Sleep dependent consolidation of gross motor sequence learning with motor imagery

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 (PP_sleep and MIP_sleep groups) or an equivalent daytime period (PP_day and MIP_day groups). Control groups without training were tested following similar timespans (CTRL_sleep and CTRL_day 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 MIP_sleep 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.     

Offline Improvement during Motor Sequence Learning Is Not Restricted to Developing Motor Chunks

Robust offline performance gains, beyond those that would be anticipated by being exposed to additional physical practice, have been reported during procedural learning and have been attributed to enhancement consolidation, a process by which memory is transformed in such a way that it is not only more resistant to forgetting but may also involve a reorganization of information that supports superior task execution. The authors assessed the impact of increasing within-session practice extent on the emergence of offline performance gains. Practice-dependent improvements occurred across 12 and 24 30-s practice trials of a 5-element motor sequencing task. Offline improvements were observed following both 12 and 24 trials. The improvement following 12 trials was associated with the formation of motor chunks important for establishing movement sequence structure. In contrast, the offline improvement after 24 trials was not related to further changes in movement structure beyond those that had emerged during practice. These data suggest that additional memory operations, beyond those needed to amalgamate subsequences of the SRT task, are susceptible to enhancement consolidation.     

Paradoxical Sleep Deprivation and Sleep Recording Following Training in a Brightness Discrimination Avoidance Task in Sprague–Dawley Rats: Paradoxical Effects

Previously, we reported that posttraining paradoxical sleep deprivation (PSD) resulted in an enhancement of the subsequent avoidance performance for rats trained for 15 trials in a Y-maze brightness avoidance discrimination task. A series of experiments were conducted to try to further understand the reasons for results which were contrary to those of the bulk of the sleep-learning literature. Experiment 1 investigated the effectiveness of the PSD technique. Rats (N= 4) were sleep recorded while residing on a “swimming pool” apparatus for 24 h. Compared to their baseline values, all animals showed a very large reduction in paradoxical sleep and spent significantly more time awake. Slow-wave sleep was unchanged. In Experiment 2, proactive motor effects were tested. Rats were deprived of PS for 24 h and then tested in a hole board motor activity task. There was a slight effect of PS deprivation on the day following the PSD and no effect when the rats were retested 1 week later. Experiment 3 investigated possible proactive effects of PSD on avoidance performance. Rats exposed to PSD in the 24 h before training in the Y-maze task did not demonstrate any facilitative effect on the subsequent avoidance performance. Experiment 4 investigated the possibility that the PSD facilitative effect could be due to partial training. Rats were given 75 acquisition trials in the brightness discrimination Y-maze avoidance before being subjected to 24 h of PSD. PS-deprived animals showed superior avoidance scores compared to non-PSD controls when retested 24 h later. In Experiment 5, the same strain of rats (N= 11) were sleep recorded after exposure to a partial acquisition in a Y-maze brightness avoidance discrimination task. They were then continuously monitored for 4 consecutive days. The percent PS for the Trained rats was significantly lower than that for the Control animals. This drop in percent PS was not confined to any particular time period in the 24-h day. None of the other sleep parameters reached significance. Analyses of the present results suggest that PSD exerts its facilitative effects on posttraining consolidation processes. We present arguments suggesting that PSD can have effects opposite to those generally reported, in animals demonstrating poor avoidance abilities, in an avoidance task.     

Motor interference does not impair the memory consolidation of imagined movements

The present study aimed to investigate whether an interference task might impact the sleep-dependent consolidation process of a mentally learned sequence of movements. Thirty-two participants were subjected to a first training session through motor imagery (MI) or physical practice (PP) of a finger sequence learning task. After 2 h, half of the participants were requested to perform a second interfering PP task (reversed finger sequence). All participants were finally re-tested following a night of sleep on the first finger sequence. The main findings revealed delayed performance gains following a night of sleep in the MI group, i.e. the interfering task did not alter the consolidation process, by contrast to the PP group. These results confirm that MI practice might result in less retroactive interference than PP, and further highlight the relevance of the first night of sleep for the consolidation process following MI practice. These data might thus contribute to determine in greater details the practical implications of mental training in motor learning and rehabilitation.     

