Promoting memory consolidation during sleep: A meta-analysis of targeted memory reactivation.

Abstract

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.

Meta-Regression Methods to Characterize Evidence Strength Using Meaningful-Effect Percentages Conditional on Study Characteristics

“…We first robustly meta-analyzed k = 208 point estimates from 87 experiments b , using a working exchangeable correlation structure to model clustering of estimates within experiments, 20,21 to estimate an overall average effect size on the standardized mean difference (SM D) scale c of 0.29 (95% CI: [0.19, 0.35]; p < 0.0001). We used existing methods for b As in the original meta-analysis, 15 we excluded 4 outlying point estimates from an original sample size of 212 estimates, leaving k = 208 estimates used in analysis.…”

“…We illustrate by re-analyzing data from two real meta-analyses, 14,15 demonstrating that the proposed metrics can provide more information than standard reporting alone (Section 3). We assess the methods' performance in a simulation study that includes a variety of realistic and challenging scenarios (Section 4) and use the results to inform practical reporting guidelines (Discussion).…”

Does sleep selectively strengthen certain memories over others? A critical review of the literature

“…Further evidence that this re-activation has beneficial effects on memory consolidation in humans has been shown by studies that have replayed cues (smells or sounds) present during the encoding situation during subsequent sleep. This technique, called "Targeted Memory Re-activation" (TMR), has been shown to increase memory performance (for review and meta-analysis, see Hu et al, 2020), suggesting that replay during sleep is an active mechanism in sleep-dependent memory consolidation. If the emotional and reward centers of the brain guide which memories are reactivated during sleep, this would make sleep an optimal state for preserving relevant memories while forgetting irrelevant ones.…”

Prefrontal Transcranial Direct Current Stimulation globally improves learning, but does not selectively potentiate the benefits of Targeted Memory Reactivation on awake memory consolidation

“…Born & Wilhelm, 2012;S. Diekelmann & Born, 2010;Hu, Cheng, Chiu, & Paller, 2020;Westermann, Lange, Textor, & Born, 2015), others showed that quiet wakefulness can also benefit memory consolidation (e.g., Craig, Ottaway, & Dewar, 2018;Dewar, Alber, Butler, Cowan, & Della Sala, 2012;Dewar, Garcia, Cowan, & Della Sala, 2009;Humiston et al, 2019;Tambini & Davachi, 2019;Tambini, Ketz, & Davachi, 2010;Wamsley, 2019). For instance, memory for stories was found superior after 10 minutes spent in a wakeful resting state than after an equivalent period of time spent in active wakefulness (Dewar et al, 2012).…”

“…the presentation of learning-related cues during offline periods, can additionally enhance memory consolidation (for reviews see e.g. Hu et al, 2020;. For instance, TMR during post-training wakefulness was found to rescue targeted memories from forgetting (Farthouat, Gilson, & Peigneux, 2017;Oudiette, Antony, Creery, & Paller, 2013), although this was not always replicated (see e.g.…”