Targeted memory reactivation in REM but not SWS selectively reduces arousal responses.
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ABSTRACT:
SUBMITTER: Hutchison IC
PROVIDER: S-EPMC7994443 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description: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.
| S-EPMC5159847 | biostudies-literature
Project description:It is now well established that memories can reactivate during non-rapid eye movement (non-REM) sleep, but the question of whether equivalent reactivation can be detected in rapid eye movement (REM) sleep is hotly debated. To examine this, we used a technique called targeted memory reactivation (TMR) in which sounds are paired with learned material in wake, and then re-presented in subsequent sleep, in this case REM, to trigger reactivation. We then used machine learning classifiers to identify reactivation of task-related motor imagery from wake in REM sleep. Interestingly, the strength of measured reactivation positively predicted overnight performance improvement. These findings provide the first evidence for memory reactivation in human REM sleep after TMR that is directly related to brain activity during wakeful task performance.
| S-EPMC10425171 | biostudies-literature
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.
| S-EPMC9281560 | biostudies-literature
Project description:A widely accepted view in memory research is that previously acquired information can be reactivated during sleep, leading to persistent memory storage. Targeted memory reactivation (TMR) was developed as a technique whereby specific memories can be reactivated during sleep using a sensory stimulus linked to prior learning. As a research tool, TMR can improve memory, raising the possibility that it may be useful for cognitive enhancement and clinical therapy. A major challenge for the expanded use of TMR is that a skilled operator must manually control stimulation, which is impractical in many settings. To address this limitation, we developed the SleepStim system for automated TMR in the home. SleepStim includes a smartwatch to collect movement and heart-rate data, plus a smartphone to emit auditory cues. A machine-learning model identifies periods of deep sleep and triggers TMR sounds within these periods. We tested whether this system could replicate the spatial-memory benefit of in-laboratory TMR. Participants learned locations of objects on a grid, and then half of the object locations were reactivated during sleep over 3 nights. Recall was tested each morning. In an experiment with 61 participants, the TMR effect was not significant but varied systematically with stimulus intensity; low-intensity but not high-intensity stimuli produced memory benefits. In a second experiment with 24 participants, we limited stimulus intensity and found that TMR reliably improved spatial memory, consistent with effects observed in laboratory studies. We conclude that SleepStim can effectively accomplish automated TMR, and that avoiding sleep disruption is critical for TMR benefits.
| S-EPMC9649863 | biostudies-literature
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.
| S-EPMC6688536 | biostudies-literature
Project description:Sleep is a complex physiological process with an important role in memory consolidation characterised by a series of spatiotemporal changes in brain activity and connectivity. Here, we investigate how task-related responses differ between pre-sleep wake, sleep, and post-sleep wake. To this end, we trained participants on a serial reaction time task using both right and left hands using Targeted Memory Reactivation (TMR), in which auditory cues are associated with learned material and then re-presented in subsequent wake or sleep periods in order to elicit memory reactivation. The neural responses just after each cue showed increased theta band connectivity between frontal and other cortical regions, as well as between hemispheres, in slow wave sleep compared to pre- or post-sleep wake. This pattern was consistent across the cues associated with both right- and left-handed movements. We also searched for hand-specific connectivity and found that this could be identified in within-hemisphere connectivity after TMR cues during sleep and post-sleep sessions. The fact that we could identify which hand had been cued during sleep suggests that these connectivity measures could potentially be used to determine how successfully memory is reactivated by our manipulation. Collectively, these findings indicate that TMR modulates the brain cortical networks showing clear differences between wake and sleep connectivity patterns.
| S-EPMC10886727 | biostudies-literature
Project description:STUDY OBJECTIVES:To investigate the mechanisms by which auditory targeted memory reactivation (TMR) during slow wave sleep (SWS) influences the consolidation of emotionally negative and neutral memories. DESIGN:Each of 72 (36 negative, 36 neutral) picture-location associations were encoded with a semantically related sound. During a subsequent nap, half of the sounds were replayed in SWS, before picture-location recall was examined in a final test. SETTING:Manchester Sleep Laboratory, University of Manchester. PARTICIPANTS:15 adults (3 male) mean age = 20.40 (standard deviation ± 3.07). INTERVENTIONS:TMR with auditory cues during SWS. MEASUREMENTS AND RESULTS:Performance was assessed by memory accuracy and recall response times (RTs). Data were analyzed with a 2 (sound: replayed/not replayed) × 2 (emotion: negative/neutral) repeated measures analysis of covariance with SWS duration, and then SWS spindles, as the mean-centered covariate. Both analyses revealed a significant three-way interaction for RTs but not memory accuracy. Critically, SWS duration and SWS spindles predicted faster memory judgments for negative, relative to neutral, picture locations that were cued with TMR. CONCLUSIONS:TMR initiates an enhanced consolidation process during subsequent SWS, wherein sleep spindles mediate the selective enhancement of reactivated emotional memories.
