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How to become an expert: A new perspective on the role of sleep in the mastery of procedural skills
Abstract
How do you get to Carnegie Hall? Practice, sleep, practice. With enough practice - and sleep - we adopt new strategies that eventually become automatic, and subsequently require only the refinement of the existing skill to become an "expert". It is not known whether sleep is involved in the mastery and refinement of new skills that lead to expertise, nor is it known whether this may be primarily dependent on rapid eye movement (REM), non-REM stage 2 (NREM2) or slow wave sleep (SWS). Here, we employed behavioural and scalp-recorded electroencephalography (EEG) techniques to investigate the post-learning changes in the architecture (e.g., REM, NREM2 and SWS duration) and the electrophysiological features (e.g., rapid eye movements, sleep spindles and slow wave activity) that characterize these sleep states as individuals progress from night to night, from "Novice" to "Experts" on a cognitive procedural task (e.g., the Tower of Hanoi task). Here, we demonstrate that speed of movements improves over the course of training irrespective of whether sleep or wake intervenes training sessions, whereas accuracy improves gradually, but only significantly over a night of sleep immediately prior to mastery of the task. On the night that subjects are first exposed to the task, the density of fast spindles increased significantly during both NREM2 and SWS accompanied by increased NREM2 sigma power and SWS delta power, whereas, on the night that subjects become experts on the task, they show increased REM sleep duration and spindles became larger in terms of amplitude and duration during SWS. Re-exposure to the task one-week after it had already been mastered resulted in increased NREM sleep duration, and again, increased spindle density of fast spindles during SWS and NREM2 and increased NREM2 sigma power and SWS delta power. Importantly, increased spindle density was correlated with overnight improvement in speed and accuracy. Taken together, these results help to elucidate how REM and NREM sleep are uniquely involved in memory consolidation over the course of the mastery of a new cognitively complex skill, and help to resolve controversies regarding sequential nature of memory processing during sleep in humans, for which consistent evidence is currently lacking.
... Sleep is important for good physical and mental health as well as memory (for review, see Rasch and Born 2013), including declarative memory (Plihal and Born 1997;Gais et al. 2000), procedural motor skills (Smith and MacNeill 1994;Nader and Smith 2003;Fogel et al. 2007Fogel et al. , 2015, and cognitively complex procedural skills necessary for problem-solving (van den Berg et al. 2019). However, the benefit of sleep for offline memory consolidation is impacted by reductions in both quantity and quality of sleep with increasing age (Fogel et al. 2012;Mander et al. 2017;Sergeeva et al. 2020). ...
... There was also limited REM sleep, which precluded further analysis of REM-related covariates. This type of procedural memory consolidation has been found to be related to the features of REM sleep (Conway and Smith 1994;Smith and Smith 2003;Fogel et al. 2015). Future studies using overnight sleep recordings could address these important issues. ...
... Thus, the optimal sequence of movements was not likely to have been memorized or learned explicitly; rather, the underlying cognitive strategy needed to arrive at the optimal solution to the ToH was most likely acquired implicitly, possibly through trial and error. This interpretation is consistent with several other studies investigating problem-solving skills (e.g., Baker et al. 1996;Dagher et al. 1999Dagher et al. , 2001Ronnlund et al. 2001;Rowe et al. 2001;Beauchamp et al. 2003;Smith and Smith 2003;Anderson et al. 2005;Boghi et al. 2006;Unterrainer and Owen 2006;Brand et al. 2010;Ashworth et al. 2014;Fogel et al. 2014Fogel et al. , 2015Fogel et al. , 2017aBalachandar et al. 2015;Nielsen et al. 2015;van den Berg et al. 2019). ...
As we age, the added benefit of sleep for memory consolidation is lost. One of the hallmark age-related changes in sleep is the reduction of sleep spindles and slow waves. Gray matter neurodegeneration is related to both age-related changes in sleep and age-related changes in memory, including memory for problem-solving skills. Here, we investigated whether spindles and slow waves might serve as biological markers for neurodegeneration of gray matter and for the related memory consolidation deficits in older adults. Forty healthy young adults (20–35 yr) and 30 healthy older adults (60–85 yr) were assigned to either nap or wake conditions. Participants were trained on the Tower of Hanoi in the morning, followed by either a 90-min nap opportunity or period of wakefulness, and were retested afterward. We found that age-related changes in sleep spindles and slow waves were differentially related to gray matter intensity in young and older adults in brain regions that support sleep-dependent memory consolidation for problem-solving skills. Specifically, we found that spindles were related to gray matter in neocortical areas (e.g., somatosensory and parietal cortex), and slow waves were related to gray matter in the anterior cingulate, hippocampus, and caudate, all areas known to support problem-solving skills. These results suggest that both sleep spindles and slow waves may serve as biological markers of age-related neurodegeneration of gray matter and the associated reduced benefit of sleep for memory consolidation in older adults.
... A few of the most famous anecdotal accounts include Albert Einstein's theory of relativity, Dimitry Mendeleev's inception of the periodic table, the discovery of insulin by Frederick Banting, Niels Bohr's insight into the structure of the atom, and Larry Page's inspiration for Google. There is indeed something special about sleep that facilitates the process of insight into the solution to a problem (Lewicki et al. 1987;Walker et al. 2002;Stickgold and Walker 2004;Cai et al. 2009;Brand et al. 2010;Durrant et al. 2011;Sio et al. 2013;Beijamini et al. 2014;Fogel et al. 2015;Monaghan et al. 2015;Lewis et al. 2018;Perdomo et al. 2018;van den Berg et al. 2019). Problem solving involves reasoning, planning, strategies, and skills, which are important aspects of certain forms of procedural memory-the "how to" of long-term memory. ...
... At the system level, the newly encoded memory is stabilized through memory consolidation, which transforms the memory into a lasting, integrated, and more easily retrievable form. Sleep is becoming increasingly recognized as an optimal time for consolidating procedural memory and related skills (for reviews see Rasch and Born 2013;King et al. 2017), including memory involving the acquisition of novel cognitive strategies (Mandai et al. 1989;Smith and Weeden 1990;Smith and Wong 1991;Smith 1995Smith , 1996Smith , 2001Plihal and Born 1997;Smith and Smith 2003;Fogel et al. 2007;Fogel et al. 2015;Nielsen et al. 2015;van den Berg et al. 2019). Still, it remains Hanoi (left) and the graphical representation of the optimal solution for the 3-disk version (right). ...
... More complicated versions (e.g., the 5-disk problem) can be solved by recursively applying the logic needed to solve the 3-disk problem, iteratively, several times. Figure adapted from Fogel et al. (2015). unclear how sleep transforms and enhances memory traces for novel strategies, which are needed to solve problems. ...
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.
... The implication of sleep spindles has been most robustly documented for motor refinement tasks of the second category, which suggests that they favor some degree of explicit recall in memory formation. Instead, both sleep spindles and SWA, as well as REMS, are involved in tasks that are cognitively more complex such as the mirror tracing task (212,216,279,506,582,583), a visuomotor learning task (213,285), or the tower of Hanoi task (213,216). An interesting case is the tower of Hanoi task that is learned over several days and where both refinement of motor skills and learning of optimal strategies are required. ...
... The implication of sleep spindles has been most robustly documented for motor refinement tasks of the second category, which suggests that they favor some degree of explicit recall in memory formation. Instead, both sleep spindles and SWA, as well as REMS, are involved in tasks that are cognitively more complex such as the mirror tracing task (212,216,279,506,582,583), a visuomotor learning task (213,285), or the tower of Hanoi task (213,216). An interesting case is the tower of Hanoi task that is learned over several days and where both refinement of motor skills and learning of optimal strategies are required. ...
... An interesting case is the tower of Hanoi task that is learned over several days and where both refinement of motor skills and learning of optimal strategies are required. In this case, increases in fast sleep spindle density and frequency were observed at early learning stages, whereas REMS duration was greater when performance was close to optimal (213). Increases seemed to be mostly related to fast spindles (47,216,358,438,456) and best for the hemisphere contralateral to the hand used for the task (77,456). ...
Sleep spindles are burst-like signals in the electroencephalogram (EEG) of the sleeping mammalian brain and electrical surface correlates of neuronal oscillations in thalamus. As one of the most inheritable sleep EEG signatures, sleep spindles probably reflect the strength and malleability of thalamocortical circuits that underlie individual cognitive profiles. We review the characteristics, organization, regulation and origins of sleep spindles and their implication in non-rapid-eye-movement sleep (NREMS) and its functions, focusing on human and rodent. Spatially, sleep spindle-related neuronal activity appears on scales ranging from small thalamic circuits to functional cortical areas, and generates a cortical state favoring intracortical plasticity while limiting cortical output. Temporally, sleep spindles are discrete events, part of a continuous power band, and elements grouped on an infraslow time scale over which NREMS alternates between continuity and fragility. We synthetize diverse and seemingly unlinked functions of sleep spindles for sleep architecture, sensory processing, synaptic plasticity, memory formation and cognitive abilities into a unifying sleep spindle concept, according to which sleep spindles a) generate neural conditions of large-scale functional connectivity and plasticity that outlast their appearance as discrete EEG events, b) appear preferentially in thalamic circuits engaged in learning and attention-based experience during wakefulness c) enable a selective re-activation and routing of wake-instated neuronal traces between brain areas such as hippocampus and cortex. Their fine spatiotemporal organization reflects NREMS as a physiological state coordinated over brain and body and may indicate, if not anticipate and ultimately differentiate, pathologies in sleep and neurodevelopmental, -degenerative and -psychiatric conditions.
... Several human studies have shown lengthened Stage 2 sleep after cognitive training, both in night sleep episodes [11,28,39,40] and in naps [29,41]. Of note, these changes emerged only after tasks involving procedural skills. ...
... In one study [28], the post-learning increases of Stage 2 sleep, compared to baseline, were observed only in subjects showing high performance levels at acquisition. Fogel et al. [40], studied the role of different sleep features over the time course of skill acquisition by recording sleep in four different conditions: (a) control sleep (preceeded by a simple cognitive task), (b) novice sleep (following administration of the Tower of Hanoi task), (c) expert sleep (recorded after a week during which subjects gained proficiency on the task through repeated exercise), and (d) re-test sleep (following readministration of the task a week after the previous condition). The increase in Stage 2 proportion and total duration appeared only in the re-test condition, supporting Smith et al.'s hypothesis [42] of a role for Stage 2 sleep in the stabilization and maintenance of existing skills. ...
... Increases of SWA have been reported after intensive exploratory activity in rats [8]. For human subjects, SWA increases have been reported following complex motor skills training (threeball cascade juggling) [37] and an intensive training at the Tower of Hanoi task [40]. In the latter study, the increase in SWA emerged both in the novice and re-test conditions compared to control, suggesting an involvement of SWA both in initial acquisition of a skill and in its stabilization once expertise is attained [40]. ...
Studies over the last 40 years have mainly investigated sleep structure changes as a result of wakeduration, in the frame of the classical sleep regulation theories. However, wake intervals of the sameduration can profoundly differ in their intensity, which actually reflects the degree of cognitive andphysical activity. Data on how sleep can be modified by wake intensity changes (initially sparse and oflittle consistence) have become much more substantial, especially in the frame of the intense researchdebate on sleep-memory relationships. Our aim is to examine the vast repertoire of sleep modificationsthat depend on waking cognitive manipulations, highlighting the sleep features that appear mostaffected. By systematically addressing this issue, we want to set the basis for future research exploring both the specific nature of the mechanisms involved and the applicative psychosocial and clinical fall-outs, in terms of possible behavioural interventions for sleep quality improvement.
... In addition, there is a long history of evidence suggesting that sleep affords optimal consolidation for other forms of procedural memory. In particular, for tasks that require the acquisition of a novel cognitive strategy, and may involve problem solving and rule-based learning (Fogel et al., 2007(Fogel et al., , 2015Mandai, Guerrien, Sockeel, Dujardin, & Leconte, 1989;Nielsen et al., 2015;Plihal & Born, 1997;Smith & Smith, 2003;Smith & Weeden, 1990;Smith & Wong, 1991;Smith, 1995Smith, , 1996Smith, , 2001. For example, reduced rapid eye movement (REM) sleep impairs procedural memory consolidation for cognitive procedural strategies, but not procedural memory for cognitively simple motor skills and MSL (Conway & Smith, 1994;Karni, Tanne, Rubenstein, Askenasy, & Sagi, 1994;Sandys-Wunsch & Smith, 1991;Smith & MacNeill, 1994;Smith, 1993). ...
