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Fine-Tuning the Methodology of Sleep and Memory Research From a Human Behavioral Perspective
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Abstract
Understanding the complex relationship between sleep and memory is a major challenge in neuroscience. Many studies on memory consolidation in humans suggest that sleep triggers offline memory processes, resulting in less forgetting of declarative memory and performance stabilization in non-declarative memory. However, an increasing number of contradictory findings reveal potential issues with how research is conducted in this field and call into question the reliability and interpretation of the results. All scientific disciplines face similar challenges. In this regard, research on the relationship between sleep and memory is still very fortunate. Yet, there is a constant need to fine-tune the methodology. In this article, we describe four behavioral methodological issues in human sleep and memory research that should be improved: non-optimal experimental designs, task complexity, fatigue effects in repetitive tasks, and inappropriate data analysis practices. We then offer solutions to each of these issues. We believe that implementing these solutions in future sleep and memory research will lead to more reliable results and significantly advance our understanding in this field.
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In registered reports (RRs), initial peer review and in-principle acceptance occur before knowing the research outcomes. This combats publication bias and distinguishes planned from unplanned research. How RRs could improve the credibility of research findings is straightforward, but there is little empirical evidence. Also, there could be unintended costs such as reducing novelty. Here, 353 researchers peer reviewed a pair of papers from 29 published RRs from psychology and neuroscience and 57 non-RR comparison papers. RRs numerically outperformed comparison papers on all 19 criteria (mean difference 0.46, scale range −4 to +4) with effects ranging from RRs being statistically indistinguishable from comparison papers in novelty (0.13, 95% credible interval [−0.24, 0.49]) and creativity (0.22, [−0.14, 0.58]) to sizeable improvements in rigour of methodology (0.99, [0.62, 1.35]) and analysis (0.97, [0.60, 1.34]) and overall paper quality (0.66, [0.30, 1.02]). RRs could improve research quality while reducing publication bias and ultimately improve the credibility of the published literature. Soderberg et al. asked scientists to peer review registered reports and standard articles post-publication, after information explicitly identifying the article type had been removed. Registered reports scored higher on some dimensions, including quality and rigour.
Memories benefit from a retention interval filled with sleep. Current theories assume that this beneficial effect relies on consolidation processes occurring during slow-wave sleep (SWS). However, in the last years, several key findings supporting these theories could not be replicated or occurred only under certain conditions, suggesting that effects of sleep on memory are smaller, more task-dependent, less SWS-related, less robust and less long-lasting than previously assumed. In this review, we summarize recent replication failures, null-findings, meta-analyses and studies reporting important boundary conditions for the effect of sleep on declarative memory. We argue that more attempts to replicate and meta-analytic approaches together with higher standards for reproducible science are critical to advance the field of sleep and memory.
Initially independent lines of research suggest that sleep‐specific brain activity patterns, observed as electroencephalographic slow oscillatory and sleep spindle activity, promote memory consolidation and underlying synaptic refinements. Here, we further tested the emerging concept that specifically the coordinated interplay of slow oscillations and spindle activity (phase‐amplitude coupling) support memory consolidation. Particularly, we associated indices of the interplay between slow oscillatory (0.16–1.25 Hz) and spindle activity (12–16 Hz) during non‐rapid eye movement sleep (strength [modulation index] and phase degree of coupling) in 20 healthy adults with parameters of overnight declarative (word‐list task) and procedural (mirror‐tracing task) memory consolidation. The pattern of results supports the notion that the interplay between oscillations facilitates memory consolidation. The coincidence of the spindle amplitude maximum with the up‐state of the slow oscillation (phase degree) was significantly associated with declarative memory consolidation (r = .65, p = .013), whereas the overall strength of coupling (modulation index) correlated with procedural memory consolidation (r = .45, p = .04). Future studies are needed to test for potential causal effects of the observed association between neural oscillations during sleep and memory consolidation, and to elucidate ways of modulating these processes, for instance through non‐invasive brain‐stimulation techniques.
Simultaneous electroencephalography and functional magnetic resonance imaging (EEG–fMRI) studies have revealed brain activations time-locked to spindles. Yet, the functional significance of these spindle-related brain activations is not understood. EEG studies have shown that inter-individual differences in the electrophysiological characteristics of spindles (e.g., density, amplitude, duration) are highly correlated with “Reasoning” abilities (i.e., “fluid intelligence”; problem solving skills, the ability to employ logic, identify complex patterns), but not short-term memory (STM) or verbal abilities. Spindle-dependent reactivation of brain areas recruited during new learning suggests night-to-night variations reflect offline memory processing. However, the functional significance of stable, trait-like inter-individual differences in brain activations recruited during spindle events is unknown. Using EEG–fMRI sleep recordings, we found that a subset of brain activations time-locked to spindles were specifically related to Reasoning abilities but were unrelated to STM or verbal abilities. Thus, suggesting that individuals with higher fluid intelligence have greater activation of brain regions recruited during spontaneous spindle events. This may serve as a first step to further understand the function of sleep spindles and the brain activity which supports the capacity for Reasoning.
Recent studies show that brief periods of rest after learning facilitate consolidation of new memories. This effect is associated with memory-related brain activity during quiet rest and suggests that in our daily lives, moments of unoccupied rest may serve an essential cognitive function.
