Slow oscillation‐spindle coupling is negatively associated with emotional memory formation following stress

• Published in: The European journal of neuroscience Vol. 55; no. 9-10; pp. 2632 - 2650
• Main Authors: Denis, Dan, Kim, Sara Y., Kark, Sarah M., Daley, Ryan T., Kensinger, Elizabeth A., Payne, Jessica D.
• Format: Journal Article
• Language: English
• Published: France Wiley Subscription Services, Inc 01.05.2022
• Subjects: Activity patterns; Cortisol; Electroencephalography; Emotions; Emotions - physiology; Humans; Oscillations; Polysomnography; Sleep; Sleep - physiology; Sleep, Slow-Wave; slow waves; sleep; cortisol; slow waves; polysomnography
• ISSN: 0953-816X; 1460-9568; 1460-9568
• DOI: 10.1111/ejn.15132

Both stress and sleep enhance emotional memory. They also interact, with the largest effect of sleep on emotional memory being seen when stress occurs shortly before or after encoding. Slow wave sleep (SWS) is critical for long‐term episodic memory, facilitated by the temporal coupling of slow oscillations and sleep spindles. Prior work in humans has shown these associations for neutral information in non‐stressed participants. Whether coupling interacts with stress to facilitate emotional memory formation is unknown. Here, we addressed this question by reanalyzing an existing dataset of 64 individuals. Participants underwent a psychosocial stressor (32) or comparable control (32) prior to the encoding of 150‐line drawings of neutral, positive, and negative images. All participants slept overnight with polysomnography, before being given a surprise memory test the following day. In the stress group, time spent in SWS was positively correlated with memory for images of all valences. Results were driven by those who showed a high cortisol response to the stressor, compared to low responders. The amount of slow oscillation‐spindle coupling during SWS was negatively associated with neutral and emotional memory in the stress group only. The association with emotional memory was significantly stronger than for neutral memory within the stress group. These results suggest that stress around the time of initial memory formation impacts the relationship between slow wave sleep and memory. When emotional memories are formed under stress, the effects of slow wave sleep on retention of those memories differs depending on the sleep measure. Although time spent in slow wave sleep was positively associated with emotional memory following stress, the coupling of sleep spindles and slow oscillations during slow wave sleep was negatively associated with emotional memory following stress. These results suggest that stress around the time of initial memory formation impacts the relationship between slow wave sleep and memory.