Individual variability in performance reflects selectivity of the multiple demand network among children and adults.

Abstract

Executive function (EF) is essential for human cognition, allowing individuals to effectively engage in cognitively demanding tasks. In adults, EF is subserved by a set of frontoparietal brain regions (termed the multiple demand (MD) network) which show robust responses to a wide variety of cognitively demanding tasks (i.e., domain-general) and reflect cognitive effort exerted on the task. But while essential, children initially show poor EF skills with prolonged development of these skills. Do children recruit the same network as adults? Is it functionally and connectionally distinct from adjacent language cortex as it is in adults? And is this activation or connectivity dependent on age or on the individuals EF task performance? We scanned 44 adults and 37 children ages 4-12 years for two separate tasks (MD spatial working memory task and passive language task) and a resting-state fMRI scan. Because motion is a concern in child samples, we asked a subset of adult subjects to participate in additional "wiggly" scans of the MD task and to move slightly during those scans. We defined subject-specific functional regions of interest (ss-fROIs) and found bilateral activation of the MD network in children. In both children and adults, these ss-fROIs are not recruited for linguistic processing and are also connectionally distinct from language ss-fROIs. MD activation in children was lower than that observed in adults, but it was unrelated to motion as evidenced by motion-matched comparisons between children and adult groups and by repeated measures comparisons within the adult group. Right-lateralized ss-fROIs showed increasing load-based MD responses that were robustly associated with performance, demonstrated both cross-sectionally and in a subset of children scanned longitudinally about one year apart. These data suggest that even in young children the MD network is selective to cognitive demand, is distinct from adjacent cortex, and increases in its selectivity as a child improves their EF skills, independently of age. Overall, these findings show that neural structures subserving domain-general EF emerge early and are sensitive to ability in both children and adults. This research advances our understanding of how high-level human cognition emerges and can inform interventions targeting cognitive control. Significance statementThis study provides evidence that young children already show differentiated brain network organization between regions that process cognitive demand and language. These data support the hypothesis that children recruit a similar network as adults to process cognitive demand, and despite immature characteristics, childrens selectivity looks more adult-like as their executive function ability increases. Mapping early stages of network organization furthers our understanding of the functional architecture underlying domain-general executive function. Determining typical variability underlying cognitive processing across developmental periods helps establish a threshold for executive dysfunction. Early markers of risk are necessary for effective early identification, prevention, and intervention efforts for individuals struggling with deficits in processing cognitive demand.