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Objective: The role of sleep architecture in consolidation of memory has not been extensively
investigated. In this study, the association of continuous positive airway pressure (CPAP) and sleep
architecture and quality, and sleep disordered breathing on changes in memory are explored during
the course of a 6 month clinical trial of CPAP or sham CPAP (APPLES). Methods: 848 participants
had polysomnographic and memory assessments (Buschke Selective Reminding Test [Buschke] and
Digit Symbol Substitution Test [DSST]) at baseline, CPAP/Sham CPAP titration, and the 2 and 6
month time points. Half were assigned to the CPAP and Sham CPAP groups respectively. Changes
in performance on the Buschke and the DSST were analyzed over the course of the study between
CPAP and Sham CPAP as well as in relationship to changes in sleep architecture, sleep quality and
sleep disordered breathing (SDB). Results: Sleep architecture, sleep quality and SDB improved in
the CPAP group at 6 months; performance on the Buschke and DSST improved equally in both
CPAP and Sham CPAP groups. There also were no significant correlations between changes in
the amount or percentage of sleep stages between baseline and the 6 months, and corresponding
changes in either the Buschke or the DSST. However, when stratified by the upper quartile and
lower 3 quartiles, greater changes in the Buschke occurred over 6 months in the top quartile of
total sleep time (5.7±7.3 vs. 4.0±6.8, p≤0.01) and amount of N3 sleep (55.9±7.7 vs. 53.6±8.9
min, p≤0.01). Those with more %N3 at 6 months scored better on the Buschke as well (55.9±7.8
vs. 53.6±8.9, p≤0.01). Borderline improvement in the DSST over 6 months was observed in the
top quartiles of amount of N3 and %N3. Those in the top quartile of the amount of REM and
%REM also showed greater improvement in the Buschke after 6 months. No differences were
observed for the AHI, but those in the top quartile of oxygen desaturation had worse scores on
the Buschke at 6 months. CPAP/Sham CPAP adherence did not impact 6 month Buschke or DSST
performance. Conclusions: CPAP improved long-term sleep duration, quality and architecture,
but did not memory. However, large changes in REM and N3 sleep as well as moderate amounts of
nocturnal hypoxemia are associated with changes in assessments of memory.
Procedural learning is a fundamental cognitive function that facilitates efficient processing of and automatic responses to complex environmental stimuli. Here, we examined training-dependent and off-line changes of two sub-processes of procedural learning: namely, sequence learning and statistical learning. Whereas sequence learning requires the acquisition of order-based relationships between the elements of a sequence, statistical learning is based on the acquisition of probabilistic associations between elements. Seventy-eight healthy young adults (58 females and 20 males) completed the modified version of the Alternating Serial Reaction Time task that was designed to measure Sequence and Statistical Learning simultaneously. After training, participants were randomly assigned to one of three conditions: active wakefulness, quiet rest, or daytime sleep. We examined off-line changes in Sequence and Statistical Learning as well as further improvements after extended practice. Performance in Sequence Learning increased during training, while Statistical Learning plateaued relatively rapidly. After the off-line period, both the acquired sequence and statistical knowledge was preserved, irrespective of the vigilance state (awake, quiet rest or sleep). Sequence Learning further improved during extended practice, while Statistical Learning did not. Moreover, within the sleep group, cortical oscillations and sleep spindle parameters showed differential associations with Sequence and Statistical Learning. Our findings can contribute to a deeper understanding of the dynamic changes of multiple parallel learning and consolidation processes that occur during procedural memory formation.
Study objectives
Daytime naps benefit long-term memory relative to taking a break and remaining awake. However, the use of naps as a practical way to improve learning has not been examined, in particular, how memory following a nap compares with spending the equivalent amount of time cramming.
Methods
Young adults learned detailed factual knowledge in sessions that flanked one-hour spent napping (n=27), taking a break (n=27), or cramming that information (n=30). Recall was examined 30-mins and one week after learning.
Results
When tested 30-mins after learning, cramming and napping led to significantly better memory than taking a break. After a week, napping maintained this significant advantage, but cramming did not.
Conclusions
These findings demonstrate the longer-term benefits of napping for retention of memoranda akin to what students encounter daily, and encourage more widespread adoption of napping in education.
The hippocampus replays experiences during quiet rest periods, and this replay benefits subsequent memory. A critical open question is how memories are prioritized for this replay. We used functional magnetic resonance imaging (fMRI) pattern analysis to track item-level replay in the hippocampus during an awake rest period after participants studied 15 objects and completed a memory test. Objects that were remembered less well were replayed more during the subsequent rest period, suggesting a prioritization process in which weaker memories-memories most vulnerable to forgetting-are selected for replay. In a second session 12 hours later, more replay of an object during a rest period predicted better subsequent memory for that object. Replay predicted memory improvement across sessions only for participants who slept during that interval. Our results provide evidence that replay in the human hippocampus prioritizes weakly learned information, predicts subsequent memory performance, and relates to memory improvement across a delay with sleep.
A fundamental problem in the field of obstructive sleep apnea (OSA) and memory is that it has historically minimized the basic neurobiology of sleep’s role in memory. Memory formation has been classically divided into phases of encoding, processing/consolidation, and retrieval. An abundance of evidence suggests that sleep plays a critical role specifically in the processing/consolidation phase, but may do so differentially for memories that were encoded using particular brain circuits. In this review, we discuss some of the more established evidence for sleep’s function in the processing of declarative, spatial navigational, emotional, and motor/procedural memories and more emerging evidence highlighting sleep’s importance in higher order functions such as probabilistic learning, transitive inference, and category/gist learning. Furthermore, we discuss sleep’s capacity for memory augmentation through targeted/cued memory reactivation. OSA – by virtue of its associated sleep fragmentation, intermittent hypoxia, and potential brain structural effects – is well positioned to specifically impact the processing/consolidation phase, but testing this possibility requires experimental paradigms in which memory encoding and retrieval are separated by a period of sleep with and without the presence of OSA. We argue that such paradigms should focus on the specific types of memory tasks for which sleep has been shown to have a significant effect. We discuss the small number of studies in which this has been done, in which OSA nearly uniformly negatively impacts offline memory processing. When periods of offline processing are minimal or absent and do not contain sleep, as is the case in the broad literature on OSA and memory, the effects of OSA on memory are far less consistent.
