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Recollecting painful or traumatic experiences can be deeply troubling. Sleep may offer an opportunity to reduce such suffering. We developed a procedure to weaken older aversive memories by reactivating newer positive memories during sleep. Participants viewed 48 nonsense words each paired with a unique aversive image, followed by an overnight sleep. In the next evening, participants learned associations between half of the words and additional positive images, creating interference. During the following non-rapid-eye-movement sleep, auditory memory cues were unobtrusively delivered. Upon waking, presenting cues associated with both aversive and positive images during sleep, as opposed to not presenting cues, weakened aversive memory recall while increasing positive memory intrusions. Substantiating these memory benefits, computational modeling revealed that cueing facilitated evidence accumulation toward positive affect judgments. Moreover, cue-elicited theta brain rhythms during sleep predominantly predicted the recall of positive memories. A noninvasive sleep intervention can thus modify aversive recollection and affective responses.
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Señales (Psicología) , Recuerdo Mental , Sueño , Humanos , Femenino , Sueño/fisiología , Masculino , Recuerdo Mental/fisiología , Adulto , Adulto Joven , Memoria/fisiologíaRESUMEN
Consolidating memories for long-term storage depends on reactivation. Reactivation occurs both consciously, during wakefulness, and unconsciously, during wakefulness and sleep. While considerable work has examined conscious awake and unconscious sleep reactivation, in this study, we directly compare the consequences of conscious and unconscious reactivation during wakefulness. Forty-one participants learned associations consisting of adjective-object-position triads. Objects were clustered into distinct semantic groups (e.g., fruits, vehicles) such that we could examine consequences of reactivation on semantically related memories. After an intensive learning protocol, we systematically reactivated some of the triads by presenting the adjective as a cue. Reactivation was done so that it was consciously experienced for some triads, and only unconsciously processed for others. Memory for spatial positions, the most distal part of the association, was affected by reactivation in a consciousness-dependent and memory-strength-dependent manner. Conscious reactivation resulted in weakening of semantically related memories that were strong initially, resonating with prior findings of retrieval-induced forgetting. Unconscious reactivation, on the other hand, selectively benefited weak reactivated memories, as previously shown for reactivation during sleep. Semantically linked memories were not impaired, but rather were integrated with the reactivated memory. These results taken together demonstrate that conscious and unconscious reactivation have qualitatively different consequences. Results support a consciousness-dependent inhibition account, whereby unconscious reactivation entails less inhibition than conscious reactivation, thus allowing more liberal spread of activation. Findings set the stage for additional exploration into the role of conscious experience in memory storage and structuring.
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Aprendizaje , Consolidación de la Memoria , Humanos , Estado de Conciencia , Vigilia/fisiología , Sueño/fisiología , Inhibición Psicológica , Consolidación de la Memoria/fisiologíaRESUMEN
One can be aware of the effort needed to memorize a new fact or to recall the name of a new acquaintance. Because of experiences like this, learning can seem to have only two components, encoding information and, after some delay, retrieving information. To the contrary, learning entails additional, intervening steps that sometimes are hidden from the learner. For firmly acquiring fact and event knowledge in particular, learners are generally not cognizant of the necessity of offline consolidation. The memories that persist to be available reliably at a later time, according to the present conceptualization, are the ones we repeatedly rehearse and integrate with other knowledge, whether we do this intentionally or unknowingly, awake or asleep. This article examines the notion that learning is not a function of waking brain activity alone. What happens in the brain while we sleep also impacts memory storage, and consequently is a critical component of learning. The idea that memories can change over time and become enduring has long been present in memory research and is foundational for the concept of memory consolidation. Nevertheless, the notion that memory consolidation happens during sleep faced much resistance before eventually being firmly established. Research is still needed to elucidate the operation and repercussions of repeated reactivation during sleep. Comprehensively understanding how offline memory reactivation contributes to learning is vital for both theoretical and practical considerations.
