Short-term Motor Learning Research Articles

Brain connectome correlates of short-term motor learning in healthy older subjects

The motor learning process entails plastic changes in the brain, especially in brain network reconfigurations. In the current study, we sought to characterize motor learning by determining changes in the coupling behaviour between the brain functional and structural connectomes on a short timescale. 39 older subjects (age: mean (SD) = 69.7 (4.7) years, men:women = 15:24) were trained on a visually guided sequential hand grip learning task. The brain structural and functional connectomes were constructed from diffusion-weighted MRI and resting-state functional MRI, respectively. The association of motor learning ability with changes in network topology of the brain functional connectome and changes in the correspondence between the brain structural and functional connectomes were assessed. Motor learning ability was related to decreased efficiency and increased modularity in the visual, somatomotor, and frontoparietal networks of the brain functional connectome. Between the brain structural and functional connectomes, reduced correspondence in the visual, ventral attention, and frontoparietal networks as well as the whole-brain network was related to motor learning ability. In addition, structure–function correspondence in the dorsal attention, ventral attention, and frontoparietal networks before motor learning was predictive of motor learning ability. These findings indicate that, in the view of brain connectome changes, short-term motor learning is represented by a detachment of the brain functional from the brain structural connectome. The structure–function uncoupling accompanied by the enhanced segregation into modular structures over the core functional networks involved in the learning process may suggest that facilitation of functional flexibility is associated with successful motor learning.

A randomized controlled trial of changes in resting-state functional connectivity associated with short-term motor learning of chopstick use with the non-dominant hand

IntroductionThis study identified the offline brain networks associated with motor learning of non-dominant hand chopstick use within-session. Methods40 healthy right-handed adults were randomly assigned to the practice and control groups (20 each). The performance, resting-state functional connectivity (RSFC), and their correlation were compared within and between groups. Both groups repeated 9 cycles of 30 s task and rest. During the task, the practice group performed the chopstick-use practice with their left hand, while the control group held chopsticks without acquiring any skills. During the rest, both groups fixated their gaze on a fixation point. The number of times candies were moved using chopsticks with the left hand in 30 s was used to evaluate the performance. RSFC was obtained by resting-state fMRI scanning and extracting Z-scores between the right primary motor cortex and all other brain regions. ResultsBoth the groups improved in the post-task performance; the practice group improved more. The RSFC of the two networks increased in the practice group. One network was the RSFC between the right M1 and the right cerebellar Crus I, positively correlated with performance in the post-task. Another was the RSFC between the right M1 and the left cerebellar Crus II, positively correlated with skills in the amount of change pre- and post-task. ConclusionOffline enhancement of RSFC in these networks was shown to contribute to early chopstick-use motor learning with the left hand. These results serve as a basis for future studies on compensatory networks in individuals with stroke.

Rapid volumetric brain changes after acute psychosocial stress

Stress is an important trigger for brain plasticity: Acute stress can rapidly affect brain activity and functional connectivity, and chronic or pathological stress has been associated with structural brain changes. Measures of structural magnetic resonance imaging (MRI) can be modified by short-term motor learning or visual stimulation, suggesting that they also capture rapid brain changes. Here, we investigated volumetric brain changes (together with changes in T1 relaxation rate and cerebral blood flow) after acute stress in humans as well as their relation to psychophysiological stress measures.Sixty-seven healthy men (25.8±2.7 years) completed a standardized psychosocial laboratory stressor (Trier Social Stress Test) or a control version while blood, saliva, heart rate, and psychometrics were sampled. Structural MRI (T1 mapping / MP2RAGE sequence) at 3T was acquired 45 min before and 90 min after intervention onset. Grey matter volume (GMV) changes were analysed using voxel-based morphometry. Associations with endocrine, autonomic, and subjective stress measures were tested with linear models.We found significant group-by-time interactions in several brain clusters including anterior/mid-cingulate cortices and bilateral insula: GMV was increased in the stress group relative to the control group, in which several clusters showed a GMV decrease. We found a significant group-by-time interaction for cerebral blood flow, and a main effect of time for T1 values (longitudinal relaxation time). In addition, GMV changes were significantly associated with state anxiety and heart rate variability changes.Such rapid GMV changes assessed with VBM may be induced by local tissue adaptations to changes in energy demand following neural activity. Our findings suggest that endogenous brain changes are counteracted by acute psychosocial stress, which emphasizes the importance of considering homeodynamic processes and generally highlights the influence of stress on the brain.