The scientific discussion of sleep spindles now routinely mentions the association between these oscillations and cognitive ability. Numerous studies have been published on the topic with various methodologies and highly divergent results. In this meta-analysis of the relevant literature (total k = 22 articles, total N = 953 subjects), it is concluded that there is evidence for a modest positive association between cognitive ability and slow ( r = .113) and fast ( r = .183) spindle amplitudes and also some evidence for an association between cognitive ability and slow spindle duration ( r = .087) but none for associations with other parameters. Evidence for publication bias was found in case of fast spindle amplitude and density, but the correlation between cognitive ability and amplitude was robust to this effect. Studies with more females reported weaker associations with slow spindle duration, but this effect was driven by a single study with an all-male sample, and no other effect size was significantly moderated by age or sex. Most studies were conducted in small data sets and did not exhaustively report all measured associations. It is recommended that future studies having access to both sleep spindle and intelligence measures report their associations, regardless of their nature, that data sets be pooled across research groups for more statistical power, and that at least a basic agreement of spindle detection and classification criteria be reached in the research community.
Aims:
To illustrate how Bayes Factors are important for determining the effectiveness of interventions.
Method:
We consider a case where inappropriate conclusions were publicly drawn based on significance testing, namely the SIPS Project (Screening and Intervention Programme for Sensible drinking), a pragmatic, cluster-randomized controlled trial in each of two healthcare settings and in the criminal justice system. We show how Bayes Factors can disambiguate the non-significant findings from the SIPS Project and thus determine whether the findings represent evidence of absence or absence of evidence. We show how to model the sort of effects that could be expected, and how to check the robustness of the Bayes Factors.
Results:
The findings from the three SIPS trials taken individually are largely uninformative but, when data from these trials are combined, there is moderate evidence for a null hypothesis (H0) and thus for a lack of effect of brief intervention compared with simple clinical feedback and an alcohol information leaflet (B = 0.24, p = 0.43).
Conclusion:
Scientists who find non-significant results should suspend judgment - unless they calculate a Bayes Factor to indicate either that there is evidence for a null hypothesis (H0) over a (well-justified) alternative hypothesis (H1), or else that more data are needed.
Bayesian parameter estimation and Bayesian hypothesis testing present attractive alternatives to classical inference using confidence intervals and p values. In part I of this series we outline ten prominent advantages of the Bayesian approach. Many of these advantages translate to concrete opportunities for pragmatic researchers. For instance, Bayesian hypothesis testing allows researchers to quantify evidence and monitor its progression as data come in, without needing to know the intention with which the data were collected. We end by countering several objections to Bayesian hypothesis testing. Part II of this series discusses JASP, a free and open source software program that makes it easy to conduct Bayesian estimation and testing for a range of popular statistical scenarios (Wagenmakers et al. this issue).
Study Objectives
Sleep during the biological night facilitates memory consolidation. Here we determined the impact of sleep and wake on motor skill learning (acquisition) and subsequent off-line skill improvement (memory consolidation), independent of circadian phase, and compared this to the impact of the endogenous circadian system, independent of whether sleep occurred during the biological night or day.
Methods
Participants completed two 8-day sleep laboratory visits, adhering on one visit to a circadian aligned (“normal”) sleep schedule for the full duration of the protocol, and on the other to a circadian misaligned (12-hr inverted) schedule, with alignment during the first three days, a 12-h ‘slam shift’ on Day 4, followed by circadian misalignment during the last four days of the protocol. Participants were repeatedly trained and tested on different versions of the finger-tapping motor sequence tasks (MST) across each visit.
Results
Sleep facilitated offline memory consolidation regardless of whether it occurred during the biological day or night, while circadian phase had no significant impact. These sleep-related benefits remained after accounting for general motor speed, measured in the absence of learning. In addition, motor skill acquisition was facilitated when the training session followed shortly after sleep, without significant impact of circadian phase (biological morning vs. evening). This effect was largely driven by heightened acquisition in participants who slept during the day and were trained shortly thereafter. These benefits were also retained after controlling for general motor speed.
Conclusions
Sleep benefits both the acquisition and consolidation of motor skills regardless of whether they occur during the biological day or night. After controlling for general motor speed, a critical adjustment that few studies perform, these sleep benefits remain intact. Our findings have clear implications for night shift workers who obtain their sleep during the day.
The Open Science Framework (OSF) is a free, open source,r esearch workflow web application developed and maintained by the Center for Open Science (COS).
Inference using significance testing and Bayes factors is compared and contrasted in five case studies based on real research. The first study illustrates that the methods will often agree, both in motivating researchers to conclude that H1 is supported better than H0, and the other way round, that H0 is better supported than H1. The next four, however, show that the methods will also often disagree. In these cases, the aim of the paper will be to motivate the sensible evidential conclusion, and then see which approach matches those intuitions. Specifically, it is shown that a high-powered non-significant result is consistent with no evidence for H0 over H1 worth mentioning, which a Bayes factor can show, and, conversely, that a low-powered non-significant result is consistent with substantial evidence for H0 over H1, again indicated by Bayesian analyses. The fourth study illustrates that a high-powered significant result may not amount to any evidence for H1 over H0, matching the Bayesian conclusion. Finally, the fifth study illustrates that different theories can be evidentially supported to different degrees by the same data; a fact that P-values cannot reflect but Bayes factors can. It is argued that appropriate conclusions match the Bayesian inferences, but not those based on significance testing, where they disagree.
