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

Abstract

Executive function (EF) is essential for humans to effectively engage in cognitively demanding tasks. In adults, EF is subserved by frontoparietal regions in the multiple demand (MD) network, which respond to various cognitively demanding tasks. However, children initially show poor EF and prolonged development. Do children recruit the same network as adults? Is it functionally and connectionally distinct from adjacent language cortex, as in adults? And is this activation or connectivity dependent on age or ability? We examine task-dependent (spatial working memory and passive language tasks) and resting state functional data in 44 adults (18-38 years, 68% female) and 37 children (4-12 years, 35% female). Subject-specific functional regions of interest (ss-fROIs) show bilateral MD network activation in children. In both children and adults, these MD ss-fROIs are not recruited for linguistic processing and are connectionally distinct from language ss-fROIs. While MD activation was lower in children than in adults (even in motion- and performance-matched groups), both showed increasing MD activation with better performance, especially in right hemisphere ss-fROIs. We observe this relationship even when controlling for age, cross-sectionally and in a small longitudinal sample of children. These data suggest that the MD network is selective to cognitive demand in children, is distinct from adjacent language cortex, and increases in selectivity as performance improves. These findings show that neural structures subserving domain-general EF emerge early and are sensitive to ability even in children. This research advances understanding of how high-level human cognition emerges and could inform interventions targeting cognitive control.

Significance statement:

This 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, children’s 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 dysfunction are necessary for effective early identification, prevention, and intervention efforts for individuals struggling with deficits in processing cognitive demand.