Embodied virtual reality for the study of real-world motor learning.

Motor-learning literature focuses on simple laboratory-tasks due to their controlled manner and the ease to apply manipulations to induce learning and adaptation. Recently, we introduced a billiards paradigm and demonstrated the feasibility of real-world-neuroscience using wearables for naturalistic full-body motion-tracking and mobile-brain-imaging. Here we developed an embodied virtual-reality (VR) environment to our real-world billiards paradigm, which allows to control the visual feedback for this complex real-world task, while maintaining sense of embodiment. The setup was validated by comparing real-world ball trajectories with the trajectories of the virtual balls, calculated by the physics engine. We then ran our short-term motor learning protocol in the embodied VR. Subjects played billiard shots when they held the physical cue and hit a physical ball on the table while seeing it all in VR. We found comparable short-term motor learning trends in the embodied VR to those we previously reported in the physical real-world task. Embodied VR can be used for learning real-world tasks in a highly controlled environment which enables applying visual manipulations, common in laboratory-tasks and rehabilitation, to a real-world full-body task. Embodied VR enables to manipulate feedback and apply perturbations to isolate and assess interactions between specific motor-learning components, thus enabling addressing the current questions of motor-learning in real-world tasks. Such a setup can potentially be used for rehabilitation, where VR is gaining popularity but the transfer to the real-world is currently limited, presumably, due to the lack of embodiment.

Effect of the brain-derived neurotrophic factor gene Val66Met polymorphism on sensory-motor integration during a complex motor learning exercise

The brain-derived neurotrophic factor (BDNF) gene Val66Met polymorphism may cause impairment in short-term motor learning by reducing activity-dependent BDNF expression, which causes alterations in synaptic plasticity by changing glutamatergic and GABAergic synaptic transmissions. Sensory-motor integration (SMI) plays an important role in motor learning. In this study, we investigated the role of this polymorphism on SMI during a complex motor learning practice. Forty-three healthy participants performed standardized 5-day basketball shooting exercises under supervision. Electrophysiologic SMI studies were performed before the first day exercise (T0) and after the first and fifth day exercises (T1 and T2, respectively). SMI was studied using electrical median nerve stimulation at the wrist, followed by transcranial magnetic stimulation (TMS) of the contralateral motor cortex with various inter-stimulus intervals (ISIs). Recordings were made from the thenar and forearm flexor muscles. Participants were divided into two groups according to their BDNF genotype. Group 1 consisted of 26 subjects with the Val66Val genotype and group 2 included 17 subjects with the BDNF Met allele. Group 2 had a lower increase in basketball scores at day 5. Moreover, they had higher afferent facilitation for the responses recorded from both thenar and forearm flexor muscles at T1, but these changes could not be maintained until T2. This non-persistent early hyper-responsivity of the sensory-motor cortex in subjects with the BDNF Met allele might be explained by a transient upsurge of cortical excitability to compensate the insufficient cortical plasticity during motor learning, which could be considered as a sign of lower performance in motor skill learning.

The Impact of Paternal Alcohol Consumption on Offspring Brain and Behavioral Development.

Fetal alcohol spectrum disorders (FASD) describe the wide array of long-lasting developmental abnormalities in offspring due to prenatal alcohol (ethanol [EtOH]) exposure via maternal gestational drinking. Although the teratogenic consequences of prenatal EtOH exposure, are apparent, the effects of preconception paternal EtOH exposure (PatEE) are still unclear. Previous research suggests that PatEE can induce molecular changes and abnormal behavior in the offspring. However, it is not known whether PatEE impacts the development of the neocortex and behavior in offspring as demonstrated in maternal consumption models of FASD (J Neurosci, 33, 2013, 18893). In this study, we utilized a novel mouse model of PatEE where male mice self-administered 25% EtOH for an extended period prior to conception, generating indirect exposure to the offspring through the paternal germline. Following mating, we examined the effects of PatEE on offspring neocortical development at postnatal day (P) 0 and evaluated several aspects of behavior at both P20 and P30 using a battery of behavioral assays. PatEE resulted in significant impact on neocortical development, including abnormal patterns of gene expression within the neocortex at P0 and subtle alterations in patterns of intraneocortical connections. Additionally, PatEE mice exhibited a sex-specific increase in activity and sensorimotor integration deficits at P20, and decreased balance, coordination, and short-term motor learning at P30. This suggests that PatEE may generate long-lasting, sex-specific effects on offspring behavior. These results demonstrate that the developmental impact of preconception PatEE is more harmful than previously thought and provide additional insights into the biological mechanisms that may underlie atypical behavior observed in children of alcoholic fathers.

