Dreaming of a learning task is associated with enhanced sleep-dependent memory consolidation

Abstract

It is now well established that postlearning sleep is beneficial for human memory performance. Meanwhile, human and animal studies have demonstrated that learning-related neural activity is re-expressed during posttraining nonrapid eye movement (NREM) sleep. NREM sleep processes appear to be particularly beneficial for hippocampus-dependent forms of memory. These observations suggest that learning triggers the reactivation and reorganization of memory traces during sleep, a systems-level process that in turn enhances behavioral performance. Here, we hypothesized that dreaming about a learning experience during NREM sleep would be associated with improved performance on a hippocampus-dependent spatial memory task. Subjects were trained on a virtual navigation task and then retested on the same task 5 hr after initial training. Improved performance at retest was strongly associated with task-related dream imagery during an intervening afternoon nap. Task-related thoughts during wakefulness, in contrast, did not predict improved performance. These observations suggest that sleep-dependent memory consolidation in humans is facilitated by the offline reactivation of recently formed memories, and furthermore that dream experiences reflect this memory processing. That similar effects were not observed during wakefulness suggests that these mnemonic processes are specific to the sleep state.

(c) 2010 Elsevier Ltd. All rights reserved.

Figures

Figure 1. The virtual maze task

In this spatial memory task, subjects first learned the layout of a complex maze (Left, level 3 shown). Route memory was then probed across a series of trials, as subjects repeatedly navigated to a specified goal point, beginning from pseudorandomized starting locations. An example view of the maze environment is pictured (Right). For summary of task-related mentation, see Supplemental Table S1.

Figure 2. Participants with maze-related verbal reports improved more than other subjects at retest

Left: Sleep subjects with verbal reports related to the maze improved tenfold more at retest than did participants without task-related mentation. In contrast, thoughts about the task during Wake did not provide a similar benefit. Error bars = SEM. Right: Baseline performance was a strong predictor of later improvement (regression lines and 95% CI lines for all subjects). Sleep participants reporting maze-related dreams (n=4, large circles) were amongst those with the poorest baseline performance, but improved significantly more at retest than other poor performers. In contrast, subjects who reported thoughts of the maze task during Wake (n=2, large circles) did not differ from others in terms of baseline performance, and improved similarly to those with comparable baseline performance. See also Supplemental Figure S1.

Figure 3. Protocol for collection of subjective reports

“Repeated Awakenings” participants (n=52) were interrupted for reporting during the sleep onset period, and provided a total of three verbal reports during the post-training Sleep/Wake period. “Questionnaire Protocol” participants (n=47) were not interrupted during sleep onset, and instead provided only one verbal report at the end of the nap, in addition to completing a questionnaire regarding task-related mentation at the end of the study. Total sleep time (TST) did not differ between these participant subsets (p>.3).