... One classic example of a task used to investigate the role of sleep for procedural memory that requires the acquisition of novel cognitive strategies, is the Tower of Hanoi (ToH; Édouard Lucas first marketed the task in 1883 as "Dots and Boxes"). Improved performance on the ToH has been attributed to a consolidation interval containing sleep vs. wake (Brand, Opwis, Hatzinger, & Holsboer-Trachsler, 2010;Fogel et al., 2015;Nielsen et al., 2015;Smith, Nixon, & Nader, 2004). The ToH consists of three vertical pegs, equally spaced apart, and comprises a variable number of disks (typically three or five) of ascending size that can be moved from one peg to another. ...
... In the present study, two variants of the ToH task were used: (1) an uncued 3-disk version used only during the Training session, and, (2) a cued 5-disk version, where participants are guided on which move to make, used at the Immediate Test session, at Retest 1 and Retest 2 (see below for details of the experimental protocol). The uncued version of the ToH has been used in previous studies (Brand et al., 2010;Fogel et al., 2015;Nielsen et al., 2015;Smith et al., 2004), and has been shown to improve following sleep compared to wake. Immediate Test and Retest sessions were cued in order to be able to compare ToH performance to cued MSL performance. ...
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.
... They found a stronger overnight performance improvement (completion time) on the TOH in participants with more Stage 2 sleep, less slow-wave sleep (SWS) and a higher sleep spindle density in both Stage 2 and SWS. Another study in adults investigated how the pre-sleep acquisition of the TOH task affected subsequent sleep (Fogel, Ray, Binnie, & Owen, 2015). As compared with the baseline night, the densities of fast sleep spindles during Stage 2 sleep and SWS increased after the first task completion. ...
... Therefore, the present study aimed to investigate the associations of sleep stages and a wide range of microstructural sleep characteristics (fast and slow sleep spindle features, SWA) with improvement in EF performance across 12-hr periods that included primarily sleep or wakefulness only. Based on previous findings in adults (Fogel et al., 2015;Nielsen et al., 2015), we hypothesized that overnight performance improvements on the TOH are associated with increased Stage 2 sleep and higher spindle density. We complemented the investigation by exploring associations of sleep stages, spindles and SWA for performance improvements across wakefulness. ...
... So far, studies in children did not focus on mastery of planning and problem-solving skills. In adults, overnight TOH performance improvement was associated with higher spindle density (Nielsen et al., 2015), specifically for fast spindles (Fogel et al., 2015). In contrast, the current study in children showed TOH performance improvement to be associated with a higher density of slow spindles and a lower density of fast spindles. ...
The macro‐ and microstructural characteristics of sleep electroencephalography have been associated with several aspects of executive functioning. However, only a few studies have addressed the association of sleep characteristics with the learning involved in the acquisition of executive functions, and no study has investigated this for planning and problem‐solving skills in the developing brain of children. The present study examined whether children's sleep stages and microstructural sleep characteristics are associated with performance improvement over repeated assessments of the Tower of Hanoi task, which requires integrated planning and problem‐solving skills. Thirty children (11 boys, mean age 10.7 years, SD = 0.8) performed computerized parallel versions of the Tower of Hanoi three times across 2 days, including a night with polysomnographically assessed sleep. Pearson correlations were used to evaluate the associations of Tower of Hanoi solution time improvements across repeated assessments with sleep stages (% of total sleep time), slow‐wave activity, and fast and slow spindle features. The results indicated a stronger performance improvement across wake in children with more Stage N2 sleep and less slow‐wave sleep. Stronger improvements across sleep were present in children in whom slow spindles were more dense, and in children in whom fast spindles were less dense, of shorter duration and had less power. The findings indicate that specific sleep electroencephalography signatures reflect the ability of the developing brain to acquire and improve on integrated planning and problem‐solving skills.
... According to their model, REM sleep is required when a task is new and/or skill level is poor, whereas sleep spindles are required when a task is already well learned and needs further refinement. Additionally, Fogel, Ray, Binnie, and Owen (2015) reported that REM sleep duration increased until participants mastered a procedural task. ...
... Regarding task accuracy, not only an increase in slow SpA, but also a decrease in REM seemed to be favourable for improvements in performance. This result fits with the model of Smith et al. (2004) and the work of Fogel et al. (2015) suggesting that REM is only involved when a skill is particularly novel and has not yet been mastered. Thus, subjects with a decrease in REM might have already reached a higher skill level, possibly allowing for more refined processing during NREM sleep. ...
Sleep has been shown to facilitate the consolidation of newly acquired motor memories in adults. However, the role of sleep in motor memory consolidation is less clear in children and adolescents, especially concerning real-life gross-motor skills. Therefore, we investigated the effects of sleep and wakefulness on a complex gross-motor adaptation task by using a bicycle with an inverse steering device. A total of 29 healthy adolescents aged between 11 and 14 years (five female) were either trained to ride an inverse steering bicycle (learning condition) or a stationary bicycle (control condition). Training took place in the morning (wake, n = 14) or in the evening (sleep, n = 15) followed by a 9-hr retention interval and a subsequent re-test session. Slalom cycling performance was assessed by speed (riding time) and accuracy (standard deviation of steering angle) measures. Behavioural results showed no evidence for sleep-dependent memory consolidation. However, overnight gains in accuracy were associated with an increase in left hemispheric N2 slow sleep spindle activity from control to learning night. Furthermore, decreases in REM and tonic REM duration were related to higher overnight improvements in accuracy. Regarding speed, an increase in REM and tonic REM duration was favourable for higher overnight gains in riding time. Thus, although not yet detectable on a beha-vioural level, sleep seemed to play a role in the acquisition of gross-motor skills. A promising direction for future research is to focus on the possibility of delayed performance gains in adolescent populations.
... Automatic spindle detection was carried out using a previously published (Albouy et al., 2013;Fang et al., 2019;Fogel et al., 2014Fogel et al., , 2015Thompson et al., 2021), and validated in-house method employing EEGlab-compatible (Delorme and Makeig, 2004) software (github.com/stuartfogel/detect_spindles) written for MATLAB R2014a or newer (The MathWorks Inc., Natick, MA). ...
... The cortical arousal induced by cognitive activity interferes with the sleep process, such as increaseing sleep latency [6,48]. On the other hand, the large amount of data on post-learning sleep, mostly from sleep-related memory research, suggests a beneficial effect, such as the increase of sleep efficiency (SE) and slow wave sleep (SWS), as well as the decreased frequency of awakenings [11,12,49,50]. One possibility for these conflicting findings is the variety of content and form of cognitive activity. ...
Objectives:
Understanding the influence of cognitive activity on subsequent sleep has both theoretical and applied implications. This study aims to investigate the effect of pre-sleep cognitive activity, in the context of avoiding emotional interference, on macro-sleep and sleep spindles.
Methods:
In a within-subjects design, participants' sleep electroencephalography was collected in both the with and without pre-sleep cognitive activity conditions. Subsequent macro-sleep (i.e., sleep stage distribution and sleep parameters) and spindle characteristics (i.e., density, amplitude, duration, and frequency) were analyzed. In addition, a novel machine learning framework (i.e., deep neural network, DNN) was used to discriminate between cognitive activity and control conditions.
Results:
There were no significant differences in macro-sleep and sleep spindles between the cognitive activity and control conditions. Spindles-based DNN models achieved over 96% accuracy in differentiating between the two conditions, with fast spindles performing better than full-range and slow spindles.
Conclusions:
These results suggest a weak but positive effect of pre-sleep cognitive activity on subsequent sleep. It sheds light on a possible low-cost and easily accessible sleep intervention strategy for clinical and educational purposes.
... EMs during REM sleep have been linked to the consolidation of cognitively complex novel motor skills [16,17] and to cognitive strategies [7,8,21,22,24]. The benefit of sleep for this type of procedural memory has been frequently observed in studies which have employed the ToH [1,7,9,27,28,82], although the neural activity that accompanies rapid EMs during REM sleep has not been thoroughly examined. However, studies in rodents have shown that the theta rhythm during REM sleep is implicated in memory for novel environments, spatial navigation, and reward/ avoidance learning [56,[58][59][60]. ...
The hallmark eye movement (EM) bursts that occur during Rapid Eye Movement (REM) sleep are markers of consolidation for procedural memory involving novel cognitive strategies and problem-solving skills. Examination of the brain activity associated with EMs during REM sleep might elucidate the processes involved in memory consolidation, and may uncover the functional significance of REM sleep and EMs themselves. Participants performed a REM-dependent, novel procedural problem-solving task (i.e., the Tower of Hanoi; ToH) before and after intervals of either overnight sleep (n=20) or a daytime 8-hour wake period (n=20). In addition, event-related spectral perturbation (ERSP) of the electroencephalogram (EEG) time-locked to EMs occurring either in bursts (i.e., phasic REM), or in isolation (i.e., tonic REM), were compared to sleep on a non-learning control night. ToH improvement was greater following sleep compared to wakefulness. During sleep, frontal-central theta (~2-8 Hz) and central-parietal-occipital sensorimotor rhythm (SMR) activity (~8-16 Hz) time-locked to EMs, were greater on the ToH night vs. control night, and during phasic REM sleep, were both positively correlated with overnight memory improvements. Furthermore, SMR power during tonic REM increased significantly from the control night to ToH night, but was relatively stable from night-to-night during phasic REM. These results suggest that EMs are markers of learning-related increases in theta and SMR during phasic and tonic REM sleep. Phasic and tonic REM sleep may be functionally distinct in terms of their contribution to procedural memory consolidation.
... These data resemble those of Alsaad and colleagues [40], who found beneficial effects of VG playing on vigilance and attention, and of previous research from our group, showing that polysomnographically monitored sleep after an intensive VG session was even improved in terms of sleep continuity, stability, and cyclic organization [32,33]. Furthermore, the observed positive association between hours of VG playing and daytime functioning is consistent with research from the sleepmemory field, showing that performance at cognitive tasks administered at bedtime (often in the form of VGs) is enhanced after the sleep episode [48,49]. ...
Research on the effects of videogames (VGs) on health has produced mixed results. Here, we assess the relationships of VG playing with sleep; chronotype; sleepiness; and levels of depression, anxiety, and stress; and how they are modulated by the level of exposure to VGs. Four hundred-and two adult participants (age = 26.2 ± 7.84; 227 F) completed an online survey including questions on VG use and a set of standardized questionnaires. The sample was divided into three groups: habitual gamers (HGs, 42.2%), nonhabitual gamers (NHGs, 36.5%), and non-gamers (NGs, 21.3%). No between-group differences emerged in sleepiness (Epworth Sleepiness Scale) or Pittsburgh Sleep Quality Index measures except the sleep disturbances subscore, which was higher in NHGs. HGs showed delayed bed- and risetimes and higher eveningness (reduced Morningness–Eveningness Questionnaire). HGs and NHGs showed higher depression subscores (Depression Anxiety Stress Scale) but remained in the subclinical range. Moreover, hours/week of VG playing predicted delayed sleep timing, lower daytime dysfunction, and lower sleepiness. Our data suggest that VG playing does not necessarily compromise sleep quality and may even benefit daytime functioning, underlining the need to reconsider the relationships between VG use and health by taking into account possible modulating factors such as habitual VG exposure.
... Furthermore, over the course of a night, motor activity showed steeper hourly increases in infants with more walk experience. REM sleep has been implicated in the consolidation of procedural motor skills such as finger tapping in adulthood (Pereira & Lewis, 2020;Schönauer et al., 2014) and changes based on individual levels of expertise (Fogel et al., 2015). Perhaps the increase in movement reflects a change in the proportion of REM sleep in the latter half of the night, fluctuating as walking is further consolidated with practice. ...
