Delineating memory reactivation in sleep with verbal and non-verbal retrieval cues.

Sleep supports memory consolidation via the reactivation of newly formed memory traces. One way to investigate memory reactivation in sleep is by exposing the sleeping brain to auditory retrieval cues; a paradigm known as targeted memory reactivation. To what extent the acoustic properties of memory cues influence the effectiveness of targeted memory reactivation, however, has received limited attention. We addressed this question by exploring how verbal and non-verbal memory cues affect oscillatory activity linked to memory reactivation in sleep. Fifty-one healthy male adults learned to associate visual stimuli with spoken words (verbal cues) and environmental sounds (non-verbal cues). Subsets of the verbal and non-verbal memory cues were then replayed during sleep. The voice of the verbal cues was either matched or mismatched to learning. Memory cues (relative to unheard control cues) prompted an increase in theta/alpha and spindle power, which have been heavily implicated in sleep-associated memory processing. Moreover, verbal memory cues were associated with a stronger increase in spindle power than non-verbal memory cues. There were no significant differences between the matched and mismatched verbal cues. Our findings suggest that verbal memory cues may be most effective for triggering memory reactivation in sleep, as indicated by an amplified spindle response.

Sleep preferentially consolidates negative aspects of human memory: Well-powered evidence from two large online experiments.

Research suggests that sleep benefits memory. Moreover, it is often claimed that sleep selectively benefits memory for emotionally salient information over neutral information. However, not all scientists are convinced by this relationship [e.g., J. M. Siegel. Curr. Sleep Med. Rep., 7, 15-18 (2021)]. One criticism of the overall sleep and memory literature-like other literature-is that many studies are underpowered and lacking in generalizability [M. J. Cordi, B. Rasch. Curr. Opin. Neurobiol., 67, 1-7 (2021)], thus leaving the evidence mixed and confusing to interpret. Because large replication studies are sorely needed, we recruited over 250 participants spanning various age ranges and backgrounds in an effort to confirm sleep's preferential emotional memory consolidation benefit using a well-established task. We found that sleep selectively benefits memory for negative emotional objects at the expense of their paired neutral backgrounds, confirming our prior work and clearly demonstrating a role for sleep in emotional memory formation. In a second experiment also using a large sample, we examined whether this effect generalized to positive emotional memory. We found that while participants demonstrated better memory for positive objects compared to their neutral backgrounds, sleep did not modulate this effect. This research provides strong support for a sleep-specific benefit on memory consolidation for specifically negative information and more broadly affirms the benefit of sleep for cognition.

The influence of encoding strategy on associative memory consolidation across wake and sleep.

Sleep benefits memory consolidation. However, factors present at initial encoding may moderate this effect. Here, we examined the role that encoding strategy plays in subsequent memory consolidation during sleep. Eighty-nine participants encoded pairs of words using two different strategies. Each participant encoded half of the word pairs using an integrative visualization technique, where the two items were imagined in an integrated scene. The other half were encoded nonintegratively, with each word pair item visualized separately. Memory was tested before and after a period of nocturnal sleep (N = 47) or daytime wake (N = 42) via cued recall tests. Immediate memory performance was significantly better for word pairs encoded using the integrative strategy compared with the nonintegrative strategy (P < 0.001). When looking at the change in recall across the delay, there was significantly less forgetting of integrated word pairs across a night of sleep compared with a day spent awake (P < 0.001), with no significant difference in the nonintegrated pairs (P = 0.19). This finding was driven by more forgetting of integrated compared with not-integrated pairs across the wake delay (P < 0.001), whereas forgetting was equivalent across the sleep delay (P = 0.26). Together, these results show that the strategy engaged in during encoding impacts both the immediate retention of memories and their subsequent consolidation across sleep and wake intervals.

The associations between paranormal beliefs and sleep variables.

Previous studies have found significant associations between paranormal beliefs and sleep variables. However, these have been conducted on a small scale and are limited in the number of sleep variables investigated. This study aims to fill a gap in the literature by investigating paranormal beliefs in relation to a wide range of sleep variables in a large sample. Participants (N = 8853) completed a survey initiated by the BBC Focus Magazine. They reported on their demographics, sleep disturbances and paranormal beliefs. Poorer subjective sleep quality (lower sleep efficiency, longer sleep latency, shorter sleep duration and increased insomnia symptoms) was associated with greater endorsement of belief in: (1) the soul living on after death; (2) the existence of ghosts; (3) demons; (4) an ability for some people to communicate with the dead; (5) near-death experiences are evidence for life after death; and (6) aliens have visited earth. In addition, episodes of exploding head syndrome and isolated sleep paralysis were associated with the belief that aliens have visited earth. Isolated sleep paralysis was also associated with the belief that near-death experiences are evidence for life after death. Findings obtained here indicate that there are associations between beliefs in the paranormal and various sleep variables. This information could potentially better equip us to support sleep via psychoeducation. Mechanisms underlying these associations are likely complex, and need to be further explored to fully understand why people sometimes report "things that go bump in the night".

