Abnormal timing of slow wave synchronization processes in non-rapid eye movement sleep parasomnias.

Abstract

Sleepwalking, confusional arousals, and sleep terrors are parasomnias occurring out of non-rapid eye movement (NREM) sleep. Several previous studies have described EEG changes associated with NREM parasomnia episodes, but it remains unclear whether these changes are specific to parasomnia episodes or whether they are part of the normal awakening process. Here we directly compared regional brain activity, measured with high-density (hd-) EEG, between parasomnia episodes and normal awakenings (without behavioral manifestations of parasomnia). Twenty adult patients with non-rapid eye movement parasomnias underwent a baseline hd-EEG recording (256 electrodes) followed by a recovery sleep recording after 25 h of total sleep deprivation, during which auditory stimuli were administered to provoke parasomnia episodes. Both normal awakenings (n = 25) and parasomnia episodes (n = 96) were preceded by large, steep, and "K-complex-like" slow waves in frontal and central brain regions, and by a concomitant increase in high-frequency EEG (beta) activity. Compared to normal awakenings, parasomnia episodes occurred on a less activated EEG background and displayed higher slow wave activity (SWA) and lower beta activity in frontal and central brain regions after movement onset. Our results suggest that non-rapid eye movement awakenings, irrespective of behavioral manifestations of parasomnia episodes, involve an arousal-related slow wave synchronization process that predominantly recruits frontal and central brain areas. In parasomnia episodes, this synchronization process comes into play abnormally during periods of high SWA and is associated with higher SWA after movement onset. Thus, an abnormal timing of arousal-related slow wave synchronization processes could underlie the occurrence of NREM parasomnias.