The characteristics of infant sleep change over the first year. Generally, infants wake and move less at night as they grow older. However, acquisition of new motor skills leads to temporary increases in night waking and movement at night. Indeed, sleep-dependent movement at night is important for sensorimotor development. Nevertheless, little is known about how movement during sleep changes as infants accrue locomotor experience. The current study investigated whether infant sleep and movement during sleep were predicted by infants' walking experience. Seventy-eight infants wore an actigraph to measure physical activity during sleep. Parents reported when their infants first walked across a room >10 feet without stopping or falling. Infants in the midst of walking skill acquisition had worse sleep than an age-group estimate. Infants with more walk experience had more temporally sporadic movement during sleep and a steeper hourly increase in physical activity over the course of the night. Ongoing motor skill consolidation changes the characteristics of movement during sleep and may alter sleep state-dependent memory consolidation. We propose a model whereby changes in gross motor activity during night sleep reflect movement-dependent consolidation.
... Such behavioral coding has confirmed that infants' ability to solve the tunnel task varied as a function of walk experience; expert walkers with more than 30 days of experience and very new walkers who still crawled regularly could navigate the tunnel with ease, whereas those with a moderate amount of experience struggled (Horger & Berger, 2019). Controlling for expertise, and thus task difficulty, is also important because the adult literature suggests that it mediates the role of sleep in consolidation (Fogel et al., 2015). ...
The current study sought to tease apart the unique contributions of napping and nighttime sleep to infant learning, specifically in the context of motor problem solving. We challenged 54 walking infants to solve a novel locomotor problem at three time points—training, test, and follow-up the next morning. One group of infants napped during the delay between training and test. Another group did not sleep during the delay. A third group received the test immediately after training with no delay. Only the Nap group’s strategy choices continued to improve through the follow-up session, suggesting that daytime sleep has an active role in strengthening otherwise fragile memory. Although group did not affect strategy maintenance, walk experience did, suggesting that task difficulty may shape the impact of sleep on learning. Thus, day sleep and night sleep make independent contributions to the consolidation of motor problem-solving strategies during infancy.
... Results showed peculiar benefits in the cognitive strategy dimension following a night of sleep but not after an equivalent waking period, while no changes in performance following a period of consolidation were observed for the series of movements executed to apply the strategy. These results are in accordance with previous studies reporting sleep-dependent consolidation after procedural tasks that require a high level of cognitive functioning or a new (but complex) cognitive strategy for achieving one's goal (Conte, et al., 2020;Fogel, Ray, Binnie, & Owen, 2015;Kuriyama, Mishima, Suzuki, Aritake, & Uchiyama, 2008;Smith, Nixon, & Nader, 2004). Mental rehearsal of movements drives multiple cognitive processes in which conscious elaboration (e.g., selection and assembly of action elements stored in the working memory) and motor (simulation toward a goal and inhibition) processes are implicated, and which therefore involve executive resources to a much greater extent than PP (Glover, Bibby, & Tuomi, 2020;O'Shea & Moran, 2017). ...
Acquisition of gross motor sequence learning with physical and mental training elicits gains in performance. However, the effects of sleep or daytime consolidation after both types of practice remain unclear, especially the effects upon the goal- and movement-based components of a gross motor sequential task. The main purpose of this study was to test the effect of physical practice (PP) and motor imagery practice (MIP) on the acquisition and consolidation processes of gross motor sequence learning.
Seventy-six participants were tested before and after PP or MIP on a whole-body sequential paradigm, following either a night of sleep (PPsleep and MIPsleep groups) or an equivalent daytime period (PPday and MIPday groups). Control groups without training were tested following similar timespans (CTRLsleep and CTRLday groups). The number of sequential movements and the centre of mass displacement – corresponding to goal and movement-based components, respectively – were assessed.
Results showed that relative to the CTRL groups, the PP and MIP groups improved performance during acquisition. Importantly, only the MIPsleep group further improved performance after a night of sleep; participants of other groups stabilised their performance after consolidation. Additionally, the number of sequential movements and the centre of mass displacement evolved conjointly without being influenced by the type of training or the nature of the consolidation.
To conclude, these results confirm that sleep contributes to the consolidation of gross motor sequence learning acquired with MIP but not PP. The relationship between the goal- and movement-based components of a gross motor sequential task is discussed.
... In fact, it is plausible that the improvements of sleep continuity, stability and organization emerged in our study reflect the involvement of such sleep parameters in the consolidation process. In this regard, a limitation of our study resides in the fact that we did not employ an active control condition (i.e., in which the sleep episode is preceded by a non-learning control task, as in [10,12,49,50]), which would have allowed us to disentangle learning-dependent from general use-dependent effects on sleep features. However, we have previously shown, in a sample of poor sleepers, that several sleep stability and organization measures were specifically affected by training rather than by a control task [12]. ...
Several studies show that pre-sleep learning determines changes in subsequent sleep, including improvements of sleep quality. Our aims were to confirm this finding using a more ecological task (learning a theatrical monologue) and to investigate whether the effect is modulated by expertise. Using a mixed design, we compared polysomnographic recordings of baseline sleep (BL, 9-h TIB) to those of post-training sleep (TR, with the same TIB but preceded by the training session), in one group of actors (N = 11) and one of non-actors (N = 11). In both groups, TR appears reorganized and re-compacted by the learning session, as shown, among others, by a significant decrease of WASO%, awakenings, arousals, and state transitions and by a trend towards an increased number of complete cycles and total cycle time. Concerning memory performance, the number of synonyms produced was significantly higher in the morning relative to immediate recall. No between-groups differences emerged either for sleep or memory variables. Our data confirm pre-sleep learning’s beneficial effect on sleep quality in an ecological context. While expertise appears not to influence memory-related sleep mechanisms, results on morning recall support the recent view that sleep’s role in memory processes consists in trace “transformation” for adaptive purposes, rather than rote consolidation.
... One particularly promising avenue of future research would be to explore the therapeutic benefit of orexin drug therapies for memory by normalizing REM abnormalities in conditions with orexin abnormalities. Specifically, REM sleep has been shown to support, in particular, memory that involves procedures and skills which rely on cognitively complex rules, grammar, logic, and reasoning [103,104], and non-REM sleep supports motor skills memory and declarative memory [105,106]. Future studies employing orexin therapies that enhance both nocturnal REM and non-REM sleep (e.g., DO-RAs) may lead to novel treatments for the various symptoms, conditions, and disorders, including anorexia nervosa and neurodegenerative disease. ...
Orexins regulate a wide variety of biological functions, most notably the sleep-wake cycle, reward and stress processing, alertness, vigilance, and cognitive functioning. Alterations of central and peripheral orexin levels are linked to conditions such as narcolepsy, anorexia nervosa, age-related cognitive decline, and neurodegenerative disease. Preliminary studies suggest that orexin mimetics can safely promote the wake signal via orexin agonism during the day and that orexin receptor antagonists can promote the sleep signal during the night. Thus, novel orexin therapies have the potential to either improve memory, cognition, and daytime performance directly or indirectly, through promotion of good sleep. The full scope of the therapeutic potential of orexin therapies remains to be elucidated.
... Future studies could assess how these different REM sleep memory markers evolve over time following learning and how they relate to dream activity. The present findings might be better understood in the context of dual and sequential process hypotheses in which memory consolidation requires both NREM and REM sleep within the same night (Giuditta et al., 1995) or over several nights (Fogel, Ray, Binnie, & Owen, 2015). REM sleep may facilitate acquiring a complex and novel procedural skill, but NREM sleep may further refine a well-learned skill or be required for more explicit memory features (Smith, Aubrey, & Peters, 2004). ...
Although new learning is known to reappear in later dream scenarios, the timing of such reappearances remains unclear. Sometimes, references to new learning occur relatively quickly, 1 day post-learning (day-residue effect); at other times there may be a substantive delay, 5-7 days, before such references appear (dream-lag effect). We studied temporal delays in dream reactivation following the learning of a virtual reality (VR) flying task using 10-day home sleep/dream logs, and how these might be influenced by targeted memory reactivation (TMR). Participants were exposed twice to a VR task in the sleep laboratory; once before and once after a 2-hr opportunity to nap (n = 65) or to read (n = 32). Auditory cues associated with the VR task were replayed in either wake, rapid eye movement (REM) sleep, slow-wave sleep (SWS) or were not replayed. Although we previously showed that TMR cueing did not have an immediate effect on dream content, in the present study we extend these results by showing that TMR in sleep has instead a delayed effect on task-dream reactivations: participants dreamed more about the task 1-2 days later when TMR was applied in REM sleep and 5-6 days later when it was applied in SWS sleep, compared to participants with no cueing. Findings may help explain the temporal relationships between dream and memory reactivations and clarify the occurrence of day-residue and dream-lag phenomena.
... Physiological mechanisms. In adults, both REM and nREM2 sleep characteristics are implicated in procedural memory, possibly interacting to aid learning and consolidation [58]. How sleep facilitates infants' procedural memory is poorly understood. ...
Emerging studies across learning domains have shed light on mechanisms underlying sleep’s benefits during numerous developmental periods. In this conceptual review, we survey recent studies of sleep and cognition across infancy, childhood, and adolescence. By summarizing recent findings and integrating across studies with disparate approaches, we provide a novel understanding of sleep’s role in human cognitive function. Collectively, these studies point to an interrelation between brain development, sleep, and cognition. Moreover, we point to gaps in our understanding, which inform the agenda for future research in developmental and sleep science.
... Future research should test this hypothesis by assessing the association between incremental increases in skill level and changes in sleep quality. Teasing apart the temporal relationship between change in skill and change in sleep could inform the study of developmental transitions revealing how simultaneous change across domains shapes developmental trajectories (Berger & Moore, n.d., under review;Fogel, Ray, Binnie, & Owen, 2015). ...
Sleep is part of the process that prepares children and adults for next day cognitive activity. Insufficient or fragmented sleep has a detrimental impact on subsequent encoding (Rouleau et al., 2002) and cognitive functioning (Joo et al., 2012). However, fragmented sleep early in life is a developmental norm, limiting the extent to which conclusions derived from older populations can be generalized. To directly test the continuity of this relationship, newly-walking infants’ (N = 58) sleep was monitored overnight using actigraphy. The next morning they were taught a motor problem-solving task. The task required infants to navigate through a tunnel to reach a goal at the other end. We coded infants’ exploratory behaviors and the extent of training required to solve the task. Using a cluster analysis that accounted for exploratory behaviors and number of training prompts, infants were sorted into three profiles: those who found the task Easy to solve, those who found it Difficult, and those who Never solved it. Wake episodes and sleep efficiency were entered as predictors of cluster membership in a multinomial logistic regression. Of the infants who ultimately solved the task, those with more wake episodes and lower sleep efficiency had more difficulty. Specifically, fragmentation appeared to negatively impact preparedness to learn. Contrary to our expectations, infants who Never solved the task had the least fragmented sleep, indicating that an optimal level of fragmentation is needed for efficient problem-solving. For infants, some level of sleep fragmentation is needed the night before learning in order to solve a task efficiently. These findings highlight the interaction between developmental domains, from sleep quality to motor experience, and their impact on infant learning in real time.
... As an individual moves into stage 2 sleep, the pattern of the brain activity is dominated by theta waves (4-8 Hz) which are interrupted by short bursts of in ceased frequency waves known as sleep spindles. Actually, the sleep spindle is a rapid burst of high frequency brain waves (12-16 Hz) that are probably important for learning and memory (25)(26)(27)(28). ...
Sleep and wakefulness are two main types of human and animal behavior. On the average human beings spend about one-third of their lives asleep. The sleep-wake cycle is the most important circadian rhythms which alternates in a periodic manner lasting for about 24 hours. Sleep is determined as the natural periodic suspension of consciousness characterized by relative immobility
and reduced responsiveness to external stimuli. The researchers have found and identified many special brain structures and systems controlling waking, rapid eye movement (REM) sleep and nonrapid eye (NREM) sleep and the transitions among these states. Currently, there is an enhanced interest of researchers toward sleep and its neurophysiological mechanisms of regulation because the number of people suffering from various sleep disturbance such
as insomnia, delayed sleep onset, duration and propensity of sleep, worldwide dramatically increases. In addition to the next day drowsiness, nervousness, tiredness and decreased workability, it has been suggested that sleep is important also for the maintaining of mood, memory and cognitive function of
the brain and is essential for the normal functioning of the endocrine and immune systems. More recently, new studies show a sustained link between sleep disorders and different serious health problems, including obesity, insulin resistance, type 2 diabetes mellitus, cardio-vascular diseases and
depression.