Combining Unassisted and Robot-Guided Practice Benefits Motor Learning for a Golf Putting Task

Robotic guidance has been employed with limited effectiveness in neurologically intact and patient populations. For example, our lab has effectively used robotic guidance to acutely improve movement smoothness of a discrete trajectory without influencing movement endpoint distributions. The purpose of the current study was to investigate the efficacy of combining robotic guidance and unassisted trials in the learning of a golf putting task. Participants completed a pre-test, an acquisition phase, and an immediate and delayed (24-hour) post-test. During the pre-test, kinematic data from the putter was converted into highly accurate, consistent, and smooth trajectories delivered by a robot arm. During acquisition, three groups performed putts towards three different targets with robotic guidance on either 0%, 50%, or 100% of acquisition trials. Only the 50% guidance group statistically reduced both the ball endpoint distance and variability between the pre-test and the immediate or 24-hr post-test. The results of the 50% guidance group yielded seminal evidence that combining both unassisted and robotic guidance trials (i.e., mixed practice) could facilitate at least short-term motor learning for a golf putting task. Such work is relevant to incorporating robotic guidance in sport skills and other practical areas (e.g., rehabilitation).

Explaining Individual Differences in Fine Motor Performance and Learning in Older Adults: The Contribution of Muscle Strength and Cardiovascular Fitness.

It remains controversial whether aging influences motor learning and whether physiological factors, such as local strength or fitness, are associated with fine motor performance and learning in older adults (OA). OA (n = 51) and young adults (YA, n = 31) performed a short-term motor learning session using a precision grip force modulation task. The rate of improvement of OA compared with YA was steeper with respect to performance variability and temporal precision. Both age groups showed positive transfer during an unpracticed variant of the force modulation task. Local muscle strength (pinch and grip strength) and high cardiovascular fitness positively predicted fine motor performance, whereas initial performance, muscle strength, and motor fitness (heterogeneous motor test battery) negatively predicted rate of improvement. Analyses indicated potentials, but also limits of plasticity for OA.

P22 Cerebellar network neuromodulation improves short-term motor learning in Parkinson’s disease

P22 Cerebellar network neuromodulation improves short-term motor learning in Parkinson’s disease

Connexin43 in neonatal excitatory neurons is important for short-term motor learning

In the neocortex, gap junctions are expressed at very early developmental stages, and they are involved in many processes such as neurogenesis, neuronal migration and synapse formation. Connexin43 (Cx43), a gap junction protein, has been found to be abundantly expressed in radial glial cells, excitatory neurons and astrocytes. Although accumulating evidence suggests that Cx43-mediated gap-junctional coupling between astrocytes plays an important role in the central nervous system, the function of Cx43 in early excitatory neurons remains elusive. To investigate the impact of Cx43 deficiency in excitatory neurons at early postnatal stages, we conditionally knocked out Cx43 in excitatory neurons under the Emx1 promoter by tamoxifen induction. We found that deletion of Cx43 around birth did not impair the laminar distribution of excitatory neurons in the neocortex. Moreover, mice with Cx43 deletion during the early postnatal stages had normal anxiety-like behaviors, depression-related behaviors, learning and memory-associated behaviors at adolescent stages. However, Cx43 conditional knockout mice exhibited impaired motor-learning behavior. These results suggested that Cx43 expression in excitatory neurons at early postnatal stages contributes to short-term motor learning capacity.

