Characterization of overnight slow-wave slope changes across development in an age-, amplitude-, and region-dependent manner

Abstract

Study Objectives The restorative function of sleep has been linked to a net reduction in synaptic strength. The slope of slow-waves, a major characteristic of non-rapid eye movement (NREM) sleep, has been shown to directly reflect synaptic strength, when accounting for amplitude changes across the night. In this study, we aimed to investigate overnight slope changes in the course of development in an age-, amplitude-, and region-dependent manner. Methods All-night high-density electroencephalography data were analyzed in a cross-sectional population of 60 healthy participants in the age range of 8–29 years. To control for amplitude changes across the night, we matched slow-waves from the first and the last hour of NREM sleep according to their amplitude. Results We found a reduction of slow-wave slopes from the first to the last hour of NREM sleep across all investigated ages, amplitudes, and most brain regions. The overnight slope change was largest in children and decreased toward early adulthood. A topographical analysis revealed regional differences in slope change. Specifically, for small amplitude waves the decrease was smallest in an occipital area, whereas for large amplitude waves, the decrease was smallest in a central area. Conclusions The larger slope decrease in children might be indicative of a boosted renormalization of synapses during sleep in childhood, which, in turn, might be related to increased plasticity during brain maturation. Regional differences in the extent of slow-wave slope reduction may reflect a “smart” down-selection process or, alternatively, indicate amplitude-dependent differences in the generation of slow-waves.

Sleep spindles preferentially consolidate weakly encoded memories

“…In addition, the properties of coupling across a night of sleep have yet to be explored. Giving the multiple functions of sleep, it would be interesting to ask whether coupling during the early, SWS rich periods, are significantly different from late night SWS, where overall slow oscillation amplitudes are lower (Jaramillo et al, 2020). In general, these results emphasize the importance of solidifying our understanding of what gives rise to spindle coupling events, and how they relate to subcortical activity such as hippocampal sharp-wave ripples Our results suggest that spindles are uniquely involved in selective consolidation processes, as we did not find any correlations between consolidation of prioritized memories and either slow oscillations in isolation or spectral power in either the delta or sigma bands.…”

Thalamic Influence on Slow Wave Slope Renormalization During Sleep

“…This question can be addressed by analyzing overnight slow wave slope changes, as these have been shown to reflect synaptic renormalization and therefore represent a good marker for the restorative function of sleep. [14][15][16][17] The relationship between sleep and thalamic stroke is intriguing. Given that thalamic stroke is associated with severe excessive daytime sleepiness/hypersomnia, cognitive disturbances, and sleep EEG changes (eg, reduction of sleep efficiency), it poses an ideal model to test the hypothesis of a link between sleep, wakefulness, and cognition.…”

“…The majority of studies on sleep and stroke have focused on mapping these use‐dependent changes in SWA but have not examined whether sleep‐dependent restoration is altered after stroke. This question can be addressed by analyzing overnight slow wave slope changes, as these have been shown to reflect synaptic renormalization and therefore represent a good marker for the restorative function of sleep 14–17 …”

An Infant Sleep Electroencephalographic Marker of Thalamocortical Connectivity Predicts Behavioral Outcome in Late Infancy

“…Slow waves were detected using a procedure adapted from (Jaramillo et al, 2020;Riedner et al, 2007): After low-pass filtering below 30 Hz, the signal was re-referenced to the average across all electrodes and band-pass filtered (0.5 -4 Hz, stopband 0.1 and 10 Hz, Chebyshev Type II filter).…”

“…Three slow wave and spindle features might be of particular interest as neurodevelopmental markers considering these have been linked to synaptic plasticity. 1) The slope of slow waves reflects synaptic strength within the thalamocortical system (Esser et al, 2007;Riedner et al, 2007;Vyazovskiy et al, 2007) and undergoes strong maturational changes (Jaramillo et al, 2020). 2) Spindle density (number of spindles per minute) has been connected to thalamocortical connectivity and integrity assessed with structural (Piantoni et al, 2013;Wehrle et al, 2020) and functional Magnetic Resonance Imaging (Baran et al, 2019).…”