The maturation of aperiodic EEG activity across development reveals a progressive differentiation of wakefulness from sleep

• Published in: NeuroImage (Orlando, Fla.) Fla.), 2023-08, Vol.277, p.120264-120264, Article 120264
• Main Authors: Favaro, Jacopo, Colombo, Michele Angelo, Mikulan, Ezequiel, Sartori, Stefano, Nosadini, Margherita, Pelizza, Maria Federica, Rosanova, Mario, Sarasso, Simone, Massimini, Marcello, Toldo, Irene
• Format: Article
• Language: English
• Subjects: 1/f noise; Adults; Age; Anatomy; Aperiodic activity; Brain architecture; Child development; Childrens health; Cognitive ability; EEG; Functional brain development; Maturation; Neurophysiology; Pediatrics; Rhythm; Sleep; Sleep and wakefulness; Structure-function relationships; Vigilance
• ISSN: 1053-8119; 1095-9572
• DOI: 10.1016/j.neuroimage.2023.120264

•Sleep and development cause the EEG-PSD to rotate over opposite directions.•Wake and light-sleep PSD rotates over age, displaying flatter slope and lower offset.•Deep-sleep PSD decreases its offset over age, while retaining similar slope over age.•The hot-spot with slowest PSD migrates following a postero-anterior gradient over age.•Wake and light-sleep EEG aperiodic activity diverge from deep sleep activity over age. During development, the brain undergoes radical structural and functional changes following a posterior-to-anterior gradient, associated with profound changes of cortical electrical activity during both wakefulness and sleep. However, a systematic assessment of the developmental effects on aperiodic EEG activity maturation across vigilance states is lacking, particularly regarding its topographical aspects. Here, in a population of 160 healthy infants, children and teenagers (from 2 to 17 years, 10 subjects for each year), we investigated the development of aperiodic EEG activity in wakefulness and sleep. Specifically, we parameterized the shape of the aperiodic background of the EEG Power Spectral Density (PSD) by means of the spectral exponent and offset; the exponent reflects the rate of exponential decay of power over increasing frequencies and the offset reflects an estimate of the y-intercept of the PSD. We found that sleep and development caused the EEG-PSD to rotate over opposite directions: during wakefulness the PSD showed a flatter decay and reduced offset over development, while during sleep it showed a steeper decay and a higher offset as sleep becomes deeper. During deep sleep (N2, N3) only the spectral offset decreased over age, indexing a broad-band voltage reduction. As a result, the difference between values in deep sleep and those in both light sleep (N1) and wakefulness increased with age, suggesting a progressive differentiation of wakefulness from sleep EEG activity, most prominent over the frontal regions, the latest to complete maturation. Notably, the broad-band spectral exponent values during deep sleep stages were entirely separated from wakefulness values, consistently across developmental ages and in line with previous findings in adults. Concerning topographical development, the location showing the steepest PSD decay and largest offset shifted from posterior to anterior regions with age. This shift, particularly evident during deep sleep, paralleled the migration of sleep slow wave activity and was consistent w