Local and Widespread Slow Waves in Stable NREM Sleep: Evidence for Distinct Regulation Mechanisms

Abstract

Previous work showed that two types of slow waves are temporally dissociated during the transition to sleep: widespread, large and steep slow waves predominate early in the falling asleep period (type I), while smaller, more circumscribed slow waves become more prevalent later (type II). Here, we studied the possible occurrence of these two types of slow waves in stable non-REM (NREM) sleep and explored potential differences in their regulation. A heuristic approach based on slow wave synchronization efficiency was developed and applied to high-density electroencephalographic (EEG) recordings collected during consolidated NREM sleep to identify the potential type I and type II slow waves. Slow waves with characteristics compatible with those previously described for type I and type II were identified in stable NREM sleep. Importantly, these slow waves underwent opposite changes across the night, with only type II slow waves displaying a clear homeostatic regulation. In addition, we showed that the occurrence of type I slow waves was often followed by larger type II slow waves, whereas the occurrence of type II slow waves was usually followed by smaller type I waves. Finally, type II slow waves were associated with a relative increase in spindle activity, while type I slow waves triggered periods of high-frequency activity. Our results provide evidence for the existence of two distinct slow wave synchronization processes that underlie two different types of slow waves. These slow waves may have different functional roles and mark partially distinct “micro-states” of the sleeping brain.

Changes in cross-frequency coupling following closed-loop auditory stimulation in non-rapid eye movement sleep

“…A time-resolved topographical analysis of the stimulation-related delta changes demonstrated a similar smooth transition between the near-vertex N350-like distribution and the frontocentral N550-like distribution within the first second after stimulation as found previously (Nicholas et al, 2002). K-complexes and the recently proposed type I slow waves (Siclari et al, 2014) are thought to be generated in sensorimotor areas and the medial parietal cortex and involve predominantly frontocentral regions (Bernardi et al, 2018;Caporro et al, 2012;Riedner et al, 2011;Siclari et al, 2014). Interestingly, stimulation-induced delta changes observed in our study were also distributed mainly in central areas, indirectly suggesting recruitment of the same neural mechanisms of slow-wave generation.…”

Integrity of corpus callosum is essential for the cross-hemispheric propagation of sleep slow waves: a high-density EEG study in split-brain patients

“…Slow wave detection. Slow waves were detected automatically in a composite EEG-signal generated from linked-mastoid referenced channels, as previously described (Siclari et al, 2014;Mensen et al, 2016;Bernardi et al, 2018). This method provides a unique time reference (across electrodes) for each slow wave and facilitates the detection of both local and widespread events (Mensen et al, 2016).…”

“…Only half-waves with a duration comprised between 0.25 and 1.0 s were retained for further analyses. Of note, no amplitude thresholds were applied based on previous evidence indicating that: i) slow waves with peak-to-peak amplitude < 75µV show the clear homeostatic changes commonly attributed to the slow waves of NREM-sleep (Riedner et al, 2007;Bernardi et al, 2018); ii) the application of an amplitude threshold may actually preferentially select a minority of very large slow waves that have been shown to display different regulation and synchronization mechanisms as compared to the majority of slow waves (Siclari et al, 2014Mensen et al, 2016;Bernardi et al, 2018Bernardi et al, , 2019aSpiess et al, 2018). For all the detected slow waves, various parameters of interest were calculated and stored for a subsequent evaluation, including negative amplitude (µV), descending slope (between the first zerocrossing and the maximum negative peak; µV/ms) and involvement (mean EEG-signal calculated for all electrodes in an 80-ms window centered on the wave peak; µV).…”

“…It should be noted, however, that the resection of the CC did not completely eliminate cross-hemispheric slow wave propagation. This may imply the existence of additional propagation pathways, potentially including cortico-subcortico-cortical loops (e.g., Timofeev and Steriade, 1996), or the involvement of direct subcortico-cortical synchronization mechanisms (Siclari et al, 2014;Bernardi et al, 2018). Of note, a visual inspection of the structural MRI-scans also revealed that the anterior and posterior commissures were relatively spared in all the CP individuals.…”

“…Slow wave propagation. For each detected slow wave, the pattern of propagation was calculated as described in previous work (Mensen et al, 2016;Bernardi et al, 2018). In brief, we first determined for each electrode the timing of any local negative maxima that occurred within a time-window of 300 ms centered on the maximum negative peak (reference peak) of the examined slow wave.…”