Motor Skill Consolidation Research Articles

The contribution of nocturnal sleep to the consolidation of motor skill learning in healthy ageing and Parkinson's disease

The benefits of sleep for the consolidation of procedural motor skills are less robust in older adults, although the precise reasons for this remain unclear. To date, even less is known about these processes in older adults with neurodegenerative diseases, particularly those which impact on motor functioning. While sleep disturbance and motor symptoms are frequent disabling features of Parkinson's disease, no known studies have directly probed sleep-dependent memory consolidation for motor skill learning in Parkinson's disease. Forty patients with idiopathic Parkinson's disease (age=63.7years±7.7; disease duration 4.1years± 4.4) completed a motor skill learning task pre- and post-sleep and were compared to 20 age- and sex-matched controls recruited from the community. Polysomnography was undertaken during the post-training night and measures of sleep architecture were derived. Parkinson's disease patients did not demonstrate any apparent deficits in within-session learning and overnight stabilization compared to controls, with both groups failing to demonstrate offline improvements in performance (i.e. memory consolidation). In controls, longer duration in slow wave sleep was associated with improved next-day session learning (P=0.007). However, in Parkinson's disease, no relationships between sleep parameters and learning measures were found. Slow wave sleep microarchitecture and the use of dopaminergic medications may contribute to impaired sleep-dependent multi-session acquisition of motor skill learning in Parkinson's disease.

Sleep-dependent consolidation of motor skills in patients with narcolepsy-cataplexy.

This study investigated whether the altered organization of post-training sleep in patients with narcolepsy-cataplexy (NC) is associated with a lower off-line improvement in the consolidation of motor skills compared with normal subjects. Fourteen drug-naive NC patients, fulfilling the international clinical and polysomnographic diagnostic criteria, and 14 individually-matched controls underwent training at a sequential finger tapping task (FTT) and were re-tested on the next morning (after a night with polysomnographic recording) and after another six nights (spent at home). Training and retrieval sessions were performed in a controlled laboratory setting. FTT performance was worse in NC patients than controls at training and at both retrieval sessions and showed a fairly different time course (slower than in controls) of consolidation. Several sleep indices (lower values of stage-2 NREM sleep and SWS) were compatible with a lower effectiveness of sleep for consolidation of motor skills in NC patients, although no statistically significant relationship was found between such indices and improvement rate. The consolidation process of motor skills results less effective in NC patients since training and slower than in normal subjects over the week following training. The wider variations in performance scores and sleep parameters of post.-training night in NC patients relative to controls suggest that a) the lower initial consolidation may be due to a less effective encoding consequent to altered prior sleep, and b) the consolidation process over the 24 h following training is negatively influenced not only by the altered characteristics of post-training sleep, but also by the daytime sleepiness following training.

Effect of sleep on gross motor memory

Sleep has a beneficial effect on consolidation of newly learned fine motor skills. The aim of the current study was to determine whether sleep has a similar beneficial effect on consolidation of gross motor skills. A total of 70 participants were randomly assigned to either a Sleep-Wake group or a Wake-Sleep group and were trained on an arm coordinated reaching task as a gross motor skill. Initial training occurred in the evening for the Sleep-Wake group and in the morning for the Wake-Sleep group. All participants attended two test sessions 12 and 24 hours following the initial training. Gross motor skill performance improved in both groups following a night of sleep but not after a day of wakefulness. These findings may have implications for learning of new gross motor skills in a range of activities from dance to motor rehabilitation.

