Developmental interactions between oscillatory and spontaneous neural activity support improvements in inhibitory control from adolescence into adulthood

Abstract

Adolescence is a critical period of development marked by improvements in cognitive control driven by maturation of executive brain systems. Neural mechanisms supporting inhibitory control (the ability to suppress a prepotent response in favor of generating a goal-directed response) mature into adulthood in parallel with refinements in frequency-specific neural oscillations and broadband spontaneous activity, supporting more accurate and reliable performance on response inhibition tasks, such as the antisaccade oculomotor task. Prior work has established that the maturation of neural circuitry contributes to age-related decreases in spontaneous activity, supporting higher-fidelity transmission of task-relevant activity, such as frequency-specific neural oscillations, which are crucial for antisaccade performance. Using longitudinal electroencephalography (EEG) data from 146 participants (72 F, ages 10-34, 253 total sessions) collected while participants performed an antisaccade task, we sought to understand the interplay between frontal oscillatory and spontaneous activity during cognitive processing and how it supports developmental improvements in inhibitory control. We found that spontaneous activity decreased developmentally during the preparation of an inhibitory response, and that this was associated with reduced trial-to-trial variability in response latency, indicating that reductions in spontaneous activity may increase the reliability of inhibitory control processing. Furthermore, performance-related decreases in broadband spontaneous activity were associated with the suppression of preparatory high-beta oscillations in an age-dependent manner, such that this relationship became more pronounced through development. Together, these results illustrate how developmental enhancements in the coordination of frequency-specific oscillations and spontaneous activity during inhibitory response preparation support developmental improvements in inhibitory control, providing a potential mechanism through which inhibitory control becomes more accurate and reliable from adolescence into adulthood.