The effects of cognitive reappraisal and sleep on emotional memory formation.

Emotion regulation (i.e. either up- or down-regulating affective responses to emotional stimuli) has been shown to modulate long-term emotional memory formation. Further, research has demonstrated that the emotional aspects of scenes are preferentially remembered relative to neutral aspects (known as the emotional memory trade-off effect). This trade-off is often enhanced when sleep follows learning, compared to an equivalent period of time spent awake. However, the interactive effects of sleep and emotion regulation on emotional memory are poorly understood. We presented 87 participants with pictures of neutral or negative objects on neutral backgrounds paired with instructions to either increase or decrease their emotional response by altering personal relevance, or to passively view the stimuli. Following a 12 h period of sleep or wakefulness, participants were tested for their memory of objects and backgrounds separately. Although we replicated the emotional memory trade-off effect, no differences in the magnitude of the trade-off effect were observed between regulation conditions. Sleep improved all aspects of memory, but it did not preferentially benefit memory for emotional components of scenes. Irrespective of a period of sleep or wake following encoding, findings suggest emotion regulation during encoding did not influence memory for emotional items at a 12-hour delay.

Sleep Spindles Preferentially Consolidate Weakly Encoded Memories.

Sleep has been shown to be critical for memory consolidation, with some research suggesting that certain memories are prioritized for consolidation. Initial strength of a memory appears to be an important boundary condition in determining which memories are consolidated during sleep. However, the role of consolidation-mediating oscillations, such as sleep spindles and slow oscillations, in this preferential consolidation has not been explored. Here, 54 human participants (76% female) studied pairs of words to three distinct encoding strengths, with recall being tested immediately following learning and again 6 h later. Thirty-six had a 2 h nap opportunity following learning, while the remaining 18 remained awake throughout. Results showed that, across 6 h awake, weakly encoded memories deteriorated the fastest. In the nap group, however, this effect was attenuated, with forgetting rates equivalent across encoding strengths. Within the nap group, consolidation of weakly encoded items was associated with fast sleep spindle density during non-rapid eye movement sleep. Moreover, sleep spindles that were coupled to slow oscillations predicted the consolidation of weak memories independently of uncoupled sleep spindles. 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 memory consolidation, guided in part by memory strength.SIGNIFICANCE STATEMENT Given 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, and it appears that certain memories are prioritized to receive this benefit. Here, we found that, compared with staying awake, sleep was associated with better memory for weakly encoded information. This suggests that sleep helps attenuate the forgetting of weak memory traces. Fast sleep spindles, a hallmark oscillation of non-rapid eye movement sleep, mediate consolidation processes. We extend this to show that fast spindles were uniquely associated with the consolidation of weakly encoded memories. This provides new evidence for preferential sleep-based consolidation and elucidates a physiological correlate of this benefit.

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

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.

Sleep spectral power correlates of prospective memory maintenance.

Prospective memory involves setting an intention to act that is maintained over time and executed when appropriate. Slow wave sleep (SWS) has been implicated in maintaining prospective memories, although which SWS oscillations most benefit this memory type remains unclear. Here, we investigated SWS spectral power correlates of prospective memory. Healthy young adult participants completed three ongoing tasks in the morning or evening. They were then given the prospective memory instruction to remember to press "Q" when viewing the words "horse" or "table" when repeating the ongoing task after a 12-h delay including overnight, polysomnographically recorded sleep or continued daytime wakefulness. Spectral power analysis was performed on recorded sleep EEG. Two additional groups were tested in the morning or evening only, serving as time-of-day controls. Participants who slept demonstrated superior prospective memory compared with those who remained awake, an effect not attributable to time-of-day of testing. Contrary to prior work, prospective memory was negatively associated with SWS. Furthermore, significant increases in spectral power in the delta-theta frequency range (1.56 Hz-6.84 Hz) during SWS was observed in participants who failed to execute the prospective memory instructions. Although sleep benefits prospective memory maintenance, this benefit may be compromised if SWS is enriched with delta-theta activity.