Using actigraphy and transcranial magnetic stimulation to assess the relationship between sleep and visuomotor skill learning

Sleep following training can enhance motor skill memory consolidation while chronic sleep disruption can have the converse effect. The aim of this investigation was to explore the relationship between sleep measured by wrist actigraphy, motor skill consolidation and primary motor cortex excitability in young, healthy individuals. Training was a visuospatial finger-tracking task. Dependent measures included tracking skill performance, cortical excitability, measures of sleep, and level of arousal. Assessments occurred pre-training, post-training and at 12 h and 24 h retention. An activity monitor was worn on the wrist during the nights preceding and following training. Results indicate that sleep during the night following training was predictive of 1) offline skill consolidation following training (R² = 0.34) and 2) cortical excitability at 24 h follow-up (R² = 0.35) with less time spent awake associated with better skill performance and lower cortical excitability at 24 h follow-up. No difference in measures of sleep was observed between nights of sleep (p > 0.05). Sleep the night before training did not influence skill performance, skill acquisition during training, nor measures of cortical excitability at pre-training assessment. These findings suggest a relationship between motor skill development, cortical excitability and sleep following training. These results invite further investigation into the utility of actigraphy as a low-cost, easy-to-administer alternative to polysomnography for short and long-term evaluation of the relationship between sleep, cortical excitability and motor skill learning in healthy and patient populations.

Role of the Primary Motor Cortex in the Early Boost in Performance Following Mental Imagery Training

Recently, it has been suggested that the primary motor cortex (M1) plays a critical role in implementing the fast and transient post-training phase of motor skill consolidation, known to yield an early boost in performance. Whether a comparable early boost in performance occurs following motor imagery (MIM) training is still unknown. To address this issue, two groups of subjects learned a finger tapping sequence either by MIM or physical practice (PP). In both groups, performance increased significantly in the post-training phase when compared with the pre-training phase and further increased after a 30 min resting period, indicating that both MIM and PP trainings were equally efficient and induced an early boost in motor performance. This conclusion was corroborated by the results of an additional control group. In a second experiment, we then investigated the causal role of M1 in implementing the early boost process resulting from MIM training. To do so, we inhibited M1 by applying a continuous theta-burst stimulation (cTBS) in healthy volunteers just after they learnt, by MIM, the same finger-tapping task as in Experiment #1. As a control, cTBS was applied over the vertex of subjects who underwent the same experiment. We found that cTBS applied over M1 selectively abolished the early boost process subsequent to MIM training. Altogether, the present study provides evidence that MIM practice induces an early boost in performance and demonstrates that M1 is causally involved in this process. These findings further divulge some degree of behavioral and neuronal similitude between MIM and PP.

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.

Spatiotemporal firing patterns in the cerebellum

Neurons are generally considered to communicate information by increasing or decreasing their firing rate. However, in principle, they could in addition convey messages by using specific spatiotemporal patterns of spiking activities and silent intervals. Here, we review expanding lines of evidence that such spatiotemporal coding occurs in the cerebellum, and that the olivocerebellar system is optimally designed to generate and employ precise patterns of complex spikes and simple spikes during the acquisition and consolidation of motor skills. These spatiotemporal patterns may complement rate coding, thus enabling precise control of motor and cognitive processing at a high spatiotemporal resolution by fine-tuning sensorimotor integration and coordination.

Atypical acquisition and atypical expression of memory consolidation gains in a motor skill in young female adults with ADHD

Individuals with ADHD often show performance deficits in motor tasks. It is not clear, however, whether this reflects less effective acquisition of skill (procedural knowledge), or deficient consolidation into long-term memory, in ADHD. The aim of the study was to compare the acquisition of skilled motor performance, the expression of delayed – consolidation phase – gains and retention, in persons with and without ADHD. Thirty-two participants, 16 with ADHD, were trained on a sequence of finger movements using a well-established training protocol, and tested before training and immediately, 24 h and 2 weeks after training. Both groups showed similar within-session gains in speed; additional, delayed gains were expressed at 24 h, but less robustly in ADHD, and at 2 weeks post-training. However, while controls showed significant delayed gains in accuracy at 24 h and 2 weeks post-training, accuracy deteriorated in ADHD from pre-training to 24 h post-training and was only at pre-training levels by 2-weeks post-training. Our results demonstrate a latent memory consolidation phase in motor sequence learning, expressed as delayed gains in speed and a much delayed recovery of pre-training accuracy, in individuals with ADHD. However, both the acquisition and memory consolidation of motor skills are atypical in ADHD.