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Aprendizaje , Consolidación de la Memoria , Humanos , Aprendizaje/fisiología , Sueño/fisiología , Encéfalo/fisiología , Recuerdo Mental/fisiología , Consolidación de la Memoria/fisiologíaRESUMEN
Recent work on perceptual learning for speech has suggested that while high-variability training typically results in generalization, low-variability exposure can sometimes be sufficient for cross-talker generalization. We tested predictions of a similarity-based account, according to which, generalization depends on training-test talker similarity rather than on exposure to variability. We compared perceptual adaptation to second-language (L2) speech following single- or multiple-talker training with a round-robin design in which four L2 English talkers from four different first-language (L1) backgrounds served as both training and test talkers. After exposure to 60 L2 English sentences in one training session, cross-talker/cross-accent generalization was possible (but not guaranteed) following either multiple- or single-talker training with variation across training-test talker pairings. Contrary to predictions of the similarity-based account, adaptation was not consistently better for identical than for mismatched training-test talker pairings, and generalization patterns were asymmetrical across training-test talker pairs. Acoustic analyses also revealed a dissociation between phonetic similarity and cross-talker/cross-accent generalization. Notably, variation in adaptation and generalization related to variation in training phase intelligibility. Together with prior evidence, these data suggest that perceptual learning for speech may benefit from some combination of exposure to talker variability, training-test similarity, and high training phase intelligibility.
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Aprendizaje , Habla , Fonética , Generalización Psicológica , LenguajeRESUMEN
Newly formed memories are not passively stored for future retrieval; rather, they are reactivated offline and thereby strengthened and transformed. However, reactivation is not a uniform process: it occurs throughout different states of consciousness, including conscious rehearsal during wakefulness and unconscious processing during both wakefulness and sleep. In this study, we explore the consequences of reactivation during conscious and unconscious awake states. Forty-one participants learned associations consisting of adjective-object-position triads. Objects were clustered into distinct semantic groups (e.g., multiple fruits, vehicles, musical instruments) which allowed us to examine the consequences of reactivation on semantically-related memories. After an extensive learning phase, some triads were reactivated consciously, through cued retrieval, or unconsciously, through subliminal priming. In both conditions, the adjective was used as the cue. Reactivation impacted memory for the most distal association (i.e., the spatial position of associated objects) in a consciousness-dependent and memory-strength-dependent manner. First, conscious reactivation of a triad resulted in a weakening of other semantically related memories, but only those that were initially more accurate (i.e., memories with lower pre-reactivation spatial errors). This is similar to what has been previously demonstrated in studies employing retrieval-induced forgetting designs. Unconscious reactivation, on the other hand, benefited memory selectively for weak cued items. Semantically linked associations were not impaired, but rather integrated with the reactivated memory. Taken together, our results demonstrate that conscious and unconscious reactivation of memories during wakefulness have qualitatively different consequences on memory for distal associations. Effects are memory-strength-dependent, as has been shown for reactivation during sleep. Results support a consciousness-dependent inhibition account, according to which unconscious reactivation involves less inhibitory dynamics than conscious reactivation, thus allowing more liberal spread of activation. Our findings set the stage for additional exploration into the role of consciousness in memory structuring.
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New memories are not quarantined from each other when first encoded; rather, they are interlinked with memories that were encoded in temporal proximity or that share semantic features. By selectively biasing memory processing during sleep, here we test whether context influences sleep consolidation. Participants first formed 18 idiosyncratic narratives, each linking four objects together. Before sleep, they also memorized an on-screen position for each object. During sleep, 12 object-specific sounds were unobtrusively presented, thereby cuing the corresponding spatial memories and impacting spatial recall as a function of initial memory strength. As hypothesized, we find that recall for non-cued objects contextually linked with cued objects also changed. Post-cue electrophysiological responses suggest that activity in the sigma band supports context reinstatement and predicts context-related memory benefits. Concurrently, context-specific electrophysiological activity patterns emerge during sleep. We conclude that reactivation of individual memories during sleep evokes reinstatement of their context, thereby impacting consolidation of associated knowledge.
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Consolidación de la Memoria , Humanos , Consolidación de la Memoria/fisiología , Recuerdo Mental/fisiología , Señales (Psicología) , Sueño/fisiología , Memoria EspacialRESUMEN
A widely accepted view in memory research is that recently stored information can be reactivated during sleep, leading to memory strengthening. Two recent studies have shown that this effect can be reversed in participants with highly disrupted sleep. To test whether weakening of reactivated memories can result directly from sleep disruption, in this experiment we varied the intensity of memory reactivation cues such that some produced sleep arousals. Prior to sleep, participants (local community members) learned the locations of 75 objects, each accompanied by a sound naturally associated with that object. Location recall was tested before and after sleep, and a subset of the sounds was presented during sleep to provoke reactivation of the corresponding locations. Reactivation with sleep arousal weakened memories, unlike the improvement typically found after reactivation without sleep arousal. We conclude that reactivated memories can be selectively weakened during sleep, and that memory reactivation may strengthen or weaken memories depending on additional factors such as concurrent sleep disruption.
