Feeling awake while asleep: a high-denstiy EEG assessment of sleep perception

Objectives/Introduction: The impression of being awake despite polysomnographically documented sleep is sometimes observed in healthy individuals and to an extreme degree in patients with paradoxical insomnia. The mechanisms underlying the subjective perception of sleep are not well understood. Here we asked whether high-density (hd)-EEG, a technique with a refined spatial resolution, could identify local patterns of brain activity related to the subjective perception of sleep. Methods: 14 healthy subjects (age 33.6 ± 8.5 years, 10 females) underwent a serial awakening paradigm in the sleep lab while recorded with hd-EEG (256 electrodes). 969 awakenings were performed across all sleep stages. At each awakening, subjects were asked to describe what was going through their mind and to estimate if immediately prior to the awakening they had been asleep or awake. Results: 10 of 14 subjects presented at least one instance in which they reported feeling awake (FAW) during sleep (15.92 ± 8.76% times per subject, total of n = 99 times). 70.83% of FAW instances occurred in N1, 18.77% in N3, 9.79% in N2 and 3.57% in REM sleep. Only stages N2 and N3 were further considered for analysis. Compared to when subjects reported feeling asleep (FAS), FAW instances occurred earlier in the night (147 ± 79 min after lights off vs 231 ± 25 min; p = 0.0038). The presence of conscious experiences during sleep did not distinguish FAW from FAS, but experiences associated with FAW tended to be more thought-like and less perceptual compared to FAS (Score: 0.52 ± 1.17 for FAS; -1.00 ± 1.84 for FAW; p = 0.076). FAW was associated with increased alpha (8-12 Hz) and sigma power (12-16 Hz) in central and posterior brain regions in the 20 s before the awakening. No significant differences were observed for other frequency bands. Conclusions: The preferential occurrence of FAW early in the night (N3 > N2), its quasi-absence during REM sleep and its association with increased alpha power in posterior (sensory) brain regions may indicate that the subjective perception of sleep depends on the degree of sleep-related environmental disconnection.