What drives slow wave activity during early non-REM sleep: Learning during prior wake or effort?

Abstract

What is the function of sleep in humans? One claim is that sleep consolidates learning. Slow wave activity (SWA), i.e. slow oscillations of frequency < 4 Hz, has been observed in electroencephalograms (EEG) during sleep; it increases with prior wakefulness and decreases with sleep. Studies have claimed that increase in SWA in specific regions of the sleeping brain is correlated with overnight improved performance, i.e. overnight consolidation, on a demanding motor learning task. We wondered if SWA change during sleep is attributable to overnight consolidation or to metabolic demand. Participants executed out-and-back movements to a target using a pen-like cursor with their dominant hand while the target and cursor position were displayed on a screen. They trained on three different conditions on separate nights, differing in the amount and degree of rotation between the actual hand movement direction and displayed cursor movement direction. In the no-rotation (NR) condition, there was no rotation. In the single rotation (SR) condition, the amount of rotation remained the same throughout, and performance improved both across pre-sleep training and after sleep, i.e. overnight consolidation occurred; in the random rotation (RR) condition, the amount of rotation varied randomly from trial to trial, and no overnight consolidation occurred; SR and RR were cognitively demanding. The average EEG power density of SWA for the first 30 min. of non-rapid eye movement sleep after training was computed. Both SR and RR elicited increase in SWA in the parietal region; furthermore, the topographic distribution of SWA in each was remarkably similar. No correlation was found between the overnight performance improvement on SR and the SWA change in the parietal region on measures of learning. Our results argue that regulation of SWA in early sleep is associated with high levels of cognitive effort during prior wakefulness, and not just overnight consolidation.