Using EEG microstates to examine post-encoding quiet rest and subsequent word-pair memory.

Evidence suggests that the brain preferentially consolidates memories during "offline" periods, in which an individual is not performing a task and their attention is otherwise undirected, including spans of quiet, resting wakefulness. Moreover, research has demonstrated that factors such as the initial encoding strength of information influence which memories receive the greatest benefit. Recent studies have begun to investigate these periods of post-learning quiet rest using EEG microstate analysis to observe the electrical dynamics of the brain during these stretches of memory consolidation, specifically finding an increase in the amount of the canonical microstate D during a post-encoding rest period. Here, we implement an exploratory analysis to probe the activity of EEG microstates during a post-encoding session of quiet rest in order to scrutinize the impact of learning on microstate dynamics and to further understand the role these microstates play in the consolidation of memories. We examined 54 subjects (41 female) as they completed a word-pair memory task designed to use repetition to vary the initial encoding strength of the word-pair memories. In this study, we were able to replicate previous research in which there was a significant increase (p < .05) in the amount of microstate D (often associated with the dorsal attention network) during post-encoding rest. This change was accompanied by a significant decrease (p < .05) in the amount of microstate C (often associated with the default mode network). We also found preliminary evidence indicating a positive relationship between the amount of microstate D and improved memory for weakly encoded memories, which merits further exploration.

The roles of item exposure and visualization success in the consolidation of memories across wake and sleep.

Memory consolidation during sleep does not benefit all memories equally. Initial encoding strength appears to play a role in governing where sleep effects are seen, but it is unclear whether sleep preferentially consolidates weaker or stronger memories. We manipulated encoding strength along two dimensions-the number of item presentations, and success at visualizing each item, in a sample of 82 participants. Sleep benefited memory of successfully visualized items only. Within these, the sleep-wake difference was largest for more weakly encoded information. These results suggest that the benefit of sleep on memory is seen most clearly for items that are encoded to a lower initial strength.

Subjective sleep-related variables in those who have and have not experienced sleep paralysis.

Research suggests that poor sleep quality is related to the occurrence of sleep paralysis, although the precise relationship between these two variables is unknown. This association has generated interest due to the related possibility that improving sleep quality could help to combat episodes of sleep paralysis. To date, studies examining the association between sleep quality and sleep paralysis have typically measured sleep quality using general measures such as the global score of the Pittsburgh Sleep Quality Index (PSQI). The aim of this study was to increase the precision of our understanding of the relationship between sleep paralysis and other aspects of sleep by investigating associations between different sleep-related variables and sleep paralysis. Using data from the G1219 twin/sibling study, analyses were performed on 860 individuals aged 22-32 years (66% female). Results showed that two components of the PSQI, sleep latency and daytime dysfunction, were predictors of sleep paralysis. In addition, a number of other sleep-related variables were related significantly to sleep paralysis. These were: insomnia symptoms, sleep problems commonly related to traumatic experiences, presleep arousal, cognitions about sleep and excessive daytime sleepiness. There was no relationship with sleep-disordered breathing, diurnal preference or sleeping arrangements. Potential mechanisms underlying these results and suggestions for future research are discussed.

The role of cortical sensorimotor oscillations in action anticipation.

The human mirror neuron system is believed to play an important role in facilitating the ability of athletes to anticipate the actions of an opponent. This system is often assessed with EEG by measuring event-related changes in mu (8-13Hz) sensorimotor oscillations. However, traditional channel-based analyses of this measure are flawed in that due to volume conduction effects mu and non-mu alpha activity can become mixed. This flaw means it is unclear the extent to which mu activity indexes the mirror system, as opposed to other processes such as attentional demand. As a solution to this problem, we use independent component analysis to separate out the underlying brain processes during a tennis-related action observation and anticipation task. We investigated expertise-related differences in independent component activity. Experienced tennis players (N=18) were significantly more accurate than unexperienced novices (N=21) on the anticipation task. EEG results found significant group differences in both the mu and beta (15-25Hz) frequency bands in sensorimotor components, with earlier and greater desynchronisation in the experienced tennis players. In particular, only experienced players showed desynchronisation in the high mu (11-13Hz) band. No group differences were found in posterior alpha components. These results show for the first time that expertise differences during action observation and anticipation are unique to sensorimotor sources, and that no expertise-related differences exist in attention modulated, posterior alpha sources. As such, this paper provides a much cleaner measure of the human mirror system during action observation, and its modulation by motor expertise, than has been possible in previous work.

