Cognitive replay of visuomotor learning at sleep onset: temporal dynamics and relationship to task performance.

A SUBSTANTIAL BODY OF EVIDENCE NOW DEMONSTRATES THAT RECENT EXPERIENCES ARE “REPLAYED” IN CORTICAL AND HIPPOCAMPAL NETWORKS during sleep.1–4 Rodent studies utilizing single-cell recordings have clearly established that neuronal activation patterns seen during waking exploration are later re-expressed in sleeping animals.1,2,4 Functional imaging studies in humans complement this work.3,5 The observation that memories are reactivated during sleep suggests that “replay” of memory in the sleeping brain could be accompanied, at least in humans, by related subjective experience (i.e., dreaming or sleep mentation).6–8 In fact, several key features of neural-level memory reactivation in sleep exhibit strong parallels with emerging cognitive data on the appearance of recently encoded memories in reports of sleep mentation: Neural-level reactivation of recent experience has most often been observed during NREM sleep. Similarly, subjective reports elicited from NREM are more likely to contain episodic memory sources than reports from REM sleep.9 Within NREM sleep, the strength of neural-level memory replay decays quickly across time.2,4 Similarly, sleep mentation may be most strongly related to recent memories early in the sleep phase.10,11 Recent experience is not replayed veridically during sleep. Neuronal firing sequences established during wake are re-expressed only intermittently during rodent NREM sleep, with relatively low fidelity and on a faster time scale than the original experience.12,13 Similarly, only intermittent fragments of recent episodic memories appear in sleep mentation, intermingled with remote and semantic material.14 We propose that reports of subjective experience may provide a valuable methodology for exploring the characteristics of memory traces recruited for reactivation during sleep. Though little empirical work has thus far addressed this question, some preliminary evidence is at least suggestive of a link between sleep mentation and recent learning. Smith and Hanke,15 for example, report evidence of sleep mentation related to a pre-sleep learning task, present to a greater degree in participants cued during sleep using a task-associated sound. Meanwhile, Fiss et al.16 report that dreaming symbolically of stories presented to participants prior to sleep is associated with enhanced morning recall, suggesting that task-related mentation could have a beneficial effect on memory performance. Stickgold et al.11 have previously demonstrated that an engaging, visually salient learning task (the popular video game Tetris®) exerts a direct influence on subsequent sleep onset mentation. The present study extends this work by asking how specific features of this cognitive-level memory reactivation change across time, and by examining task performance as a predictor of this replay effect. To approach these questions, we employed a highly engaging visuomotor video game (downhill skiing arcade game Alpine Racer™ II) as an intensive learning task, and observed the effects of this training on mentation during subsequent periods of light NREM sleep (stages 1 and 2). It is well known that a general correspondence exists between waking life experience and dream content, in that predominant persons, concerns, and activities in an individual's waking life also are consistently evident in their his or her sleep mentation reports.17,18 Yet historically, controlled laboratory studies have met with little success in experimentally manipulating sleep mentation through the use of specific pre-sleep interventions.19 This difficulty has likely arisen, in part, from reliance on passive visual stimulation as a pre-sleep stimulus, the effects of which are often overshadowed by the much more salient experience of spending the night in a sleep laboratory.20 Unlike the passive stimuli used in many prior studies, the task we employed here actively engages participants in a multi-sensory learning experience, within an immersive 3D-style virtual environment. Furthermore, the confounds of the sleep laboratory environment were eliminated by recording sleep and mentation in the home. Although dream research has most often focused on REM sleep, periods of early NREM sleep may actually provide the ideal opportunity to examine the effects of a learning task on subsequent mentation. Accumulating behavioral and neurophysiologic data suggest that consolidation of recent memory is supported by NREM-specific physiology, including sleep spindles21–24 and hippocampal sharp wave ripples.25,26 Furthermore, memories of recent episodes are proportionally greater in mentation from NREM sleep, and are particularly prevalent during the sleep onset period.9 Taken together with the observation that neural-level memory replay is strongest immediately following training, as noted above,1 the available data suggest that cognitive-level replay of recent learning may be most apparent during periods of early NREM sleep. In the present study, we therefore focused on collecting mentation samples from light NREM sleep, shortly after sleep onset (stages 1 and 2). Though considerable evidence supports the notion that memories are consolidated during sleep, we still have a relatively poor understanding of the processes controlling which recent experiences are “selected” for offline reactivation and consolidation. By studying the incorporation of recent waking experience into dreams, we can gain valuable insight into the processes controlling the activation of memory networks during sleep. As prior research suggests that task difficulty and/or initial skill level may be important mediators of sleep dependent memory processing,27–29 here we asked whether Alpine Racer performance at baseline would predict the extent of cognitive-level task replay observed in subsequent sleep mentation. Furthermore, we examined how the incorporation of recent experience into sleep mentation is altered across time. Though the appearance of recent events in dreams has been reported to decline across the course of a night,10 the processes accounting for this effect remain obscure. Temporal proximity to waking experience provides a potential explanation, but it could also be that reactivation of memory on a cognitive level is incrementally transformed across time due to consolidation/processing occurring during intervening sleep. In the present experiment, we approached this question by independently manipulating the clock time of report collection and the position of mentation reports within the sleep phase.