Recently there has been a growing concern that many published research findings do not hold up in attempts to replicate them. We argue that this problem may originate from a culture of ‘you can publish if you found a significant effect’. This culture creates a systematic bias against the null hypothesis which renders meta-analyses questionable and may even lead to a situation where hypotheses become difficult to falsify. In order to pinpoint the sources of error and possible solutions, we review current scientific practices with regard to their effect on the probability of drawing a false-positive conclusion. We explain why the proportion of published false-positive findings is expected to increase with (i) decreasing sample size, (ii) increasing pursuit of novelty, (iii) various forms of multiple testing and researcher flexibility, and (iv) incorrect P-values, especially due to unaccounted pseudoreplication, i.e. the non-independence of data points (clustered data). We provide examples showing how statistical pitfalls and psychological traps lead to conclusions that are biased and unreliable, and we show how these mistakes can be avoided. Ultimately, we hope to contribute to a culture of ‘you can publish if your study is rigorous’. To this end, we highlight promising strategies towards making science more objective. Specifically, we enthusiastically encourage scientists to preregister their studies (including a priori hypotheses and complete analysis plans), to blind observers to treatment groups during data collection and analysis, and unconditionally to report all results. Also, we advocate reallocating some efforts away from seeking novelty and discovery and towards replicating important research findings of one's own and of others for the benefit of the scientific community as a whole. We believe these efforts will be aided by a shift in evaluation criteria away from the current system which values metrics of ‘impact’ almost exclusively and towards a system which explicitly values indices of scientific rigour.
This study examined the differential effects of aging on consolidation processes that strengthen newly acquired memory traces in veridical form (memory stabilization) versus consolidation processes that are responsible for integrating these memory traces into an existing body of knowledge (item integration). Older adults learned 13 nonwords and were tested on their memory for the nonwords, and on whether these nonwords impacted upon processing of similar-sounding English words immediately and 24 hours later. Participants accurately recognized the nonwords immediately, but showed significant decreases in delayed recognition and recall. In comparison, the nonwords impacted upon processing of similar-sounding words only in the delayed test. Together, these findings suggest that memory consolidation processes may be more evident in item integration than memory stabilization processes for new declarative memories in older adults.
Electronic supplementary material
The online version of this article (doi:10.3758/s13423-016-1197-0) contains supplementary material, which is available to authorized users.
Sleep is known to support the consolidation of newly encoded and initially labile memories. Once consolidated, remote memories can return to a labile state upon reactivation and need to become reconsolidated in order to persist. Here we asked whether sleep also benefits the reconsolidation of remote memories after their reactivation and how reconsolidation during sleep compares to sleep-dependent consolidation processes. In three groups, participants were trained on a visuo-spatial learning task in the presence of a contextual odor. Participants in the 'reconsolidation' group learned the task on day 1. On day 2, they were subjected to a reactivation procedure by presenting the odor cue and a mock recall test in the learning context before a 40-minute sleep or wake period. Participants in the 'remote consolidation' group followed the same procedure but did not receive reactivation on day 2. Participants in the 'recent consolidation' group skipped the procedure on day 1 and learned the task immediately before the sleep or wake period. After the sleep or wake interval, memory stability was tested in all subjects. The results show that this short 40-minute sleep period significantly facilitated the reconsolidation of reactivated memories, whereas the consolidation of non-reactivated remote memories was less affected and recently encoded memories did not benefit at all. These findings tentatively suggest that sleep has a beneficial effect on the reconsolidation of remote memories, acting at a faster rate than sleep-associated consolidation.
In recent years sleep-related memory consolidation has become a central topic in the sleep research field. Several studies have shown that in healthy individuals sleep promotes memory consolidation. Notwithstanding this, the consequences of sleep disorders on offline memory consolidation remain poorly investigated. Research studies indicate that patients with insomnia, obstructive sleep apnea, and narcolepsy often exhibit sleep-related impairment in the consolidation of declarative and procedural information. On the other hand, patients with parasomnias, such as sleep-walking, night terrors and REM behavior disorder, do not present any memory impairment. These studies suggest that only sleep disorders characterized by increased post-learning arousal and disrupted sleep architecture seem to be associated with offline memory consolidation issues. Such impairments, arising already in childhood, may potentially affect the development and maintenance of an individual’s cognitive abilities, reducing their quality of life and increasing the risk of accidents. However, promising findings suggest that successfully treating sleep symptoms can result in the restoration of memory functions and marked reduction of direct and indirect societal costs of sleep disorders
Sleep supports memory consolidation. However, the conceptually important influence of the amount of items encoded in a memory test on this effect has not been investigated. In two experiments, participants (n = 101) learned lists of word-pairs varying in length (40, 160, 320 word-pairs) in the evening before a night of sleep (sleep group) or of sleep deprivation (wake group). After 36 h (including a night allowing recovery sleep) retrieval was tested. Compared with wakefulness, post-learning sleep enhanced retention for the 160 word-pair condition (p < 0.01), importantly, this effect completely vanished for the 320 word-pair condition. This result indicates a limited capacity for sleep-dependent memory consolidation, which is consistent with an active system consolidation view on sleep’s role for memory, if it is complemented by processes of active forgetting and/or gist abstraction. Whereas the absolute benefit from sleep should have increased with increasing amounts of successfully encoded items, if sleep only passively protected memory from interference. Moreover, the finding that retention performance was significantly diminished for the 320 word-pair condition compared to the 160 word-pair condition in the sleep group, makes it tempting to speculate that with increasing loads of information encoded during wakefulness, sleep might favor processes of forgetting over consolidation.
Bayes factors provide a symmetrical measure of evidence for one model versus another (e.g. H1 versus H0) in order to relate theory to data. These properties help solve some (but not all) of the problems underlying the credibility crisis in psychology. The symmetry of the measure of evidence means that there can be evidence for H0 just as much as for H1; or the Bayes factor may indicate insufficient evidence either way. P-values cannot make this three-way distinction. Thus, Bayes factors indicate when the data count against a theory (and when they count for nothing); and thus they indicate when replications actually support H0 or H1 (in ways that power cannot). There is every reason to publish evidence supporting the null as going against it, because the evidence can be measured to be just as strong either way (thus the published record can be more balanced). Bayes factors can be B-hacked but they mitigate the problem because a) they allow evidence in either direction so people will be less tempted to hack in just one direction; b) as a measure of evidence they are insensitive to the stopping rule; c) families of tests cannot be arbitrarily defined; and d) falsely implying a contrast is planned rather than post hoc becomes irrelevant (though the value of pre-registration is not mitigated).
