Slow oscillation-spindle coupling impairs emotional memory consolidation following stress

Sleep and stress have both been shown to enhance emotional memory consolidation. They also interact, with the largest benefit of sleep on emotional memory being seen when stress occurs either shortly before or after memory encoding. Slow wave sleep (SWS) is believed to be critical for episodic memory consolidation, facilitated by the coupling of slow oscillations and sleep spindles. However, prior work in humans has only demonstrated slow oscillation-spindle coupling to be associated with consolidation of neutral information in non-stressed participants. Whether coupling interacts with stress to facilitate emotional memory consolidation is unknown. To address this exploratory question, we reanalyzed an existing dataset of N=64 individuals. Participants underwent a psychosocial stressor (n=32) or comparable control (n=32) prior to the encoding of 150 line drawings of neutral, positive, and negative images. All participants then slept overnight with polysomnographic recordings. The next day, they were given a surprise memory test. In the stress group, percentage of time spent in SWS was positively correlated with memory for images of all valences (all r>.35, p .65, p .25). However, the amount of slow oscillation-spindle coupling during SWS was negatively associated with neutral (r=-.45, p=.01) and emotional (r=-.66, p<.001) memory in the stress group. The negative association with emotional memory was significantly stronger than for neutral memory (Meng z=2.04, p=.04). Between stress and control groups, there were no differences in any of the sleep measures assessed. These results highlight the importance of considering sleep microarchitecture events in addition to overall sleep stage time and suggests that stress may alter the relationship between SWS and memory consolidation.