Subthalamic neuromodulation improves short-term motor learning in Parkinson’s disease

The basal ganglia and cerebellum are implicated in both motor learning and Parkinson's disease. Deep brain stimulation (DBS) is an established treatment for advanced Parkinson's disease that leads to motor and non-motor effects by modulating specific neural pathways. Recently, a disynaptic projection from the subthalamic nucleus (STN) to cerebellar hemispheres was discovered. To investigate the functional significance of this pathway in motor learning, short-term improvement in motor execution in 20 patients with Parkinson's disease on and off STN-DBS and 20 age-matched healthy controls was studied in a visuomotor task combined with whole-brain connectomics. Motor learning was impaired in Parkinson's disease off stimulation but was partially restored through DBS. Connectivity between active DBS contacts and a distributed network of brain regions correlated with improvement in motor learning. Region of interest analysis revealed connectivity from active contact to cerebellar hemisphere ipsilateral to hand movement as the strongest predictor for change in motor learning. Peak predictive voxels in the cerebellum localized to Crus II of lobule VII, which also showed higher STN than motor cortex connectivity, suggestive of a connection surpassing motor cortex. Our findings provide new insight into the circuit nature of Parkinson's disease and the distributed network effects of DBS in motor learning.

Cortical beta oscillations are associated with motor performance following visuomotor learning

People vary in their capacity to learn and retain new motor skills. Although the relationship between neuronal oscillations in the beta frequency range (15–30 Hz) and motor behaviour is well established, the electrophysiological mechanisms underlying individual differences in motor learning are incompletely understood. Here, we investigated the degree to which measures of resting and movement-related beta power from sensorimotor cortex account for inter-individual differences in motor learning behaviour in the young and elderly. Twenty young (18–30 years) and twenty elderly (62–77 years) healthy adults were trained on a novel wrist flexion/extension tracking task and subsequently retested at two different time points (45–60 min and 24 h after initial training). Scalp EEG was recorded during a separate simple motor task before each training and retest session.Although short-term motor learning was comparable between young and elderly individuals, there was considerable variability within groups with subsequent analysis aiming to find the predictors of this variability. As expected, performance during the training phase was the best predictor of performance at later time points. However, regression analysis revealed that movement-related beta activity significantly explained additional variance in individual performance levels 45–60 min, but not 24 h after initial training. In the context of disease, these findings suggest that measurements of beta-band activity may offer novel targets for therapeutic interventions designed to promote rehabilitative outcomes.

Effect of Paired Associative Stimulation on Corticomotor Excitability in Chronic Smokers.

Chronic smoking has been shown to have deleterious effects on brain function and is an important risk factor for ischemic stroke. Reduced cortical excitability has been shown among chronic smokers compared with non-smokers to have a long-term effect and so far no study has assessed the effect of smoking on short-term motor learning. Paired associative stimulation (PAS) is a commonly used method for inducing changes in excitability of the motor cortex (M1) in a way that simulates short-term motor learning. This study employed PAS to investigate the effect of chronic cigarette smoking on plasticity of M1. Stimulator output required to elicit a motor-evoked potential (MEP) of approximately 1 mV was similar between the groups prior to PAS. MEP response to single pulse stimuli increased in the control group and remained above baseline level for at least 30 min after the intervention, but not in the smokers who showed no significant increase in MEP size. The silent period was similar between groups at all time points of the experiment. This study suggests that chronic smoking may have a negative effect on the response to PAS and infers that chronic smoking may have a deleterious effect on the adaptability of M1.

Resting-state brain network features associated with short-term skill learning ability in humans and the influence of N-methyl-d-aspartate receptor antagonism.