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Señales (Psicología) , Consolidación de la Memoria , Humanos , Recuerdo Mental/fisiología , Aprendizaje/fisiología , Sueño/fisiología , Nivel de AlertaRESUMEN
During sleep, recently acquired episodic memories (i.e., autobiographical memories for specific events) are strengthened and transformed, a process termed consolidation. These memories are contextual in nature, with details of specific features interwoven with more general properties such as the time and place of the event. In this study, we hypothesized that the context in which a memory is embedded would guide the process of consolidation during sleep. To test this idea, we used a spatial memory task and considered changes in memory over a 10-h period including either sleep or wake. In both conditions, participants (N = 62) formed stories that contextually bound four objects together and then encoded the on-screen spatial position of all objects. Results showed that the changes in memory over the sleep period were correlated among contextually linked objects, whereas no such effect was identified for the wake group. These results demonstrate that context-binding plays an important role in memory consolidation during sleep.
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Consolidación de la Memoria , Memoria Episódica , Sueño , Humanos , Memoria EspacialRESUMEN
Post-learning sleep contributes to memory consolidation. Yet it remains contentious whether sleep affords opportunities to modify or update emotional memories, particularly when people would prefer to forget those memories. Here, we attempted to update memories during sleep, using spoken positive words paired with cues to recent memories of aversive events. Affective updating using positive words during human non-rapid eye movement (NREM) sleep, compared with using neutral words instead, reduced negative affective judgments in post-sleep tests, suggesting that the recalled events were perceived as less aversive. Electroencephalogram (EEG) analyses showed that positive words modulated theta and spindle/sigma activity; specifically, to the extent that theta power was larger for the positive words than for the memory cues that followed, participants judged the memory cues less negatively. Moreover, to the extent that sigma power was larger for the positive words than for the memory cues that followed, participants forgot more episodic details about aversive events. Notably, when the onset of individual positive words coincided with the up-phase of slow oscillations (a state characterized by increased cortical excitability during NREM sleep), affective updating was more successful. In sum, we altered the affective content of memories via the strategic pairing of positive words and memory cues during sleep, linked with EEG theta power increases and the slow oscillation up-phase. These findings suggest novel possibilities for modifying unwanted memories during sleep, which would not require people to consciously confront memories that they prefer to avoid.
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Memoria , Sueño , Humanos , Aprendizaje , Recuerdo Mental , Emociones , ElectroencefalografíaRESUMEN
To understand how memories are reactivated and consolidated during sleep, experimenters have employed the unobtrusive re-presentation of memory cues from a variety of pre-sleep learning tasks. Using this procedure, known as targeted memory reactivation (TMR), we previously found that reactivation of counter-social-bias training during post-training sleep could selectively enhance training effects in reducing unintentional social biases. Here, we describe re-analyses of electroencephalographic (EEG) data from this previous study to characterize neurophysiological correlates of TMR-induced bias reduction. We found that TMR benefits in bias reduction were associated with (a) the timing of memory-related cue presentation relative to the 0.1-1.5 Hz slow-oscillation phase and (b) cue-elicited EEG power within the 1-4 Hz delta range. Although cue delivery was at a fixed rate in this study and not contingent on the slow-oscillation phase, cues were found to be clustered in slow-oscillation upstates for those participants with stronger TMR benefits. Similarly, higher cue-elicited delta power 250-1000 ms after cue onset was also linked with larger TMR benefits. These electrophysiological results substantiate the claim that memory reactivation altered social bias in the original study, while also informing neural explanations of these benefits. Future research should consider these sleep physiology parameters in relation to TMR applications and to memory reactivation in general.