睡眠对知觉与动作序列内隐学习离线巩固效应的影响

离线阶段发生的学习被称为离线巩固, 即在最初获得知识之后, 即使没有额外的练习, 其记忆痕迹也会保持稳定或提高。有研究初步探究了睡眠对知觉和动作序列内隐学习离线巩固的影响, 然而, 这些研究未能实现知觉序列与动作序列的完全分离, 序列类型是否调节睡眠对内隐序列学习离线巩固的影响仍需进一步探讨。此外, 既往外显学习的研究发现相对于简单的序列, 复杂的序列更容易从睡眠中获益, 表现出基于睡眠的离线巩固效应。睡眠对知觉序列与动作序列内隐学习离线巩固的影响是否会受到序列复杂程度的调节尚不明确。为此, 本研究在完全分离知觉序列和动作序列的情况下, 通过3个实验操纵序列的长度及结构, 设置3种不同复杂程度的序列规则, 考察了这一问题。结果发现, 对于动作序列, 序列规则复杂程度较低时, 无论是否经过睡眠都会发生离线巩固效应, 而当动作序列规则较为复杂时, 只有经历睡眠才会引起离线巩固效应; 对于知觉序列, 无论何种难易程度的规则, 均未发生离线巩固效应。上述结果表明内隐序列知识基于睡眠的离线巩固会受到序列类型及序列复杂程度的调节, 这为内隐学习的离线巩固争论提供了新的视角。     

Daytime naps improve motor imagery learning

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.     

Sleep-dependent consolidation of procedural motor memories in children and adults: the pre-sleep level of performance matters

In striking contrast to adults, in children sleep following training a motor task did not induce the expected (offline) gain in motor skill performance in previous studies. Children normally perform at distinctly lower levels than adults. Moreover, evidence in adults suggests that sleep dependent offline gains in skill essentially depend on the pre-sleep level of performance. Against this background, we asked whether improving children's performance on a motor sequence learning task by extended training to levels approaching those of adults would enable sleep-associated gains in motor skill in this age group also. Children (4-6 years) and adults (18-35 years) performed on the motor sequence learning task (button-box task) before and after ~2-hour retention intervals including either sleep (midday nap) or wakefulness. Whereas one group of children and adults, respectively, received the standard amount of 10 blocks of training before retention intervals of sleep or wakefulness, a further group of children received an extended training on 30 blocks (distributed across 3 days). A further group of adults received a restricted training on only two blocks before the retention intervals. Children after standard training reached lowest performance levels, whereas in adults performance after standard training was highest. Children with extended training and adults after reduced training reached intermediate performance levels. Only at these intermediate performance levels did sleep induce significant gains in motor sequence skill, whereas performance did not benefit from sleep in the low-performing children or in the high-performing adults. Spindle counts in the post-training nap were correlated with performance gains at retrieval only in the adults benefitting from sleep. We conclude that, across age groups, sleep induces the most robust gain in motor skill at an intermediate pre-sleep performance level. In low-performing children sleep-dependent improvements in skill may be revealed only after enhancing the pre-sleep performance level by extended training.     

Sleep deprivation selectively impairs memory consolidation for contextual fear conditioning

Many behavioral and electrophysiological studies in animals and humans have suggested that sleep and circadian rhythms influence memory consolidation. In rodents, hippocampus-dependent memory may be particularly sensitive to sleep deprivation after training, as spatial memory in the Morris water maze is impaired by rapid eye movement sleep deprivation following training. Spatial learning in the Morris water maze, however, requires multiple training trials and performance, as measured by time to reach the hidden platform is influenced by not only spatial learning but also procedural learning. To determine if sleep is important for the consolidation of a single-trial, hippocampus-dependent task, we sleep deprived animals for 0–5 and 5–10 h after training for contextual and cued fear conditioning. We found that sleep deprivation from 0–5 h after training for this task impaired memory consolidation for contextual fear conditioning whereas sleep deprivation from 5–10 h after training had no effect. Sleep deprivation at either time point had no effect on cued fear conditioning, a hippocampus-independent task. Previous studies have determined that memory consolidation for fear conditioning is impaired when protein kinase A and protein synthesis inhibitors are administered at the same time as when sleep deprivation is effective, suggesting that sleep deprivation may act by modifying these molecular mechanisms of memory storage.     

