Abstract

During adolescence, the integration of specialized functional brain networks related to cognitive control continues to increase. Slow frequency oscillations (4–10 Hz) have been shown to support cognitive control processes, especially within prefrontal regions. However, it is unclear how neural oscillations contribute to functional brain network development and improvements in cognitive control during adolescence. To bridge this gap, we employed magnetoencephalography (MEG) to explore changes in oscillatory power and phase coupling across cortical networks in a sample of 68 adolescents and young adults. We found a redistribution of power from lower to higher frequencies throughout adolescence, such that delta band (1–3 Hz) power decreased, whereas beta band power (14–16 and 22–26 Hz) increased. Delta band power decreased with age most strongly in association networks within the frontal lobe and operculum. Conversely, beta band power increased throughout development, most strongly in processing networks and the posterior cingulate cortex, a hub of the default mode (DM) network. In terms of phase, theta band (5–9 Hz) phase-locking robustly decreased with development, following an anterior-to-posterior gradient, with the greatest decoupling occurring between association networks. Additionally, decreased slow frequency phase-locking between frontolimbic regions was related to decreased impulsivity with age. Thus, greater decoupling of slow frequency oscillations may afford functional networks greater flexibility during the resting state to instantiate control when required.

Highlights

  • The transition from adolescence to adulthood is characterized by significant enhancements in brain function, supporting increased cognitive control and normative decreases in impulsivity [1,2]

  • The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript

  • Developmental task-based functional magnetic resonance imaging studies indicate that core regions supporting cognitive control are engaged in adolescence during cognitive tasks, but their blood oxygen level–dependent (BOLD) signal activation [3,4] and connectivity with other brain regions continue to increase into adulthood [5,6,7]

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Summary

Introduction

The transition from adolescence to adulthood is characterized by significant enhancements in brain function, supporting increased cognitive control and normative decreases in impulsivity [1,2]. Developmental task-based functional magnetic resonance imaging (fMRI) studies indicate that core regions supporting cognitive control (e.g., anterior cingulate cortex [ACC] and anterior insula [aIns]) are engaged in adolescence during cognitive tasks, but their blood oxygen level–dependent (BOLD) signal activation [3,4] and connectivity with other brain regions continue to increase into adulthood [5,6,7]. Developmental resting-state fMRI (rs-fMRI) studies analyzing whole-brain connectivity patterns parallel this principle, such that the organization of functional brain networks is relatively stable by childhood [7,9,10], while integration (between-network functional connectivity) continues to refine well into late adolescence and early adulthood, supporting improvements in cognitive control [7]. Because fMRI is not sensitive to this timescale of oscillation, magnetoencephalography (MEG) serves as a complementary tool to understand resting-state network development by allowing us to explore this relatively faster oscillatory range

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