| S-EPMC3954173 | biostudies-literature
Project description:ObjectivesCatathrenia is an uncommon and poorly understood disorder, characterized by groaning during sleep occurring in tandem with prolonged expiration. Its classification, pathogenesis, and clinical relevance remain debated, substantially due to the limited number of cases reported to date. We report a series of consecutive cases of catathrenia, their clinical and polysomnographic characteristics, and their subsequent management.MethodsConsecutive patients with catathrenia who had undergone full polysomnography in our institution over a 5.5-year period were included. Catathrenia events (CEs) were examined in clusters, which formulated catathrenia periods (CPs). The relationships between CPs, sleep stage distribution, electroencephalogram (EEG) arousals, and other sleep parameters were assessed, along with the clinical presentation and management of catathrenic patients.ResultsA total of 427 CPs were identified in 38 patients, 81% arising from rapid eye movement (REM) sleep. EEG arousals preceded or coincided with the onset of 84% of CPs, which were of longer duration than those not associated with an arousal (57.3 ± 56.8 vs. 32.2 ± 29.4 s, p < 0.001). Each CE had a characteristic airflow signal, with inspiration preceding a protracted expiration and a brief more rapid exhalation, followed by deep inspiration. Although the majority of patients were referred on the basis of bed partner complaints, 44.7% complained of daytime sleepiness. Continuous positive airway pressure therapy and sleep-consolidating pharmacotherapy led to subjective improvement, but were limited by poor long-term adherence.ConclusionsIn the largest series of catathrenia patients reported to date, we found that this rare disorder is characterized by a distinct breathing pattern and arises predominantly from REM sleep, with arousals almost uniformly preceding or coinciding with the onset of CPs.
| S-EPMC6554196 | biostudies-literature
Project description:Targeted memory reactivation (TMR) is a methodology employed to manipulate memory processing during sleep. TMR studies have great potential to advance understanding of sleep-based memory consolidation and corresponding neural mechanisms. Research making use of TMR has developed rapidly, with over 70 articles published in the last decade, yet no quantitative analysis exists to evaluate the overall effects. Here we present the first meta-analysis of sleep TMR, compiled from 91 experiments with 212 effect sizes (N = 2,004). Based on multilevel modeling, overall sleep TMR was highly effective (Hedges' g = 0.29, 95% CI [0.21, 0.38]), with a significant effect for two stages of non-rapid-eye-movement (NREM) sleep (Stage NREM 2: Hedges' g = 0.32, 95% CI [0.04, 0.60]; and slow-wave sleep: Hedges' g = 0.27, 95% CI [0.20, 0.35]). In contrast, TMR was not effective during REM sleep nor during wakefulness in the present analyses. Several analysis strategies were used to address the potential relevance of publication bias. Additional analyses showed that TMR improved memory across multiple domains, including declarative memory and skill acquisition. Given that TMR can reinforce many types of memory, it could be useful for various educational and clinical applications. Overall, the present meta-analysis provides substantial support for the notion that TMR can influence memory storage during NREM sleep, and that this method can be useful for understanding neurocognitive mechanisms of memory consolidation. (PsycINFO Database Record (c) 2020 APA, all rights reserved).
| S-EPMC7144680 | biostudies-literature
Project description:It is believed that neural representations of recent experiences become reactivated during sleep, and that this process serves to stabilize associated memories in long-term memory. Here, we initiated this reactivation process for specific memories during slow-wave sleep. Participants studied 50 object-location associations with object-related sounds presented concurrently. For half of the associations, the related sounds were re-presented during subsequent slow-wave sleep while participants underwent functional MRI. Compared with control sounds, related sounds were associated with increased activation of right parahippocampal cortex. Postsleep memory accuracy was positively correlated with sound-related activation during sleep in various brain regions, including the thalamus, bilateral medial temporal lobe, and cerebellum. In addition, postsleep memory accuracy was also positively correlated with pre- to postsleep changes in parahippocampal-medial prefrontal connectivity during retrieval of reactivated associations. Our results suggest that the brain is differentially activated by studied and unstudied sounds during deep sleep and that the thalamus and medial temporal lobe are involved in establishing the mnemonic consequences of externally triggered reactivation of associative memories.
| S-EPMC3387124 | biostudies-other