Sleep-Dependent Improvement in Visuomotor Learning: A Causal Role for Slow Waves

A NUMBER OF STUDIES HAVE SHOWN THAT SLEEP CAN ENHANCE PERFORMANCE OF PREVIOUSLY LEARNED TASKS.1 SOME STUDIES SUGGEST THAT A COMBINATION of both non-rapid eye movement (NREM) and rapid eye movement (REM) sleep is important,2,3 whereas others emphasize either NREM or REM sleep.4 However, assigning a role in memory enhancement to different stages of sleep, or to a combination of stages, is problematic because sleep function likely depends on specific electrophysiologic events, such as slow waves or spindles, rather than on conventionally defined sleep stages. Furthermore, most experiments so far have been correlative. Thus, it is important to determine whether sleep-dependent improvements in performance are causally related to specific electrophysiologic features of sleep. During NREM sleep, virtually all cortical neurons undergo approximately 1-Hz slow oscillations, characterized by periods of membrane depolarization and firing activity (up states) followed by periods of membrane hyperpolarization and cessation of firing (down states).5 Slow oscillations are synchronized by cortico-cortical connections,6,7 giving rise to slow waves of low frequency (0.5-4.5 Hz) and high amplitude (often > 75 uV) that can be recorded in the sleep electroencephalogram (EEG). This slow wave activity (SWA, the EEG power density between 0.5 and 4.5 Hz during NREM sleep) is thought to be a marker of sleep need, in that it is high at sleep onset, declines during sleep, is further increased after sleep deprivation, and is reduced by naps.8–10 Recently, we used a visuomotor adaptation task in which subjects learn to reach for targets on a visual display while the cursor trajectory, unbeknownst to them, is rotated by the computer.11 We showed that visuomotor performance in this task was enhanced by a night of sleep but not by an equivalent period of wakefulness and found, using high-density EEG, that learning led to a local increase in sleep SWA over a right parietal cortical area involved in rotation adaptation. Moreover, we found that the postsleep improvement correlated with the local increase in sleep SWA.11 These results demonstrated that sleep slow waves are regulated locally as a consequence of learning and raised the possibility that they may be causally involved in sleep-dependent visuomotor performance improvements. To test this hypothesis in the current study, subjects learned the same rotation task,11 after which sleep slow waves were disrupted with acoustic stimuli. We investigated whether selective slow wave deprivation (SWD) prevented the improvement in postsleep visuomotor performance and whether changes in visuomotor performance correlated with changes in SWA.