Interactive effects of stress reactivity and rapid eye movement sleep theta activity on emotional memory formation

Kim, Sara Y.; Kark, Sarah M.; Daley, Ryan T.; Alger, Sara E.; Rebouças, Daniella; Kensinger, Elizabeth A.; Payne, Jessica D.

doi:10.1002/hipo.23138

Cited by 34 publications

(60 citation statements)

References 99 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…In this sense, being weakly encoded may be low in the hierarchy, and only be consolidated after other information with more "important" tags has been consolidated. Relatedly, a number of studies have implicated REM sleep in emotional memory consolidation (Nishida et al, 2009;van der Helm et al, 2011;Groch et al, 2013;Kim et al, 2019). Our findings on initial encoding strength imply NREM processes, suggesting that different prioritization tags or tags on different types of memories may be read during different stages of sleep.…”

Section: Discussionsupporting

confidence: 57%

Sleep spindles preferentially consolidate weakly encoded memories

Denis

Mylonas

Poskanzer

et al. 2020

Preprint

Self Cite

View full text Add to dashboard Cite

Sleep has been shown to be critical for memory consolidation, and recent research has demonstrated that this consolidation effect is selective, with certain memories being prioritized for strengthening. Initial strength of a memory appears to be one metric the brain uses to prioritize memory traces for sleep-based consolidation, but the role of consolidation-mediating cortical oscillations, such as sleep spindles and slow oscillations, has not been explored. Here, N=54 participants studied pairs of words to three distinct encoding strengths, with recall being tested immediately following learning and again six hours later.N=36 had a two-hour afternoon nap opportunity following learning, whilst the remaining (n=18) remained awake throughout. Results showed a selective benefit of sleep on memory, with sleep preferentially consolidating weakly encoded items (p=.003). The magnitude of this effect (d=0.90, 95%CI=0.29-1.50) was similar when compared to a previous study examining the benefits of a full night of sleep (d=1.36, 95% CI=0.59-2.12). Within the nap group, consolidation of weakly encoded items was associated with sleep spindle density during slow wave sleep (r=.48, p=.003). This association was present when separately examining spindles coupled (r=.41, p=.013), and uncoupled (r=.44, p=.007) with slow oscillations. Memory was significantly better in individuals who showed an amount of slow oscillation-spindle coupling that was greater than what would be expected by chance (p=.006, d=1.15).These relationships were unique to weakly encoded items, with spindles not correlating with memory for intermediate or strong items. This suggests that sleep spindles facilitate selective memory consolidation, guided in part by memory strength. Significance statementGiven the countless pieces of information we encode each day, how does the brain select which memories to commit to long-term storage? Sleep is known to aid in memory consolidation, but less research has examined which memories are prioritized to receive this benefit. Here, we found that compared to staying awake, sleep was associated with better memory for weakly encoded information. This suggests sleep helps to rescue weak memory traces from being forgotten. Sleep spindles, a hallmark oscillation of nonrapid eye movement sleep, mediates consolidation processes. We extended this to show that spindles selectively facilitated consolidation of weakly encoded memories. This provides new evidence for the selective nature of sleep-based consolidation and elucidates a physiological correlate of this preferential benefit.

show abstract

Section: Discussionsupporting

confidence: 57%

Sleep spindles preferentially consolidate weakly encoded memories

Denis

Mylonas

Poskanzer

et al. 2020

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…For analyses of coupling, one participant from the stress group had their data excluded on the basis of being an outlier (>3SD from the mean). Although behavioral results, including efficacy of the TSST in evoking stress, are reported in our previous publication (Kim et al, 2019), we summarize them briefly here. Memory at the recognition test was significantly better for emotional compared to neutral items (t (63) = 2.67, p = .010), a pattern that was true for both negative (t (63) = 2.57, p = .013) and positive (t (63) = .2.28, p = .026) images.…”

Section: Discussionmentioning

confidence: 99%

“…Although much research has linked the consolidation of emotional memories to rapid eye movement sleep (Groch et al, 2013;Kim et al, 2019;Nishida et al, 2009;Sopp et al, 2017;Wagner et al, 2001), newer work suggests SWS plays a role as well (Alger et al, 2018;Kim & Payne, 2020;Payne et al, 2015). In fact, several studies have found relationships between emotional memory and SWS but not REM sleep, raising the question of whether SWS and REM sleep differentially contribute to emotional memory consolidation (Benedict et al, 2009;Payne, 2011Payne, ,, 2014Payne et al, 2015;Wagner et al, 2002).…”

Section: Introductionmentioning

confidence: 99%

“…Although recent theories (Hutchison & Rathore, 2015) and empirical studies (Kim et al, 2019;Nishida et al, 2009;Sopp et al, 2017) of REM sleep and emotional memory consolidation have examined EEG characteristics during REM sleep (e.g. REM theta (4-7Hz) activity), to our knowledge no studies in humans have assessed the role of slow oscillation-spindle coupling during SWS in emotional memory consolidation.…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

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

Denis

Kim

Kark

et al. 2020

Preprint

Self Cite

View full text Add to dashboard Cite

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<.043). Results were primarily driven by those who showed a high cortisol response to the stressor (all r>.65, p<.007), compared to low cortisol responders (all r<.31, all 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.

show abstract

“…Sleep disruptions may, in turn, contribute to effects of stress on memory, affect, autonomic and immune functions. Several recent studies suggest that REM theta and non-REM sharp wave ripple frequencies may serve as useful biosignatures for stress-mediated alterations in brain function (Girardeau et al, 2017;Kim et al, 2019;Nolett et al, 2019).…”

Section: Speeding Translationmentioning

confidence: 99%

Priorities in stress research: a view from the U.S. National Institute of Mental Health

Simmons

Winsky

Zehr

et al. 2020

Stress

View full text Add to dashboard Cite

The mission of the National Institute of Mental Health is to transform the understanding and treatment of mental illnesses through basic and clinical research, paving the way for prevention, recovery, and cure. In consultation with a broad range of experts, the NIMH has identified a set of priorities for stress biology research aimed squarely at creating the basic and clinical knowledge bases for reducing and alleviating mental health burden across the lifespan. Here, we discuss these priority areas in stress biology research, which include: understanding the heterogeneity of stressors and outcomes; refining and expanding the experimental systems used to study stress and its effects; embracing and exploiting the complexity of the stress response; and prioritizing translational studies that seek to test mechanistic hypotheses in human beings. We emphasize the challenge of establishing mechanistic links across levels of analysis to explain how and when specific and diverse stressors lead to enduring changes in neural systems and produce lasting functional deficits in mental health relevant behaviors. An improved understanding of mechanisms underlying stress responses and the functional consequences of stress can and will speed translation from basic research to predictive markers of risk and to improved, personalized interventions for mental illness.

show abstract

Interactive effects of stress reactivity and rapid eye movement sleep theta activity on emotional memory formation

Abstract: This is the author manuscript accepted for publication and has undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. Please cite this article as

Cited by 34 publications

References 99 publications

Sleep spindles preferentially consolidate weakly encoded memories

Sleep spindles preferentially consolidate weakly encoded memories

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

Priorities in stress research: a view from the U.S. National Institute of Mental Health

Contact Info

Product

Resources

About