerebral Cortex, 14, 986–994.Google Scholar
Holmes, A., & Wellman, C. L. (2009). Stress-induced prefrontal reorganization and executive dysfunction in rodents. Neuroscience & Biobehavioral Reviews, 33, 773–783.Google Scholar
Karayanidis, F., Robaey, P., Bourassa, M., De Koning, D., Geoffroy, G., & Pelletier, G. (2000). ERP differences in visual attention processing between attention-deficit hyperactivity disorder and control boys in the absence of preformance differences. Psychophysiology, 37, 319–333.Google Scholar
Kessler, R. C., Pecora, P. J., Williams, J., Hiripi, E., O'Brien, K., English, D., et al. (2008). Effects of enhanced foster care on the long-term physical and mental health of foster care alumni. Archives of General Psychiatry, 65, 625–633.CrossRefGoogle ScholarPubMed
Kochanska, G., Murray, K., & Coy, K. C. (1997). Inhibitory control as a contributor to conscience in childhood: From toddler to early school age. Child Development, 68, 263–277.Google Scholar
Kochanska, G., Murray, K., Jacques, T. Y., Koenig, A. L., & Vandegeest, K. (1996). Inhibitory control in young children and its role in emerging internalization. Child Development, 67, 490–507.Google Scholar
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, 220–232.CrossRefGoogle ScholarPubMed
Lengua, L. J., Honorado, E., & Bush, N. R. (2007). Contextual risk and parenting as predictors of effortful control and social competence in preschool children. Journal of Applied Developmental Psychology, 28, 40–55.Google Scholar
Leslie, L. K., Gordon, J. N., Ganger, W., & Gist, K. (2002). Developmental delay in young children in child welfare by initial placement type. Infant Mental Health Journal, 23, 496–516.CrossRefGoogle Scholar
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, 1415–1427.Google Scholar
Liddle, P. F., Kiehl, K. A., & Smith, A. M. (2001). Event-related fMRI study of response inhibition. Human Brain Mapping, 12, 100–109.Google Scholar
Liu, T. T., & Frank, L. R. (2004). Efficiency, power, and entropy in event-related fMRI with multiple trial types: Part I. Theory. NeuroImage, 21, 387–400.CrossRefGoogle ScholarPubMed
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, 947–959.Google Scholar
Menon, V., Adleman, N. E., White, C. D., Glover, G. H., & Reiss, A. L. (2001). Error-related brain activation during a Go/NoGo response inhibition task. Human Brain Mapping, 12, 131–143.Google Scholar
Office of Applied Studies in the Substance Abuse and Mental Health Services Administration. (2005). The National Survey on Drug Use and Health: Substance use and need for treatment among youths who have been in foster care. Rockville, MD: Author.Google Scholar
Pears, K. C., Bruce, J., Fisher, P. A., & Kim, H. K. (2010). Indiscriminate friendliness in maltreated foster children. Child Maltreatment, 15, 64–75.Google Scholar
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, 373–386.Google Scholar
Pears, K. C., & Fisher, P. A. (2005). Developmental, cognitive, and neuropsychological functioning in preschool-aged foster children: Associations with prior maltreatment and placement history. Developmental and Behavioral Pediatrics, 26, 112–122.Google Scholar
Pears, K. C., Fisher, P. A., Bruce, J., Kim, H. K., & Yoerger, K. (2010). Early elementary school adjustment of maltreated children in foster care: The roles of inhibitory control and caregiver involvement. Child Development, 81, 1550–1564.Google Scholar
Pilowsky, D. (1995). Psychopathology among children placed in family foster care. Psychiatric Services, 46, 906–910.Google Scholar
Pliszka, S. R., Glahn, D. C., Semrud-Clikeman, M., Franklin, C., Perez, R. I., Xiong, J., et al. (2006). Neuroimaging of inhibitory control areas in children with attention deficit hyperactivity disorder who were treatment naive or in long-term treatment. American Journal of Psychiatry, 163, 1052–1060.Google Scholar