Therefore, the purpose of this review is to summarize and analyze the available data about the neurological control of wakefulness, non-rapid-eye-movement (NREM) sleep and rapid- eyemovement (REM) sleep creating a substantial basis for better understanding different sleep disorders.
Special attention is paid on the pharmacological aspects and use of some new classes of sleep promoting agents – melatonin, melatonin receptor agonists and orexin receptor antagonists.
... R. Soc. B 375: 20190232 other learning-related cortical and subcortical brain structures during memory consolidation, and that this mnemonic process engages two complementary neurophysiological mechanisms: 'synaptic' and 'systems' consolidation processes [1,5,[63][64][65][66][67][68]. At the synaptic level, it has recently been demonstrated that, irrespective of the memory system, post-learning sleep is characterized by enhanced temporal synchrony between cortical SO and spindle activity, topographically restricted to the brain regions that were initially involved during learning [50,52,53]. ...
Sleep spindle activity has repeatedly been found to contribute to brain plasticity and consolidation of both declarative and procedural memories. Here we propose a framework for motor memory consolidation that outlines the essential contribution of the hierarchical and multi-scale periodicity of spindle activity, as well as of the synchronization and interaction of brain oscillations during this sleep-dependent process. We posit that the clustering of sleep spindles in ‘trains', together with the temporally organized alternation between spindles and associated refractory periods, is critical for efficient reprocessing and consolidation of motor memories. We further argue that the long-term retention of procedural memories relies on the synchronized (functional connectivity) local reprocessing of new information across segregated, but inter-connected brain regions that are involved in the initial learning process. Finally, we propose that oscillatory synchrony in the spindle frequency band may reflect the cross-structural reactivation, reorganization and consolidation of motor, and potentially declarative, memory traces within broader subcortical–cortical networks during sleep.
This article is part of the Theo Murphy meeting issue ‘Memory reactivation: replaying events past, present and future'.
... Alternatively, nREM2 sleep and sleep spindles during nREM2 have also been associated with procedural memory consolidation (Smith and MacNeill 1994;Walker et al. 2002;Fogel and Smith 2006;Nishida and Walker 2007;Fogel et al. 2007b;Laventure et al. 2016). It is possible that both nREM and REM sleep contribute to procedural learning, but in different capacities Smith et al. 2004;Fogel et al. 2015). ...
Sleep is the single most common form of human behavior, indicating that sleep likely has an important evolutionary function. Yet the functions of sleep are still debated. Intriguingly, sleep is not static across the life span, changing in duration, pattern, structure, and physiology. This chapter reviews the transformations of sleep, from the first appearance of sleep prenatally to sleep in older adulthood, and assesses how the functions of sleep may change in response. This review focuses on the memory function of sleep and examines sleep-dependent consolidation across declarative, procedural, and emotional memory domains. With respect to the memory function of sleep, changes in SWS in particular appear to have the greatest impact on the resultant age-related alterations in sleep-dependent memory consolidation.
... Most interestingly, we found this association to be independent of age, making it tempting to speculate that this mediation effect could potentially explain, in large part, the discrepancies in the literature regarding issues such as the beneficial effect of sleep for explicit motor sequence consolidation (Adi-Japha & Karni, 2016;Rickard & Pan, 2017) or even the existence of a sleep-dependent motor memory consolidation deficits in older adults (Fogel et al., 2014;Fogel, Ray, Binnie, & Owen, 2015;Gudberg, Wulff, & Johansen-Berg, 2015;Spencer, Gouw, & Ivry, 2007). Indeed, the present pattern of results lead us to propose that the integrity of the thalamo-cortical projections, through its impact on sleep spindle production, could represent one of the critical mechanisms modulating the expression of sleep-dependent offline gains following motor sequence learning in young and older adults. ...
Ample evidence suggests that consolidation of the memory trace associated with a newly acquired motor sequence is supported by thalamo-cortical spindle activity during subsequent sleep, as well as functional changes in a distributed cortico-striatal network. To date, however, no studies have investigated whether the structural white matter connections between these regions affect motor sequence memory consolidation in relation with sleep spindles. Here, we used diffusion weighted imaging (DWI) tractography to reconstruct the major fascicles of the cortico-striato-pallido-thalamo-cortical loop in both young and older participants who were trained on an explicit finger sequence learning task before and after a daytime nap. Thereby, this allowed us to examine whether post-learning sleep spindles measured using polysomnographic recordings interact with consolidation processes and this specific neural network. Our findings provide evidence corroborating the critical role of NREM2 thalamo-cortical sleep spindles in motor sequence memory consolidation, and show that the post-learning changes in these neurophysiological events relate specifically to white matter characteristics in thalamo-cortical fascicles. Moreover, we demonstrate that microstructure along this fascicle relates indirectly to offline gains in performance through an increase of spindle density over motor-related cortical areas. These results suggest that the integrity of thalamo-cortical projections, via their impact on sleep spindle generation, may represent one of the critical mechanisms modulating the expression of sleep-dependent offline gains following motor sequence learning in healthy adults.
... I. Merikanto et al. Neurobiology of Learning and Memory 157 (2019) 106-113 particularly fast spindles (Fogel, Ray, Binnie, & Owen, 2015;Mölle, Bergmann, Marshall, & Born, 2011). Sleep spindle activity can, however, reflect non-adaptive processes in brain function that associates with various psychiatric diseases (Tesler, Gerstenberg, & Huber, 2013). ...
ADHD and its subclinical symptoms have been associated with both disturbed sleep and weakened overnight memory consolidation. As sleep spindle activity during NREM sleep plays a key role in both sleep maintenance and memory consolidation, we examined the association between subclinical ADHD symptoms and sleep spindle activity. Furthermore, we hypothesized that sleep spindle activity mediates the effect of ADHD symptoms on overnight learning outcome in a procedural memory task. We studied these questions in a community-based cohort of 170 adolescents (58% girls, mean age = 16.9, SD = 0.1 years), who filled in the Adult ADHD Self-Report Scale (ASRS-v1.1), and underwent an overnight sleep EEG coupled with a mirror tracing task before and after sleep. Elevated ADHD symptoms were associated with weaker fast sleep spindle activity, and poorer overnight learning in the procedural memory test. However, sleep spindles, contrary to the hypothesis, did not mediate the association between ADHD symptoms and overnight learning. Our results showed that a higher level of ADHD symptoms in adolescence is associated with similar alterations in sleep spindle activity as observed in many neuropsychiatric conditions and might contribute to altered synaptic connectivity and sleep fragmentation observed in ADHD.
... There is a large body of evidence suggesting that one of the functions of sleep is for memory consolidation, as reflected by performance improvements (e.g., from training to retest) over an intervening period of sleep (Maquet, 2001;Stickgold and Walker, 2005;Rasch and Born, 2013;Peigneux et al., 2015). More specifically, sleep has been shown to benefit memory for facts, places, and events [i.e., "declarative memory" (Plihal and Born, 1997;Smith, 2001;Gais et al., 2002;Gais and Born, 2004;Schabus et al., 2004;Clemens et al., 2005;Ellenbogen et al., 2006;Fogel et al., 2007b;Payne et al., 2012)], as well as for skills [i.e., "procedural memory" (Nader and Smith, 2003;Fogel and Smith, 2006;Fogel et al., 2007bFogel et al., , 2015Barakat et al., 2011)]. More specifically, recent evidence from human neuroimaging studies suggest that after new learning, there is physiological reactivation of brain areas recruited during learning (Peigneux et al., 2003(Peigneux et al., , 2006Bergmann et al., 2011;Antony et al., 2012;Schönauer et al., 2014;Fogel et al., 2017). ...
Can dreams reveal insight into our cognitive abilities and aptitudes (i.e., “human intelligence”)? The relationship between dream production and trait-like cognitive abilities is the foundation of several long-standing theories on the neurocognitive and cognitive-psychological basis of dreaming. However, direct experimental evidence is sparse and remains contentious. On the other hand, recent research has provided compelling evidence demonstrating a link between dream content and new learning, suggesting that dreams reflect memory processing during sleep. It remains to be investigated whether the extent of learning-related dream incorporation (i.e., the semantic similarity between waking experiences and dream content) is related to inter-individual differences in cognitive abilities. The relationship between pre–post sleep memory performance improvements and learning-related dream incorporation was investigated (N = 24) to determine if this relationship could be explained by inter-individual differences in intellectual abilities (e.g., reasoning, short term memory (STM), and verbal abilities). The extent of dream incorporation using a novel and objective method of dream content analysis, employed a computational linguistic approach to measure the semantic relatedness between verbal reports describing the experience on a spatial (e.g., maze navigation) or a motor memory task (e.g., tennis simulator) with subsequent hypnagogic reverie dream reports and waking “daydream” reports, obtained during a daytime nap opportunity. Consistent with previous studies, the extent to which something new was learned was related (r = 0.47) to how richly these novel experiences were incorporated into the content of dreams. This was significant for early (the first 4 dream reports) but not late dreams (the last 4 dream reports). Notably, here, we show for the first time that the extent of this incorporation for early dreams was related (r = 0.41) to inter-individual differences in reasoning abilities. On the other hand, late dream incorporation was related (r = 0.46) to inter-individual differences in verbal abilities. There was no relationship between performance improvements and intellectual abilities, and thus, inter-individual differences in cognitive abilities did not mediate the relationship between performance improvements and dream incorporation; suggesting a direct relationship between reasoning abilities and dream incorporation. This study provides the first evidence that learning-related dream production is related to inter-individual differences in cognitive abilities.
... Recommended standard for the age is 9 to 13 hours (U.S. National Sleep Foundation, 2015). There are evidences that training affect sleep quality, increasing the rem sleep compared to other stages of sleep in adults (Fogel et al. 2015) albeit there is any study in children. It has been proposed (Maculano- Esteves et al. 2014, Lang et al. 2015) the type of sport training influences selectively sleep duration. ...
... Sleep fosters memory consolidation. [50][51][52][53] It is well established that, for learning goals requiring extensive rehearsal, spaced practice over a prolonged time is more effective than massed practice in a condensed time, despite similar investments of practice hours. [54][55][56][57] Evidently, something happens in periods of nonpractice that contributes to a learning effect, akin to muscle development after physical training. ...
The introduction of competency-based medical education has shifted thinking from a fixed-time model to one stressing attained competencies, independent of the time needed to arrive at those competencies. In this article, the authors explore theoretical and conceptual issues related to time variability in medical training, starting with the Carroll model from the 1960s that put time in the equation of learning. They discuss mastery learning, deliberate practice, and learning curves.
While such behaviorist theories apply well to structured courses and highly structured training settings, learning in the clinical workplace is not well captured in such theories or in the model that Carroll proposed. Important in clinical training are self-regulation and motivation; neurocognitive perspectives of time and learning; professional identity formation; and entrustment as an objective of training—all of which may be viewed from the perspective of the time needed to complete training. The authors conclude that, in approaching time variability, the Carroll equation is too simplistic in its application to the breadth of medical training. The equation may be expanded to include variables that determine effective workplace learning, but future work will need to examine the validity of these additional factors.
... One of the most important functions of sleep is to support learning and memory (for reviews, see Maquet 2001;Smith 2001;Doyon et al. 2009b;Fogel and Smith 2011;Rasch and Born 2013;Stickgold and Walker 2013;Stickgold 2013;Tononi and Cirelli 2014). A period of sleep, compared with wake, is known to enhance and transform labile memories into enduring long-term storage (Korman et al. 2003;Walker 2005;Sirota and Buzsáki 2007;Takehara-Nishiuchi and McNaughton 2008;Squire 2009;Giuditta 2014), enhance the performance of newly learned skills (Fischer et al. 2002;Peigneux et al. 2004;Bergmann et al. 2008;Doyon et al. 2009a;Albouy et al. 2013;Fogel et al. 2015), and can even promote conscious insight into otherwise unconscious knowledge (Wagner et al. 2004;Drosopoulos et al. 2005;Gómez et al. 2006;Yordanova et al. 2008;Payne et al. 2009). These enhancements in memory and skill performance after sleep are a phenomenon collectively referred to as "sleep-dependent memory consolidation." ...
