Characteristics of sleep slow waves in children and adolescents

THE MOST PROMINENT ELECTROENCEPHALOGRAPHIC (EEG) CHARACTERISTIC OF DEEP NON-RAPID EYE MOVEMENT (NREM) SLEEP IS SLOW WAVES. THE neuronal correlate of slow waves is the slow oscillation first described in detail by Steriade and coworkers, who showed that membrane potentials of cortical neurons alternate about every second between a depolarized upstate and a hyperpolarized downstate during slow oscillations.1 When these oscillations are near synchronous and involve the majority of the cortical neurons in a given region, they become visible in the surface EEG as slow waves of large amplitude. The alternation of upstates and downstates in cortical neurons is thought to be involved in memory consolidation,2,3 synaptic homeostasis,4 and the recuperative function of sleep.5 Slow waves in the sleep EEG undergo dramatic changes during brain maturation. As early as the 1980s, Feinberg and colleagues reported that the amplitude of slow waves increases until shortly before puberty and then shows a prominent decrease across adolescence.6 Sleep slow-wave activity (SWA, EEG spectral power between 0.5 and 4.5 Hz), a quantitative measure of the activity in the slow-wave frequency range reflecting the homeostatic regulation of sleep,5 follows a similar time course. SWA sharply declines across puberty,7–9 followed by a smaller decrease during the twenties.6,10 The brain undergoes striking morphologic and functional changes during early human development.11–13 For example, Huttenlocher and Dabholkar11 reported that maximum cortical synapse density is achieved shortly before puberty. Furthermore, the course of adolescence is accompanied by a reduction in density of synapses in the grey matter, a process termed pruning.14–17 Longitudinal neuroimaging findings of cortical maturation corroborate these findings and reveal concomitant changes in grey matter. For instance, grey-matter volume has been shown to be greatest in frontal regions of the cortex around early puberty and to decrease thereafter.18,19 With the exception of the temporal lobe, the majority of the other cortical areas show a similar time course.18 In view of the similar time course of cortical synapse density and the amplitude of sleep slow waves, some authors have proposed a link between the two.6,8,9 In fact, recent computer simulations of the thalamocortical system have provided evidence for an association of the number and strength of synapses involved in the generation of sleep slow waves and their amplitude.20 In this simulation, the morphology of sleep slow waves changed as a function of the level of synchronization of cortical neurons. The synchronization level, on the other hand, depended on synaptic strength and synaptic density. Thus, the stronger and denser synapses are on neurons of a certain population, the faster those neurons can synchronize their activity; the faster they show synchronized activity, the steeper is the resulting potential change within that population. It is those potential changes that are measured by EEG recordings.21 Therefore, this computer model implied that the slope of slow waves is a good measure of the synchronization level of the neurons in the cortex, i.e., the slope of slow waves may represent a direct electrophysiological measure of changes in synaptic strength or density.20 On the basis of this observation, we hypothesized that the higher slow-wave amplitude in prepubertal children, compared with mature adolescents, results from higher synaptic strength or density, which should also be seen as a steeper slope of sleep slow waves. Therefore, we compare the characteristics of sleep slow waves in prepubertal children and mature adolescents. With this study, we propose the analysis of slow-wave characteristics as a novel approach to assessing developmental differences in overall cortical structure with possible functional associations.