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. 2021 Dec 23:12:734055.
doi: 10.3389/fneur.2021.734055. eCollection 2021.

A Preliminary DTI Tractography Study of Developmental Neuroplasticity 5-15 Years After Early Childhood Traumatic Brain Injury

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A Preliminary DTI Tractography Study of Developmental Neuroplasticity 5-15 Years After Early Childhood Traumatic Brain Injury

Elisabeth A Wilde et al. Front Neurol. .

Abstract

Plasticity is often implicated as a reparative mechanism when addressing structural and functional brain development in young children following traumatic brain injury (TBI); however, conventional imaging methods may not capture the complexities of post-trauma development. The present study examined the cingulum bundles and perforant pathways using diffusion tensor imaging (DTI) in 21 children and adolescents (ages 10-18 years) 5-15 years after sustaining early childhood TBI in comparison with 19 demographically-matched typically-developing children. Verbal memory and executive functioning were also evaluated and analyzed in relation to DTI metrics. Beyond the expected direction of quantitative DTI metrics in the TBI group, we also found qualitative differences in the streamline density of both pathways generated from DTI tractography in over half of those with early TBI. These children exhibited hypertrophic cingulum bundles relative to the comparison group, and the number of tract streamlines negatively correlated with age at injury, particularly in the late-developing anterior regions of the cingulum; however, streamline density did not relate to executive functioning. Although streamline density of the perforant pathway was not related to age at injury, streamline density of the left perforant pathway was significantly and positively related to verbal memory scores in those with TBI, and a moderate effect size was found in the right hemisphere. DTI tractography may provide insight into developmental plasticity in children post-injury. While traditional DTI metrics demonstrate expected relations to cognitive performance in group-based analyses, altered growth is reflected in the white matter structures themselves in some children several years post-injury. Whether this plasticity is adaptive or maladaptive, and whether the alterations are structure-specific, warrants further investigation.

Keywords: brain development; diffusion tensor imaging; neuroplasticity; pediatric traumatic brain injury; structural neuroimaging; tractography.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Tractography of the cingulum bundle (CB) and perforant pathway (PP). Directional color maps of the right CB (A) and PP (B) are shown on the sagittal (left) and axial (right) planes, overlaid by a 3D cortical isosurface. The colors represent the 3D fiber rendering direction; red, left-to-right (along the x-axis); green, anterior-to-posterior (along the y-axis); and blue, superior-to-inferior (along the z-axis). The bottom panel (C) demonstrates the spatial relationship of the CB (orange) and PP (blue), which are overlaid on the subject's T1-weighted image. The right side of the brain is depicted in the left side of the screen in the axial views.
Figure 2
Figure 2
Delination of regions-of-interest for the CB and PP on the FA color map. Fiber tracts of cingulum bundle (CB) and perforant pathway (PP) are isolated via regions of interest (ROIs). Two ROIs of the CB are selected on the coronal plane. The first ROI of the CB (A1) is selected at the level of the fornix body four slices posterior to the second ROI (A2), which is selected at the level of the fornix column. Three ROIs are selected on the coronal plane for the PP. The first ROI is selected on the most anterior slice of the splenium of the corpus callosum (B1), the second ROI of PP is selected three slices anterior to the first (B2), and the third ROI is selected six slices anterior to the first ROI (B3). The right side of the brain is depicted in the left side of the screen. The colors represent the 3D fiber rendering direction; red, left-to-right (along the x-axis); green, anterior-to-posterior (along the y-axis); and blue, superior-to-inferior (along the z-axis). FA, fractional anisotropy.
Figure 3
Figure 3
Executive functioning and CB tractography in typically-developing children and children with traumatic brain injury. Executive functioning is reflected by scaled scores (mean = 10 ± 3) on the color naming (CN), word reading (WR), inhibition (IN), and interference/switching (IS) trials of the Delis-Kaplan Executive Function System (D-KEFS) Color-Word Interference Test (CWIT). CB, cingulum bundle; GCS, Glasgow Coma Scale score.
Figure 4
Figure 4
Verbal memory and PP tractography in typically-developing children and children with traumatic brain injury. Verbal memory performance is measured by T-scores (mean = 50 ± 10) on Trials 1–5 (T1–5) and z-scores (mean = 0.0 ± 1.0) on short-delay free recall (SDFR) and long-delay free recall (LDFR) trials of the California Verbal Learning Test (CVLT). PP, perforant pathway; GCS, Glasgow Coma Scale score.
Figure 5
Figure 5
Relation between white matter integrity of the CB and age at brain injury. In the top panel, younger age at injury is associated with increased fractional anisotropy (FA) of the cingulum bundle (CB), but not the perforant pathway (PP; not shown). Younger age at injury is also associated with an increased number of streamline points for the right CB (middle panel) and the left CB (bottom panel) but not the PP (not shown).

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