The ages of sleep onset: spatio-temporal eeg patterns in preadolescents, young and older adults

Sleep and wakefulness are no more considered mutually exclusive states. In the last decades, several findings pointed out the local and use-dependent nature of sleep features, demonstrating that electrophysiological patterns of both sleep and wakefulness can co-occur simultaneously, in different cortical areas. By definition, Sleep Onset (SO) is an instable state of transition between wakefulness and sleep, and its spatiotemporal dynamics have been exhaustively described in healthy adulthood. The human sleep electroencephalographic (EEG) topography is characterized by strong age-related changes. However, the specific local EEG features of SO during preadolescence and healthy aging have been not extensively described. Materials and Methods: We aimed to investigate regional and temporal electrophysiological patterns of SO in a group of 23 preadolescents (9-14 years, Exp. 1) and in a group of 36 older participants (59-81 years, Exp 2). Specifically, the pre- vs- post-SO changes in the topography of the 1 Hz bins’ EEG power and the time course of the EEG frequency bands during the wake-sleep transition were assessed in both experimental groups. Furthermore, we compared delta activity and delta/beta ratio during the SO between these two groups (Exp. 1: preadolescent, Exp. 2: elderly) and a group of 40 healthy young adults (18-29 years). Results: In Exp. 1 preadolescents exhibited: a) a generalized post-SO increase in the low frequencies (0.5-6 Hz), especially in the lowest bins (0.5-2 Hz) with a central predominance; b) activity in the 12-13 and 14-15 Hz increased over frontal or central areas, respectively; c) the slowest bins in the beta band showed a slight central increase post-SO. Compared to young adults, delta/beta ratio in preadolescents was higher in posterior areas in both pre- and post-SO and lower in frontal areas in the post-SO. This finding was paralleled by higher delta power in posterior (pre-SO) and centro-posterior areas (post-SO) and lower delta activity in frontal areas (post-SO) in preadolescents. Exp. 2 showed that elderly had: a) a generalized post-SO power increase in the slowest frequencies; b) a specific pattern of post-SO changes of the alpha frequency; c) a slight post-SO increase of the sigma activity, whereas its highest bins exhibited a frontotemporal decrease. Older adults showed a global decline of the delta power and delta/beta ratio in both pre- and post-SO intervals compared to young adults. Conclusions: In preadolescents the predominance of the delta activity in more posterior areas compared to young adults and the observation of a not completely mature spindles should be ascribed to development-related maturational processes, pointing to higher homeostatic need from the more mature areas, rather than to different SO dynamics. The reduced delta activity and delta/beta ratio observed in elderly likely depict lightened homeostatic pressure at SO. Taken together, findings parallel the SO process in adults, with a notable difference concerning homeostatic process. In fact, most differences point to crucial developmental changes in homeostatic regulation that play a role in determining age-related wake-sleep transition features.