Terror and bliss? Commonalities and distinctions between sleep paralysis, lucid dreaming, and their associations with waking life experiences.

Sleep paralysis and lucid dreaming are both dissociated experiences related to rapid eye movement (REM) sleep. Anecdotal evidence suggests that episodes of sleep paralysis and lucid dreaming are related but different experiences. In this study we test this claim systematically for the first time in an online survey with 1928 participants (age range: 18-82 years; 53% female). Confirming anecdotal evidence, sleep paralysis and lucid dreaming frequency were related positively and this association was most apparent between lucid dreaming and sleep paralysis episodes featuring vestibular-motor hallucinations. Dissociative experiences were the only common (positive) predictor of both sleep paralysis and lucid dreaming. Both experiences showed different associations with other key variables of interest: sleep paralysis was predicted by sleep quality, anxiety and life stress, whereas lucid dreaming was predicted by a positive constructive daydreaming style and vividness of sensory imagery. Overall, results suggest that dissociative experiences during wakefulness are reflected in dissociative experiences during REM sleep; while sleep paralysis is related primarily to issues of sleep quality and wellbeing, lucid dreaming may reflect a continuation of greater imaginative capacity and positive imagery in waking states.

A twin and molecular genetics study of sleep paralysis and associated factors.

Sleep paralysis is a relatively common but under-researched phenomenon. In this paper we examine prevalence in a UK sample and associations with candidate risk factors. This is the first study to investigate the heritability of sleep paralysis in a twin sample and to explore genetic associations between sleep paralysis and a number of circadian expressed single nucleotide polymorphisms. Analyses are based on data from the Genesis1219 twin/sibling study, a community sample of twins/siblings from England and Wales. In total, data from 862 participants aged 22-32 years (34% male) were used in the study. This sample consisted of monozygotic and dizygotic twins and siblings. It was found that self-reports of general sleep quality, anxiety symptoms and exposure to threatening events were all associated independently with sleep paralysis. There was moderate genetic influence on sleep paralysis (53%). Polymorphisms in the PER2 gene were associated with sleep paralysis in additive and dominant models of inheritance-although significance was not reached once a Bonferroni correction was applied. It is concluded that factors associated with disrupted sleep cycles appear to be associated with sleep paralysis. In this sample of young adults, sleep paralysis was moderately heritable. Future work should examine specific polymorphisms associated with differences in circadian rhythms and sleep homeostasis further in association with sleep paralysis.

Targeted Memory Reactivation during Nonrapid Eye Movement Sleep Enhances Neutral, But Not Negative, Components of Memory.

Emotionally salient components of memory are preferentially remembered at the expense of accompanying neutral information. This emotional memory trade-off is enhanced over time, and possibly sleep, through a process of memory consolidation. Sleep is believed to benefit memory through a process of reactivation during nonrapid eye movement sleep (NREM). Here, targeted memory reactivation (TMR) was used to manipulate the reactivation of negative and neutral memories during NREM sleep. Thirty-one male and female participants encoded composite scenes containing either a negative or neutral object superimposed on an always neutral background. During NREM sleep, sounds associated with the scene object were replayed, and memory for object and background components was tested the following morning. We found that TMR during NREM sleep improved memory for neutral, but not negative scene objects. This effect was associated with sleep spindle activity, with a larger spindle response following TMR cues predicting TMR effectiveness for neutral items only. These findings therefore do not suggest a role of NREM memory reactivation in enhancing the emotional memory trade-off across a 12 h period but do align with growing evidence of spindle-mediated memory reactivation in service of neutral declarative memory.

Age-related positivity effect in emotional memory consolidation from middle age to late adulthood.

Background: While younger adults are more likely to attend to, process, and remember negative relative to positive information, healthy older adults show the opposite pattern. The current study evaluates when, exactly, this positivity shift begins, and how it influences memory performance for positive, negative, and neutral information. Methods: A total of 274 healthy early middle-aged (35-47), late middle-aged (48-59), and older adults (>59) viewed scenes consisting of a negative, positive, or a neutral object placed on a plausible neutral background, and rated each scene for its valence and arousal. After 12 h spanning a night of sleep (n = 137) or a day of wakefulness (n = 137), participants completed an unexpected memory test during which they were shown objects and backgrounds separately and indicated whether the scene component was the "same," "similar," or "new" to what they viewed during the study session. Results and conclusions: We found that both late middle-aged and older adults rated positive and neutral scenes more positively compared to early middle-aged adults. However, only older adults showed better memory for positive objects relative to negative objects, and a greater positive memory trade-off magnitude (i.e., remembering positive objects at the cost of their associated neutral backgrounds) than negative memory trade-off magnitude (i.e., remembering negative objects at the cost of their associated neutral backgrounds). Our findings suggest that while the positivity bias may not emerge in memory until older adulthood, a shift toward positivity in terms of processing may begin in middle age.