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.
... On the other hand, sleep improves cerebellar learning as learning-dependent timing, procedural memory formation, and spatiotemporal predictions of motor actions (Verweij et al., 2016). Fogel et al. (2015) reported that sleep after a procedural task showed an increment in SWS density, highlighting a putative cerebellar involvement. ...
... The role of sleep in consolidation of cerebellar memory formation is also supported by the precise sequence of changes that occur over the course of long-term skill learning. For example, Fogel and colleagues [99] showed that on the night that human subjects are first exposed to a procedural task, the density of fast spindles increases significantly during both NREM2 and SWS, whereas on the night that the subjects become experts, they show increased REM sleep duration while the spindles become larger in terms of amplitude and duration during SWS. Re-exposure to the task 1 week later results in increased NREM sleep duration, and again, increased spindle density of fast spindles during SWS and NREM2, which is correlated with overnight improvement in speed and accuracy of the task, highlighting putative cerebellar involvement. ...
We sleep almost one-third of our lives and sleep plays an important role in critical brain functions like memory formation and consolidation. The role of sleep in cerebellar processing, however, constitutes an enigma in the field of neuroscience; we know little about cerebellar sleep-physiology, cerebro-cerebellar interactions during sleep, or the contributions of sleep to cerebellum-dependent memory consolidation. Likewise, we do not understand why cerebellar malfunction can lead to changes in the sleep-wake cycle and sleep disorders. In this review, we evaluate how sleep and cerebellar processing may influence one another and highlight which scientific routes and technical approaches could be taken to uncover the mechanisms underlying these interactions.
... Since in the present study we found a trend toward a correlation between sleep-dependent consolidation of rewarded behavior and non-REM sleep in healthy children, it seems likely that parameters like slow oscillations or sleep spindles might be involved. This would match a recent study, in which fast sleep spindles and delta power during non-REM sleep were shown to help in the development of procedural skills (Fogel et al., 2015). In future studies the amount of REM sleep and slow-wave sleep in children suffering from ADHD + CD/ODD should be manipulated -e.g., using the splitnight paradigm (Yaroush et al., 1971) -to further assess the role of REM sleep and non-REM sleep as well as their accompanying waveforms on the consolidation of rewarded behavior. ...
Children suffering from attention-deficit hyperactivity disorder (ADHD) often also display impaired learning and memory. Previous research has documented aberrant reward processing in ADHD as well as impaired sleep-dependent consolidation of declarative memory. We investigated whether sleep also fosters the consolidation of behavior learned by probabilistic reward and whether ADHD patients with a comorbid disorder of social behavior show deficits in this memory domain, too. A group of 17 ADHD patients with comorbid disorders of social behavior aged 8–12 years and healthy controls matched for age, IQ, and handedness took part in the experiment. During the encoding task, children worked on a probabilistic learning task acquiring behavioral preferences for stimuli rewarded most often. After a 12-hr retention interval of either sleep at night or wakefulness during the day, a reversal task was presented where the contingencies were reversed. Consolidation of rewarded behavior is indicated by greater resistance to reversal learning. We found that healthy children consolidate rewarded behavior better during a night of sleep than during a day awake and that the sleep-dependent consolidation of rewarded behavior by trend correlates with non-REM sleep but not with REM sleep. In contrast, children with ADHD and comorbid disorders of social behavior do not show sleep-dependent consolidation of rewarded behavior. Moreover, their consolidation of rewarded behavior does not correlate with sleep. The results indicate that dysfunctional sleep in children suffering from ADHD and disorders of social behavior might be a crucial factor in the consolidation of behavior learned by reward.
... Automatic spindle detection was carried out using a previously published (Fogel, Ray, Binnie, & Owen, 2015;Fogel et al., 2014;Albouy et al., 2013) and validated in-house method employing EEGlab-compatible (Delorme & Makeig, 2004) software (github.com/stuartfogel/ detect_spindles) written for MATLAB R2014a (The MathWorks Inc., Natick, MA). ...
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.
... For example, it has been shown that as a person masters a complex procedural task that requires training across multiple days (the Tower of Hanoi task), changes in EEG-derived sleep features associate with improvements from initial training to mastery of the skill. 46 At present, however, it remains unclear whether sleep contributes to day-to-day improvements in declarative memory consolidation beyond the first night after encoding. ...
Study objectives:
The ability to recall facts is improved when learning takes place at spaced intervals, or when sleep follows shortly after learning. However, many students cram for exams and trade sleep for other activities. The aim of this study was to examine the interaction of study spacing and time in bed (TIB) for sleep on vocabulary learning in adolescents.
Methods:
In the Need for Sleep Study, which used a parallel-group design, 56 adolescents aged 15-19 years were randomly assigned to a week of either 5 h or 9 h of TIB for sleep each night as part of a 14-day protocol conducted at a boarding school. During the sleep manipulation period, participants studied 40 Graduate Record Examination (GRE)-type English words using digital flashcards. Word pairs were presented over 4 consecutive days (spaced items), or all at once during single study sessions (massed items), with total study time kept constant across conditions. Recall performance was examined 0 h, 24 h, and 120 h after all items were studied.
Results:
For all retention intervals examined, recall of massed items was impaired by a greater amount in adolescents exposed to sleep restriction. In contrast, cued recall performance on spaced items was similar between sleep groups.
Conclusions:
Spaced learning conferred strong protection against the effects of sleep restriction on recall performance, whereas students who had insufficient sleep were more likely to forget items studied over short time intervals. These findings in adolescents demonstrate the importance of combining good study habits and good sleep habits to optimize learning outcomes.
We examined how aging affects the role of sleep in the consolidation of newly learned cognitive strategies. Forty healthy young adults (20-35 years) and 30 healthy older adults (60-85 years) were included. Participants were trained on the Tower of Hanoi (ToH) task, then, half of each age group were assigned to either the 90-minute nap condition, or stayed awake, before retesting. The temporal co-occurrence between slow-waves (SW) and sleep spindles (SP) during NREM sleep was examined as a function of age in relation to memory consolidation of problem-solving skills. We found that despite intact learning, older adults derived a reduced benefit of sleep for problem-solving skills relative to younger adults. As expected, the percentage of coupled spindles was lower in older compared to younger individuals from control to testing sessions. Furthermore, coupled spindles in young adults were more strongly coupled to the SW upstate compared to older individuals. Coupled spindles in older individuals were lower in amplitude (mean area under curve; μV) compared to the young group. Lastly, there was a significant relationship between offline gains in accuracy on the ToH and percent change of spindles coupled to the upstate of the slow wave in older, but not younger adults. Multiple regression revealed that age accounted for differences in offline gains in accuracy, as did spindle coupling during the upstate. These results suggest that with aging, spindle-slow wave coupling decreases. However, the degree of the preservation of coupling with age correlates with the extent of problem-solving skill consolidation during sleep.
Accumulating evidence suggests a central role for sleep spindles in the consolidation of new memories. However, no meta-analysis of the association between sleep spindles and memory performance has been conducted so far. Here, we report meta-analytical evidence for spindle-memory associations and investigate how multiple factors, including memory type, spindle type, spindle characteristics, and EEG topography affect this relationship. The literature search yielded 53 studies reporting 1427 effect sizes, resulting in a small to moderate effect for the average association. We further found that spindle-memory associations were significantly stronger for procedural memory than for declarative memory. Neither spindle types nor EEG scalp topography had an impact on the strength of the spindle-memory relation, but we observed a distinct functional role of global and fast sleep spindles, especially for procedural memory. We also found a moderation effect of spindle characteristics, with power showing the largest effect sizes. Collectively, our findings suggest that sleep spindles are involved in learning, thereby representing a general physiological mechanism for memory consolidation.
Sleep consolidates procedural memory for motor skills, and this process is associated with strengthened functional connectivity in hippocampal–striatal–cortical areas. It is unknown whether similar processes occur for procedural memory that requires cognitive strategies needed for problem-solving. It is also unclear whether a full night of sleep is indeed necessary for consolidation to occur, compared with a daytime nap. We examined how resting-state functional connectivity within the hippocampal–striatal–cortical network differs after offline consolidation intervals of sleep, nap, or wake. Resting-state fMRI data were acquired immediately before and after training on a procedural problem-solving task that requires the acquisition of a novel cognitive strategy and immediately prior to the retest period (i.e., following the consolidation interval). ROI to ROI and seed to whole-brain functional connectivity analyses both specifically and consistently demonstrated strengthened hippocampal–prefrontal functional connectivity following a period of sleep versus wake. These results were associated with task-related gains in behavioral performance. Changes in functional communication were also observed between groups using the striatum as a seed. Here, we demonstrate that at the behavioral level, procedural strategies benefit from both a nap and a night of sleep. However, a full night of sleep is associated with enhanced functional communication between regions that support problem-solving skills.
Accumulating evidence suggests a central role for sleep spindles in the consolidation of new memories. However, no metaanalysis of the association between sleep spindles and memory performance has been conducted so far. Here, we report meta-analytical evidence for spindle-memory associations and investigate how multiple factors, including memory type, spindle type, spindle characteristics, and EEG topography affect this relationship. The literature search yielded 53 studies reporting 1424 effect sizes, resulting in a small to moderate effect for the average association. We further found that spindle-memory relationships were significantly stronger for procedural memory than for declarative memory. Neither spindle types nor EEG scalp topography had an impact on the strength of the spindlememory relation, but we observed a distinct functional role of global and fast sleep spindles, especially for procedural memory. We also found a moderation effect of spindle characteristics, with spindle frequency and power showing the largest effect sizes. Collectively, our findings suggest that sleep spindles are involved in learning and plasticity, thereby representing a general physiological mechanism for memory consolidation.
Highlights
Spindle measures showed a small to medium-sized association with memory performance.
This relationship was stronger for procedural memory than declarative memory.
No moderation effects of spindle type and EEG scalp topography have been observed.
Spindle frequency and power emerged as the strongest predictors.
Naps showed similar spindle-related consolidation mechanisms to whole-night sleep.
We investigated the behavioural and neuronal functional consequences of age-related differences in sleep for gaining insight into novel cognitive strategies. Forty healthy young adults (20-35 years), and twenty-nine healthy older adults (60-85 years) were assigned to either nap or wake conditions. Participants were trained on the Tower of Hanoi in the AM, followed by either a 90-minute nap opportunity or period of wakefulness, and were retested afterward. fMRI scans examined differences in brain activation from training to retest in young vs. older adults as a function of sleep. Sleep enhanced performance and transformed the memory trace in young adults via hippocampal-neocortical transfer, but not older adults. This is consistent with the notion that as the consolidation of a newly formed memory trace progresses, the hippocampus becomes less involved; especially so when sleep occurs during that time. These results demonstrate a critical role for sleep in supporting problem-solving skills and suggest that the benefit of sleep for consolidation of these skills is reduced with age.
Introduction
Second-language learning (SLL) depends on distinct functional-neuroanatomical systems including procedural and declarative long-term memory. Characteristic features of rapid eye movement (REM) and non-REM sleep such as rapid eye movements and sleep spindles are electrophysiological markers of cognitively complex procedural and declarative memory consolidation, respectively. In adults, grammatical learning depends at first on declarative memory (“early SLL”) then shifts to procedural memory with experience (“late SLL”). However, it is unknown if the shift from declarative to procedural memory in early vs late SLL is supported by sleep. Here, we hypothesized that increases in sleep spindle characteristics would be associated with early SLL, whereas increases in REM activity (eg, density and EEG theta-band activity time-locked to rapid eye movements) would be associated with late SLL.
Methods
Eight Anglophone (English first language) participants completed four polysomnographic recordings throughout an intensive 6-week French immersion course. Sleep spindle data and electroencephalographic spectral power time-locked to rapid eye movements were extracted from parietal temporal electrodes.
Results
As predicted, improvements in French proficiency were associated with changes in spindles during early SLL. Furthermore, we observed increased event-related theta power time-locked to rapid eye movements during late SLL compared with early SLL. The increases in theta power were significantly correlated with improvements in French proficiency.