Sleep has no critical role in implicit motor sequence learning in young and old adults

The influence of sleep on motor skill consolidation has been a research topic of increasing interest. In this study, we distinguished general skill learning from sequence-specific learning in a probabilistic implicit sequence learning task (alternating serial reaction time) in young and old adults before and after a 12-h offline interval which did or did not contain sleep (p.m.-a.m. and a.m.-p.m. groups, respectively). The results showed that general skill learning, as assessed via overall reaction time, improved offline in both the young and older groups, with the young group improving more than the old. However, the improvement was not sleep-dependent, in that there was no difference between the a.m.-p.m. and p.m.-a.m. groups. We did not find sequence-specific offline improvement in either age group for the a.m.-either p.m. or p.m.-a.m. groups, suggesting that consolidation of this kind of implicit motor sequence learning may not be influenced by sleep.

Contribution of night and day sleep vs. simple passage of time to the consolidation of motor sequence and visuomotor adaptation learning

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.

Impaired Off-Line Consolidation of Motor Memories After Combined Blockade of Cholinergic Receptors During REM Sleep-Rich Sleep

Rapid eye movement (REM) sleep has been considered important for the consolidation of memories, particularly of procedural skills. REM sleep, in contrast to slow-wave sleep (SWS), is hallmarked by the high, wake-like activity of the neurotransmitter acetylcholine (ACh), which promotes certain synaptic plastic processes underlying the formation of memories. Here, we show in healthy young men that off-line consolidation of a motor skill during a period of late sleep with high amounts of REM sleep depends essentially on high cholinergic activity. After a 3-h sleep period during the early night to satisfy the need for SWS, subjects learned a procedural finger sequence tapping task and a declarative word-pair learning task. After learning, they received either placebo or a combination of the muscarinic receptor antagonist scopolamine (4 microg/kg bodyweight, intravenously) and the nicotinic receptor antagonist mecamylamine (5 mg, orally), and then slept for another 3 h, ie, the late nocturnal sleep period, which is dominated by REM sleep. Retrieval was tested the following evening. Combined cholinergic receptor blockade significantly impaired motor skill consolidation, whereas word-pair memory remained unaffected. Additional data show that the impairing effect of cholinergic receptor blockade is specific to sleep-dependent consolidation of motor skill and does not occur during a wake-retention interval. Taken together, these results identify high cholinergic activity during late, REM sleep-rich sleep as an essential factor promoting sleep-dependent consolidation of motor skills.

Protein synthesis is essential not only for consolidation but also for maintenance and post-retrieval reconsolidation of acrobatic motor skill in rats

It has been reported that consolidation of motor skill, a type of non-declarative memories, requires protein synthesis, as hippocampus-dependent declarative memory does. However, little is known about the importance of protein synthesis in maintenance and especially post-retrieval reconsolidation of acrobatic motor skill. Here, we show that protein synthesis is essential not only for the consolidation but also for the maintenance and reconsolidation of a rotarod-running skill. Intra-ventricle infusion of the protein synthesis inhibitor anisomycin 0 h but not 2 h post-training caused a severe deficit in the acquisition of the rotarod-running skill. Protein synthesis inhibition (PSI) also caused a deficit in the maintenance of the rotarod-running skill, as well-trained rats demonstrated a deficit in the rotarod-running performance upon treatment with anisomycin. Similarly, PSI impaired the post-retrieval reconsolidation of the rotarod-running skill: well-trained rats treated with anisomycin 0 h but not 0.5, 2 and 4 h after the task performance exhibited amnesia for the running skill later on. Interestingly, rats treated with anisomycin 6 and 12 h post-retrieval exhibited amnesia for the running skill. Thus, protein synthesis is essential not only for the consolidation but also for the maintenance and post-retrieval reconsolidation of rotarod-running acrobatic motor skill.

