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

Abstract

Study Objectives: Studies of neural activity in animals and humans suggest that experiences are "replayed" in cortical and hippocampal networks during NREM sleep. Here, we examine whether memory reactivation in sleeping humans might also be evident within reports of concomitant subjective experience (i.e., dreaming). Design: Participants were trained on an engaging visuomotor learning task across a period of one or more days, and sleep onset mentation was collected at variable intervals using the "Nightcap" home-monitoring device. Verbal reports of sleep onset mentation were obtained either at the beginning of the night, or following 2 h of initial sleep. Setting: Data were collected in participants' home environments, via the Nightcap monitoring system, and at The Center for Sleep and Cognition, Beth Israel Deaconess Medical Center, Boston MA. Participants: 43 healthy, medication-free college students (16 males, age 18-25 years). Interventions: N/A Measurements and Results: The learning task exerted a powerful, direct effect on verbal reports of mentation during light NREM sleep (stages 1 and 2). On post-training nights, a full 30% of all verbal reports were related to the task. The nature of this cognitive "replay" effect was altered with increasing durations of sleep, becoming more abstracted from the original experience as time into sleep increased. Conclusions: These observations are interpreted in light of memory consolidation theory, and demonstrate that introspective reports can provide a valuable window on cognitive processing in the sleeping brain.