Discussion
This supports the notion that sleep spindles are involved in early SLL when grammar depends on declarative memory, whereas cortical theta activity time-locked to rapid eye movements is involved in late SLL when grammar depends on procedural memory.
Sleep has been shown to facilitate the consolidation of newly acquired motor memories. However, the role of sleep in gross motor learning, especially in motor adaptation, is less clear. Thus, we investigated the effects of nocturnal sleep on the performance of a gross motor adaptation task, i.e. riding an inverse steering bicycle. Twenty-six male participants (M = 24.19, SD = 3.70 years) were randomly assigned to a PM-AM-PM (n = 13) or an AM-PM-AM (n = 13) group, i.e. they trained in the evening/morning and were re-tested the next morning/evening and the following evening/morning (PM-AM-PM/AM-PM-AM group) so that every participant spent one sleep as well as one wake interval between the three test sessions. Inverse cycling performance was assessed by speed (riding time) and accuracy (standard deviation of steering angle) measures. Behavioural results showed that in the PM-AM-PM group a night of sleep right after training stabilized performance (accuracy and speed) and was further improved over the subsequent wake interval. In the AM-PM-AM group, a significant performance deterioration after the initial wake interval was followed by the restoration of subjects' performance levels from right after training when a full night of sleep was granted. Regarding sleep, right hemispheric fast N2 sleep spindle activity was related to better stabilization of inverse cycling skills, thus possibly reflecting the ongoing process of updating the participants' mental model from "how to ride a bicycle" to "how to ride an inverse steering bicycle". Our results demonstrate that sleep facilitates the consolidation of gross motor adaptation, thus adding further insights to the role of sleep for tasks with real-life relevance.
Sleep plays an important role in forming procedural motor memories. Whether sleep plays a similar role for cognitive procedures related to working memory function, is not yet clear. Here we investigated if sleep enhances training-induced improvements in working memory in children. Because children show more intense slow wave sleep (e.g., higher slow wave activity, more spindles) we expected sleep-related improvements to be greater than in adults. Twenty-four children (10-12 years) and 24 adults were trained on three sessions of an n-back task comprising three runs of blocks (6 blocks with 20 responses each) presented in ascending levels of difficulty. The sessions were separated by ∼12h. Between the training sessions, participants first spent a full night sleeping and then a normal day awake (evening groups) or vice versa (morning groups). We analysed performance on the whole blocks and, to estimate the individual's optimum performance, on only the first 10 trials of each block. Results showed a distinct gain in training-induced working memory performance with post-training overnight sleep compared to wakefulness. The sleep-induced gain was revealed only for performance on the first block-halves and, in absolute terms, was closely comparable in children and adults. Taking differences in working memory performance into account sleep-dependent gains expressed as percentages of baseline performance were, however, greater in children than in adults. The data thus indicate that sleep after training facilitates cognitive procedures related to executive control, i.e., the ability to operate sequences of events in working memory, with a particular benefit in developing populations.
Periodic limb movements (PLMs) during sleep increase with age and are associated with striatal neurodegeneration and dopamine deficiency. Limb movements are often associated with disruptions to non-rapid eye movement (NREM) sleep. Motor skill memory consolidation recruits the striatum, and learning-dependent striatal activation is associated with NREM sleep. Therefore, we investigated whether de novo individuals who experience significantly elevated levels of PLMs but have not been formally diagnosed with periodic limb movement disorder had learning and sleep-related memory deficits, and if these deficits related to sleep quality and symptom severity.
Fourteen adults with significantly elevated PLMs (PLM condition); fifteen aged-matched controls (CTRL); and fourteen age-matched “disturbed” sleep (via induced leg movements) controls (CTRL-ES) participated. Participants were trained (PM) and retested (AM) on procedural motor sequence learning (MSL) and declarative paired associates memory tasks.
Baseline sleep quality was significantly worse in the PLM vs. CTRLs. Despite the continued presence of PLMs in the PLM condition on the experimental night, remarkably, sleep quality was improved and arousals were reduced vs. baseline, and did not differ from CTRL. MSL was significantly slower in the PLM condition compared to CTRL at training, but surprisingly, did exhibit overnight performance gains; which correlated with reduced arousals. As predicted, CTRL but not CTRL-ES had overnight gains in MSL. Together, suggesting that, in the PLM condition, sleep quality was normalized following MSL, where they derived the same benefit of sleep to procedural memory consolidation as CTRL. Sleep did not benefit declarative memory.
Although preliminary, these results suggest that motor sequence learning in individuals with PLMs may provide a benefit to sleep, which in turn, may benefit memory consolidation.
Scientific investigation into the possible role of sleep in memory consolidation began with the early studies of Jenkins and Dallenbach (1924). Despite nearly a century of investigation with a waxing and waning of interest, the role of sleep in memory processing remains controversial and elusive. This review provides the historical background for current views and considers the relative contribution of two sleep states, rapid eye movement sleep and slow-wave sleep, to offline memory processing. The sequential hypothesis, until now largely ignored, is discussed, and recent literature supporting this view is reviewed.
Sleep is necessary for the optimal consolidation of procedural learning, and in particular, for motor sequential skills. Motor sequence learning (MSL) remains intact with age, but sleep-dependent consolidation is impaired, suggesting that memory deficits for procedural skills are specifically impacted by age-related changes in sleep. Age-related changes in spindles may be responsible for impaired MSL consolidation, but the morphological basis for this deficit is unknown. Here we found that grey matter in the hippocampus and cerebellum was positively correlated with both sleep spindles and offline improvements in performance in young participants, but not in older participants. These results suggest that age-related changes in grey matter in the hippocampus relate to spindles, and may underlie age-related deficits in sleep-related motor sequence memory consolidation. In this way, spindles can serve as a biological marker for structural brain changes and the related memory deficits in older adults.
Posttraining rapid eye movement (REM) sleep has been reported to be important for efficient memory consolidation. The present results demonstrate increases in the intensity of REM sleep during the night of sleep following cognitive procedural/implicit task acquisition. These REM increases manifest as increases in total number of rapid eye movements (REMs) and REM densities, whereas the actual time spent in REM sleep did not change. Further, the participants with the higher intelligence (IQ) scores showed superior task acquisition scores as well as larger posttraining increases in number of REMs and REM density. No other sleep state changes were observed. None of the pretraining baseline measures of REM sleep were correlated with either measured IQ or task performance. Posttraining increases in REM sleep intensity implicate REM sleep mechanisms in further off-line memory processing, and provide a biological marker of learning potential.
Study objectives:
Memory reactivation appears to be a fundamental process in memory consolidation. In this study we tested the influence of memory reactivation during rapid eye movement (REM) sleep on memory performance and brain responses at retrieval in healthy human participants.
Participants:
Fifty-six healthy subjects (28 women and 28 men, age [mean ± standard deviation]: 21.6 ± 2.2 y) participated in this functional magnetic resonance imaging (fMRI) study.
Methods and results:
Auditory cues were associated with pictures of faces during their encoding. These memory cues delivered during REM sleep enhanced subsequent accurate recollections but also false recognitions. These results suggest that reactivated memories interacted with semantically related representations, and induced new creative associations, which subsequently reduced the distinction between new and previously encoded exemplars. Cues had no effect if presented during stage 2 sleep, or if they were not associated with faces during encoding. Functional magnetic resonance imaging revealed that following exposure to conditioned cues during REM sleep, responses to faces during retrieval were enhanced both in a visual area and in a cortical region of multisensory (auditory-visual) convergence.
Conclusions:
These results show that reactivating memories during REM sleep enhances cortical responses during retrieval, suggesting the integration of recent memories within cortical circuits, favoring the generalization and schematization of the information.
Neutral memories unbind from their emotional acquisition context when sleep is allowed the night after learning and testing takes place after two additional nights of sleep. However, mood-dependent memory (MDM) effects are not abolished after a restricted sleep episode mostly featuring non rapid-eye-movement (NREM) or rapid-eye-movement (REM) sleep. Here, we tested whether (1) one night of sleep featuring several NREM-REM sleep cycles is sufficient to suppress MDM effects and (2) a neutral mood is a sufficiently contrasting state to induce MDM effects, i.e. interfere with the recall of information learned in happy or sad states. Results disclosed MDM effects both in the post-learning sleep and wake conditions, with better recall in congruent than incongruent emotional contexts. Our findings suggest that the emotional unbinding needs several consecutive nights of sleep to be complete, and that even subtle mood changes are sufficient to produce MDM effects.
Study objectives:
In schizophrenia there is a dramatic reduction of sleep spindles that predicts deficient sleep-dependent memory consolidation. Eszopiclone (Lunesta), a non-benzodiazepine hypnotic, acts on γ-aminobutyric acid (GABA) neurons in the thalamic reticular nucleus where spindles are generated. We investigated whether eszopiclone could increase spindles and thereby improve memory consolidation in schizophrenia.
Design:
In a double-blind design, patients were randomly assigned to receive either placebo or 3 mg of eszopiclone. Patients completed Baseline and Treatment visits, each consisting of two consecutive nights of polysomnography. On the second night of each visit, patients were trained on the motor sequence task (MST) at bedtime and tested the following morning.
Setting:
Academic research center.
Participants:
Twenty-one chronic, medicated schizophrenia outpatients.
Measurements and results:
We compared the effects of two nights of eszopiclone vs. placebo on stage 2 sleep spindles and overnight changes in MST performance. Eszopiclone increased the number and density of spindles over baseline levels significantly more than placebo, but did not significantly enhance overnight MST improvement. In the combined eszopiclone and placebo groups, spindle number and density predicted overnight MST improvement.
Conclusion:
Eszopiclone significantly increased sleep spindles, which correlated with overnight motor sequence task improvement. These findings provide partial support for the hypothesis that the spindle deficit in schizophrenia impairs sleep-dependent memory consolidation and may be ameliorated by eszopiclone. Larger samples may be needed to detect a significant effect on memory. Given the general role of sleep spindles in cognition, they offer a promising novel potential target for treating cognitive deficits in schizophrenia.
Compared retention of a paired-associate list in 3 groups of 10 undergraduates each who all learned and recalled at the same time of day (the retention interval was always defined from 2:50-6:50 a.m.). 1 group was awake during the interval, 1 group experienced sleep characterized by high amounts of Stage IV sleep and low amounts of REM sleep, and the 3rd group experienced sleep characterized by low amounts of Stage IV and high amounts of REM. Results demonstrate that memory over a sleep interval was superior to memory over a waking interval. Of the 2 sleep intervals, retention over the high REM sleep interval was inferior to retention over the high Stage IV interval. These 2 effects cannot be explained as artifacts of a circadian rhythm effect on memory. Implications of the results for understanding the effects of sleep on memory are discussed.
Consolidation makes it possible for memories of our daily experiences to be stored in an enduring way. We propose that memory consolidation depends on the covert reactivation of previously learned material both during sleep and wakefulness. Here we tested whether the operation of covert memory reactivation influences the fundamental selectivity of memory storage-of all the events we experience each day, which will be retained and which forgotten? We systematically manipulated the value of information learned by 60 young subjects; they learned 72 object-location associations while hearing characteristic object sounds, and a number on each object indicated the reward value that could potentially be earned during a future memory test. Recall accuracy declined to a greater extent for low-value than for high-value associations after either a 90 min nap or a 90 min wake interval. Yet, via targeted memory reactivation of half of the low-value associations using the corresponding sounds, these memories were rescued from forgetting. Only cued associations were rescued when sounds were applied during wakefulness, whereas the entire set of low-value associations was rescued from forgetting when the manipulation occurred during sleep. The benefits accrued from presenting corresponding sounds show that covert reactivation is a major factor determining the selectivity of memory consolidation in these circumstances. By extension, covert reactivation may determine the ultimate fate of our memories, though wake and sleep reactivation might play distinct roles in this process, the former helping to strengthen individual, salient memories, and the latter strengthening, while also linking, categorically related memories together.
