Targeted memory reactivation during sleep depends on prior learning

Abstract

Study Objectives: When sounds associated with learning are presented again during slow-wave sleep, targeted memory reactivation (TMR) can produce improvements in subsequent location recall. Here we used TMR to investigate memory consolidation during an afternoon nap as a function of prior learning. Participants: Twenty healthy individuals (8 male, 19-23 y old). Measurements and Results: Participants learned to associate each of 50 common objects with a unique screen location. When each object appeared, its characteristic sound was played. After electroencephalography (EEG) electrodes were applied, location recall was assessed for each object, followed by a 90-min interval for sleep. During EEG-verified slow-wave sleep, half of the sounds were quietly presented over white noise. Recall was assessed 3 h after initial learning. A beneficial effect of TMR was found in the form of higher recall accuracy for cued objects compared to uncued objects when pre-sleep accuracy was used as an explanatory variable. An analysis of individual differences revealed that this benefit was greater for participants with higher pre-sleep recall accuracy. In an analysis for individual objects, cueing benefits were apparent as long as initial recall was not highly accurate. Sleep physiology analyses revealed that the cueing benefit correlated with delta power and fast spindle density. Conclusions: These findings substantiate the use of targeted memory reactivation (TMR) methods for manipulating consolidation during sleep. TMR can selectively strengthen memory storage for object-location associations learned prior to sleep, except for those near-perfectly memorized. Neural measures found in conjunction with TMR-induced strengthening provide additional evidence about mechanisms of sleep consolidation.