Graph theoretical functional magnetic resonance imaging (fMRI) studies have demonstrated that brain networks reorganize significantly during motor skill acquisition, yet the associations between motor learning ability, brain network features, and the underlying biological mechanisms remain unclear. In the current study, we applied a visually guided sequential pinch force learning task and graph theoretical analyses to investigate the associations between short-term motor learning ability and resting-state brain network metrics in 60 healthy subjects. We further probed the test-retest reliability (n = 26) and potential effects of the N-methyl-d-aspartate (NMDA) antagonist ketamine (n = 19) in independent healthy volunteers. Our results show that the improvement of motor performance after short-term training was positively correlated with small-worldness (p = 0.032) and global efficiency (p = 0.025), whereas negatively correlated with characteristic path length (p = 0.014) and transitivity (p = 0.025). In addition, using network-based statistics (NBS), we identified a learning ability–associated (p = 0.037) and ketamine-susceptible (p = 0.027) cerebellar-cortical network with fair to good reliability (intraclass correlation coefficient [ICC] > 0.7) and higher functional connectivity in better learners. Our results provide new evidence for the association of intrinsic brain network features with motor learning and suggest a role of NMDA-related glutamatergic processes in learning-associated subnetworks.

Transient visual perturbations boost short-term balance learning in virtual reality by modulating electrocortical activity.

Immersive virtual reality can expose humans to novel training and sensory environments, but motor training with virtual reality has not been able to improve motor performance as much as motor training in real-world conditions. An advantage of immersive virtual reality that has not been fully leveraged is that it can introduce transient visual perturbations on top of the visual environment being displayed. The goal of this study was to determine whether transient visual perturbations introduced in immersive virtual reality modify electrocortical activity and behavioral outcomes in human subjects practicing a novel balancing task during walking. We studied three groups of healthy young adults (5 male and 5 female for each) while they learned a balance beam walking task for 30 min under different conditions. Two groups trained while wearing a virtual reality headset, and one of those groups also had half-second visual rotation perturbations lasting ~10% of the training time. The third group trained without virtual reality. We recorded high-density electroencephalography (EEG) and movement kinematics. We hypothesized that virtual reality training with perturbations would increase electrocortical activity and improve balance performance compared with virtual reality training without perturbations. Our results confirmed the hypothesis. Brief visual perturbations induced increased theta spectral power and decreased alpha spectral power in parietal and occipital regions and improved balance performance in posttesting. Our findings indicate that transient visual perturbations during immersive virtual reality training can boost short-term motor learning by inducing a cognitive change, minimizing the negative effects of virtual reality on motor training. NEW & NOTEWORTHY We found that transient visual perturbations in virtual reality during balance training can boost short-term motor learning by inducing a cognitive change, overcoming the negative effects of immersive virtual reality. As a result, subjects training in immersive virtual reality with visual perturbations have equivalent performance improvement as training in real-world conditions. Visual perturbations elicited cortical responses in occipital and parietal regions and may have improved the brain's ability to adapt to variations in sensory input.

BDNF Val66Met polymorphism is associated with altered activity-dependent modulation of short-interval intracortical inhibition in bilateral M1.

The BDNF Val66Met polymorphism is associated with impaired short-term plasticity in the motor cortex, short-term motor learning, and intermanual transfer of a procedural motor skill. Here, we investigated the impact of the Val66Met polymorphism on the modulation of cortical excitability and interhemispheric inhibition through sensorimotor practice of simple dynamic skills with the right and left first dorsal interosseous (FDI) muscles. To that end, we compared motor evoked potentials (MEP) amplitudes and short-interval intracortical inhibition (SICI) in the bilateral representations of the FDI muscle in the primary motor cortex (M1), and interhemispheric inhibition (IHI) from the left to right M1, before and after right and left FDI muscle training in an alternated sequence. Val66Met participants did not differ from their Val66Val counterparts on motor performance at baseline and following motor training, or on measures of MEP amplitude and IHI. However, while the Val66Val group displayed significant SICI reduction in the bilateral M1 in response to motor training, SICI remained unchanged in the Val66Met group. Further, Val66Val group’s SICI decrease in the left M1, which was also observed following unimanual training with the right hand in the Control Right group, was correlated with motor improvement with the left hand. The potential interaction between left and right M1 activity during bimanual training and the implications of altered activity-dependent cortical excitability on short-term motor learning in Val66Met carriers are discussed.

Achievement of Virtual and Real Objects Using a Short-Term Motor Learning Protocol in People with Duchenne Muscular Dystrophy: A Crossover Randomized Controlled Trial.