An important function of sleep is the consolidation of memories, and features of sleep, such as rapid eye movement (REM) or sleep spindles, have been shown to correlate with improvements in discrete memory domains. Because of the methodological difficulties in modulating sleep, however, a causal link between specific sleep features and human memory consolidation is lacking. Here, we experimentally manipulated specific sleep features during a daytime nap via direct pharmacological intervention. Using zolpidem (Ambien), a short-acting GABAA agonist hypnotic, we show increased sleep spindle density and decreased REM sleep compared with placebo and sodium oxybate (Xyrem). Naps with increased spindles produced significantly better verbal memory and significantly worse perceptual learning but did not affect motor learning. The experimental spindles were similar to control spindles in amplitude and frequency, suggesting that the experimental intervention enhanced normal sleep processes. Furthermore, using statistical methods, we demonstrate for the first time a critical role of spindles in human hippocampal memory performance. The gains in memory consolidation exceed sleep-alone or control conditions and demonstrate the potential for targeted, exceptional memory enhancement in healthy adults with pharmacologically modified sleep.
Motor sequence learning is known to rely on more than a single process. As the skill develops with practice, two different representations of the sequence are formed: a goal representation built under spatial allocentric coordinates and a movement representation mediated through egocentric motor coordinates. This study aimed to explore the influence of daytime sleep (nap) on consolidation of these two representations. Through the manipulation of an explicit finger sequence learning task and a transfer protocol, we show that both allocentric (spatial) and egocentric (motor) representations of the sequence can be isolated after initial training. Our results also demonstrate that nap favors the emergence of offline gains in performance for the allocentric, but not the egocentric representation, even after accounting for fatigue effects. Furthermore, sleep-dependent gains in performance observed for the allocentric representation are correlated with spindle density during non-rapid eye movement (NREM) sleep of the post-training nap. In contrast, performance on the egocentric representation is only maintained, but not improved, regardless of the sleep/wake condition. These results suggest that motor sequence memory acquisition and consolidation involve distinct mechanisms that rely on sleep (and specifically, spindle) or simple passage of time, depending respectively on whether the sequence is performed under allocentric or egocentric coordinates.
Although we know that emotional events enjoy a privileged status in our memories, we still have much to learn about how emotional memories are processed, stored, and how they change over time. Here we show a positive association between REM sleep and the selective consolidation of central, negative aspects of complex scenes. Moreover, we show that the placement of sleep is critical for this selective emotional memory benefit. When testing occurred 24 h post-encoding, subjects who slept soon after learning (24 h Sleep First group) had superior memory for emotional objects compared to subjects whose sleep was delayed for 16 h post-encoding following a full day of wakefulness (24 h Wake First group). However, this increase in memory for emotional objects corresponded with a decrease in memory for the neutral backgrounds on which these objects were placed. Furthermore, memory for emotional objects in the 24 h Sleep First group was comparable to performance after just a 12 h delay containing a night of sleep, suggesting that sleep soon after learning selectively stabilizes emotional memory. These results suggest that the sleeping brain preserves in long-term memory only what is emotionally salient and perhaps most adaptive to remember.
Information acquired during waking can be reactivated during sleep, promoting memory stabilization. After people learned to produce two melodies in time with moving visual symbols, we produced a relative improvement in performance by presenting one melody during an afternoon nap. Electrophysiological signs of memory processing during sleep corroborated the notion that appropriate auditory stimulation that does not disrupt sleep can nevertheless bias memory consolidation in relevant brain circuitry.
It is now clear that states of sleep are involved with the off-line memory reprocessing or consolidation of a variety of tasks. The large majority of these sleep sensitive tasks has been of the procedural type, tasks that are usually learned implicitly. It is still unclear which states of sleep are most important. For motor skills tasks, Stage 2 sleep has sometimes been implicated, while at other times the important sleep state appears to be rapid eye movement (REM). This paper is an attempt to more clearly identify the characteristics that differentiate REM-dependent from Stage 2-dependent motor tasks and to examine the nature of the brain state differences between the two stages at the neurophysiological and neurochemical levels. We have developed a model to explain how motor skills tasks involving REM and Stage 2 sleep might be dependent on two separate, but overlapping, neural systems. (PsycINFO Database Record (c) 2007 APA ) (journal abstract)
Thalamo-cortical spindles driven by the up-state of neocortical slow (< 1 Hz) oscillations (SOs) represent a candidate mechanism of memory consolidation during sleep. We examined interactions between SOs and spindles in human slow wave sleep, focusing on the presumed existence of 2 kinds of spindles, i.e., slow frontocortical and fast centro-parietal spindles.
Two experiments were performed in healthy humans (24.5 ± 0.9 y) investigating undisturbed sleep (Experiment I) and the effects of prior learning (word paired associates) vs. non-learning (Experiment II) on multichannel EEG recordings during sleep.
Only fast spindles (12-15 Hz) were synchronized to the depolarizing SO up-state. Slow spindles (9-12 Hz) occurred preferentially at the transition into the SO down-state, i.e., during waning depolarization. Slow spindles also revealed a higher probability to follow rather than precede fast spindles. For sequences of individual SOs, fast spindle activity was largest for "initial" SOs, whereas SO amplitude and slow spindle activity were largest for succeeding SOs. Prior learning enhanced this pattern.
The finding that fast and slow spindles occur at different times of the SO cycle points to disparate generating mechanisms for the 2 kinds of spindles. The reported temporal relationships during SO sequences suggest that fast spindles, driven by the SO up-state feed back to enhance the likelihood of succeeding SOs together with slow spindles. By enforcing such SO-spindle cycles, particularly after prior learning, fast spindles possibly play a key role in sleep-dependent memory processing.
Sleep is known to contribute to motor memory consolidation. Recent studies have provided evidence that a night of sleep plays a similar functional role following motor imagery (MI), while the simple passage of time does not result in performance gains. Here, we examined the benefits of a daytime nap on motor memory consolidation after MI practice. Participants were trained by MI on an explicitly known sequence of finger movements at 11:00. Half of the participants were then subjected (at 14:00) to either a short nap (10 min of stage 2 sleep) or a long nap (60-90 min, including slow wave sleep and rapid eye movement sleep). We also collected data from both quiet and active rest control groups. All participants remained in the lab until being retested at 16:00. The data revealed that a daytime nap after imagery practice improved motor performance and, therefore, facilitated motor memory consolidation, as compared with spending a similar time interval in the wake state. Interestingly, the results revealed that both short and long naps resulted in similar delayed performance gains. The data might also suggest that the presence of slow wave and rapid eye movement sleep does not provide additional benefits for the sleep-dependent motor skill consolidation following MI practice.
Memory consolidation has been proposed as a function of sleep. However, sleep is a complex phenomenon characterized by several features including duration, intensity, and continuity. Sleep continuity is disrupted in different neurological and psychiatric conditions, many of which are accompanied by memory deficits. This finding has raised the question of whether the continuity of sleep is important for memory consolidation. However, current techniques used in sleep research cannot manipulate a single sleep feature while maintaining the others constant. Here, we introduce the use of optogenetics to investigate the role of sleep continuity in memory consolidation. We optogenetically targeted hypocretin/orexin neurons, which play a key role in arousal processes. We used optogenetics to activate these neurons at different intervals in behaving mice and were able to fragment sleep without affecting its overall amount or intensity. Fragmenting sleep after the learning phase of the novel object recognition (NOR) task significantly decreased the performance of mice on the subsequent day, but memory was unaffected if the average duration of sleep episodes was maintained at 62-73% of normal. These findings demonstrate the use of optogenetic activation of arousal-related nuclei as a way to systematically manipulate a specific feature of sleep. We conclude that regardless of the total amount of sleep or sleep intensity, a minimal unit of uninterrupted sleep is crucial for memory consolidation.
It has recently been reported that selective REM sleep deprivation (REMD) in college students results in memory impairment of the application of a set of rules in a logic task, but not recall of a paired associate task. The present experiments were designed to examine the effects of Total Sleep Deprivation (TSD) and (REMD) following acquisition of a pure motor task, the pursuit rotor. In Experiment 1, subjects (N = 90) were exposed to TSD for one of several nights following training. Results showed that TSD on the same night as training resulted in poorer performance on retest one week later. In Experiment 2, subjects (N = 42) were exposed to various kinds of sleep deprivation on the night of task acquisition. One group was subjected to REMD. Other groups included a non-REM awakening control group (NREMA), a TSD group, a normally rested Control group and a group allowed the first 4 h of sleep in the night before being subjected to TSD (LH - TSD) for the rest of the night. Results showed the REMD and Control groups to have excellent memory for this task while the TSD and LH - TSD subjects had significantly poorer memory for the task. The NREMA group showed a slight, but not significant deficit. It was concluded that Stage 2 sleep, rather than REM sleep was the important stage of sleep for efficient memory processing of the pursuit rotor task.
Over the past two decades, research has accumulated compelling evidence that sleep supports the formation of long-term memory. The standard two-stage memory model that has been originally elaborated for declarative memory assumes that new memories are transiently encoded into a temporary store (represented by the hippocampus in the declarative memory system) before they are gradually transferred into a long-term store (mainly represented by the neocortex), or are forgotten. Based on this model, we propose that sleep, as an offline mode of brain processing, serves the 'active system consolidation' of memory, i.e. the process in which newly encoded memory representations become redistributed to other neuron networks serving as long-term store. System consolidation takes place during slow-wave sleep (SWS) rather than rapid eye movement (REM) sleep. The concept of active system consolidation during sleep implicates that (a) memories are reactivated during sleep to be consolidated, (b) the consolidation process during sleep is selective inasmuch as it does not enhance every memory, and (c) memories, when transferred to the long-term store undergo qualitative changes. Experimental evidence for these three central implications is provided: It has been shown that reactivation of memories during SWS plays a causal role for consolidation, that sleep and specifically SWS consolidates preferentially memories with relevance for future plans, and that sleep produces qualitative changes in memory representations such that the extraction of explicit and conscious knowledge from implicitly learned materials is facilitated.
Previously the application of a weak electric anodal current oscillating with a frequency of the sleep slow oscillation (∼0.75 Hz) during non-rapid eye movement sleep (NonREM) sleep boosted endogenous slow oscillation activity and enhanced sleep-associated memory consolidation. The slow oscillations occurring during NonREM sleep and theta oscillations present during REM sleep have been considered of critical relevance for memory formation. Here transcranial direct current stimulation (tDCS) oscillating at 5 Hz, i.e., within the theta frequency range (theta-tDCS) is applied during NonREM and REM sleep. Theta-tDCS during NonREM sleep produced a global decrease in slow oscillatory activity conjoint with a local reduction of frontal slow EEG spindle power (8-12 Hz) and a decrement in consolidation of declarative memory, underlining the relevance of these cortical oscillations for sleep-dependent memory consolidation. In contrast, during REM sleep theta-tDCS appears to increase global gamma (25-45 Hz) activity, indicating a clear brain state-dependency of theta-tDCS. More generally, results demonstrate the suitability of oscillating-tDCS as a tool to analyze functions of endogenous EEG rhythms and underlying endogenous electric fields as well as the interactions between EEG rhythms of different frequencies.
Newly formed memories are initially fragile and require consolidation to be transformed into an enduring state. Memory consolidation may occur during increased postlearning REM sleep. REM deprivation during these periods (termed REM sleep windows [RSWs]) impairs subsequent performance. The pedunculopontine nucleus (PPT) and adjacent deep mesencephalic reticular nuclei (DpMe) have been implicated in the generation of REM sleep. Following 24-hr baseline recording, rats were trained on the 2-way avoidance task for 50 trials/day over 2 days and retested on Day 3. EEG was recorded 22 hr after training on training Days 1 and 2. Rats were injected with the GABAB agonist baclofen or saline into the PPT/DpMe region at 0300 to coincide with the start of a known RSW. Based on shuttle performance, saline rats were assigned post hoc to a learning group (LG) that avoided the footshock at least 60% at retest or nonlearning group (NLG) that performed below this criterion. Baclofen-injected rats were not assigned post hoc into separate groups as all rats performed below the learning criterion. PPN/DpMe infusions of the inhibitory GABAB agonist baclofen decreased REM and impaired subsequent memory performance. Normal GABAergic transmission in the PPN/DpMe may be necessary for REM to occur and for the consolidation of incentive learning.