We examined the impact of repeated testing and repeated studying on long-term learning. In Experiment 1, we replicated Karpicke and Roediger's (2008) influential results showing that once information can be recalled, repeated testing on that information enhances learning, whereas restudying that information does not. We then examined whether the apparent ineffectiveness of restudying might be attributable to the spacing differences between items that were inherent in the between-subjects design employed by Karpicke and Roediger. When we controlled for these spacing differences by manipulating the various learning conditions within subjects in Experiment 2, we found that both repeated testing and restudying improved learning, and that learners' awareness of the relative mnemonic benefits of these strategies was enhanced. These findings contribute to understanding how two important factors in learning-test-induced retrieval processes and spacing-can interact, and they illustrate that such interactions can play out differently in between-subjects and within-subjects experimental designs.
Substantial empirical evidence suggests that sleep benefits the consolidation and reorganization of learned information. Consequently, the concept of “sleep-dependent memory consolidation” is now widely accepted by the scientific community, in addition to influencing public perceptions regarding the functions of sleep. There are, however, numerous studies that have presented findings inconsistent with the sleep-memory hypothesis. Here, we challenge the notion of “sleep-dependency” by summarizing evidence for effective memory consolidation independent of sleep. Plasticity mechanisms thought to mediate or facilitate consolidation during sleep (e.g., neuronal replay, reactivation, slow oscillations, neurochemical milieu) also operate during non-sleep states, particularly quiet wakefulness, thus allowing for the stabilization of new memories. We propose that it is not sleep per se, but the engagement of plasticity mechanisms, active during both sleep and (at least some) waking states, that constitutes the critical factor determining memory formation. Thus, rather than playing a "critical" role, sleep falls along a continuum of behavioral states that vary in their effectiveness to support memory consolidation at the neural and behavioral level.
Sleep is a key determinant of healthy and cognitive aging. Sleep patterns change with aging, independent of other factors, and include advanced sleep timing, shortened nocturnal sleep duration, increased frequency of daytime naps, increased number of nocturnal awakenings and time spent awake during the night, and decreased slow-wave sleep. The sleep-related hormone secretion changes with aging. Most changes seem to occur between young and middle adulthood; sleep parameters remain largely unchanged among healthy older adults. The circadian system and sleep homeostatic mechanisms become less robust with normal aging. The causes of sleep disturbances in older adults are multifactorial.
We explored the possibility of publication bias in the sleep and explicit motor sequence learning literature by applying precision effect test (PET) and precision effect test with standard errors (PEESE) weighted regression analyses to the 88 effect sizes from a recent comprehensive literature review (Pan & Rickard, 2015). Basic PET analysis indicated pronounced publication bias; that is, the effect sizes were strongly predicted by their standard error. When variables that have previously been shown to both moderate the sleep gain effect and substantially reduce unaccounted for effect size heterogeneity were included in that analysis, evidence for publication bias remained strong. The estimated postsleep gain was negative, suggesting forgetting rather than facilitation, and it was statistically indistinguishable from the estimated postwake gain. In a qualitative review of a smaller group of more recent studies we observed that (a) small sample sizes-a major factor behind the publication bias-are still the norm, (b) use of demonstrably flawed experimental design and analysis remains prevalent, and (c) when authors conclude in favor of sleep-dependent consolidation, they frequently do not cite the articles in which those methodological flaws have been demonstrated. We conclude that there is substantial publication bias, that there is no consolidation-based, absolute performance gain following sleep, and that strong conclusions regarding the hypothesis of less forgetting after sleep than after wakefulness should await further research. Recommendations are made for reducing publication bias in future work. (PsycInfo Database Record (c) 2022 APA, all rights reserved).
Sleep consolidates memory for procedural motor skills, reflected by sleep-dependent changes in the hippocampal-striatal-cortical network. Other forms of procedural skills require the acquisition of a novel strategy to solve a problem, which recruit overlapping brain regions and specialized areas including the caudate and prefrontal cortex. Sleep preferentially benefits strategy and problem-solving skills over the accompanying motor execution movements. However, it is unclear how acquiring new strategies benefit from sleep. Here, participants performed a task requiring the execution of a sequence of movements to learn a novel cognitive strategy. Participants performed this task while undergoing fMRI before and after an interval of either a full night sleep, a daytime nap, or wakefulness. Participants also performed a motor control task, which precluded the opportunity to learn the strategy. In this way, we subtracted motor execution-related brain activations from activations specific to the strategy. The sleep and nap groups experienced greater behavioral performance improvements compared to the wake group on the strategy-based task. Following sleep, we observed enhanced activation of the caudate in addition to other regions in the hippocampal-striatal-cortical network, compared to wakefulness. This study demonstrates that sleep is a privileged time to enhance newly acquired cognitive strategies needed to solve problems.
Understanding the brain requires us to answer both what the brain does, and how it does it. Using a series of examples, I make the case that behavior is often more useful than neuroscientific measurements for answering the first question. Moreover, I show that even for "how" questions that pertain to neural mechanism, a well-crafted behavioral paradigm can offer deeper insight and stronger constraints on computational and mechanistic models than do many highly challenging (and very expensive) neural studies. I conclude that purely behavioral research is essential for understanding the brain-especially its cognitive functions-contrary to the opinion of prominent funding bodies and some scientific journals, who erroneously place neural data on a pedestal and consider behavior to be subsidiary. (PsycInfo Database Record (c) 2021 APA, all rights reserved).