To evaluate whether people with Duchenne muscular dystrophy (DMD) practicing a task in a virtual environment could improve performance given a similar task in a real environment, as well as distinguishing whether there is transference between performing the practice in virtual environment and then a real environment and vice versa. Twenty-two people with DMD were evaluated and divided into two groups. The goal was to reach out and touch a red cube. Group A began with the real task and had to touch a real object, and Group B began with the virtual task and had to reach a virtual object using the Kinect system. ANOVA showed that all participants decreased the movement time from the first (M = 973 ms) to the last block of acquisition (M = 783 ms) in both virtual and real tasks and motor learning could be inferred by the short-term retention and transfer task (with increasing distance of the target). However, the evaluation of task performance demonstrated that the virtual task provided an inferior performance when compared to the real task in all phases of the study, and there was no effect for sequence. Both virtual and real tasks promoted improvement of performance in the acquisition phase, short-term retention, and transfer. However, there was no transference of learning between environments. In conclusion, it is recommended that the use of virtual environments for individuals with DMD needs to be considered carefully.

Functional performance comparison between real and virtual tasks in older adults: A cross-sectional study.

Introduction:Ageing is usually accompanied by deterioration of physical abilities, such as muscular strength, sensory sensitivity, and functional capacity, making chronic diseases, and the well-being of older adults new challenges to global public health.Objective:The purpose of this study was to evaluate whether a task practiced in a virtual environment could promote better performance and enable transfer to the same task in a real environment.Method:The study evaluated 65 older adults of both genders, aged 60 to 82 years (M = 69.6, SD = 6.3). A timing coincident task was applied to measure the perceptual-motor ability to perform a motor response. The participants were divided into 2 groups: started in a real interface and started in a virtual interface.Results:All subjects improved their performance during the practice, but improvement was not observed for the real interface, as the participants were near maximum performance from the beginning of the task. However, there was no transfer of performance from the virtual to real environment or vice versa.Conclusions:The virtual environment was shown to provide improvement of performance with a short-term motor learning protocol in a timing coincident task. This result suggests that the practice of tasks in a virtual environment seems to be a promising tool for the assessment and training of healthy older adults, even though there was no transfer of performance to a real environment.Trial registration:ISRCTN02960165. Registered 8 November 2016.

Behavioral and neural effects of congruency of visual feedback during short-term motor learning

Visual feedback can facilitate or interfere with movement execution. Here, we describe behavioral and neural mechanisms by which the congruency of visual feedback during physical practice of a motor skill modulates subsequent performance gains. 18 healthy subjects learned to execute rapid sequences of right hand finger movements during fMRI scans either with or without visual feedback. Feedback consisted of a real-time, movement-based display of virtual hands that was either congruent (right virtual hand movement), or incongruent (left virtual hand movement yoked to the executing right hand). At the group level, right hand performance gains following training with congruent visual feedback were significantly higher relative to training without visual feedback. Conversely, performance gains following training with incongruent visual feedback were significantly lower. Interestingly, across individual subjects these opposite effects correlated. Activation in the Supplementary Motor Area (SMA) during training corresponded to individual differences in subsequent performance gains. Furthermore, functional coupling of SMA with visual cortices predicted individual differences in behavior. Our results demonstrate that some individuals are more sensitive than others to congruency of visual feedback during short-term motor learning and that neural activation in SMA correlates with such inter-individual differences.

Limited generalization with varied, as compared to specific, practice in short-term motor learning

The schema theory of learning predicts that varied training in motor learning should give rise to better transfer than specific training. For example, throwing beanbags during practice to targets 5 and 9ft away should better generalize to targets 7 and 11ft away, as compared to only throwing to a target 7ft away. In this study, we tested this prediction in a throwing task, when the pretest, practice, and posttest were all completed within an hour. Participants in the varied group practiced throwing at 5 and 9ft targets, while participants in the specific group practiced throwing at 7ft only. All participants reliably reduced errors from pretest to posttest. The varied group never outperformed the specific group at the 7ft target (the trained target for the specific group). They did not reliably outperform the specific group at 11ft, either. The numerically better performance at 11ft by the varied group was due, as it turned out in a subsequent experiment, to the fact that 11ft was closer to 9ft (one of the two training targets for the varied group) than to 7ft (the training target for the specific group). We conclude that varied training played a very limited role in short-term motor learning.