Motor Memory Consolidation Research Articles

Role of the somatosensory cortex in motor memory consolidation.

Motor memories become resistant to interference by the process of consolidation, which leads to long-term retention. Studies have shown involvement of the somatosensory cortex in motor learning-related plasticity, but not directly in motor memory consolidation. This Neuro Forum article reviews evidence from a continuous theta-burst transcranial magnetic stimulation (cTBS) study by Kumar and colleagues (Kumar N, Manning TF, Ostry DJ. PLoS Biol 17: e3000469, 2019) that demonstrates the role of somatosensory, rather than motor, cortex in human motor memory consolidation during implicit motor learning.

0104 The Effect of Time, Sleep, and Wake on Motor Memory Consolidation: A Partial Replication of Walker, Et Al. (2002)

Abstract Introduction Findings from Walker, et al (2002) ‘Practice with Sleep Makes Perfect: Sleep-Dependent Motor Skill Learning’ demonstrate that performance on a widely used motor memory task (motor sequence task (MST)) benefits from a 12hr period of sleep (and not wake) even if the sleep period does not occur for approximately 12hrs after task acquisition, suggesting that sleep is crucial for motor memory consolidation. Using a larger sample, we attempted to replicate this finding, which is derived from Groups B & D from Walker et al (2002). Methods Participants (64 medical students: Age 21.2±0.8; N=33 females) were trained on the MST in the morning (10am; N=40) or evening (10pm; N=24) and then returned 12 and 24hrs later to be retested. The MST is a simple typing task that requires participants, at training, to type a 5-digit sequence (e.g., 4-1-3-2-4) as fast and accurately as possible over a series of 12 30-second trials with a 30-second break between each trial. At each retest, participants performed three 30-second trials. Results With 75% of the data collected we have found that when sleep follows training in the evening (first 12hr interval), the number of correctly typed sequences increased by 19.1% (cf. 20.5% in Walker (2002)). After a subsequent day of wake (second 12hr interval) performance increased by an additional 7.3% (cf. 2.0%). However, when a day of wake spanned the first 12hrs following training, performance increased by 14.5% (cf. 3.9%) followed by another 14.5% increase over the subsequent night (cf. 14.4%). Performance differences between sleep and wake participants were nonsignificant over the first 12hrs (p=0.38) and second 12hrs (p=0.49). Conclusion With most of data collection complete, our findings only partially replicate those of Walker et al (2002), and may draw into question the robustness of sleep for the processing motor memory. Support None

Consolidation of use-dependent motor memories induced by passive movement training

Motor adaptation, a type of motor learning, is often thought to involve two distinct processes: error-based and use-dependent learning. Passive movement training, which is associated with use-dependent learning, can facilitate motor adaptation, although it is unknown how long its facilitative effect can last. The objective of this study was to examine the lasting effect of passive training on visuomotor adaptation for the duration of up to 24 h. Neurotypical, right-handed subjects experienced four experimental sessions: baseline, training, time delay and testing. In the training session, all subjects received passive training of their dominant arm that was moved by an exoskeletal robot in a “desired” target direction repeatedly. Following that, the subjects experienced a time delay of 5 min, 1 h or 24 h. In the testing session, the subjects performed reaching movements under a novel visuomotor condition, in which the visual display was rotated 30 degrees counterclockwise about the start circle. Control subjects experienced the baseline and testing sessions with a time delay of 5 min between the two sessions. Results indicate that the 1-h and 24-h groups, but not the 5-min group, adapted to the rotation significantly better than the controls. This finding has an implication for neurorehabilitation suggesting, for example, that passive proprioceptive training may indeed be a viable option for improving arm motor function in stroke survivors with severe hemiparesis, for whom efficient intervention techniques are very limited.

