Spontaneous cortical MEG activity undergoes unique age- and sex-related changes during the transition to adolescence

Abstract

Background: While numerous studies have examined the developmental trajectory of task-based neural oscillations during childhood and adolescence, far less is known about the evolution of spontaneous cortical activity during this time period. Likewise, many studies have shown robust sex differences in task-based oscillations during this developmental period, but whether such sex differences extend to spontaneous activity is not understood. Methods: Herein, we examined spontaneous cortical activity in 111 typically-developing youth (ages 9–15 years; 55 male). Participants completed a resting state magnetoencephalographic (MEG) recording and a structural MRI. MEG data were source imaged and the power within five canonical frequency bands (delta, theta, alpha, beta, gamma) was computed. The resulting power spectral density maps were analyzed via vertex-wise ANCOVAs to identify spatially-specific effects of age, sex, and their interaction. Results: We found robust increases in power with age in all frequencies except delta, which decreased over time, with findings largely confined to frontal cortices. Sex effects were distributed across frontal and temporal regions; females tended to have greater delta and beta power, whereas males had greater alpha. Importantly, there was a significant age-by-sex interaction in theta power, such that males exhibited decreasing power with age while females showed increasing power with age in the bilateral superior temporal cortices. Discussion: These data suggest that the strength of spontaneous activity undergoes robust change during the transition from childhood to adolescence (i.e., puberty onset), with intriguing sex differences in some cortical areas. Future developmental studies should probe task-related oscillations and spontaneous activity in parallel.

Decreased resting-state alpha peak frequency in children and adolescents with fetal alcohol spectrum disorders or prenatal alcohol exposure

“…However, the relationship is typically linked to advanced pubertal stage in males ( Howsley and Levita, 2018 ). In a recent study, males (9–15 years of age) had higher alpha power in the left dorsal prefrontal cluster ( Ott et al, 2021 ) along with frequency specific changes in global normalized power ( Candelaria-Cook et al, 2022 ). We also did not find any evidence of a PAE and sex interaction.…”

Eyes-closed versus eyes-open differences in spontaneous neural dynamics during development

“…Multiple studies have documented that, across the entire lifespan, younger compared to older subjects tend to show stronger oscillatory power in lower frequency bands and weaker power in the higher frequency bands, as measured by both EEG ( Michels et al, 2013 ; Segalowitz et al, 2010 ) and MEG ( Gómez et al, 2013 ; Hoshi and Shigihara, 2020 ; Hunt et al, 2019 ; Uhlhaas et al, 2010 ). A recent study using MEG observed this age-related effect specifically within a peri-adolescent age range ( Ott et al, 2021 ). Consistent with previous work, this study also demonstrated that these changes occur predominantly in association cortices which show robust structural changes during the pubertal transition period in particular ( Gogtay et al, 2004 ; Wierenga et al, 2014 ) relative to low-level sensory regions.…”

“…Each MEG dataset was individually corrected for head motion and subjected to noise reduction using the signal space separation method with temporal extension (tSSS; MaxFilter v 2.2; correlation limit: 0.950; correlation window duration: 6 s; Taulu and Simola, 2006 ). The preprocessing of MEG data was conducted in Brainstorm ( Tadel et al, 2019 ) and was modeled after that of previous studies ( Niso et al, 2019 ; Ott et al, 2021 ). A high pass filter of 0.3 Hz and notch filters at 60 Hz and its harmonics were applied.…”

“…Further, MEG possesses exquisite spatial (~3–5 mm; Baillet, 2017 ; Wilson et al, 2016 ) and temporal (1 ms) precision, which enables a multispectral approach whereby neural activity at different frequencies can be quantified and characterized discretely. Importantly, MEG is noninvasive and silent, making it ideal for the assessment of resting brain activity in developing youth ( Hoshi and Shigihara, 2020 ; Ott et al, 2021 ), who may be particularly sensitive to the noise and restricted environment of MRI data collection.…”

Longitudinal changes in the neural oscillatory dynamics underlying abstract reasoning in children and adolescents

“…Given the smaller, somewhat imbalanced sample size, we were limited in the breadth and depth of analyses we were able to perform, including explorations of sex-specific changes in neural oscillatory dynamics over time. Several recent studies have shown unique trajectories of development among male versus female youths in investigations of both task-based ( Fung et al, 2021 ; Taylor et al, 2021 , 2020 ) and spontaneous cortical dynamics ( Ott et al, 2021 ). Future longitudinal studies should aim to acquire data from larger samples of equally-balanced male and female youths to further disentangle the unique trajectories of fluid reasoning maturation in this dynamic period of development.…”