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Señales (Psicología) , Electroencefalografía , Humanos , Sesgo , Aprendizaje , SueñoRESUMEN
Memories of waking-life events are incorporated into dreams, but their incorporation is not uniform across a night of sleep. This study aimed to elucidate ways in which such memory sources vary by sleep stage and time of night. Twenty healthy participants (11 F; 24.1 ± 5.7 years) spent a night in the laboratory and were awakened for dream collection approximately 12 times spread across early, middle, and late periods of sleep, while covering all stages of sleep (N1, N2, N3, REM). In the morning, participants identified and dated associated memories of waking-life events for each dream report, when possible. The incorporation of recent memory sources in dreams was more frequent in N1 and REM than in other sleep stages. The incorporation of distant memories from over a week ago, semantic memories not traceable to a single event, and anticipated future events remained stable throughout sleep. In contrast, the relative proportions of recent versus distant memory sources changed across the night, independently of sleep stage, with late-night dreams in all stages having relatively less recent and more remote memory sources than dreams earlier in the night. Qualitatively, dreams tended to repeat similar themes across the night and in different sleep stages. The present findings clarify the temporal course of memory incorporations in dreams, highlighting a specific connection between time of night and the temporal remoteness of memories. We discuss how dream content may, at least in part, reflect the mechanisms of sleep-dependent memory consolidation.
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Sueños , Sueño REM , Humanos , Fases del Sueño , Sueño , MemoriaRESUMEN
Human accomplishments depend on learning, and effective learning depends on consolidation. Consolidation is the process whereby new memories are gradually stored in an enduring way in the brain so that they can be available when needed. For factual or event knowledge, consolidation is thought to progress during sleep as well as during waking states and to be mediated by interactions between hippocampal and neocortical networks. However, consolidation is difficult to observe directly but rather is inferred through behavioral observations. Here, we investigated overnight memory change by measuring electrical activity in and near the hippocampus. Electroencephalographic (EEG) recordings were made in five patients from electrodes implanted to determine whether a surgical treatment could relieve their seizure disorders. One night, while each patient slept in a hospital monitoring room, we recorded electrophysiological responses to 10 to 20 specific sounds that were presented very quietly, to avoid arousal. Half of the sounds had been associated with objects and their precise spatial locations that patients learned before sleep. After sleep, we found systematic improvements in spatial recall, replicating prior results. We assume that when the sounds were presented during sleep, they reactivated and strengthened corresponding spatial memories. Notably, the sounds also elicited oscillatory intracranial EEG activity, including increases in theta, sigma, and gamma EEG bands. Gamma responses, in particular, were consistently associated with the degree of improvement in spatial memory exhibited after sleep. We thus conclude that this electrophysiological activity in the hippocampus and adjacent medial temporal cortex reflects sleep-based enhancement of memory storage.
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Consolidación de la Memoria , Humanos , Sueño/fisiología , Recuerdo Mental/fisiología , Encéfalo , Hipocampo/fisiología , Memoria EspacialRESUMEN
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.
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Consolidación de la Memoria , Sueño , Humanos , Estimulación Acústica , Sueño/fisiología , Recuerdo Mental/fisiología , Señales (Psicología) , Aprendizaje/fisiología , Consolidación de la Memoria/fisiologíaRESUMEN
For a large proportion of our daily lives, spontaneously occurring thoughts tend to disengage our minds from goal-directed thinking. Previous studies showed that EEG features such as the P3 and alpha oscillations can predict mind-wandering to some extent, but only with accuracies of around 60%. A potential candidate for improving prediction accuracy is the Steady-State Visual Evoked Potential (SSVEP), which is used frequently in single-trial contexts such as brain-computer interfaces as a marker of the direction of attention. In this study, we modified the sustained attention to response task (SART) that is usually employed to measure spontaneous thought to incorporate the SSVEP elicited by a 12.5-Hz flicker. We then examined whether the SSVEP could track and allow for the prediction of the stickiness and task-relatedness dimensions of spontaneous thought. Our results show that the SSVEP evoked by flickering words was able to distinguish between more and less sticky thinking but not between whether a participant was on- or off-task. This suggests that the SSVEP is able to track spontaneous thinking when it is strongly disengaged from the task (as in the sticky form of off-task thinking) but not off-task thought in general. Future research should determine the exact dimensions of spontaneous thought to which the SSVEP is most sensitive.
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Face memory, including the ability to recall a person's name, is of major importance in social contexts. Like many other memory functions, it may rely on sleep. We investigated whether targeted memory reactivation during sleep could improve associative and perceptual aspects of face memory. Participants studied 80 face-name pairs, and then a subset of spoken names with associated background music was presented unobtrusively during a daytime nap. This manipulation preferentially improved name recall and face recognition for those reactivated face-name pairs, as modulated by two factors related to sleep quality; memory benefits were positively correlated with the duration of stage N3 sleep (slow-wave sleep) and negatively correlated with measures of sleep disruption. We conclude that (a) reactivation of specific face-name memories during sleep can strengthen these associations and the constituent memories, and that (b) the effectiveness of this reactivation depends on uninterrupted N3 sleep.