Adrenergic enhancement of consolidation of object recognition memory

Extensive evidence indicates that epinephrine (EPI) modulates memory consolidation for emotionally arousing tasks in animals and human subjects. However, previous studies have not examined the effects of EPI on consolidation of recognition memory. Here we report that systemic administration of EPI enhances consolidation of memory for a novel object recognition (NOR) task under different training conditions. Control male rats given a systemic injection of saline (0.9% NaCl) immediately after NOR training showed significant memory retention when tested at 1.5 or 24, but not 96h after training. In contrast, rats given a post-training injection of EPI showed significant retention of NOR at all delays. In a second experiment using a different training condition, rats treated with EPI, but not SAL-treated animals, showed significant NOR retention at both 1.5 and 24-h delays. We next showed that the EPI-induced enhancement of retention tested at 96h after training was prevented by pretraining systemic administration of the beta-adrenoceptor antagonist propranolol. The findings suggest that, as previously observed in experiments using aversively motivated tasks, epinephrine modulates consolidation of recognition memory and that the effects require activation of beta-adrenoceptors.     

Spatial and reversal learning in the Morris water maze are largely resistant to six hours of REM sleep deprivation following training

This first test of the role of REM (rapid eye movement) sleep in reversal spatial learning is also the first attempt to replicate a much cited pair of papers reporting that REM sleep deprivation impairs the consolidation of initial spatial learning in the Morris water maze. We hypothesized that REM sleep deprivation following training would impair both hippocampus-dependent spatial learning and learning a new target location within a familiar environment: reversal learning. A 6-d protocol was divided into the initial spatial learning phase (3.5 d) immediately followed by the reversal phase (2.5 d). During the 6 h following four or 12 training trials/day of initial or reversal learning phases, REM sleep was eliminated and non-REM sleep left intact using the multiple inverted flowerpot method. Contrary to our hypotheses, REM sleep deprivation during four or 12 trials/day of initial spatial or reversal learning did not affect training performance. However, some probe trial measures indicated REM sleep-deprivation-associated impairment in initial spatial learning with four trials/day and enhancement of subsequent reversal learning. In naive animals, REM sleep deprivation during normal initial spatial learning was followed by a lack of preference for the subsequent reversal platform location during the probe. Our findings contradict reports that REM sleep is essential for spatial learning in the Morris water maze and newly reveal that short periods of REM sleep deprivation do not impair concurrent reversal learning. Effects on subsequent reversal learning are consistent with the idea that REM sleep serves the consolidation of incompletely learned items.     

Sleep-related improvements in motor learning following mental practice

A wide range of experimental studies have provided evidence that a night of sleep may enhance motor performance following physical practice (PP), but little is known, however, about its effect after motor imagery (MI). Using an explicitly learned pointing task paradigm, thirty participants were assigned to one of three groups that differed in the training method (PP, MI, and control groups). The physical performance was measured before training (pre-test), as well as before (post-test 1) and after a night of sleep (post-test 2). The time taken to complete the pointing tasks, the number of errors and the kinematic trajectories were the dependent variables. As expected, both the PP and the MI groups improved their performance during the post-test 1. The MI group was further found to enhance motor performance after sleep, hence suggesting that sleep-related effects are effective following mental practice. Such findings highlight the reliability of MI in learning process, which is thought consolidated when associated with sleep.     

Sustained increase in hippocampal sharp-wave ripple activity during slow-wave sleep after learning

High-frequency oscillations, known as sharp-wave/ripple (SPW-R) complexes occurring in hippocampus during slow-wave sleep (SWS), have been proposed to promote synaptic plasticity necessary for memory consolidation. We recorded sleep for 3 h after rats were trained on an odor-reward association task. Learning resulted in an increased number SPW-Rs during the first hour of post-learning SWS. The magnitude of ripple events and their duration were also elevated for up to 2 h after the newly formed memory. Rats that did not learn the discrimination during the training session did not show any change in SPW-Rs. Successful retrieval from remote memory was likewise accompanied by an increase in SPW-R density and magnitude, relative to the previously recorded baseline, but the effects were much shorter lasting and did not include increases in ripple duration and amplitude. A short-lasting increase of ripple activity was also observed when rats were rewarded for performing a motor component of the task only. There were no increases in ripple activity after habituation to the experimental environment. These experiments show that the characteristics of hippocampal high-frequency oscillations during SWS are affected by prior behavioral experience. Associative learning induces robust and sustained (up to 2 h) changes in several SPW-R characteristics, while after retrieval from remote memory or performance of a well-trained procedural aspect of the task, only transient changes in ripple density were induced.     

