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

AbstractSleep 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.

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How mood challenges emotional memory formation: An fMRI investigation

NeuroImage ◽

10.1016/j.neuroimage.2011.02.061 ◽

2011 ◽

Vol 56 (3) ◽

pp. 1783-1790 ◽

Cited By ~ 29

Author(s):

Daniel A. Fitzgerald ◽

Jennifer F. Arnold ◽

Eni S. Becker ◽

Anne E.M. Speckens ◽

Mike Rinck ◽

...

Keyword(s):

Emotional Memory ◽

Memory Formation

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Effects of Acute Methamphetamine on Emotional Memory Formation in Humans: Encoding vs Consolidation

PLoS ONE ◽

10.1371/journal.pone.0117062 ◽

2015 ◽

Vol 10 (2) ◽

pp. e0117062 ◽

Cited By ~ 3

Author(s):

Michael E. Ballard ◽

Jessica Weafer ◽

David A. Gallo ◽

Harriet de Wit

Keyword(s):

Emotional Memory ◽

Memory Formation

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Author response: Slow oscillation-spindle coupling predicts enhanced memory formation from childhood to adolescence

10.7554/elife.53730.sa2 ◽

2020 ◽

Cited By ~ 1

Author(s):

Michael A Hahn ◽

Dominik Heib ◽

Manuel Schabus ◽

Kerstin Hoedlmoser ◽

Randolph F Helfrich

Keyword(s):

Memory Formation ◽

Slow Oscillation ◽

Author Response

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Genetic variation of the α2b-adrenoceptor affects neural correlates of successful emotional memory formation

Human Brain Mapping ◽

10.1002/hbm.21171 ◽

2011 ◽

Vol 32 (12) ◽

pp. 2096-2103 ◽

Cited By ~ 12

Author(s):

Maren Urner ◽

Guido van Wingen ◽

Barbara Franke ◽

Mark Rijpkema ◽

Guillén Fernández ◽

...

Keyword(s):

Genetic Variation ◽

Neural Correlates ◽

Emotional Memory ◽

Memory Formation

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Longitudinal brain changes in MDD during emotional encoding: effects of presence and persistence of symptomatology

Psychological Medicine ◽

10.1017/s0033291719001259 ◽

2019 ◽

Vol 50 (8) ◽

pp. 1316-1326 ◽

Cited By ~ 2

Author(s):

Hui Ai ◽

Esther M. Opmeer ◽

Jan-Bernard C. Marsman ◽

Dick J. Veltman ◽

Nic J. A. van der Wee ◽

...

Keyword(s):

Depressive Symptoms ◽

Symptom Severity ◽

Recognition Task ◽

Brain Activation ◽

Emotional Memory ◽

Symptomatic Improvement ◽

Memory Formation ◽

State Dependency ◽

State Dependent ◽

Over Time

AbstractBackgroundThe importance of the hippocampus and amygdala for disrupted emotional memory formation in depression is well-recognized, but it remains unclear whether functional abnormalities are state-dependent and whether they are affected by the persistence of depressive symptoms.MethodsThirty-nine patients with major depressive disorder and 28 healthy controls were included from the longitudinal functional magnetic resonance imaging (fMRI) sub-study of the Netherlands Study of Depression and Anxiety. Participants performed an emotional word-encoding and -recognition task during fMRI at baseline and 2-year follow-up measurement. At baseline, all patients were in a depressed state. We investigated state-dependency by relating changes in brain activation over time to changes in symptom severity. Furthermore, the effect of time spent with depressive symptoms in the 2-year interval was investigated.ResultsSymptom change was linearly associated with higher activation over time of the left anterior hippocampus extending to the amygdala during positive and negative word-encoding. Especially during positive word encoding, this effect was driven by symptomatic improvement. There was no effect of time spent with depression in the 2-year interval on change in brain activation. Results were independent of medication- and psychotherapy-use.ConclusionUsing a longitudinal within-subjects design, we showed that hippocampal–amygdalar activation during emotional memory formation is related to depressive symptom severity but not persistence (i.e. time spent with depression or ‘load’), suggesting functional activation patterns in depression are not subject to functional ‘scarring’ although this hypothesis awaits future replication.

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The costs and benefits of emotional memory formation

10.26481/dis.20071025rh ◽

2007 ◽

Author(s):

R. Hurlemann

Keyword(s):

Emotional Memory ◽

Memory Formation ◽

Costs And Benefits

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Stress Alters the Neural Context for Building New Memories

Journal of Cognitive Neuroscience ◽

10.1162/jocn_a_01613 ◽

2020 ◽

Vol 32 (12) ◽

pp. 2226-2240

Author(s):

Jacqueline Katharina Meier ◽

Mathias Weymar ◽

Lars Schwabe

Keyword(s):

Neural Activity ◽

Human Memory ◽

Emotional Memory ◽

Stimulus Onset ◽

Memory Formation ◽

Stressful Events ◽

Oscillatory Activity ◽

Control Procedure ◽

Alternative Mechanism ◽

Stress Changes

Stressful events affect mnemonic processing, in particular for emotionally arousing events. Previous research on the mechanisms underlying stress effects on human memory focused on stress-induced changes in the neural activity elicited by a stimulus. We tested an alternative mechanism and hypothesized that stress may already alter the neural context for successful memory formation, reflected in the neural activity preceding a stimulus. Therefore, 69 participants underwent a stress or control procedure before encoding neutral and negative pictures. During encoding, we recorded high-density EEG and analyzed—based on multivariate searchlight analyses—oscillatory activity and cross-frequency coupling patterns before stimulus onset that were predictive of memory tested 24 hr later. Prestimulus theta predicted subsequent memory in controls but not in stressed participants. Instead, prestimulus gamma predicted successful memory formation after stress, specifically for emotional material. Likewise, stress altered the patterns of prestimulus theta–beta and theta–gamma phase–amplitude coupling predictive of subsequent memory, again depending on the emotionality of the presented material. Our data suggest that stress changes the neural context for building new memories, tuning this neural context specifically to the encoding of emotionally salient events. These findings point to a yet unknown mechanism through which stressful events may change (emotional) memory formation.

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