Prioritized memory consolidation over sleep

Abstract

Emotion enhances memory longevity and vividness. Perceiving an experience as emotional, as well as the autonomic and functional brain responses involved in initially encoding an emotional experience, have been theorized to “tag” these memories. Tagged memories may then be prioritized for consolidation during sleep. However, direct evidence supporting this theory is sparse. The aim of the present study was to determine which encoding-related indicators of memory tagging interact with post-encoding sleep oscillations to promote emotional memory retention and vividness. To test this, participants incidentally encoded positive, neutral and negative multisensory stimuli during 3T fMRI scanning with concurrent heart rate monitoring. Participants provided emotional intensity ratings after each stimulus presentation. Following a 120-min post-encoding nap opportunity recorded with polysomnography, participants completed a surprise memory test. Memory for emotional and neutral stimuli was equivalent, though emotional stimuli tended to be remembered more vividly. Perceived emotional intensity, but not heart rate deceleration (HRD) magnitude or functional brain activity, was diagnostic of later successful retrieval of emotional, but not neutral stimuli. Higher REM sleep theta power during the nap was associated with a greater emotional intensity (EI) subsequent memory effect (i.e., higher EI for later remembered compared to forgotten stimuli) for positive stimuli, which were also remembered more vividly. Higher NREM spindle density was associated with a greater EI subsequent memory effect for neutral stimuli and lesser EI subsequent memory effect for negative stimuli. Lastly, higher numbers of NREM spindle-slow oscillation coupling events predicted a negative relationship between perceived emotional intensity at encoding and memory vividness for negative stimuli. Taken together, the present findings suggest that subjective, rather than objective, encoding-related arousal responses acted as emotion “tags”. How subjective arousal impacted later memory varied as a function of the memory’s emotion category and REM and NREM-specific oscillations. Future work is needed to clarify the underlying mechanisms for these observed effects.