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Source memory retention and schematic congruency (recalculated at 24 h). Memory retention at the 24 h follow-up with retention scores recalculated as the proportion of retention at the 12 h follow-up (scores > 100% indicate an improvement between the time points). Data are collapsed across the rehearsal conditions. Error bars represent SEM. �� p � .01, NS = not significant. https://doi.org/10.1371/journal.pone.0269439.g005
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Our ability to recall memories is improved when sleep follows learning, suggesting that sleep facilitates memory consolidation. A number of factors are thought to influence the impact of sleep on newly learned information, such as whether or not we rehearse that information (e.g. via restudy or retrieval practice), or the extent to which the inform...
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Citations
... We used the "classic" 12-h sleep versus wake design, motivated on the basis that this design elicits sleep effects in an online setting, giving us increased confidence that the effect of sleep could be successfully studied here (Ashton and Cairney 2021;Ashton et al. 2022;Denis et al. 2022). However, this design has two limitations that should be addressed in future research. ...
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 noninte-gratively, 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.
... We used the "classic" 12-h sleep versus wake design, motivated on the basis that this design elicits sleep effects in an online setting, giving us increased confidence that the effect of sleep could be successfully studied here (Ashton and Cairney 2021;Ashton et al. 2022;Denis et al. 2022). However, this design has two limitations that should be addressed in future research. ...
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.
... Increased spindle activity in turn predicted a cueing benefit for prior known associations only, supporting the notion that prior knowledge is an essential element for the beneficial effects of TMR to unfold (Groch et al. 2017). Thus, the processing trajectory of sleep-reactivated memories may depend on the nature of the learned material, and continue throughout subsequent sleep states (for a challenging view, see Ashton et al. 2022;Cordi et al. 2023). ...
... This is in line with a well-established effect of prior knowledge in facilitating learning of new information consistent with existing schemata (Tse et al. 2007;Van Kesteren et al. 2012). Additionally, the acquisition of familiar or schema conformant information was proposed to further benefit from sleep-mediated consolidation processes (Durrant et al. 2015;Hennies et al. 2016), although recent studies have challenged this view (Ashton et al. 2022;Cordi et al. 2023). Indeed, it was suggested that sleep-mediated benefits may stem from a difference in memory strength at encoding, that can be compensated by giving additional practice rounds for more difficult, unfamiliar associations (Cordi et al. 2023). ...
Presentation of learning-related cues during NREM sleep has been shown to improve memory consolidation. Past studies suggest that REM sleep may contribute to the beneficial effect of reactivating memories during NREM sleep, but the relationship between REM sleep and induced reactivations in NREM remains unclear. We investigated whether a naturally ensuing REM sleep episode is necessary for prior NREM targeted memory reactivation (TMR) to exert a beneficial effect on memory consolidation. Results disclosed better name recognition for words reactivated during NREM TMR followed by REM sleep, as compared to NREM-TMR without subsequent REM sleep. Sleep spindle activity increased only when NREM TMR preceded REM sleep, and associations with subsequent REM theta activity and memory benefits were contingent upon the level of relatedness with prior knowledge for the learned material. Our findings suggest a complex interplay between NREM and REM sleep subtending memory reactivation and consolidation processes.
... 23 While a third study reported no preferential benefits of sleep to schema-conformant memories. 24 These discrepancies could have stemmed from use of different methodologies and Downloaded from https://academic.oup.com/sleepadvances/advance-article/doi/10.1093/sleepadvances/zpad019/7119802 by guest on 15 April 2023 A c c e p t e d M a n u s c r i p t experiments with small sample sizes. Importantly, lack of an active wake control, not examining the extent to which these observed benefits are specific to sleep, and uncertainty over the persistence of memory benefits, warrant further investigation. ...
... This finding concurs with the recent findings that the benefits of post-learning sleep diminished across 24-hours. 24,45 Furthermore, this observation is consistent with a study by Schönauer and colleagues, ...
... Ashton and colleagues found that sleep bolstered schematically incongruent rather than congruent memories. 24 However, the the 'schema-learning paradigm' used in that study lacks essential features such as an overlapping associative network structure, adaptability, development across multiple episodes, and in particular facilitation of inference. 18,28,50 Moreover, recognition-based tasks have been reported to favour the no-schema condition due to novelty effects while recall-based tasks like the one used here tend to bring out the benefits of schema. ...
Study Objectives
Sleep contributes to declarative memory consolidation. Independently, schemas benefit memory. Here we investigated how sleep compared with active wake benefits schema consolidation 12 and 24 hours after initial learning.
Methods
53 adolescents (age: 15–19 year) randomly assigned into sleep and active wake groups participated in a schema-learning protocol based on transitive inference (i.e. If B>C and C>D then B>D). Participants were tested immediately after learning and following 12-hr, and 24-hr intervals of wake or sleep for both the adjacent (e.g., B-C,C-D; relational memory) and inference pairs: (e.g.: B-D,B-E,C-E). Memory performance following the respective 12-hour and 24-hour intervals were analysed using a mixed ANOVA with schema (schema, no-schema) as the within-subject factor, and condition (sleep, wake) as the between-subject factor.
