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 accompanying neurophysiological changes, focusing on the most dominant feature of the human EEG signal: the alpha oscillation. Recent developments in EEG signal-processing 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 changes during brain maturation. Using multivariate Bayesian generalized linear models, we examined aperiodic and periodic parameters of alpha activity in the largest openly available pediatric dataset (N=2529, age 5-22 years) and replicated these findings in a preregistered analysis of an independent validation sample (N=369, age 6-22 years). First, the welldocumented age-related decrease in total alpha power was replicated. However, when controlling for the aperiodic signal component, our findings provided strong evidence for an age-related increase in the aperiodic-adjusted alpha power. As reported in previous studies, also relative alpha power revealed a maturational increase, yet indicating an underestimation of the underlying relationship between periodic alpha power and brain maturation. The aperiodic intercept and slope decreased with increasing age and were highly correlated with total alpha power. Consequently, earlier interpretations on age-related changes of total alpha power need to be reconsidered, as elimination of active synapses rather links to decreases in the aperiodic intercept. Instead, analyses of diffusion tensor imaging data indicate that the maturational increase in aperiodic-adjusted 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.

Developmental changes in individual alpha frequency: Recording EEG data during public engagement events

“…This is an important distinction, because unadjusted alpha power (i.e., including aperiodic signal) is likely to reflect a mixture of different physiological processes and may be misleading when used to link alpha rhythms to specific cognitive states. For example, we were able to replicate previous findings of a decreased aperiodic slope and intercept with increasing age (Tröndle et al, 2022;Cellier et al, 2021, Cesnaite et al, 2023. The markedly steeper slope in our 6-21 year olds (see Fig 3C) relative to both the 22-36 and 37-76 year olds may reflect a higher prevalence of low-, relative to high-frequency activity in the youngest participants, increased neural "noise" in older age (McIntosh et al, 2010), and/or developmental changes in skull thickness.…”

“…For the sake of simplicity, and to facilitate testing of a large number of people very quickly, we also decided not to collect additional demographic or clinical information from the participants, other than their age and gender. There was no indication that peak alpha frequency or power differed between male and female participants in our dataset, although differences between groups in one, or both, of these measures have been described in previous studies (Cragg et al, 2011;Tröndle et al, 2022). Due to the open nature of our recruitment process, we may have included participants, by design, whose alpha oscillations may be classed as "atypical" relative to the healthy population.…”

“…Peak occipital alpha frequency is typically slower in young children, at around 6 Hz, and peaking at around 10 Hz in older children and adults (Marshall et al, 2002). The total power of this peak alpha oscillation has also been shown across many studies to decrease with advancing age, both during childhood (Tröndle et al, 2022) and into older adulthood (Whitford et al, 2007). This may reflect a change in white matter integrity and/or loss of grey matter volume throughout the lifespan (Grandy et al, 2013).…”

“…However, a more recent analytic approach, of dissociating the periodic from aperiodic EEG signal, has shown that older adults may simply experience more broadband 1/f 'noise' in their visual systems (Voytek et al, 2015), which may have confounded previous analyses of IAF. In an analysis of 2529 people aged 5-22 years old, Tröndle et al (2022) found that, after correcting for aperiodic signal, alpha power may in fact increase rather than decrease during childhood and adolescence, and decrease between 60-79 years old (Cesnaite et al, 2023). We aimed to address these questions in a large sample of participants.…”

Human sensorimotor beta event characteristics and aperiodic signal are highly heritable

“…The rhythmic and aperiodic components are important to disentangle as they are probably generated by different mechanisms. Aperiodic signal is believed to represent excitation-inhibition balance (Gao et al, 2017) and is modulated, e.g ., by brain maturation (McSweeney et al, 2021; Hill et al, 2022; Tröndle et al, 2022), aging (Voytek et al, 2015; Wilson et al, 2022) and several neurological and psychiatric conditions (Molina et al, 2020; Ostlund et al, 2021; Semenova et al, 2021).…”