Ridderinkhof, K. R., van der Molan, M. W., Band, G. P. H., & Bashore, T. R. (1997). Sources of interference from irrelevant information: A developmental study. Journal of Experimental Child Psychology, 65, 315–341.Google Scholar
Rubia, K., Smith, A. B., Brammer, M. J., & Taylor, E. (2003). Right inferior prefrontal cortex mediates response inhibition while medial prefrontal cortex is responsible for error detection. NeuroImage, 20, 351–358.Google Scholar
Rubia, K., Smith, A. B., Taylor, E., & Brammer, M. (2007). Linear age-correlated functional development of right inferior fronto-striato-cerebellar networks during response inhibition and anterior cingulate during error-related processes. Human Brain Mapping, 28, 1163–1177.Google Scholar
Rubia, K., Smith, A. B., Woolley, J., Nosarti, C., Heyman, I., Taylor, E., et al. (2006). Progressive increase of frontostriatal brain activation from childhood to adulthood during event-related tasks of cognitive control. Human Brain Mapping, 27, 973–993.Google Scholar
Smith, S. M. (2002). Fast robust automated brain extraction. Human Brain Mapping, 17, 143–155.CrossRefGoogle ScholarPubMed
Smith, S., Bannister, P. R., Beckmann, C., Brady, M., Clare, S., Flitney, D. H., et al. (2001). FSL: New tools for functional and structural brain image analysis. NeuroImage, 13, S249.Google Scholar
Song, X.-W., Dong, Z.-Y., Long, X.-Y., Li, S.-F., Zuo, X.-N., Zhu, C.-Z., et al. (2011). REST: A toolkit for resting-state functional magnetic resonance imaging data processing. PLos ONE, 6, e25031.Google Scholar
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, 8223–8231.Google Scholar
Stein, E. (1997). Teachers’ assessments of children in foster care. Developmental Disabilities Bulletin, 25, 1–17.Google Scholar
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, 99–114.Google Scholar
Tamm, L., Menon, V., & Reiss, A. L. (2002). Maturation of brain function associated with response inhibition. Journal of the American Academy of Child & Adolescent Psychiatry, 41, 1231–1238.Google Scholar
Tarter, R. E., Kirisci, L., Mezzich, A., Cornelius, J. R., Pajer, K, Vanyukov, M., et al. (2003). Neurobehavioral disinhibition in childhood predicts early age at onset of substance use disorder. American Journal of Psychiatry, 160, 1078–1085.Google Scholar
Thatcher, R. W., Walker, R. A., & Giudice, S. (1987). Human cerebral hemispheres develop at different rates and ages. Science, 236, 1110–1113.Google Scholar
Thesen, S., Heid, O., Mueller, E., & Schad, L. R. (2000). Prospective acquisition correction for head motion with image-based tracking for real-time fMRI. Magnetic Resonance in Medicine, 44, 457–465.Google Scholar
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, 333–344.Google Scholar
US Department of Health and Human Services. (2011). The AFCARS report: Preliminary FY 2010 estimates as of July 2011. Washington, DC: Author.Google Scholar
Valiente, C., Lemery-Chalfant, K., & Reiser, M. (2007). Pathways to problem behaviors: Chaotic homes, parent and child effortful control, and parenting. Social Development, 16, 249–267.Google Scholar
van Veen, V., & Carter, C. S. (2002). The timing of action-monitoring processes in the anterior cingulate cortex. Journal of Cognitive Neuroscience, 14, 593–602.Google Scholar
Vaughn, M. G., Ollie, M. T., McMillen, J. C., Scott, L., & Munson, M. (2007). Substance use and abuse among older youth in foster care. Addictive Behaviors, 32, 1929–1935.Google Scholar
Zhou, Q., Eisenberg, N., Wang, Y., & Reiser, M. (2004). Chinese children's effortful control and dispositional anger/frustration: Relations to parenting styles and children's social functioning. Developmental Psychology, 40, 352–366.Google Scholar
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, 87–103.Google Scholar