Acute Exercise Protects Newly Formed Motor Memories Against rTMS-induced Interference Targeting Primary Motor Cortex

Acute cardiovascular exercise can promote motor memory consolidation following motor practice, and thus long-term retention, but the underlying mechanisms remain sparsely elucidated. Here we test the hypothesis that the positive behavioral effects of acute exercise involve the primary motor cortex and the corticospinal pathway by interfering with motor memory consolidation using non-invasive, low frequency, repetitive transcranial magnetic stimulation (rTMS). Forty-eight able-bodied, young adult male participants (mean age = 24.8 y/o) practiced a visuomotor accuracy task demanding precise and fast pinch force control. Following motor practice, participants either rested or exercised (20 min total: 3 × 3 min at 90% VO2peak) before receiving either sham rTMS or supra-threshold rTMS (115% RMT, 1 Hz) targeting the hand area of the contralateral primary motor cortex for 20 min. Retention was evaluated 24 h following motor practice, and motor memory consolidation was operationalized as overnight changes in motor performance. Low-frequency rTMS resulted in off-line decrements in motor performance compared to sham rTMS, but these were counteracted by a preceding bout of intense exercise. These findings demonstrate that a single session of exercise promotes early motor memory stabilization and protects the primary motor cortex and the corticospinal system against interference.

Intrinsic Plasticity of Cerebellar Purkinje Cells Contributes to Motor Memory Consolidation.

Intrinsic plasticity of cerebellar Purkinje cells (PCs) has recently been demonstrated in cerebellar local circuits; however, its physiological impact on cerebellar learning and memory remains elusive. Here, we suggest that intrinsic plasticity of PCs is tightly involved in motor memory consolidation based on findings from PC-specific STIM1 knockout male mice, which show severe memory consolidation deficiency in vestibulo-ocular reflex memory. Gain-up training of the vestibulo-ocular reflex produced a decrease in the synaptic weight of PCs in both the WT and KO groups. However, intrinsic plasticity was impaired only in the knockout mice. Furthermore, the observed defects in the intrinsic plasticity of PCs led to the formation of aberrant neural plasticity in the vestibular nucleus neurons. Our results suggest that synergistic modulation of intrinsic and synaptic plasticity in PCs is required for the changes in downstream plasticity in the vestibular nucleus, and thereby contributing to the long-term storage of motor memory.SIGNIFICANCE STATEMENT Synaptic plasticity is a well-known mechanism for learning and memory. Although plasticity of excitability, intrinsic plasticity, of the cerebellar Purkinje cell has been reported in both directions (potentiation and depression), the physiological role of intrinsic plasticity still remains ambiguous. In this study, we suggest that both synaptic and intrinsic plasticity are required for successful memory consolidation in cerebellar eye movement learning. Despite successful induction and maintenance of synaptic plasticity, we found deficits of memory consolidation when there were defects in intrinsic plasticity. Our results suggest that intrinsic plasticity of cerebellar Purkinje cell has a significant role in motor memory consolidation.

A sleep spindle framework for motor memory consolidation.

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'.

Does sleep contribute to the consolidation of motor memory?

Abstract Background It has been assumed that sleep promotes consolidation in motor learning; however, some publications have questioned its supposed effect. Differentiated statements on the subject are difficult because the conglomerate of influencing factors is large. The fact that memory, sleep, consolidation and motor task can be considered generic terms for different processes also contributes to the complexity. Objective The aim of this literature overview is to clarify the terminology and to describe what is known about how sleep contributes to the consolidation of motor memory regarding the different characteristics of consolidation and motor tasks. Methods A first literature screening in PubMed included the terms consolidation, sleep, memory, motor learning and memory in various combinations. Furthermore, keywords describing distinct parts of the generic terms were used for searching. Results The current evidence for the dependency of the different neurophysiological characteristics of the generic terms on sleep is presented including resulting contradictions and methodological criticism. Based on the literature, the question whether sleep promotes consolidation can only be answered in reductionist approaches and for individual influencing factors. The results even suggest that improvements in exercise quality may have been achieved through errors in study design, which, however, may lead to recommendations for future studies. Conclusion No final statement can be made on the subject at this time; however, at least it can be considered as evidence-based that sleep does not harm motor memory consolidation.

Triggering Motor Memory Consolidation in PD: Complex Practice of Fine Motor Tasks and Brain Activity During Learning

Triggering Motor Memory Consolidation in PD: Complex Practice of Fine Motor Tasks and Brain Activity During Learning

Sleep deprivation directly following eyeblink-conditioning impairs memory consolidation.

