Altered resting‐state functional connectivity within the developing social brain after pediatric traumatic brain injury

Abstract

Traumatic brain injury (TBI) in childhood and adolescence can interrupt expected development, compromise the integrity of the social brain network (SBN) and impact social skills. Yet, no study has investigated functional alterations of the SBN following pediatric TBI. This study explored functional connectivity within the SBN following TBI in two independent adolescent samples. First, 14 adolescents with mild complex, moderate or severe TBI and 16 typically developing controls (TDC) underwent resting-state functional magnetic resonance imaging 12-24 months post-injury.Region of interest analyses were conducted to compare the groups' functional connectivity using selected SBN seeds. Then, replicative analysis was performed in an independent sample of adolescents with similar characteristics (9 TBI, 9 TDC). Results were adjusted for age, sex, socioeconomic status and total gray matter volume, and corrected for multiple comparisons. Significant between-group differences were detected for functional connectivity in the dorsomedial prefrontal cortex and left fusiform gyrus, and between the left fusiform gyrus and left superior frontal gyrus, indicating positive functional connectivity for the TBI group (negative for TDC). The replication study revealed group differences in the same direction between the left superior frontal gyrus and right fusiform gyrus. This study indicates that pediatric TBI may alter functional connectivity of the social brain. Frontal-fusiform connectivity has previously been shown to support affect recognition and changes in the function of this network could relate to more effortful processing and broad social impairments.

Abnormal Functional Network Topology and its Dynamics during Sustained Attention Processing Significantly Implicate Post-TBI Attention Deficits in Children

“…Fusiform gyrus is part of the temporal and occipital lobes, which has been found to be a key structure for high-order visual (such as face, body and high special frequency objects) and imagery processing [68, 69]. Functional brain activation and connectivity studies in children with TBI have also reported fusiform gyrus-related abnormalities, such as reduced activations during sustained attention processing [18], significantly increased activation during working memory processing [7], and altered functional connectivity between fusiform gyrus and frontal lobe during resting state [21]. On the other hand, studies have demonstrated significant involvement of the fusiform gyrus in severe psychopathology, especially psychosocial and emotional dysregulation and thought problems in patients with Major Depression Disorder [70, 71], Schizophrenia [72, 73], and other mental disorders [74, 75].…”

“…Resting-state fMRI (rs-fMRI) studies in TBI have also reported inconsistent results. Relative to matched controls, children with chronic TBI have been found to have reduced functional connectivity (FC) between caudate and motor network [20], increased FC between frontal and fusiform gyrus [21], or reduced FC between rostral anterior cingulate cortex and amygdala [22]. In addition, graph theoretical technique (GTT)-based rs-fMRI studies have reported systems-level topological alterations in adults with TBI, relative to controls [23].…”

Abnormal Functional Network Topology and Its Dynamics during Sustained Attention Processing Significantly Implicate Post-TBI Attention Deficits in Children

“…Resting-state fMRI (rs-fMRI) studies in TBI have also reported inconsistent results. Relative to matched controls, children with chronic TBI have been found to have reduced functional connectivity (FC) between caudate and motor network [24], increased FC between the frontal and fusiform gyrus [25], or reduced FC between rostral anterior cingulate cortex and amygdala [26]. In addition, graph theoretical technique (GTT)-based rs-fMRI studies have reported system-level topological alterations in adults with TBI, relative to controls [27].…”

Early Brain Injury and Adaptive Functioning in Middle Childhood: The Mediating Role of Pragmatic Language

“…Disruption to any of these neurobiological processes can alter the development of functional and structural connections that are necessary for complex adaptive behaviors. Indeed, pediatric TBI has been linked to white matter alterations in the corpus callosum (Ewing-Cobbs et al, 2008) via neural vasculature changes (Wendel et al, 2019) as well as altered functional connectivity of social processing networks (Tuerk et al, 2019) years after injury, suggesting that pediatric TBI contributes to lasting alterations in behaviorally relevant brain structure and function.…”