The emergence of age‐dependent social cognitive deficits after generalized insult to the developing brain: A longitudinal prospective analysis using susceptibility‐weighted imaging

Abstract

Childhood and adolescence are critical periods for maturation of neurobiological processes that underlie complex social and emotional behavior including Theory of Mind (ToM). While structural correlates of ToM are well described in adults, less is known about the anatomical regions subsuming these skills in the developing brain or the impact of cerebral insult on the acquisition and establishment of high-level social cognitive skills. This study aimed to examine the differential influence of age-at-insult and brain pathology on ToM in a sample of children and adolescents with traumatic brain injury (TBI). Children and adolescents with TBI (n = 112) were categorized according to timing of brain insult: (i) middle childhood (5-9 years; n = 41); (ii) late childhood (10-11 years; n = 39); and (iii) adolescence (12-15 years; n = 32) and group-matched for age, gender, and socioeconomic status to a typically developing (TD) control group (n = 43). Participants underwent magnetic resonance imaging including a susceptibility-weighted imaging (SWI) sequence 2-8 weeks postinjury and were assessed on a battery of ToM tasks at 6- and 24-months after injury. Results showed that for adolescents with TBI, social cognitive dysfunction at 6- and 24-months postinjury was associated with diffuse neuropathology and a greater number of lesions detected using SWI. In the late childhood TBI group, we found a time-dependent emergence of social cognitive impairment, linked to diffuse neuropathology. The middle childhood TBI group demonstrated performance unrelated to SWI pathology and comparable to TD controls. Findings indicate that the full extent of social cognitive deficits may not be realized until the associated skills reach maturity. Evidence for brain structure-function relationships suggests that the integrity of an anatomically distributed network of brain regions and their connections is necessary for the acquisition and establishment of high-level social cognitive skills.

Recovery of Working Memory Following Pediatric Traumatic Brain Injury: A Longitudinal Analysis

“…This slower rate of development appeared to underlie the apparent widening over time of performance levels between injury groups for the younger children. This pattern may be related to the notion of deficits that may emerge later in children injured at an earlier age, first posited by Goldman-Rakic and colleagues (Goldman, 1971, 1974; Goldman & Alexander, 1977; Goldman, Rosvold, & Mishkin, 1970), with more recent studies providing support for this notion (Chapman et al, 2010; Ewing-Cobbs, Prasad, et al, 2004; Ryan et al, 2015). With regard to the current study, given the maintenance and manipulation requirements of the WM measures utilized, and the finding that there are significant developmental changes in maintenance and manipulation of information in school-aged children and adolescents (Crone, Wendelken, Donohue, Van Leijenhorst, & Bunge, 2006), it is not surprising that children in the younger age at injury groups demonstrated the slowest rate of development resulting in discrepancies in levels of performance that appeared to increase over time.…”

Longitudinal outcome and recovery of social problems after pediatric traumatic brain injury (TBI): Contribution of brain insult and family environment

“…At the simplest level, social problems may increase with time as children fail to adapt to the limitations associated with their injuries, such as reduced cognitive and academic skills or physical and speech impairments. Secondly, it may that diffuse axonal injury commonly associated with severe TBI disrupts structural connectivity within distributed neural networks implicated in social functioning, which in turn contributes to a failure to make age‐appropriate gains in skills that are not yet acquired or undergoing rapid maturation at the time of injury (Anderson et al, 2009; Ryan et al, 2015). Although the significant relationship between social problems and micro‐hemorrhagic lesions in the corpus callosum lesions offers broad support for this hypothesis, it is noteworthy that the overall injury model was not statistically significant.…”

Social dysfunction after pediatric traumatic brain injury: A translational perspective

“…In addition, new evidence suggests that this technique has potential to unlock early prognostic biomarkers that may add predictive value for social affective outcomes. In a recent longitudinal study that examined prospective links between social cognition and SWI, children with TBI underwent MRI including SWI sequences at 2–8 weeks post injury and subsequently completed a social cognitive test battery at 6- and 24-months post injury (Ryan et al, 2015b; Ryan et al, 2014). In line with previous evidence for heterogeneity of brain lesions in children with TBI (Bigler et al, 2013a), SWI revealed a highly variable and anatomically distributed pattern of microhemorrhagic lesions across children in the sample (Beauchamp et al, 2013).…”

“…In a subsequent sub-study that examined the relation between SWI lesions and higher level aspects of ToM, findings showed that the effect of SWI lesions on ToM may interact with the child’s developmental stage, such that more diffuse acute micro-bleeds may contribute to the time-dependent emergence of social cognitive dysfunction particularly during adolescence (Ryan et al, 2015b). …”