Longitudinal changes in cortical thickness in children after traumatic brain injury and their relation to behavioral regulation and emotional control

Elisabeth A. Wilde, Tricia L. Merkley, Erin D. Bigler, Jeffrey E. Max, Adam T. Schmidt, Kareem W. Ayoub, Stephen R. McCauley, Jill V. Hunter, Gerri Hanten, Xiaoqi Li, Zili D. Chu, Harvey S. Levin

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Abstract

The purpose of this study was to assess patterns of cortical development over time in children who had sustained traumatic brain injury (TBI) as compared to children with orthopedic injury (OI), and to examine how these patterns related to emotional control and behavioral dysregulation, two common post-TBI symptoms. Cortical thickness was measured at approximately 3 and 18 months post-injury in 20 children aged 8.2-17.5 years who had sustained moderate-to-severe closed head injury and 21 children aged 7.4-16.7 years who had sustained OI. At approximately 3 months post-injury, the TBI group evidenced decreased cortical thickness bilaterally in aspects of the superior frontal, dorsolateral frontal, orbital frontal, and anterior cingulate regions compared to the control cohort, areas of anticipated vulnerability to TBI-induced change. At 18 months post-injury, some of the regions previously evident at 3 months post-injury remained significantly decreased in the TBI group, including bilateral frontal, fusiform, and lingual regions. Additional regions of significant cortical thinning emerged at this time interval (bilateral frontal regions and fusiform gyrus and left parietal regions). However, differences in other regions appeared attenuated (no longer areas of significant cortical thinning) by 18 months post-injury including large bilateral regions of the medial aspects of the frontal lobes and anterior cingulate. Cortical thinning within the OI group was evident over time in dorsolateral frontal and temporal regions bilaterally and aspects of the left medial frontal and precuneus, and right inferior parietal regions. Longitudinal analyses within the TBI group revealed decreases in cortical thickness over time in numerous aspects throughout the right and left cortical surface, but with notable " sparing" of the right and left frontal and temporal poles, the medial aspects of both the frontal lobes, the left fusiform gyrus, and the cingulate bilaterally. An analysis of longitudinal changes in cortical thickness over time (18 months-3 months) in the TBI versus OI group demonstrated regions of relative cortical thinning in the TBI group in bilateral superior parietal and right paracentral regions, but relative cortical thickness increases in aspects of the medial orbital frontal lobes and bilateral cingulate and in the right lateral orbital frontal lobe. Finally, findings from analyses correlating the longitudinal cortical thickness changes in TBI with symptom report on the Emotional Control subscale of the Behavior Rating Inventory of Executive Function (BRIEF) demonstrated a region of significant correlation in the right medial frontal and right anterior cingulate gyrus. A region of significant correlation between the longitudinal cortical thickness changes in the TBI group and symptom report on the Behavioral Regulation Index was also seen in the medial aspect of the left frontal lobe.Longitudinal analyses of cortical thickness highlight an important deviation from the expected pattern of developmental change in children and adolescents with TBI, particularly in the medial frontal lobes, where typical patterns of thinning fail to occur over time. Regions which fail to undergo expected cortical thinning in the medial aspects of the frontal lobes correlate with difficulties in emotional control and behavioral regulation, common problems for youth with TBI. Examination of post-TBI brain development in children may be critical to identification of children that may be at risk for persistent problems with executive functioning deficits and the development of interventions to address these issues.

Original languageEnglish
Pages (from-to)267-276
Number of pages10
JournalInternational Journal of Developmental Neuroscience
Volume30
Issue number3
DOIs
StatePublished - May 1 2012

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Keywords

  • Behavior
  • Child
  • Cortical thickness
  • Emotion
  • Frontal lobes
  • Imaging
  • Longitudinal
  • Traumatic brain injury
  • Volumetrics

Cite this

Wilde, E. A., Merkley, T. L., Bigler, E. D., Max, J. E., Schmidt, A. T., Ayoub, K. W., McCauley, S. R., Hunter, J. V., Hanten, G., Li, X., Chu, Z. D., & Levin, H. S. (2012). Longitudinal changes in cortical thickness in children after traumatic brain injury and their relation to behavioral regulation and emotional control. International Journal of Developmental Neuroscience, 30(3), 267-276. https://doi.org/10.1016/j.ijdevneu.2012.01.003