Frontostriatal White Matter Integrity Relations with ‘Cool’ and ‘Hot’ Self-Regulation Following Pediatric Traumatic Brain Injury

Traumatic brain injury (TBI) produces microstructural damage to white matter pathways connecting neural structures that support top-down control of prefrontal regions over striatal regions involved in self-regulation (SR). Frontostriatal white matter can be separated into dorsal and ventral pathways, and has been linked to cognitive (‘cool’) and emotional (‘hot’) types of SR. The aims of the current study were to (1) evaluate the impact of pediatric TBI, age at injury, and sex on the integrity of dorsal (dorsal anterior cingulate, ventrolateral prefrontal cortex, and dorsolateral prefrontal cortex to caudate) and ventral (medial orbitofrontal cortex and rostral anterior cingulate cortex to nucleus accumbens) frontostriatal pathways assessed 2 months after injury, and on the cool and hot self-regulatory behaviors they are believed to support; and (2) investigate whether the impact of TBI on cool and hot self-regulatory behaviors at 6 months after injury was mediated by the integrity of dorsal and ventral frontostriatal pathways, respectively. The current study used archival data from a prospective, longitudinal study consisting of 84 children and adolescents with TBI (24 uncomplicated mild, 30 complicated mild, 6 moderate, 24 severe) and 55 typically developing (TD) children, aged 8-15. Children with TBI were classified into uncomplicated mild TBI (mTBI), and more severe TBI (sTBI; complicated mild, moderate, and severe TBI). Diffusion tensor tractography was used to map dorsal and ventral white matter pathways. Measures of cool SR included focused and sustained attention (Continuous Performance Task omission errors and reaction time by block), and parent reported attention via the Strengths and Weaknesses of ADHD and Normal Behavior scale. Hot SR measures included risk-taking via Balloon Analogue Risk Task pumps and emotional control via the Behavior Rating in Executive Functioning parent report. Multivariate general linear models (GLM) showed that, in comparison to TD children, children with sTBI had lower fractional anisotropy (FA) in dorsal pathways connecting bilateral dorsal anterior cingulate to caudate and the ventral pathway linking the right medial orbitofrontal cortex to nucleus accumbens. Children with sTBI also had significantly greater difficulties than healthy children with parent reported cool and hot SR, but not on task performance of SR (focused or sustained attention and risk taking). Focused attention, risk taking, and emotional control were significantly correlated with FA of specific dorsal and ventral pathways. Although frontostriatal white matter integrity predicted both cool and hot SR difficulties, only the effect of TBI on focused attention 6 months after injury was mediated by dorsal pathway integrity 2 months post-TBI. Frontostriatal pathways may serve as a biomarker to identify children at risk for specific SR difficulties as well as to assess response to interventions targeted at cool or hot SR. Findings can guide future research on dorsal and ventral neural correlates of SR difficulties following pediatric TBI, and can inform theoretical and clinical understanding of attention and frontostriatal neural circuitry in broader neurodevelopmental populations.