Shifting gradients of macroscale cortical organization mark the transition from childhood to adolescence

Abstract

The transition from childhood to adolescence is marked by pronounced shifts in brain structure and function that coincide with the development of physical, cognitive, and social abilities. Prior work in adult populations has characterized the topographical organization of cortex, revealing macroscale functional gradients that extend from unimodal (somato/motor and visual) regions through the cortical association areas that underpin complex cognition in humans. However, the presence of these core functional gradients across development as well as their maturational course have yet to be established. Here, leveraging 378 resting-state fMRI scans from 190 healthy individuals aged 6-17 years, we demonstrate that the transition from childhood to adolescence is reflected in the gradual maturation of gradient patterns across the cortical sheet. In children, the overarching organizational gradient is anchored within unimodal cortex, between somato/motor and visual territories. Conversely, in adolescence the principal gradient of connectivity transitions into an adult-like spatial framework, with the default network at the opposite end of a spectrum from primary sensory and motor regions. The observed gradient transitions are gradually refined with age, reaching a sharp inflection point in 13- and 14-year-olds. Functional maturation was nonuniformly distributed across cortical networks. Unimodal networks reached their mature positions early in development, while association regions, in particular medial prefrontal cortex, reached a later peak during adolescence. These data reveal age-dependent changes in the macroscale organization of cortex and suggest the scheduled maturation of functional gradient patterns may be critically important for understanding how cognitive and behavioral capabilities are refined across development. SignificanceHuman abilities and behavior change dramatically across development, emerging from a cascade of hierarchical changes in brain circuitry. Here, we describe age-dependent shifts in the macroscale functional organization of cortex in childhood and adolescence. The characterization of functional connectivity patterns in children revealed an overarching organizational framework anchored within unimodal cortex, between somato/motor and visual regions. Conversely, in adolescents we observed a transition into an adult-like gradient that situates the default network at the opposite end of a spectrum from primary sensory and motor regions. This spatial framework emerged gradually with age, reaching a sharp inflection point at the transition from childhood to adolescence. These data reveal the presence of a developmental change from a functional motif first dominated by the distinction between sensory and motor systems, and then balanced through interactions with later-maturing aspects of association cortex that support more abstract cognitive functions.