Stability of neural encoding moderates the contribution of sleep and repeated testing to memory consolidation

Abstract

There is evidence suggesting that online consolidation during retrieval-mediated learning interacts with offline consolidation during subsequent sleep to transform memory. Here we investigate whether this interaction persists when retrieval-mediated learning follows post-training sleep and whether the direction of this interaction is conditioned by the quality of encoding resulting from manipulation of the amount of sleep on the previous night. The quality of encoding was determined by computing the degree of similarity between EEG-activity patterns across restudy of face pairs in two groups of young participants, one who slept the last 4 h of the pre-training night, and another who slept 8 h. The offline consolidation was assessed by computing the degree of coupling between slow oscillations (SOs) and spindles (SPs) during post-training sleep, while the online consolidation was evaluated by determining the degree of similarity between EEG-activity patterns recorded during the study phase and during repeated recognition of either the same face pair (i.e., specific similarity) or face pairs sharing sex and profession (i.e., categorical similarity) to evaluate differentiation and generalization, respectively. The study and recognition phases were separated by a night of normal sleep duration. Mixed-effects models revealed that the stability of neural encoding moderated the relationship between sleep- and retrieval-mediated consolidation processes over left frontal regions. For memories showing lower encoding stability, the enhanced SO-SP coupling was associated with increased reinstatement of category-specific encoding-related activity at the expense of content-specific activity, whilst the opposite occurred for memories showing greater encoding stability. Overall, these results suggest that offline consolidation during post-training sleep interacts with online consolidation during retrieval the next day to favor the reorganization of memory contents, by increasing specificity of stronger memories and generalization of the weaker ones.

Keywords: Differentiation; EEG pattern similarity; Generalization; Memory consolidation; Sleep; Slow oscillation-spindle coupling.