Age-related decline of sleep-dependent consolidation

Sleep-dependent memory consolidation is observed following motor skill learning: Performance improvements are greater over a 12-h period containing sleep relative to an equivalent interval without sleep. Here we examined whether older adults exhibit sleep-dependent consolidation on a sequence learning task. Participants were trained on one of two sequence learning tasks. Performance was assessed after a 12-h break that included sleep and after a 12-h break that did not include sleep. Older and younger adults showed similar degrees of initial learning. However, performance of the older adults did not improve following sleep, providing evidence that sleep-dependent consolidation is diminished with age.     

Targeted Memory Reactivation During Sleep,But Not Wake,Enhances Sensorimotor Skill Performance: A Pilot Study

The benefits of sleep on memory consolidation have been enhanced for declarative and motor sequence learning through replaying classically conditioned auditory stimuli during sleep, known as targeted memory reactivation (TMR). However, it is unknown if TMR can influence performance of a sensorimotor skill, in the absence of the cognitive requirements of sequence learning. Here, young adults performed a nondominant arm throwing task separated by a full night of sleep or a full day of wake, with half of all participants receiving TMR between sessions. Participants who received TMR during sleep demonstrated enhanced sensorimotor performance relative to all other groups. In conclusion, this pilot study indicates that it is feasible to influence sensorimotor skill performance through TMR during sleep and may serve as a future adjunct to physical rehabilitation. Future studies will aim to confirm the present results with a larger sample size as well as investigate the effects of TMR during sleep on older adults both with and without a history of stroke.     

A latent consolidation phase in auditory identification learning: time in the awake state is sufficient

Large gains in performance, evolving hours after practice has terminated, were reported in a number of visual and some motor learning tasks, as well as recently in an auditory nonverbal discrimination task. It was proposed that these gains reflect a latent phase of experience-triggered memory consolidation in human skill learning. It is not clear, however, whether and when delayed gains in performance evolve following training in an auditory verbal identification task. Here we show that normal-hearing young adults trained to identify consonant-vowel stimuli in increasing levels of background noise showed significant, robust, delayed gains in performance that became effective not earlier than 4 h post-training, with most participants improving at more than 6 h post-training. These gains were retained for over 6 mo. Moreover, although it has been recently argued that time including sleep, rather than time per se, is necessary for the evolution of delayed gains in human perceptual learning, our results show that 12 h post-training in the waking state were as effective as 12 h, including no less than 6 h night's sleep. Altogether, the results indicate, for the first time, the existence of a latent, hours-long, consolidation phase in a human auditory verbal learning task, which occurs even during the awake state.     

Changes in processing of masked stimuli across early- and late-night sleep: a study on behavior and brain potentials

Sleep has proven to support the memory consolidation in many tasks including learning of perceptual skills. Explicit, conscious types of memory have been demonstrated to benefit particularly from slow-wave sleep (SWS), implicit, non-conscious types particularly from rapid eye movement (REM) sleep. By comparing the effects of early-night sleep, rich in SWS, and late-night sleep, rich in REM sleep, we aimed to separate the contribution of these two sleep stages in a metacontrast masking paradigm in which explicit and implicit aspects in perceptual learning could be assessed separately by stimulus identification and priming, respectively. We assumed that early sleep intervening between two sessions of task performance would specifically support stimulus identification, while late sleep would specifically support priming. Apart from overt behavior, event-related EEG potentials (ERPs) were measured to record the cortical mechanisms associated with behavioral changes across sleep. In contrast to our hypothesis, late-night sleep appeared to be more important for changes of behavior, both for stimulus identification, which tended to improve across late-night sleep, and for priming, with the increase of errors induced by masked stimuli correlating with the duration of REM sleep. ERP components proved sensitive to presence of target shapes in the masked stimuli and to their priming effects. Of these components, the N2 component, indicating processing of conflict, became larger across early-night sleep and was related to the duration of S4 sleep, the deepest substage of SWS containing particularly high portions of EEG slow waves. These findings suggest that sleep promotes perceptual learning primarily by its REM sleep portion, but indirectly also by way of improved action monitoring supported by deep slow-wave sleep.     