The relation between sleep and different forms of memory formation continues to be a relevant topic in our daily life. Sleep has been found to affect cerebellum-dependent procedural memory formation, but it remains to be elucidated to what extent the level of sleep deprivation directly after motor training also influences our ability to store and retrieve memories. Here, we studied the effect of disturbed sleep in mice during two different time-windows, one covering the first four hours following eyeblink conditioning (EBC) and another window following the next period of four hours. Compared to control mice with sleep ad libitum, the percentage of conditioned responses and their amplitude were impaired when mice were deprived of sleep directly after conditioning. This impairment was still significant when the learned EBC responses were extinguished and later reacquired. However, consolidation of eyeblink responses was not affected when mice were deprived later than four hours after acquisition, not even when tested during a different day-night cycle for control. Moreover, mice that slept longer directly following EBC showed a tendency for more conditioned responses. Our data indicate that consolidation of motor memories can benefit from sleep directly following memory formation.

REM-related obstructive sleep apnea: when does it matter? Effect on motor memory consolidation versus emotional health.

The clinical importance of obstructive sleep apnea, which can be prevalent during rapid eye movement (REM) sleep, is unclear. The current study examines the effect of REM-related obstructive sleep apnea on motor memory consolidation as well as on mood states. We compared performance on the motor sequence task (MST), psychomotor vigilance test (PVT), Functional Outcomes of Sleep Questionnaire, and the Profile of Mood State (POMS) survey between 3 groups: healthy controls (n = 18), REM-exclusive OSA (n = 17), and patients with OSA with respiratory events throughout REM and non-rapid eye movement (NREM) sleep (n = 18). As expected, performance on the MST improved overnight in the healthy control group. An improvement which was similar in magnitude was also observed in the REM-exclusive OSA group whereas patients with similar OSA during REM and NREM sleep showed reduced overnight memory consolidation. Consistent with these results, we found a correlation between overnight MST improvement and the apnea hypopnea index during NREM sleep (P = .041), but not during REM sleep (P = .424). However, patients with REM-exclusive apnea demonstrated the most negative emotions based on scoring highest on the POMS survey (P = .019). Our results provide evidence that although apneas occurring only during REM sleep do not have an effect on the encoding and stabilization of motor sequence memories, they are deleterious for emotional health.

Exercise Intensity Does not Modulate the Effect of Acute Exercise on Learning a Complex Whole-Body Task

High-intensity cardiovascular exercise prior to motor skill practice is postulated to enhance motor memory consolidation (offline learning), whereas moderate-intensity bouts may benefit skill acquisition (online learning). This study aimed at investigating this suggested intensity-dependent effect of exercise in a complex whole-body task.50 healthy young adults were randomized into one of three groups performing a bout of either (1) high-intense, (2) moderate-intense, or (3) minimal-intense cycling for a total of 17 min immediately prior to skill practice. The motor task required participants to balance on a tiltable platform (stabilometer) for 30 s. During acquisition 15 practice trials were carried out, followed by a retention test 24 h later. Time in balance was calculated for each trial and within- and between-group differences in online (skill improvement during skill acquisition) and offline learning (skill change from last acquisition block to retention) were analyzed.All participants significantly improved balance time during acquisition, with no differences observed between experimental conditions. Similarly, there were no differences in offline learning between groups.Contrary to previous reports, the present data do not support an intensity-dependent effect on motor learning, when exercise is performed prior to task practice. One reason for this might be that similar muscle groups were involved in exercise and the motor task, potentially causing fatigue or interference effects. Further, the results indicate that the memory-promoting effects of acute exercise are task-dependent and may not apply equally for motor skills of different levels of complexity.

Low acetylcholine during early sleep is important for motor memory consolidation.

