Regional Delta Waves In Human Rapid Eye Movement Sleep

Abstract

Although the EEG slow wave of sleep is typically considered to be a hallmark of nonrapid eye movement (NREM) sleep, recent work in mice has shown that slow waves can also occur in REM sleep. Here, we investigated the presence and cortical distribution of negative delta (1-4 Hz) waves in human REM sleep by analyzing high-density EEG sleep recordings obtained in 28 healthy subjects. We identified two clusters of delta waves with distinctive properties: (1) a frontal-central cluster characterized by ϳ2.5-3.0 Hz, relatively large, notched delta waves (so-called "sawtooth waves") that tended to occur in bursts, were associated with increased gamma activity and rapid eye movements (EMs), and upon source modeling displayed an occipital-temporal and a frontal-central component and (2) a medialoccipital cluster characterized by more isolated, slower (Ͻ2 Hz), and smaller waves that were not associated with rapid EMs, displayed a negative correlation with gamma activity, and were also found in NREM sleep. Therefore, delta waves are an integral part of REM sleep in humans and the two identified subtypes (sawtooth and medial-occipital slow waves) may reflect distinct generation mechanisms and functional roles. Sawtooth waves, which are exclusive to REM sleep, share many characteristics with ponto-geniculo-occipital waves described in animals and may represent the human equivalent or a closely related event, whereas medial-occipital slow waves appear similar to NREM sleep slow waves.The EEG slow wave is typically considered a hallmark of nonrapid eye movement (NREM) sleep, but recent work in mice has shown that it can also occur in REM sleep. By analyzing high-density EEG recordings collected in healthy adult individuals, we show that REM sleep is characterized by prominent delta waves also in humans. In particular, we identified two distinctive clusters of delta waves with different properties: a frontal-central cluster characterized by faster, activating "sawtooth waves" that share many characteristics with ponto-geniculo-occipital waves described in animals and a medial-occipital cluster containing slow waves that are more similar to NREM sleep slow waves. These findings indicate that REM sleep is a spatially and temporally heterogeneous state and may contribute to explaining its known functional and phenomenological properties.

Fear in dreams and in wakefulness: Evidence for day/night affective homeostasis

“…Statistical analysis was carried out in MATLAB. To compare brain activity between trials with fear and those without, source‐space power was averaged within frequency bands according to literature (Bernardi et al , Olbrich et al , Marzano et al , Corsi‐Cabrera et al ) (Delta: 1‐5 Hz, Theta: 5–8 Hz, Alpha: 8‐12 Hz, Sigma: 12‐16 Hz, Beta: 16‐30 Hz, Gamma: 30‐50 Hz). We then averaged the power values within trials with fear and those trials without fear for each participant and for each frequency band separately.…”

The microstructure of REM sleep: Why phasic and tonic?

“…The third frequency range that differentiates REM microstates is within the delta and theta bands, exhibiting increased power particularly between 2 and 4 Hz during phasic REM periods [60,61,71]. These oscillations that resemble so-called sawtooth waves are prominent at fronto-central derivations, associated with increases in gamma power [71], and highly synchronized over the scalp [61]. Low frequency oscillations in NREM are known to emerge from widely distributed thalamo-cortical and corticocortical neural ensembles and to reflect the rhythmic alternation of hyperpolarized and depolarized states [72].…”

“…As this is especially true in conditions of high sleep pressure [73], widely synchronized low frequency oscillations might facilitate disconnection from the external environment. On the other hand, low frequency oscillations might reflect PGO waves and, coupled with gamma oscillations, may activate the cortex [71]. Whether such low-frequency activity during phasic periods facilitate disconnection from the external environment, or rather, are the cortical analogs of PGO waves is a matter for future research.…”

“…As discussed above, environmental alertness is largely reduced, and a thalamocortical network including limbic and parahippocampal regions provides functionally isolated, intrinsic activity during phasic microstates [39,69]. The combination of intense cortical activity and sensory disconnection is also accentuated by the coexistence of widely synchronized slow frequency oscillations and high-frequency (gamma) activity [61,71]. Whereas the former indicates a deeper sleep stage facilitating the stability of sleep and the attenuation of sensory processing, the latter is indicative of intense activity of localized cortical networks [119,120].…”

Cortical and subcortical hemodynamic changes during human sleep slow waves

“…For each participant, the first 30 minutes of N2/N3 sleep were extracted and slow waves were automatically detected using the same algorithm described above. Then, the EEG signal was band-pass filtered between 0.5 and 4.0 Hz, and 800-ms-long data segments centered on the slow wave negative peak were extracted and source-modeled using the GeoSource 3.0 software (EGI-Philips), as described in previous work (Bernardi et al, 2019a(Bernardi et al, , 2019b. In brief, a four-shell head model based on the MNI atlas and subjectspecific co-registered sets of electrode positions (obtained using the Geodesic Photogrammetry System, EGI-Philips) were used to construct the forward model.…”