Practice effects in backward masking

In two experiments we demonstrate that much larger practice effects occur in a backward masking paradigm where patterned masks are used than in similar visual processing paradigms, such as lateral masking and whole report. In additional experiments we examine four possible explanations for the large practice effects: increased familiarity with the paradigm in general, learning about the targets, learning about the masks, and enhanced sensory processing. Because of failure to observe similar practice effects in related paradigms not involving backward masking and because of the sustained nature of the improvement, we reject the first explanation as a source of practice effect. Experiment 3 allowed us to reject target learning as a source of improvement as well; target sets were switched at the end of training, but no decrement in performance was observed. In Experiment 4, mask sets were switched at the end of training, revealing a significant decrement in performance. Learning about the specific masks, then, does contribute to the observed improvement. However, it is responsible for only about one third of the overall improvement in performance. The final experiment provides evidence that the residual improvement is due to enhanced sensory processing. In that experiment, training on backward masking led to a lowered threshold in a two-flash paradigm but not to a significant change in whole-report performance.     

Involvement of the rostral anterior cingulate cortex in consolidation of inhibitory avoidance memory: interaction with the basolateral amygdala

Previous findings suggest that the rostral anterior cingulate cortex (rACC) is involved in memory for emotionally arousing training. There is also extensive evidence that the basolateral amygdala (BLA) modulates the consolidation of emotional arousing training experiences via interactions with other brain regions. The present experiments examined the effects of posttraining intra-rACC infusions of the cholinergic agonist oxotremorine (OXO) on inhibitory avoidance (IA) retention and investigated whether the BLA and rACC interact in enabling OXO effects on memory. In the first experiment, male Sprague-Dawley rats were implanted with bilateral cannulae above the rACC and given immediate posttraining OXO infusions. OXO (0.5 or 3 ng) induced significant enhancement of retention performance on a 48-h test. In the second experiment, unilateral posttraining OXO infusions (0.5, 3.0 or 10 ng) enhanced retention when infused into rACC, but not caudal ACC, consistent with previous evidence that ACC is composed of functionally distinct regions. A third experiment investigated the effects of posttraining intra-rACC OXO infusions (0.5 or 10 ng) in rats with bilateral sham or NMDA-induced lesions of the BLA. The BLA lesions did not impair IA retention, but blocked the enhancement induced by posttraining intra-rACC OXO infusions. Lastly, unilateral NMDA lesions of rACC blocked the enhancement of IA retention induced by posttraining ipsilateral OXO infusions into the BLA. These findings support the hypothesis that the rACC is involved in modulating the storage of emotional events and provide additional evidence that the BLA modulates memory consolidation through interactions with efferent brain regions, including the cortex.     

Consolidation of sensorimotor learning during sleep

Consolidation of nondeclarative memory is widely believed to benefit from sleep. However, evidence is mainly limited to tasks involving rote learning of the same stimulus or behavior, and recent findings have questioned the extent of sleep-dependent consolidation. We demonstrate consolidation during sleep for a multimodal sensorimotor skill that was trained and tested in different visual-spatial virtual environments. Participants performed a task requiring the production of novel motor responses in coordination with continuously changing audio-visual stimuli. Performance improved with training, decreased following waking retention, but recovered and stabilized following sleep. These results extend the domain of sleep-dependent consolidation to more complex, adaptive behaviors.     

关于午睡研究的概述

适当的午睡可以缓解我们午后的疲劳感,提高午后心境状态、觉醒状态;对于进行了正常夜眠的个体而言,习惯性午睡行为并不是对夜眠不足的补偿;短时午睡对恢复正常体个体身心状态有着积极的效果;然而,越来越多的研究也发现,午睡对记忆也有一定的整合作用。午睡中慢波睡眠对陈述性记忆的整合起着重要作用,此外,二期睡眠纺锤波对陈述性记忆及程序性记忆的整合也起着一定的作用。利用午睡探讨睡眠对记忆的整合作用及机制,可能是未来研究的方向