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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Targeted memory reactivation of face-name learning depends on ample and undisturbed slow-wave sleep
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.
more » « less- Award ID(s):
- 1921678
- PAR ID:
- 10361533
- Publisher / Repository:
- Nature Publishing Group
- Date Published:
- Journal Name:
- npj Science of Learning
- Volume:
- 7
- Issue:
- 1
- ISSN:
- 2056-7936
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Sleep's role in memory consolidation is widely acknowledged, but its role in weakening memories is still debated. Memory weakening is evolutionary beneficial and makes an integral contribution to cognition. We sought evidence on whether sleep-based memory reactivation can facilitate memory suppression. Participants learned pairs of associable words (e.g., DIET–CREAM) and were then exposed to hint words (e.g., DIET) and instructed to either recall (“think”) or suppress (“no-think”) the corresponding target words (e.g., CREAM). As expected, suppression impaired retention when tested immediately after a 90-min nap. To test if reactivation could selectively enhance memory suppression during sleep, we unobtrusively presented one of two sounds conveying suppression instructions during sleep, followed by hint words. Results showed that targeted memory reactivation did not enhance suppression-induced forgetting. Although not predicted, post-hoc analyses revealed that sleep cues strengthened memory, but only for suppressed pairs that were weakly encoded before sleep. The results leave open the question of whether memory suppression can be augmented during sleep, but suggest strategies for future studies manipulating memory suppression during sleep. Additionally, our findings support the notion that sleep reactivation is particularly beneficial for weakly encoded information, which may be prioritized for consolidation.
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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 non-rapid 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-hour period but do align with growing evidence of spindle-mediated memory reactivation in service of neutral declarative memory.
Significance statement Memory reactivation during sleep is believed to be a key mechanism facilitating consolidation, the strengthening and stabilisation of memories over time. Emotional memories appear to be preferentially consolidated compared to neutral information, but the role sleep-related memory reactivation in this process is still unclear. Here, we found that experimentally reactivating memories during sleep in humans did not preferentially enhance emotional memory components but did improve neutral memory when tested after one night of sleep. These findings speak against a role of memory reactivation in the early stages of emotional memory consolidation. -
The context in which learning occurs is sufficient to reconsolidate stored memories and neuronal reactivation may be crucial to memory consolidation during sleep. The mechanisms of context-dependent and sleep-dependent memory (re)consolidation are unknown but involve the hippocampus. We simulated memory (re)consolidation using a connectionist model of the hippocampus that explicitly accounted for its dorsoventral organization and for CA1 proximodistal processing. Replicating human and rodent (re)consolidation studies yielded the following results. (1) Semantic overlap between memory items and extraneous learning was necessary to explain experimental data and depended crucially on the recurrent networks of dorsal but not ventral CA3. (2) Stimulus-free, sleep-induced internal reactivations of memory patterns produced heterogeneous recruitment of memory items and protected memories from subsequent interference. These simulations further suggested that the decrease in memory resilience when subjects were not allowed to sleep following learning was primarily due to extraneous learning. (3) Partial exposure to the learning context during simulated sleep (i.e., targeted memory reactivation) uniformly increased memory item reactivation and enhanced subsequent recall. Altogether, these results show that the dorsoventral and proximodistal organization of the hippocampus may be important components of the neural mechanisms for context-based and sleep-based memory (re)consolidations.more » « less
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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.