How do we go about learning new information? This article reviews the importance of practicing retrieval of newly experienced information if one wants to be able to retrieve it again in the future. Specifically, practicing retrieval shortly after learning can slow the forgetting process. This benefit can be seen across various material types, and it seems prevalent in all ages and learner abilities and on all types of test. It can also be used to enhance student learning in a classroom setting. I review theoretical understanding of this phenomenon (sometimes referred to as the testing effect or as retrieval-based learning) and consider directions for future research.
Expected final online publication date for the Annual Review of Psychology, Volume 72 is January 5, 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
The striatum and medial temporal lobes (MTL) exhibit dissociable roles during learning. Whereas the striatum and its network of thalamic relays and cortical nodes are necessary for nondeclarative learning, the MTL and associated network are required for declarative learning. Several studies have suggested that these networks are functionally competitive during learning. Since these discoveries, however, evidence has accumulated that they can operate in a cooperative fashion. In this review, we discuss evidence for both competition and cooperation between these systems during learning, with the aim of reconciling these seemingly contradictory findings. Examples of cooperation between the striatum and MTL have been provided, especially during consolidation and generalization of knowledge, and do not appear to be precluded by differences in functional specialization. However, whether these systems cooperate or compete does seem to depend on the phase of learning and cognitive or motor aspects of the task. The involvement of other regions, such as midbrain dopaminergic nuclei and the prefrontal cortex, may promote and mediate cooperation between the striatum and the MTL during learning. Building on this body of research, we propose a model for striatum-MTL interactions in learning and memory and attempt to predict, in general terms, when cooperation or competition will occur.
Rapid Eye Movement (REM) sleep is a peculiar neural state showing a combination of muscle atonia and intense cortical activity. REM sleep is usually considered as a unitary state in neuroscientific research; however, it is composed of two different microstates: phasic and tonic REM. These differ in awakening thresholds, sensory processing, and cortical oscillations. Nevertheless, studies examining cortical oscillations during REM microstates are scarce, and used low spatial sampling. Here, we analyzed the data of 18 healthy individuals assessed by high-density sleep EEG recordings. We systematically contrasted phasic and tonic REM periods in terms of topographical distribution, source localization, as well as local, global and long-range synchronization of frequency-specific cortical activity. Tonic periods showed relatively increased high alpha and beta power over frontocentral derivations. In addition, higher frequency components of beta power exhibited increased global synchronization during tonic compared to phasic states. In contrast, in phasic periods we found increased power and synchronization of low frequency oscillations coexisting with increased and synchronized gamma activity. Source localization revealed several multimodal, higher-order associative, as well as sensorimotor areas as potential sources of increased high alpha/beta power during tonic compared to phasic REM. Increased gamma power in phasic REM was attributed to medial prefrontal and right lateralized temporal areas associated with emotional processing. Our findings emphasize the heterogeneous nature of REM sleep, expressed in two microstates with remarkably different neural activity. Considering the microarchitecture of REM sleep may provide new insights into the mechanisms of REM sleep in health and disease.
Sleep is known to be beneficial to the strengthening of two distinct forms of procedural memory: memory for novel, cognitively simple series of motor movements, and memory for novel, cognitively complex strategies required to solve problems. However, these two types of memory are intertwined, since learning a new cognitive procedural strategy occurs through practice, and thereby also requires the execution of a series of simple motor movements. As a result, it is unclear whether the benefit of sleep results from the enhancement of the cognitive strategy, or the motor skills required to execute the solution. To disentangle the role of sleep in these aspects of procedural memory, we employed two tasks: (1) the Tower of Hanoi (ToH), and, (2) a modified version of the ToH, akin to an implicit Motor Sequence Learning (MSL) task. The MSL task involved the identical series of motor movements as the ToH, but without access to the information necessary to execute the task according to the underlying cognitive procedural strategy. Participants (n = 28) were trained on the 3-disk ToH, then retested on 5-disk versions of both ToH and MSL tasks. Half (n = 15) were trained and immediately tested at 8 PM and retested at 8 AM after a night of sleep. They were retested again at 8 PM after a day of wake (PM-AM-PM condition). The other half (n = 13) were trained and immediately tested at 8 AM, retested at 8 PM after a day of wake, and retested again at 8 AM after a night of sleep (AM-PM-AM condition). ToH performance only improved following a period of sleep. There was no benefit of sleep to implicit MSL. Our results show that sleep, but not wake, allowed individuals to extrapolate what was learned on a simpler 3-disk version of the task to the larger 5-disk problem, which included new elements to which they had not yet been exposed. Here, we isolate the specific role sleep plays for cognitive procedural memory: sleep benefits the cognitive strategy, rather than strengthening implicitly acquired motor sequences required to learn and execute the underlying strategy itself.
We propose a framework for the memory function of spindle oscillations during sleep. In this framework, memories are reinstated by spindle events, and further reprocessed during subsequent spindle refractory periods. We posit that spindle refractoriness is crucial for protecting memory reprocessing from interference. We further argue that temporally-coordinated spindle refractory periods across local networks facilitate the consolidation of rich, multimodal representations, and that localized spindle refractoriness optimizes oscillatory interactions that support systems consolidation in the sleeping brain.