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Therapies focused on lucid dreaming could be useful for treating various sleep disorders and other conditions. Still, one major roadblock is the paucity of systematic information on the consequences of attempting these sorts of dreams. The current study sought to quantify positive and negative aspects of seeking lucid dreams, describe their phenomenology in detail, and identify features associated with positive or negative experiences. Observational data from a massive lucid-dream discussion forum were analyzed to capture lucid-dreaming themes. Forum posts were independently rated on multiple dimensions hypothesized to contribute to the valence of lucidity-related phenomena. Our results revealed that lucid dreams can end nightmares and prevent their recurrence, but they can also induce harrowing dysphoric dreams. The realization of dreaming (lucidity) and dreams with high-control were both associated with positive experiences. We translated our results into a process model that describes the progression from lucid dream induction to waking benefit, identifying potential areas of concern. Our results and model suggest that negative outcomes primarily result from failed induction attempts or lucid dreams with low dream control, and that successfully inducing high-control lucid dreams poses low risk for negative outcomes. Lucid dreaming has valuable therapeutic and recreational potential, but a better understanding of the risks is required. Our findings provide new insights into possible negative repercussions and how to avoid them in future applications.
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Memory reactivation during sleep reinforces various types of learning. Basic motor skills likely benefit from sleep. There is insufficient evidence, however, on whether memory reactivation during sleep contributes to learning how to execute a novel action. Here, we investigated motor learning in a myoelectric feedback task. Human male and female participants learned to control myoelectric activity in specific arm muscles to move a computer cursor to each of 16 locations. Each location was associated with a unique sound. Half of the sounds were played during slow-wave sleep to reactivate corresponding memories of muscle control. After sleep, movements cued during sleep were performed more quickly and efficiently than uncued movements. These results demonstrated that memory reactivation during sleep contributes to learning of action execution. We conclude that sleep supports learning novel actions, which also maps onto the learning required in certain neurorehabilitation procedures.SIGNIFICANCE STATEMENT Prior literature on motor learning has produced much evidence supporting a role for sleep but scant evidence on the execution component. This aspect of learning is critical for many complex skills that people value in their lives. Our results not only implicate sleep in skill learning but also pinpoint a benefit for motor execution using a method for modifying memory storage during sleep. We used targeted memory reactivation (TMR), whereby a stimulus that has been associated with learning is presented again during sleep to bring on a recapitulation of waking brain activity. Our demonstration that memory reactivation contributed to skilled performance may be relevant for neurorehabilitation as well as fields concerned with motor learning, such as kinesiology and physiology.
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Memoria/fisiología , Destreza Motora/fisiología , Refuerzo en Psicología , Sueño/fisiología , Adolescente , Adulto , Femenino , Humanos , Masculino , Adulto JovenRESUMEN
Humans are highly attuned to patterns in the environment. This ability to detect environmental patterns, referred to as statistical learning, plays a key role in many diverse aspects of cognition. However, the spatiotemporal neural mechanisms underlying implicit statistical learning, and how these mechanisms may relate or give rise to explicit learning, remain poorly understood. In the present study, we investigated these different aspects of statistical learning by using an auditory nonlinguistic statistical learning paradigm combined with magnetoencephalography. Twenty-four healthy volunteers were exposed to structured and random tone sequences, and statistical learning was quantified by neural entrainment. Already early during exposure, participants showed strong entrainment to the embedded tone patterns. A significant increase in entrainment over exposure was detected only in the structured condition, reflecting the trajectory of learning. While source reconstruction revealed a wide range of brain areas involved in this process, entrainment in areas around the left pre-central gyrus as well as right temporo-frontal areas significantly predicted behavioral performance. Sensor level results confirmed this relationship between neural entrainment and subsequent explicit knowledge. These results give insights into the dynamic relation between neural entrainment and explicit learning of triplet structures, suggesting that these two aspects are systematically related yet dissociable. Neural entrainment reflects robust, implicit learning of underlying patterns, whereas the emergence of explicit knowledge, likely built on the implicit encoding of structure, varies across individuals and may depend on factors such as sufficient exposure time and attention.