Heterogeneous and nonlinear functional development of posterior parietal cortex

Abstract

Human cognitive problem solving skills undergo complex experience-dependent changes from childhood to adulthood, yet most neurodevelopmental research has focused on linear changes with age. Here we challenge this limited view, and investigate spatially heterogeneous and nonlinear neurodevelopmental profiles between childhood, adolescence, and young adulthood, focusing on three cytoarchitectonically distinct posterior parietal cortex (PPC) regions implicated in numerical problem solving: intraparietal sulcus (IPS), angular gyrus (AG), and supramarginal gyrus (SMG). Adolescents demonstrated better behavioral performance relative to children, but their performance was equivalent to that of adults. However, all three groups differed significantly in their profile of activation and connectivity across the PPC subdivisions. Activation in bilateral ventral IPS subdivision IPS-hIP1, along with adjoining anterior AG subdivision, AG-PGa, and the posterior SMG subdivision, SMG-PFm, increased linearly with age, whereas the posterior AG subdivision, AG-PGp, was equally deactivated in all three groups. In contrast, the left anterior SMG subdivision, SMG-PF, showed an inverted U-shaped profile across age groups such that adolescents exhibited greater activation than both children and young adults. Critically, greater SMG-PF activation was correlated with task performance only in adolescents. Furthermore, adolescents showed greater task-related functional connectivity of the SMG-PF with ventro-temporal, anterior temporal and prefrontal cortices, relative to both children and adults. These results suggest that nonlinear up-regulation of SMG-PF and its interconnected functional circuits facilitate adult-level performance in adolescents. Our study provides novel insights into heterogeneous age-related maturation of the PPC underlying cognitive skill acquisition, and further demonstrates how anatomically precise analysis of both linear and nonlinear neurofunctional changes with age is necessary for more fully characterizing cognitive development.