Emotional events are preferentially retained in episodic memory. This effect is commonly attributed to enhanced consolidation and has been linked specifically to rapid eye movement (REM) sleep physiology. While several studies have demonstrated an enhancing effect of REM sleep on emotional item memory, it has not been thoroughly explored whether this effect extends to the retention of associative memory. Moreover, it is unclear how non-rapid eye movement (NREM) sleep contributes to these effects. The present study thus examined associative recognition of emotional and non-emotional material across an early morning nap (N= 23) and sustained wakefulness (N= 23). Nap group subjects demonstrated enhanced post-sleep associative memory performance, which was evident across both valence categories. Subsequent analyses revealed significant correlations between NREM spindle density and pre-sleep memory performance. Moreover, NREM spindle density was positively correlated with post-sleep neutral associative memory performance but not with post-sleep emotional associative memory. Accordingly, only neutral associative memory, but not emotional associative memory, was significantly correlated with spindle density after an additional night of sleep (+24 h). These results illustrate a temporally persistent relationship between spindle density and memory for neutral associations, whereas post-sleep emotional associative memory appears to be disengaged from NREM-sleep-dependent processes.
Progress in science relies in part on generating hypotheses with existing observations and testing hypotheses with new observations. This distinction between postdiction and prediction is appreciated conceptually but is not respected in practice. Mistaking generation of postdictions with testing of predictions reduces the credibility of research findings. However, ordinary biases in human reasoning, such as hindsight bias, make it hard to avoid this mistake. An effective solution is to define the research questions and analysis plan before observing the research outcomes-a process called preregistration. Preregistration distinguishes analyses and outcomes that result from predictions from those that result from postdictions. A variety of practical strategies are available to make the best possible use of preregistration in circumstances that fall short of the ideal application, such as when the data are preexisting. Services are now available for preregistration across all disciplines, facilitating a rapid increase in the practice. Widespread adoption of preregistration will increase distinctiveness between hypothesis generation and hypothesis testing and will improve the credibility of research findings.
Sleep facilitates the consolidation (i.e., enhancement) of simple, explicit (i.e., conscious) motor sequence learning (MSL). MSL can be dissociated into egocentric (i.e., motor) or allocentric (i.e., spatial) frames of reference. The consolidation of the allocentric memory representation is sleep-dependent, whereas the egocentric consolidation process is independent of sleep or wake for explicit MSL. However, it remains unclear the extent to which sleep contributes to the consolidation of implicit (i.e., unconscious) MSL, nor is it known what aspects of the memory representation (egocentric, allocentric) are consolidated by sleep. Here, we investigated the extent to which sleep is involved in consolidating implicit MSL, specifically, whether the egocentric or the allocentric cognitive representations of a learned sequence are enhanced by sleep, and whether these changes support the development of explicit sequence knowledge across sleep but not wake. Our results indicate that egocentric and allocentric representations can be behaviorally dissociated for implicit MSL. Neither representation was preferentially enhanced across sleep nor were developments of explicit awareness observed. However, after a 1-wk interval performance enhancement was observed in the egocentric representation. Taken together, these results suggest that like explicit MSL, implicit MSL has dissociable allocentric and egocentric representations, but unlike explicit sequence learning, implicit egocentric and allocentric memory consolidation is independent of sleep, and the time-course of consolidation differs significantly.
Rapid Eye Movement (REM) sleep is characterized by the alternation of two markedly different microstates, phasic and tonic REM. These periods differ in awakening and arousal thresholds, sensory processing, and spontaneous cortical oscillations. Previous studies indicate that whereas in phasic REM, cortical activity is independent of the external environment, attentional functions and sensory processing are partially maintained during tonic periods. Large-scale synchronization of oscillatory activity, especially in the alpha and beta frequency ranges can accurately distinguish different states of vigilance and cognitive processes of enhanced alertness and attention. Therefore, we examined long-range inter-and intrahemispheric, as well as short-range EEG synchronization during phasic and tonic REM periods quantified by the weighted phase lag index. Based on the nocturnal polysomnographic data of 19 healthy, adult participants we showed that long-range inter-and intrahemispheric alpha and beta synchrony were enhanced in tonic REM states in contrast to phasic ones, and resembled alpha and beta synchronization of resting wakefulness. On the other hand, short-range synchronization within the gamma frequency range was higher in phasic as compared to tonic periods. Increased short-range synchrony might reflect local, and inwardly driven sensorimotor activity during phasic REM periods, whereas enhanced long-range synchrony might index frontoparietal activity that reinstates environmental alertness after phasic REM periods.
Sleep is important for the physical, social and mental well-being of both children and adults. Over the years, there has been a general presumption that sleep will inevitably decline with the increase in technology and a busy 24-hour modern lifestyle. This narrative review discusses the empirical evidence for secular trends in sleep duration and the implications of these trends.
Memory consolidation, a process which stabilizes recently acquired information into long-term storage, is thought to be optimized during sleep. Although recent evidence indicates that non-rapid-eye movement sleep (NREMs) is directly involved in memory consolidation, the role of rapid-eye movement sleep (REMs) in this process has remained controversial due to the extreme difficulty in experimentally isolating neural activity during REMs. Using a combination of electrophysiological recording and optogenetic techniques, recent work demonstrated for the first time that neural activity occurring specifically during REMs is required for spatial and contextual memory consolidation. Identifying the underlying mechanisms behind these observations, precisely how they translate to humans, and clarifying the extent of REMs’ role in other modalities of memory are important challenges of future research with implications for human health.
For the past two decades, it has generally been accepted that sleep benefits motor memory consolidation processes. This notion, however, has been challenged by recent studies and thus the sleep and motor memory story is equivocal. Currently, and in contrast to the declarative memory domain, a comprehensive overview and synthesis of the effects of post-learning sleep on the behavioral and neural correlates of motor memory consolidation is not available. We therefore provide an extensive review of the literature in order to highlight that sleep-dependent motor memory consolidation depends upon multiple boundary conditions, including particular features of the motor task, the recruitment of relevant neural substrates (and the hippocampus in particular), as well as the specific architecture of the intervening sleep period (specifically, sleep spindle and slow wave activity). For our field to continue to advance, future research must consider the multifaceted nature of sleep-related motor memory consolidation.