Reconsidering the role of sleep for motor memory.

Previous studies suggest that sleep may play an important role in memory consolidation of motor skills. It has been difficult, however, to tease apart the effect of sleep from circadian and homeostatic factors. We examined the effect of sleep on a popular motor sequence task, utilizing a design that controlled for time of day and time since sleep between wake and sleep groups. When these factors were controlled, there was no benefit of sleep to motor memory, suggesting that previous work may have been influenced by circadian and homeostatic confounds.

Motor sequence learning in primate: Role of the D2 receptor in movement chunking during consolidation

Motor learning disturbances have been shown in diseases involving dopamine insufficiency such as Parkinson’s disease and schizophrenic patients under antipsychotic drug treatment. In non-human primates, motor learning deficits have also been observed following systemic administration of raclopride, a selective D2-receptor antagonist. These deficits were characterized by persistent fluctuations of performance from trial to trial, and were described as difficulties in consolidating movements following a learning period. Moreover, it has been suggested that these raclopride-induced fluctuations can result from impediments in grouping separate movements into one fluent sequence. In the present study, we explore the hypothesis that such fluctuations during movement consolidation can be prevented through the use of sumanirole – a highly selective D2 agonist – if administered before raclopride. Two monkeys were trained to execute a well known sequence of movements, which was later recalled under three pharmacological conditions: (1) no drug, (2) raclopride, and (3) sumanirole + raclopride. The same three pharmacological conditions were repeated with the two monkeys, trained this time to learn new sequences of movements. Results show that raclopride has no deleterious effect on the well known sequence, nor the sumanirole + raclopride co-administration. However, results on the new sequence to be learned revealed continuous fluctuations of performances in the raclopride condition, but not in the sumanirole + raclopride condition. These fluctuations occurred concurrently with a difficulty in merging separate movement components, known as a “chunking deficit”. D2 receptors seem therefore to be involved in the consolidation of new motor skills, and this might involve the chunking of separate movements into integrated motor sequences.

Repetitive transcranial magnetic stimulation over the primary motor cortex disrupts early boost but not delayed gains in performance in motor sequence learning

In humans the consolidation of recently learned motor skills is a multi-step process. We previously showed that performance on the finger-tapping task (FTT; i.e. a sequential motor skill) temporarily improves early on, 5-30 min after practice has ended, but not 4 h later. In the absence of any further practice to the task, this early boost in performance was predictive of the performance levels eventually achieved 48 h later, suggesting its functional relevance for long-term memory consolidation [Hotermans, Peigneux, Maertens de Noordhout, Moonen, and Maquet (2006) Early boost and slow consolidation in motor skill learning. Learn. Mem., 13, 580-583]. Here, we focused on the role of the primary motor cortex (M1) in consolidation using repetitive transcranial magnetic stimulation (rTMS) applied immediately before testing at 30 min, 4 or 24 h after practice of the FTT. Immediately after learning, rTMS over M1 depressed the early boost in performance, but did not affect the delayed improvement observed 48 h later. Four and 24 h after practice, rTMS did not disrupt performance anymore. These results suggest that M1 supports performance during the early post-training phase of motor skill consolidation, but is no longer mandatory in the subsequent, delayed stages of consolidation.

Protein synthesis inhibition blocks consolidation of an acrobatic motor skill.

To investigate whether motor skill learning depends on de novo protein synthesis, adult rats were trained in an acrobatic locomotor task (accelerating rotarod) for 7 d. Animals were systemically injected with cycloheximide (CHX, 0.5 mg/kg, i.p.) 1 h before sessions 1 and 2 or sessions 2 and 3. Control rats received vehicle injections before sessions 1, 2, and 3. Although CHX did not affect improvement of performance within session 1, between-session improvement was impaired. In overtrained animals, comparable injections of CHX had no effect on rotarod performance. These findings suggest that consolidation of motor skills requires protein synthesis.