Neural reactivation during human sleep.

Sleep promotes memory consolidation: the process by which newly acquired memories are stabilised, strengthened, and integrated into long-term storage. Pioneering research in rodents has revealed that memory reactivation in sleep is a primary mechanism underpinning sleep's beneficial effect on memory. In this review, we consider evidence for memory reactivation processes occurring in human sleep. Converging lines of research support the view that memory reactivation occurs during human sleep, and is functionally relevant for consolidation. Electrophysiology studies have shown that memory reactivation is tightly coupled to the cardinal neural oscillations of non-rapid eye movement sleep, namely slow oscillation-spindle events. In addition, functional imaging studies have found that brain regions recruited during learning become reactivated during post-learning sleep. In sum, the current evidence paints a strong case for a mechanistic role of neural reactivation in promoting memory consolidation during human sleep.

Ears Wide Shut: A Complete Failure to Recognize Relevant Acoustic Stimuli.

The filtering out of apparently extraneous and redundant stimuli is critical for the effective processing of novel and relevant sensory information. But brain mechanisms that evolved to perform this function are necessarily less than perfect, in some cases failing to filter out irrelevant stimuli and in others filtering out important information. We report here on a stimulus from everyday life-the sound made by an arriving elevator, which contains information indicating the car's direction of movement-that not one of over 1,100 study participants was aware of, despite encountering this information repeatedly throughout their lives. Evidence of implicit knowledge of this information was also absent, suggesting that this valuable information is filtered out at an early stage of sensory processing.

Beta spectral power during sleep is associated with impaired recall of extinguished fear.

The failure to retain memory for extinguished fear plays a major role in the maintenance of posttraumatic stress disorder (PTSD), with successful extinction recall necessary for symptom reduction. Disturbed sleep, a hallmark symptom of PTSD, impairs fear extinction recall. However, our understanding of the electrophysiological mechanisms underpinning sleep's role in extinction retention remains underdetermined. We examined the relationship between the microarchitecture of sleep and extinction recall in healthy humans (n = 71, both male and females included) and a pilot study in individuals with PTSD (n = 12). Participants underwent a fear conditioning and extinction protocol over 2 days, with sleep recording occurring between conditioning and extinction. Twenty-four hours after extinction learning, participants underwent extinction recall. Power spectral density (PSD) was computed for pre- and post-extinction learning sleep. Increased beta-band PSD (~17-26 Hz) during pre-extinction learning sleep was associated with worse extinction recall in healthy participants (r = 0.41, p = .004). Beta PSD was highly stable across three nights of sleep (intraclass correlation coefficients > 0.92). Results suggest beta-band PSD is specifically implicated in difficulties recalling extinguished fear.

Emotional memories are enhanced when reactivated in slow wave sleep, but impaired when reactivated in REM.

Sleep supports memory consolidation. However, it is not completely clear how different sleep stages contribute to this process. While rapid eye movement sleep (REM) has traditionally been implicated in the processing of emotionally charged material, recent studies indicate a role for slow wave sleep (SWS) in strengthening emotional memories. Here, to directly examine which sleep stage is primarily involved in emotional memory consolidation, we used targeted memory reactivation (TMR) in REM and SWS during a daytime nap. Contrary to our hypothesis, reactivation of emotional stimuli during REM led to impaired memory. Consistent with this, REM% was correlated with worse recall in the group that took a nap without TMR. Meanwhile, cueing benefit in SWS was strongly correlated with the product of times spent in REM and SWS (SWS-REM product), and reactivation significantly enhanced memory in those with high SWS-REM product. Surprisingly, SWS-REM product was associated with better memory for reactivated items and poorer memory for non-reactivated items, suggesting that sleep both preserved and eliminated emotional memories, depending on whether they were reactivated. Notably, the emotional valence of cued items modulated both sleep spindles and delta/theta power. Finally, we found that emotional memories benefited from TMR more than did neutral ones. Our results suggest that emotional memories decay during REM, unless they are reactivated during prior SWS. Furthermore, we show that active forgetting complements memory consolidation, and both take place across SWS and REM. In addition, our findings expand upon recent evidence indicating a link between sleep spindles and emotional processing.