Results
12-hours after learning, there were significant main effects of condition (sleep, wake) and schema, as well as a significant interaction, whereby schema-related memory was significantly better in the sleep condition compared to wake. Higher sleep spindle density was most consistently associated with greater overnight schema-related memory benefit. After 24 hours, the memory advantage of initial sleep was diminished.
Conclusions
Overnight sleep preferentially benefits schema-related memory consolidation following initial learning compared with active wake, but this advantage may be eroded after a subsequent night of sleep. This is possibly due to delayed consolidation that might occur during subsequent sleep opportunity in the wake group.
... Such a possibility would be consistent with previous research in the declarative memory domain. Sleep, and specific plasticity-related sleep features such as spindles and slow waves that are present in non-rapid-eye-movement (NREM) sleep, are thought to support declarative schema formation and subsequent integration of novel information [ [1,[11][12][13][14][15] although see [16]]. While our previous results hinted that sleep may be crucial for the integration of novel motor information into a previously-acquired schema [7], the design employed could not differentiate the specific effects of sleep from the influence of time. ...
... Previous literature in the declarative memory domain suggested a beneficial role of sleep in both declarative schema formation and schema-mediated integration [1,[11][12][13][14], although a recent investigation reported no such beneficial effect of sleep for schema-congruent memories [16]. Current models of the beneficial effect of sleep on schema formation and integration posit that overlapping memory replay during sleep would lead to the formation of cognitive schemas stored in the neocortex. ...
Study objectives
Novel information is rapidly learned when it is compatible with previous knowledge. This “schema” effect, initially described for declarative memories, was recently extended to the motor memory domain. Importantly, this beneficial effect was only observed 24 hours–but not immediately–following motor schema acquisition. Given the established role of sleep in memory consolidation, we hypothesized that sleep following the initial learning of a schema is necessary for the subsequent rapid integration of novel motor information.
Methods
Two experiments were conducted to investigate the effect of diurnal and nocturnal sleep on schema-mediated motor sequence memory consolidation. In Experiment 1, participants first learned an 8-element motor sequence through repeated practice (Session 1). They were then afforded a 90-minute nap opportunity (N = 25) or remained awake (N = 25) before learning a second motor sequence (Session 2) which was highly compatible with that learned prior to the sleep/wake interval. Experiment 2 was similar; however, Sessions 1 and 2 were separated by a 12-hour interval that included nocturnal sleep (N = 28) or only wakefulness (N = 29).
Results
For both experiments, we found no group differences in motor sequence performance (reaction time and accuracy) following the sleep/wake interval. Furthermore, in Experiment 1, we found no correlation between sleep features (non-REM sleep duration, spindle and slow wave activity) and post-sleep behavioral performance.
Conclusions
The results of this research suggest that integration of novel motor information into a cognitive-motor schema does not specifically benefit from post-learning sleep.
... An overreliance on small sample sizes in many experiments is likely a major contributor to conflicting results (2), with studies being underpowered to detect true effects. While it is challenging to recruit large samples for typical laboratory experiments, utilizing online tools to examine the behavioral effect of sleep on memory represents a promising avenue to increase sample size and sample from a broader portion of society (17)(18)(19). We turned to this resource to examine, in two well-powered experiments, whether sleep enhances emotional memory in human adults in the largest studies of sleep and emotional memory to date. ...
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.
... Although it is not entirely clear why this effect does not extend to tested pairs, one proposal holds that testing increases the strength of a memory to such an extent that it stays above retrieval thresholds over prolonged intervals (Kornell et al. 2011). Drawing from this, Bäuml et al. (2014) showed that sleep supports retention for memories subject to restudy, but not those tested prior to sleep (see also Ashton et al. 2022), suggesting that increases in memory strength afforded by testing may mitigate the role of sleep in memory consolidation. This may account for why some previous studies have only reported TMR-induced facilitations for pairs retrieved with low accuracy prior to sleep (Creery et al. 2015;Cairney et al. 2016). ...
Memory reactivation during sleep can shape new memories into a long-term form. Reactivation of memories can be induced via the delivery of auditory cues during sleep. Although this targeted memory reactivation (TMR) approach can strengthen newly acquired memories, research has tended to focus on single associative memories. It is less clear how TMR affects retention for overlapping associative memories. This is critical, given that repeated retrieval of overlapping associations during wake can lead to forgetting, a phenomenon known as retrieval-induced forgetting (RIF). We asked whether a similar pattern of forgetting occurs when TMR is used to cue reactivation of overlapping pairwise associations during sleep. Participants learned overlapping pairs-learned separately, interleaved with other unrelated pairs. During sleep, we cued a subset of overlapping pairs using TMR. While TMR increased retention for the first encoded pairs, memory decreased for the second encoded pairs. This pattern of retention was only present for pairs not tested prior to sleep. The results suggest that TMR can lead to forgetting, an effect similar to RIF during wake. However, this effect did not extend to memories that had been strengthened via retrieval prior to sleep. We therefore provide evidence for a reactivation-induced forgetting effect during sleep.