The synaptic homeostasis theory of sleep proposes that low neurotransmitter activity in sleep optimizes memory consolidation. We tested this theory by asking whether increasing acetylcholine levels during early sleep would weaken motor memory consolidation. We trained separate groups of adult mice on the rotarod walking task and the single pellet reaching task, and after training, administered physostigmine, an acetylcholinesterase inhibitor, to increase cholinergic tone in subsequent sleep. Post-sleep testing showed that physostigmine impaired motor skill acquisition of both tasks. Home-cage video monitoring and electrophysiology revealed that physostigmine disrupted sleep structure, delayed non-rapid-eye-movement sleep onset, and reduced slow-wave power in the hippocampus and cortex. Additional experiments showed that: (1) the impaired performance associated with physostigmine was not due to its effects on sleep structure, as 1 h of sleep deprivation after training did not impair rotarod performance, (2) a reduction in cholinergic tone by inactivation of cholinergic neurons during early sleep did not affect rotarod performance, and (3) stimulating or blocking muscarinic and nicotinic acetylcholine receptors did not impair rotarod performance. Taken together, the experiments suggest that the increased slow wave activity and inactivation of both muscarinic and nicotinic receptors during early sleep due to reduced acetylcholine contribute to motor memory consolidation.

Unfolding the Effects of Acute Cardiovascular Exercise on Neural Correlates of Motor Learning Using Convolutional Neural Networks.

Cardiovascular exercise is known to promote the consolidation of newly acquired motor skills. Previous studies seeking to understand the neural correlates underlying motor memory consolidation that is modulated by exercise, have relied so far on using traditional statistical approaches for a priori selected features from neuroimaging data, including EEG. With recent advances in machine learning, data-driven techniques such as deep learning have shown great potential for EEG data decoding for brain-computer interfaces, but have not been explored in the context of exercise. Here, we present a novel Convolutional Neural Network (CNN)-based pipeline for analysis of EEG data to study the brain areas and spectral EEG measures modulated by exercise. To the best of our knowledge, this work is the first one to demonstrate the ability of CNNs to be trained in a limited sample size setting. Our approach revealed discriminative spectral features within a refined frequency band (27–29 Hz) as compared to the wider beta bandwidth (15–30 Hz), which is commonly used in data analyses, as well as corresponding brain regions that were modulated by exercise. These results indicate the presence of finer EEG spectral features that could have been overlooked using conventional hypothesis-driven statistical approaches. Our study thus demonstrates the feasibility of using deep network architectures for neuroimaging analysis, even in small-scale studies, to identify robust brain biomarkers and investigate neuroscience-based questions.

Somatosensory cortex participates in the consolidation of human motor memory.

Newly learned motor skills are initially labile and then consolidated to permit retention. The circuits that enable the consolidation of motor memories remain uncertain. Most work to date has focused on primary motor cortex, and although there is ample evidence of learning-related plasticity in motor cortex, direct evidence for its involvement in memory consolidation is limited. Learning-related plasticity is also observed in somatosensory cortex, and accordingly, it may also be involved in memory consolidation. Here, by using transcranial magnetic stimulation (TMS) to block consolidation, we report the first direct evidence that plasticity in somatosensory cortex participates in the consolidation of motor memory. Participants made movements to targets while a robot applied forces to the hand to alter somatosensory feedback. Immediately following adaptation, continuous theta-burst transcranial magnetic stimulation (cTBS) was delivered to block retention; then, following a 24-hour delay, which would normally permit consolidation, we assessed whether there was an impairment. It was found that when mechanical loads were introduced gradually to engage implicit learning processes, suppression of somatosensory cortex following training almost entirely eliminated retention. In contrast, cTBS to motor cortex following learning had little effect on retention at all; retention following cTBS to motor cortex was not different than following sham TMS stimulation. We confirmed that cTBS to somatosensory cortex interfered with normal sensory function and that it blocked motor memory consolidation and not the ability to retrieve a consolidated motor memory. In conclusion, the findings are consistent with the hypothesis that in adaptation learning, somatosensory cortex rather than motor cortex is involved in the consolidation of motor memory.

The effects of aerobic exercise on sleep quality measures and sleep-related biomarkers in individuals with Multiple Sclerosis: A pilot randomised controlled trial.

