Resting state periodic and aperiodic brain oscillations from birth to preschool years: Aperiodic maturity predicts developmental course

Abstract

The non-invasive assessment of resting-state (RS) neural activity via electrophysiology provides information on brain function and brain health. Our understanding of RS neural activity in older children and adults is limited by our poor understanding of the maturation of RS activity (oscillatory and non- oscillatory) from infancy to preschool ages. The present study used MEG with source imaging and an adapted Dark Room eyes-open task to assess oscillatory and non-oscillatory RS activity. 107 typically developing children 2 to 68 months were enrolled. For the Dark-Room eyes-open task, each child alternated between viewing an Inscapes video without audio for 20s and then resting with their eyes open for 30s in total darkness. This was repeated for 6 cycles. Whole-brain RS activity maps were computed using Minimum Norm Estimates, with RS power spectra divided into estimates of periodic measures (dominant frequency and power) and aperiodic measures (the exponent - slope of the 1/f function; the offset - vertical displacement of the 1/f function). An infant dominant peak was observed more often in the Dark-Room (94% of children) than in the Video-On condition (83% of children). The Dark-Room condition elicited a 36% increase in dominant oscillation activity than the Video-On condition. The maturation of the parietal-occipital periodic dominant frequency increased non-linearly as a function of age. The maturation of aperiodic measures decreased nonlinearly as a function of age, with aperiodic measures as well as their maturation rate differing across the brain. Finally, more mature aperiodic values predicted better adaptive behaviors and daily living skills. Present findings demonstrate that (1) the use of an appropriate Dark-Room eyes-open task provides measures of young child RS periodic activity with excellent SNR, (2) an understanding of the development of infant RS activity is best achieved via obtaining measures in brain source space in order to detect regional differences in aperiodic activity, and (3) a more mature aperiodic value predicts higher developmental behavior scores.