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Emotional arousal modulates oscillatory correlates of targeted memory reactivation during NREM, but not REM sleep.

ABSTRACT: Rapid eye movement (REM) sleep is considered to preferentially reprocess emotionally arousing memories. We tested this hypothesis by cueing emotional vs. neutral memories during REM and NREM sleep and wakefulness by presenting associated verbal memory cues after learning. Here we show that cueing during NREM sleep significantly improved memory for emotional pictures, while no cueing benefit was observed during REM sleep. On the oscillatory level, successful memory cueing during NREM sleep resulted in significant increases in theta and spindle oscillations with stronger responses for emotional than neutral memories. In contrast during REM sleep, solely cueing of neutral (but not emotional) memories was associated with increases in theta activity. Our results do not support a preferential role of REM sleep for emotional memories, but rather suggest that emotional arousal modulates memory replay and consolidation processes and their oscillatory correlates during NREM sleep.

SUBMITTER: Lehmann M

PROVIDER: S-EPMC5159847 | biostudies-literature | 2016 Dec

REPOSITORIES: biostudies-literature

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Emotional arousal modulates oscillatory correlates of targeted memory reactivation during NREM, but not REM sleep.

Lehmann Mick M Schreiner Thomas T Seifritz Erich E Rasch Björn B

Scientific reports 20161216

Rapid eye movement (REM) sleep is considered to preferentially reprocess emotionally arousing memories. We tested this hypothesis by cueing emotional vs. neutral memories during REM and NREM sleep and wakefulness by presenting associated verbal memory cues after learning. Here we show that cueing during NREM sleep significantly improved memory for emotional pictures, while no cueing benefit was observed during REM sleep. On the oscillatory level, successful memory cueing during NREM sleep result ...[more]

PMID: 27982120

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Project description:The sleep-to-forget, sleep-to-remember (SFSR) hypothesis states that the neurobiological environment provided by rapid-eye movement (REM)-rich sleep decouples the content of an emotional memory from its attendant emotional arousal. This decoupling allows divergent attenuation and enhancement effects (i.e., erosion of the memory's emotional tone and simultaneous strengthening of its content). However, support for this proposal is mixed. An alternative account suggests there might be convergent attenuation and enhancement (i.e., elevated emotional arousal is positively coupled with enhanced emotional memory). We tested predictions emerging from the SFSR hypothesis using (a) individuals diagnosed with post-traumatic stress disorder (PTSD; n = 21), (b) trauma-exposed non-PTSD individuals (n = 19), and (c) healthy controls (n = 20). We included PTSD-diagnosed individuals because they typically experience altered REM sleep, impaired emotional memory, and heightened emotional arousal in response to threatening stimuli. Participants were assessed before and after both an 8-h period of polysomnographically monitored sleep and an 8-h period of waking activity. The assessment included exposure to negatively valenced, positively valenced, and neutral pictures before the 8-h delay, and a recognition task afterward. We measured emotional arousal by recording psychophysiological responses to the pictures, both pre- and post-delay. Results indicated no significant between-group differences in emotional memory accuracy or arousal. However, after a sleep-filled delay, pictures of all categories were recognized with equal accuracy, whereas after a wake-filled delay, negative pictures were recognized preferentially. Furthermore, the findings demonstrated that a sleep-filled delay was associated with attenuated emotional arousal to pictures of all categories, whereas a wake-filled delay was associated with a rise in emotional arousal across the day. Intriguingly, poorer recognition accuracy for valenced (but not neutral) pictures was predicted by an interaction of increased REM fragmentation and increased emotional arousal. In summary, we found some support for the SFSR hypothesis in the way it describes the REM- and arousal-based mechanisms that process emotional material. We also, however, found disconfirming evidence regarding the outcome of that process (i.e., sleep did not favor consolidation of emotional over neutral memory), and we demonstrated a convergence between attenuation of emotional arousal and weakening of emotional content relative to neutral content.

Project description:BackgroundSocial anxiety disorder (SAD) is characterized by a significant amount of fear when confronted to social situations. Exposure therapy, which is based on fear extinction, does not often lead to full remission. Here, based on evidence showing that rapid eye movement (REM) sleep promotes the consolidation of extinction memory, we used targeted memory reactivation (TMR) during REM sleep to enhance extinction learning in SAD.MethodsForty-eight subjects with SAD were randomly assigned to two groups: control or TMR group. All patients had two successive exposure therapy sessions in a virtual reality (VR) environment, where they were asked to give a public talk in front of a virtual jury. At the end of each session, and only in the TMR group (N = 24), a sound was paired to the positive feedback phase of therapy (i.e., approval of their performance), which represented the memory to be strengthened during REM sleep. All participants slept at home with a wearable headband device which automatically identified sleep stages and administered the sound during REM sleep. Participants' anxiety level was assessed using measures of parasympathetic (root mean square of successive differences between normal heartbeats, RMSSD) and sympathetic (non-specific skin conductance responses, ns-SCRs) activity, and subjective measures (Subjective Units of Distress Scale, SUDS), during the preparation phase of their talks before (T1) and after (T2) one full-night's sleep and after 1 week at home (T3). Participants also filled in a dream diary.ResultsWe observed an effect of time on subjective measures of anxiety (SUDS). We did not find any difference in the anxiety levels of the two groups after 1 week of TMR at home. Importantly, the longer the total duration of REM sleep and the more stimulations the TMR group had at home, the less anxious (increased RMSSD) these participants were. Finally, fear in dreams correlated positively with ns-SCRs and SUDS at T3 in the TMR group.ConclusionTMR during REM sleep did not significantly modulate the beneficial effect of therapy on subjective anxiety. Yet, our results support that REM sleep can contribute to extinction processes and substantiate strong links between emotions in dreams and waking stress levels in these patients.

Dataset Information

Emotional arousal modulates oscillatory correlates of targeted memory reactivation during NREM, but not REM sleep.

Publications

Emotional arousal modulates oscillatory correlates of targeted memory reactivation during NREM, but not REM sleep.

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