Sleep disturbances are highly prevalent in people with multiple sclerosis(MS), and are associated with pain, fatigue, depression, and reduced quality of life (QoL). Importantly, sleep has been considered a critical brain state for motor learning and memory consolidation. Therefore, interventions that target sleep managementin people with MS are needed. To explore the effects of a six weeks moderate-intensity aerobic exercise intervention on sleep characteristics and sleep-related biomarkers specifically serotonin, melatoninand cortisol in people with MS using a pilot randomized controlled trial. Participants were randomly allocated to either a moderate-intensity aerobic exercise program (MAE, n = 20) or a home exercise program (HEP, n = 20). Participants were assessed at baseline and follow-up. Subjective and objective measures were used to assess sleep quality. The Pittsburgh Sleep Quality Index (PSQI) and Insomnia Severity Index (ISI) were used to subjectively assess sleep. While Actigraphy was used to objectivelyassess sleep. Blood samples were collected for measurement of cortisol, melatonin and serotonin from MS participants in both groups at 8:00 am±1 hour. Seventeen participants in the MAE and 13 in the HEP group completed the study. Compared to the HEP group, people with MS who participated in a moderate-intensity aerobic exercise experienced significant improvements (P < 0.05) on the PSQI, ISI, and several objective sleep parameters measured using actigraphy. Only the serotonin levels increased significantly over the six-week period in the MAE group compared to the HEP group. The change score in serotonin (from baseline to follow up assessment) was significantly correlatedwith the change score in PSQI (r = -0.97, p < 001) and the change score in ISI (r = -0. 56, p = 0.015) only in the MAE group but not the HEP group. Exercise may be a non-pharmacological, inexpensive, safe method to improve sleep quality in people with MS. The improvement in the serotonin level due to aerobic exercisemight explain one of the physiologic mechanisms driving these improvements.

Bright light exposure advances consolidation of motor skill accuracy in humans.

Light has attracted increasing attention as a critical determinant of memory processing. While sleep selectively consolidates newly encoded memories according to their future relevance, the role of light in human memory consolidation is largely unknown. Here, we report how bright light (BL), provided during encoding, influences online and offline consolidation of motor skill learning. We sought to determine whether relatively slower and faster key-press transitions within individuals were differentially consolidated by BL. Healthy human subjects were briefly exposed to either BL (>8000 lx) or control light (CL; <500 lx) during memory encoding at 13:00 h, when light minimally affects circadian phase-shifting, and were retested 24 h later. The effects of BL on online and offline performance gains were determined by accuracy and speed. BL-exposed subjects showed better overall performance accuracy during training and lower overnight accuracy gains after a subsequent night of sleep than did CL-exposed subjects. BL preferentially improved the initially most difficult individual key-press transitions during practice; these were only improved overnight under CL. By contrast, accuracy during what had been the easiest key-press transitions at the beginning of the experiment was unaffected by light conditions or online/offline learning processes. BL effects were not observed for performance speed, mood, or sleep-wake patterns. Brief BL exposure during training may advance motor memory selection and consolidation that optimally meet individual requirements for potential gains, which would otherwise depend on post-training sleep. This suggests a new way of enhancing brain plasticity to compensate for impaired sleep-dependent memory consolidation in neuropsychiatric conditions.

Enhancing Children's Motor Memory Retention Through Acute Intense Exercise: Effects of Different Exercise Durations.

Physical exercise has been proposed as a viable means to stimulate motor learning. Exercise characteristics, including intensity and duration, may play a role in modulating the exercise effect on motor learning. While some evidence exists regarding the benefits of intense and relatively long exercise, little is known about the effect of short exercise bouts on motor learning, especially in children. This study aimed to assess the effect of long versus short intense exercise bouts on the adaptation and consolidation of a rotational visuomotor adaptation task. The participants were 71 healthy children from two sites divided into three groups: long exercise bout (LONG), short exercise bout (SHORT), and no exercise (CON). Children performed a rotated (clockwise 60° rotation) motor task on four different occasions: an adaptation set and 1 h, 24 h, and 7 days delayed retention sets. Exercise bouts were performed prior to the adaptation set. Results showed a group effect during motor adaptation [F(2,68) = 3.160; p = 0.049; = 0.087], but no statistical differences were found between groups. Regarding retention tests, both exercise groups (LONG and SHORT) showed superior retention compared to CON group [F(2,68) = 7.102; p = 0.002; = 0.175]. No differences were found between exercise groups, indicating similar benefits for the two exercise interventions. Overall, whether the exercise duration was long or short, exercise improved motor memory retention as an estimate of memory consolidation process. The use of short exercise bouts may be suitable to improve children’s motor memory consolidation in environments where time constraints exist.