Learning complex structures from stimuli requires extended exposure and often repeated observation of the same stimuli. Learning induces stimulus-dependent changes in specific performance measures. The same performance measures, however, can also be affected by processes that arise because of extended training (e.g., fatigue) but are otherwise independent from learning. Thus, a thorough assessment of the properties of learning can only be achieved by identifying and accounting for the effects of such processes. Reactive inhibition is a process that modulates behavioral performance measures on a wide range of time scales and often has opposite effects than learning. Here we develop a tool to disentangle the effects of reactive inhibition from learning in the context of an implicit learning task, the alternating serial reaction time (ASRT) task. Our method highlights that the magnitude of the effect of reactive inhibition on measured performance is larger than that of the acquisition of statistical structure from stimuli. We show that the effect of reactive inhibition can be identified not only in population measures but also at the level of performance of individuals, revealing varying degrees of contribution of reactive inhibition. Finally, we demonstrate that a higher proportion of behavioral variance can be explained by learning once the effects of reactive inhibition are eliminated. These results demonstrate that reactive inhibition has a fundamental effect on the behavioral performance that can be identified in individual participants and can be separated from other cognitive processes like learning.
Older adults do not sleep as well as younger adults. Why? What alterations in sleep quantity and quality occur as we age, and are there functional consequences? What are the underlying neural mechanisms that explain age-related sleep disruption? This review tackles these questions. First, we describe canonical changes in human sleep quantity and quality in cognitively normal older adults. Second, we explore the underlying neurobiological mechanisms that may account for these human sleep alterations. Third, we consider the functional consequences of age-related sleep disruption, focusing on memory impairment as an exemplar. We conclude with a discussion of a still-debated question: do older adults simply need less sleep, or rather, are they unable to generate the sleep that they still need?
There is compelling evidence that sleep actively supports the formation of long-lasting memory representations. Experimental cuing of memories proved that neural replay of representations during sleep plays a causal role for this consolidation, which has also been shown to promote neocortical synaptic plasticity and spine formation. Concurrently, sleep has been proposed to facilitate forgetting through processes of synaptic renormalisation. This view received indirect support by findings in humans of sleep enhancing TMS-evoked plasticity and capabilities for encoding new information. First direct behavioural evidence of sleep inducing forgetting has only recently emerged after encoding large amounts of stimuli in adults. We propose forgetting complements sleep-dependent consolidation and facilitates gist abstraction especially at high memory loads, when reactivation-based consolidation reaches capacity limits.
Sleep spindles-short, phasic, oscillatory bursts of activity that characterize non-rapid eye movement sleep-are one of the only electrophysiological oscillations identified as a biological marker of human intelligence (e.g., cognitive abilities commonly assessed using intelligence quotient tests). However, spindles are also important for sleep maintenance and are modulated by circadian factors. Thus, the possibility remains that the relationship between spindles and intelligence quotient may be an epiphenomenon of a putative relationship between good quality sleep and cognitive ability or perhaps modulated by circadian factors such as morningness-eveningness tendencies. We sought to ascertain whether spindles are directly or indirectly related to cognitive abilities using mediation analysis. Here, we show that fast (13.5-16 Hz) parietal but not slow (11-13.5 Hz) frontal spindles in both non-rapid eye movement stage 2 sleep and SWS are directly related to reasoning abilities (i.e., cognitive abilities that support "fluid intelligence," such as the capacity to identify complex patterns and relationships and the use of logic to solve novel problems) but not verbal abilities (i.e., cognitive abilities that support "crystalized intelligence"; accumulated knowledge and experience) or cognitive abilities that support STM (i.e., the capacity to briefly maintain information in an available state). The relationship between fast spindles and reasoning abilities is independent of the indicators of sleep maintenance and circadian chronotype, thus suggesting that spindles are indeed a biological marker of cognitive abilities and can serve as a window to further explore the physiological and biological substrates that give rise to human intelligence.
Both repeated practice and sleep improve long-term retention of information. The assumed common mechanism underlying these effects is memory reactivation, either on-line and effortful or off-line and effortless. In the study reported here, we investigated whether sleep-dependent memory consolidation could help to save practice time during relearning. During two sessions occurring 12 hr apart, 40 participants practiced foreign vocabulary until they reached a perfect level of performance. Half of them learned in the morning and relearned in the evening of a single day. The other half learned in the evening of one day, slept, and then relearned in the morning of the next day. Their retention was assessed 1 week later and 6 months later. We found that interleaving sleep between learning sessions not only reduced the amount of practice needed by half but also ensured much better long-term retention. Sleeping after learning is definitely a good strategy, but sleeping between two learning sessions is a better strategy.
Healthy sleep is essential in children’s cognitive, behavioral, and emotional development. However, remarkably little is known about the influence of sleep disorders on different memory processes in childhood. Such data could give us a deeper insight into the effect of sleep on the developing brain and memory functions and how the relationship between sleep and memory changes from childhood to adulthood. In the present study we examined the effect of sleep disorder on declarative and non-declarative memory consolidation by testing children with sleep-disordered breathing (SDB) which is characterized by disrupted sleep structure. We used a story recall task to measure declarative memory and Alternating Serial Reaction time (ASRT) task to assess non-declarative memory. This task enables us to measure two aspects of non-declarative memory, namely general motor skill learning and sequence-specific learning. There were two sessions: a learning phase and a testing phase, separated by a 12 h offline period with sleep. Our data showed that children with SDB exhibited a generally lower declarative memory performance both in the learning and testing phase; however, both the SDB and control groups exhibited retention of the previously recalled items after the offline period. Here we showed intact non-declarative consolidation in SDB group in both sequence-specific and general motor skill. These findings suggest that sleep disorders in childhood have a differential effect on different memory processes (online vs. offline) and give us insight into how sleep disturbances affects developing brain.