Consolidating the effects of waking and sleep on motor-sequence learning

Abstract

Sleep is widely believed to play a critical role in memory consolidation. Sleep-dependent consolidation has been studied extensively in humans using an explicit motor-sequence learning paradigm. In this task, performance has been reported to remain stable across wakefulness and improve significantly after sleep, making motor-sequence learning the definitive example of sleep-dependent enhancement. Recent work, however, has shown that enhancement disappears when the task is modified to reduce task-related inhibition that develops over a training session, thus questioning whether sleep actively consolidates motor learning. Here we use the same motor-sequence task to demonstrate sleep-dependent consolidation for motor-sequence learning and explain the discrepancies in results across studies. We show that when training begins in the morning, motor-sequence performance deteriorates across wakefulness and recovers after sleep, whereas performance remains stable across both sleep and subsequent waking with evening training. This pattern of results challenges an influential model of memory consolidation defined by a time-dependent stabilization phase and a sleep-dependent enhancement phase. Moreover, the present results support a new account of the behavioral effects of waking and sleep on explicit motor-sequence learning that is consistent across a wide range of tasks. These observations indicate that current theories of memory consolidation that have been formulated to explain sleep-dependent performance enhancements are insufficient to explain the range of behavioral changes associated with sleep.

Figure 1.

Motor-sequence performance across test trials. Performance was measured as the number of correctly completed sequences during the test trials. The completed-sequence scores for the spaced conditions (C, D) are approximately one-third of the massed conditions (A, B) because the spaced-condition scores were averaged over 10 s trials rather than 30 s trials. A, A.M. massed-training condition. B, P.M. massed-training condition. C, A.M. spaced-training condition. D, P.M. spaced-training condition. Data are the means ± SEM (*p < 0.05; **p < 0.01; ***p < 0.001).

Figure 2.

Response times across trials. Each data point represents the mean response time for each key press over a 10 s interval. For the spaced conditions, each data point corresponds to the mean response time for each 10 s trial. For the massed conditions, each 30 s trial was separated into three 10 s blocks. The data points are combined into triplets, where the massed condition triplets correspond to the 30 s trials and the spaced triplets are matched for consistency but represent independent trials. A, Response times for A.M.-massed and -spaced conditions. B, Response times for P.M.-massed and -spaced conditions.