Sleep has been identified as a state that optimizes the consolidation of newly acquired information in memory, depending on the specific conditions of learning and the timing of sleep. Consolidation during sleep promotes both quantitative and qualitative changes of memory representations. Through specific patterns of neuromodulatory activity and electric field potential oscillations, slow-wave sleep (SWS) and rapid eye movement (REM) sleep support system consolidation and synaptic consolidation, respectively. During SWS, slow oscillations, spindles and ripples - at minimum cholinergic activity - coordinate the re-activation and redistribution of hippocampus-dependent memories to neocortical sites, whereas during REM sleep, local increases in plasticity-related immediate-early gene activity - at high cholinergic and theta activity - might favour the subsequent synaptic consolidation of memories in the cortex.
The function of rapid-eye-movement (REM) sleep is still unknown. One prevailing hypothesis suggests that REM sleep is important in processing memory traces. Here, using positron emission tomography (PET) and regional cerebral blood flow measurements, we show that waking experience influences regional brain activity during subsequent sleep. Several brain areas activated during the execution of a serial reaction time task during wakefulness were significantly more active during REM sleep in subjects previously trained on the task than in non-trained subjects. These results support the hypothesis that memory traces are processed during REM sleep in humans.
What processes are involved in the formation of enduring memory traces? Sleep has been proposed to play a role in memory consolidation and the present study provides evidence to support 2-stage models of sleep and memory including both non-rapid eye movement (NREM) and rapid eye movement (REM) sleep. Previous research has shown REM sleep increases following avoidance learning and memory is impaired if REM deprivation occurs during these post-training periods indicating that REM sleep may have a role in memory consolidation processes. These discrete post-training periods have been termed REM sleep windows (RSWs). It is not known whether the electroencephalogram has unique characteristics during the RSW. Further investigation of the RSW was one of the primary goals of this study. We investigated the epidural-recorded electrophysiological learning-related changes following avoidance training in rats. Theta power increased in the learning group during the RSW, suggesting that theta is involved in memory consolidation during this period. Sleep spindles subsequently increased in slow wave sleep (SWS). The results suggest that both NREM and REM sleep are involved in sleep-dependent memory consolidation, and provide support for existing 2-stage models. Perhaps first theta increases to organize and consolidate material via hippocampal-neocortical dialogue, followed by subsequent refinement in the cortex by spindles during SWS.
There is increasing evidence supporting the notion that the contribution of sleep to consolidation of motor skills depends on the nature of the task used in practice. We compared the role of three post-training conditions in the expression of delayed gains on two different motor skill learning tasks: finger tapping sequence learning (FTSL) and visuomotor adaptation (VMA). Subjects in the DaySleep and ImmDaySleep conditions were trained in the morning and at noon, respectively, afforded a 90-min nap early in the afternoon and were re-tested 12 h post-training. In the NightSleep condition, subjects were trained in the evening on either of the two learning paradigms and re-tested 12 h later following sleep, while subjects in the NoSleep condition underwent their training session in the morning and were re-tested 12 h later without any intervening sleep. The results of the FTSL task revealed that post-training sleep (day-time nap or night-time sleep) significantly promoted the expression of delayed gains at 12 h post-training, especially if sleep was afforded immediately after training. In the VMA task, however, there were no significant differences in the gains expressed at 12 h post-training in the three conditions. These findings suggest that "off-line" performance gains reflecting consolidation processes in the FTSL task benefit from sleep, even a short nap, while the simple passage of time is as effective as time in sleep for consolidation of VMA to occur. They also imply that procedural memory consolidation processes differ depending on the nature of task demands.
The mechanisms underlying off-line consolidation of memory during sleep are elusive. Learning of hippocampus-dependent tasks increases neocortical slow oscillation synchrony, and thalamocortical spindle and hippocampal ripple activity during subsequent non-rapid eye movement sleep. Slow oscillations representing an oscillation between global neocortical states of increased (up-state) and decreased (down-state) neuronal firing temporally group thalamic spindle and hippocampal ripple activity, which both occur preferentially during slow oscillation up-states. Here we examined whether slow oscillations also group learning-induced increases in spindle and ripple activity, thereby providing time-frames of facilitated hippocampus-to-neocortical information transfer underlying the conversion of temporary into long-term memories. Learning (word-pairs in humans, odor-reward associations in rats) increased slow oscillation up-states and, in humans, shaped the timing of down-states. Slow oscillations grouped spindle and rat ripple activity into up-states under basal conditions. Prior learning produced in humans an increase in spindle activity focused on slow oscillation up-states. In rats, learning induced a distinct increase in spindle and ripple activity that was not synchronized to up-states. Event-correlation histograms indicated an increase in spindle activity with the occurrence of ripples. This increase was prolonged after learning, suggesting a direct temporal tuning between ripples and spindles. The lack of a grouping effect of slow oscillations on learning-induced spindles and ripples in rats, together with the less pronounced effects of learning on slow oscillations, presumably reflects a weaker dependence of odor learning on thalamo-neocortical circuitry. Slow oscillations might provide an effective temporal frame for hippocampus-to-neocortical information transfer only when thalamo-neocortical systems are already critically involved during learning.
To test whether instrumental conditioning of sensorimotor rhythm (SMR; 12-15 Hz) has an impact on sleep parameters as well as declarative memory performance in humans.
Randomized, parallel group design
10 instrumental conditioning sessions, pre- and posttreatment investigation including sleep evaluations
27 healthy subjects (13 male) Interventions: SMR-conditioning (experimental group) or randomized-frequency conditioning (control group); declarative memory task before and after a 90-min nap
The experimental group was trained to enhance the amplitude of their SMR-frequency range, whereas the control group participated in a randomized-frequency conditioning program (i.e., every session a different 3-Hz frequency bin between 7 and 20 Hz). During pre- and posttreatment the subjects had to attend the sleep laboratory to take a 90-min nap (2:00-3:30 pm) and to perform a declarative memory task before and after sleep. The experimental design was successful in conditioning an increase in relative 12-15 Hz amplitude within 10 sessions (d = 0.7). Increased SMR activity was also expressed during subsequent sleep by eliciting positive changes in different sleep parameters (sleep spindle number [d = 0.6], sleep onset latency [d = 0.7]); additionally, this increased 12-15 Hz amplitude was associated with enhancement in retrieval score computed at immediate cued recall (d = 0.9).
Relative SMR amplitude increased over 10 instrumental conditioning sessions (in the experimental group only) and this "shaping of one's own brain activity" improved subsequent declarative learning and facilitated the expression of 12-15 Hz spindle oscillations during sleep. Most interestingly, these electrophysiological changes were accompanied by a shortened sleep onset latency.
Rapid eye movement (REM) sleep has been considered important for consolidation of memories, particularly of skills. Contrary to expectations, we found that REM sleep suppression by administration of selective serotonin or norepinephrine re-uptake inhibitors after training did not impair consolidation of skills or word-pairs in healthy men but rather enhanced gains in finger tapping accuracy together with sleep spindles. Our results indicate that REM sleep as a unitary phenomenon is not required for skill-memory consolidation.
To investigate polysomnographic (PSG) sleep and NREM sleep characteristics, including sleep spindles and spectral activity involved in offline consolidation of a motor sequence learning task.
Counterbalanced within-subject design.
Three weekly visits to the sleep laboratory.
Fourteen healthy participants aged between 20 and 30 years (8 women).
Motor sequence learning (MSL) task or motor control (CTRL) task before sleep.
Subjects were trained on either the MSL or CTRL task in the evening and retested 12 hours later the following morning on the same task after a night of PSG sleep recording. Total number and duration of sleep spindles and spectral power between 0.5 and 24 Hz were quantified during NREM sleep. After performing the MSL task, subjects exhibited a large increase in number and duration of sleep spindles compared to after the CTRL task. Higher sigma (sigma; 13 Hz) and beta (beta; 18-20 Hz) spectral power during the post-training night's sleep were also observed after the MSL task.
These results provide evidence that sleep spindles are involved in the offline consolidation of a new sequence of finger movements known to be sleep dependent. Moreover, they expand on prior findings by showing that changes in NREM sleep following motor learning are specific to consolidation (and learning), and not to nonspecific motor activity. Finally, these data demonstrate, for the first time, higher fast rhythms (beta frequencies) during sleep after motor learning.
It is known that sleep reshapes the neural representations that subtend the memories acquired while navigating in a virtual environment. However, navigation is not process-pure, as manifold learning components contribute to performance, notably the spatial and contextual memory constituents. In this context, it remains unclear whether post-training sleep globally promotes consolidation of all of the memory components embedded in virtual navigation, or rather favors the development of specific representations. Here, we investigated the effect of post-training sleep on the neural substrates of the consolidation of spatial and contextual memories acquired while navigating in a complex 3D, naturalistic virtual town. Using fMRI, we mapped regional cerebral activity during various tasks designed to tap either the spatial or the contextual memory component, or both, 72 h after encoding with or without sleep deprivation during the first post-training night. Behavioral performance was not dependent upon post-training sleep deprivation, neither in a natural setting that engages both spatial and contextual memory processes nor when looking more specifically at each of these memory representations. At the neuronal level however, analyses that focused on contextual memory revealed distinct correlations between performance and neuronal activity in frontal areas associated with recollection processes after post-training sleep, and in the parahippocampal gyrus associated with familiarity processes in sleep-deprived participants. Likewise, efficient spatial memory was associated with posterior cortical activity after sleep whereas it correlated with parahippocampal/medial temporal activity after sleep deprivation. Finally, variations in place-finding efficiency in a natural setting encompassing spatial and contextual elements were associated with caudate activity after post-training sleep, suggesting the automation of navigation. These data indicate that post-training sleep modulates the neural substrates of the consolidation of both the spatial and contextual memories acquired during virtual navigation.
Sleep benefits memory consolidation. Previous theoretical accounts have proposed a differential role of slow-wave sleep (SWS), rapid-eye-movement (REM) sleep, and stage N2 sleep for different types of memories. For example the dual process hypothesis proposes that SWS is beneficial for declarative memories, whereas REM sleep is important for consolidation of non-declarative, procedural and emotional memories. In fact, numerous recent studies do provide further support for the crucial role of SWS (or non-REM sleep) in declarative memory consolidation. However, recent evidence for the benefit of REM sleep for non-declarative memories is rather scarce. In contrast, several recent studies have related consolidation of procedural memories (and some also emotional memories) to SWS (or non-REM sleep)-dependent consolidation processes. We will review this recent evidence, and propose future research questions to advance our understanding of the role of different sleep stages for memory consolidation.
Behavioral studies indicate that older adults exhibit normal motor sequence learning (MSL), but paradoxically, show impaired consolidation of the new memory trace. However, the neural and physiological mechanisms underlying this impairment are entirely unknown. Here, we sought to identify, through functional magnetic resonance imaging during MSL and electroencephalographic (EEG) recordings during daytime sleep, the functional correlates and physiological characteristics of this age-related motor memory deficit. As predicted, older subjects did not exhibit sleep-dependent gains in performance (i.e., behavioral changes that reflect consolidation) and had reduced sleep spindles compared with young subjects. Brain imaging analyses also revealed that changes in activity across the retention interval in the putamen and related brain regions were associated with sleep spindles. This change in striatal activity was increased in young subjects, but reduced by comparison in older subjects. These findings suggest that the deficit in sleep-dependent motor memory consolidation in elderly individuals is related to a reduction in sleep spindle oscillations and to an associated decrease of activity in the cortico-striatal network. Hum Brain Mapp, 2013. © 2013 Wiley Periodicals, Inc.
There is robust evidence that sleep facilitates procedural memory consolidation. The exact mechanisms underlying this process are still unclear. We tested whether an active replay of prior experience can underlie sleep effects on procedural memory. Participants learned a finger-tapping task in which key presses were associated with tones during practice. Later, during a consolidation interval spent either sleeping or awake, we presented auditory cues to reactivate part of the learned sequence. We show that reactivation strengthens procedural memory formation during sleep, but not during wakefulness. The improvement was restricted to those finger transitions that were cued. Thus, reactivation is a very specific process underpinning procedural memory consolidation. When comparing periods of sleep with and without reactivation, we find that it is not the time spent in a specific stage of sleep per se, but rather the occurrence of reactivation that mediates the effect of sleep on memory consolidation. Our data show that longer sleep time as well as additional reactivation by cueing during sleep can enhance later memory performance.