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 ϭ 2,004). Based on multilevel modeling, overall sleep TMR was highly effective (Hedges' g ϭ 0.29, 95% CI [0.21, 0.38]), with a significant effect for two stages of non-rapid-eyemovement (NREM) sleep (Stage NREM 2: Hedges' g ϭ 0.32, 95% CI [0.04, 0.60]; and slow-wave sleep: Hedges' g ϭ 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. Public Significance StatementSensory cues can be used to reactivate associated memories during sleep and thus promote memory consolidation. This meta-analysis shows that targeted memory reactivation during sleep can improve memory performance with a small to moderate effect, and that this effect is most clearly evident when memories are reactivated during Stages 2 and 3 of non-rapid-eye-movement (NREM) sleep.
Competition between memories can cause weakening of those memories. Here we investigated memory competition during sleep in human participants by presenting auditory cues that had been linked to two distinct picture-location pairs during wake. We manipulated competition during learning by requiring participants to rehearse picture-location pairs associated with the same sound either competitively (choosing to rehearse one over the other, leading to greater competition) or separately; we hypothesized that greater competition during learning would lead to greater competition when memories were cued during sleep. With separate-pair learning, we found that cueing benefited spatial retention. With competitive-pair learning, no benefit of cueing was observed on retention, but cueing impaired retention of well-learned pairs (where we expected strong competition). During sleep, post-cue beta power (16-30 Hz) indexed competition and predicted forgetting, whereas sigma power (11-16 Hz) predicted subsequent retention. Taken together, these findings show that competition between memories during learning can modulate how they are consolidated during sleep.
Memory encoding for important information can be enhanced both by reward anticipation and by intentional strategies. These effects are hypothesized to depend on distinct neural mechanisms, yet prior work has provided only limited evidence for their separability. We aimed to determine whether reward-driven and strategic mechanisms for prioritizing important information are separable, even if they may also interact. We examined the joint operation of both mechanisms using fMRI measures of brain activity. Participants learned abstract visual images in a value-directed recognition paradigm. On each trial, two novel images were presented simultaneously in different screen quadrants, one arbitrarily designated as high point value and one as low value. Immediately after each block of 16 study trials, the corresponding point rewards could be obtained in a test of item recognition and spatial location memory. During encoding trials leading to successful subsequent memory, especially of high-value images, increased activity was observed in dorsal frontoparietal and lateral occipitotemporal cortex. Furthermore, activity in a network associated with reward was higher during encoding when any image, of high or low value, was subsequently remembered. Functional connectivity between right medial temporal lobe and right ventral tegmental area, measured via psychophysiological interaction, was also greater during successful encoding regardless of value. Strategic control of memory, as indexed by successful prioritization of the high-value image, affected activity in dorsal posterior parietal cortex as well as connectivity between this area and right lateral temporal cortex. These results demonstrate that memory can be strengthened by separate neurocognitive mechanisms for strategic control versus reward-based enhancement of processing.
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Language input is highly variable; phonological, lexical and syntactic features vary systematically across different speakers, geographic regions, and social contexts. Previous evidence shows that language users are sensitive to these contextual changes and that they can rapidly adapt to local regularities. For example, listeners quickly adjust to accented speech, facilitating comprehension. It has been proposed that this type of adaptation is a form of implicit learning. The present study examined a similar type of adaptation, syntactic adaptation, in order to address two issues: (1) whether language comprehenders are sensitive to a subtle probabilistic contingency between an extraneous feature (font color) and syntactic structure, and (2) whether this sensitivity should be attributed to implicit learning. Participants read a large set of sentences, 40% of which were garden-path sentences containing temporary syntactic ambiguities. Critically, but unbeknownst to participants, font color probabilistically predicted the presence of a garden-path structure, with 75% of garden-path sentences (and 25% of normative sentences) appearing in a given font color. Event-related brain potentials (ERPs) were recorded during sentence processing. Almost all participants indicated no conscious awareness of the relationship between font color and sentence structure. Nonetheless, after sufficient time to learn this relationship, ERPs time-locked to the point of syntactic-ambiguity resolution in garden-path sentences differed significantly as a function of font color. End-of-sentence grammaticality judgments were also influenced by font color, suggesting that a match between font color and sentence structure increased processing fluency. Overall, these findings indicate that participants can implicitly detect subtle co-occurrences between physical features of sentences and abstract, syntactic properties, supporting the notion that implicit learning mechanisms are generally operative during online language processing.
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