Contextual Interference Effect Is Independent of Retroactive Inhibition but Variable Practice Is Not Always Beneficial.

Positive effects of variable practice conditions on subsequent motor memory consolidation and generalization are widely accepted and described as the contextual interference effect (CIE). However, the general benefits of CIE are low and these benefits might even depend on decreased retest performances in the blocked-practicing control group, caused by retroactive inhibition. The aim of this study was to investigate if CIE represents a true learning phenomenon or possibly reflects confounding effects of retroactive inhibition. We tested 48 healthy human participants adapting their reaching movements to three different force field magnitudes. Subjects practiced the force fields in either a Blocked (B), Random (R), or Constant (C) schedule. In addition, subjects of the Blocked group performed either a retest schedule that did (Blocked-Matched; BM) or did not (Blocked-Unmatched; BU) control for retroactive inhibition. Results showed that retroactive inhibition did not affect the results of the BU group much and that the Random group showed a better consolidation performance compared to both Blocked groups. However, compared to the Constant group, the Random group showed only slight benefits in its memory consolidation of the mean performance across all force field magnitudes and no benefits in absolute performance values. This indicates that CIE reflects a true motor learning phenomenon, which is independent of retroactive inhibition. However, random practice is not always beneficial over constant practice.

The Beneficial Effect of Acute Exercise on Motor Memory Consolidation is Modulated by Dopaminergic Gene Profile.

When aerobic exercise is performed following skilled motor practice, it can enhance motor memory consolidation. Previous studies have suggested that dopamine may play a role in motor memory consolidation, but whether it is involved in the exercise effects on consolidation is unknown. Hence, we aimed to investigate the influence of dopaminergic pathways on the exercise-induced modulation of motor memory consolidation. We compared the effect of acute exercise on motor memory consolidation between the genotypes that are known to affect dopaminergic transmission and learning. By combining cluster analyses and fitting linear models with and without included polymorphisms, we provide preliminary evidence that exercise benefits the carriers of alleles that are associated with low synaptic dopamine content. In line with previous reports, our findings implicate dopamine as a modulator of the exercise-induced effects on motor memory consolidation, and suggest exercise as a potential clinical tool to counteract low endogenous dopamine bioavailability. Further experiments are needed to establish causal relations.

Use of targeted memory reactivation enhances skill performance during a nap and enhances declarative memory during wake in healthy young adults

Sleep is an important component of motor memory consolidation and learning, providing a critical tool to enhance training and rehabilitation. Following initial skill acquisition, memory consolidation is largely a result of non-rapid eye movement sleep over either a full night or a nap. Targeted memory reactivation is one method used to enhance this critical process, which involves the pairing of an external cue with task performance at the time of initial motor skill acquisition, followed by replay of the same cue during sleep. Application of targeted memory reactivation during sleep leads to increased functional connectivity within task-related brain networks and improved behavioural performance in healthy young adults. We have previously used targeted memory reactivation throughout the first two slow-wave sleep cycles of a full night of sleep to enhance non-dominant arm throwing accuracy in healthy young adults. Here, we aimed to determine whether application of targeted memory reactivation throughout a 1-hr daytime nap was sufficient to enhance performance on the same non-dominant arm throwing task in healthy young adults. Participants were allocated to either nap or no nap, and within those groups half received targeted memory reactivation throughout a 1-hr between-session period, leading to four groups. Only participants who slept between sessions while receiving targeted memory reactivation enhanced their throwing accuracy upon beginning the second session. Future studies will aim to use this technique as an adjunct to traditional physical rehabilitation with individuals with neurologic diagnoses such as stroke.