Cortical synaptogenesis and motor map reorganization occur during late, but not early, phase of motor skill learning.

Extensive motor skill training induces reorganization of movement representations and synaptogenesis within adult motor cortex. Motor skill does not, however, develop uniformly across training sessions. It is characterized by an initial fast phase, followed by a later slow phase of learning. How cortical plasticity emerges during these phases is unknown. Here, we examine motor map topography and synapse number within rat motor cortex during the early and late phases of motor learning. Adult rats were placed in either a skilled or unskilled reaching condition (SRC and URC, respectively) for 3, 7, or 10 d. Intracortical microstimulation of layer V was used to determine the topography of forelimb movement representations within caudal forelimb area of motor cortex contralateral to the trained paw. Quantitative electron microscopy was used to measure the number of synapses per neuron within layer V. SRC animals showed significant increases in reaching accuracy after 3, 7, and 10 d of training. In comparison with URC animals, SRC animals had significantly larger distal forelimb representations after 10 d of training only. Furthermore, SRC animals had significantly more synapses per neuron than URC animals after 7 and 10 d of training. These results show that both motor map reorganization and synapse formation occur during the late phase of skill learning. Furthermore, synaptogenesis precedes map reorganization. We propose that motor map reorganization and synapse formation do not contribute to the initial acquisition of motor skills but represent the consolidation of motor skill that occurs during late stages of training.

Deficits in long-term retention of learned motor skills in patients with cortical or subcortical degeneration

We investigated the acquisition and long-term retention of new skills in patients with cortical (Alzheimer’s disease, AD) and subcortical (progressive supranuclear palsy, PSP; Parkinson’s disease, PD) degeneration. The motor skill task performance of the PD and PSP patients improved with training, but the improvement disappeared within a few months, whereas AD patients retained learned skills for 3–18 months. The results of our experiments show that subcortical dysfunction induces a retention deficit for newly learned motor skills. Our present study suggests that a normal striatum is necessary for the formation of long-lasting motor skills, and that the striatum plays an important role as a motor skill consolidation system.

Imaging Brain Plasticity during Motor Skill Learning

The search for the neural substrates mediating the incremental acquisition of skilled motor behaviors has been the focus of a large body of animal and human studies in the past decade. Much less is known, however, with regard to the dynamic neural changes that occur in the motor system during the different phases of learning. In this paper, we review recent findings, mainly from our own work using fMRI, which suggest that: (i) the learning of sequential finger movements produces a slowly evolving reorganization within primary motor cortex (M1) over the course of weeks and (ii) this change in M1 follows more dynamic, rapid changes in the cerebellum, striatum, and other motor-related cortical areas over the course of days. We also briefly review neurophysiological and psychophysical evidence for the consolidation of motor skills, and we propose a working hypothesis of its underlying neural substrate in motor sequence learning.

T Immediate Neural Plasticity Shapes Motor Performance

The consolidation of motor skills necessitates long-lasting changes in the nervous system. For the most part, plasticity has been documented in motor systems after training and long-term adaptation. However, there has been no demonstration of immediate neural changes associated with the rapid adaptation of motor behavior required to interact with a dynamic environment. To address this issue, we explored the changes in performance (reaction time) of rhesus monkeys that executed saccadic eye movements to one of two visual stimuli while monitoring the preparatory activity of neurons in the superior colliculus, a structure close to the motor output. Similar to the well established sequential effects observed in human manual responses, each monkey displayed reaction times to target locations that were organized in a sequential pattern, becoming progressively shorter with each preceding repeated movement and longer with each preceding nonrepeated movement. This sequential pattern of performance modification was associated with concordant changes in the preparatory activity of superior colliculus neurons in advance of the saccadic target presentation. These data indicate that neural properties are continuously shaped by use-related experience in a manner consistent with the progressive adaptation of motor behavior.