Decomposing the role of alpha oscillations during brain maturation

Abstract

Childhood and adolescence are critical stages of the human lifespan, in which fundamental neural reorganizational processes take place. A substantial body of literature investigated neurophysiological changes during brain maturation by focusing on the most dominant feature of the human EEG signal: the alpha oscillation. Ambiguous results were reported for the developmental trajectory of the power of the alpha oscillation. Simulations in this study show that conventional measures of alpha power are confounded by various factors and need to be decomposed into periodic and aperiodic components, which represent distinct underlying brain mechanisms. It is therefore unclear how each part of the signal relates to changes during brain maturation. Using multivariate Bayesian generalized linear mixed models, we examined aperiodic and periodic parameters of alpha activity in the largest openly available pediatric dataset (N=2529, age range 5-21 years) and replicated these findings in a preregistered analysis of an independent validation sample (N=369, age range 6-21yrs). First, the well documented age-related decrease in total alpha power was replicated. However, when controlling for the aperiodic signal component, our findings provide strong evidence for a reversed developmental trajectory of the periodic alpha power, whereas the aperiodic signal components, slope and offset, decreased. Consequently, earlier interpretations on age related changes of alpha power need to be fundamentally reconsidered, incorporating changes in the aperiodic signal. The interpretation of decreased total alpha power as elimination of active synapses rather links to decreases in the aperiodic intercept. Instead, additional analyses of diffusion tensor imaging data indicate that the maturational increase in periodic alpha power is related to increased thalamocortical connectivity. Functionally, our results suggest that increased thalamic control of cortical alpha power is linked to improved attentional performance during brain maturation.