Motor Learning Process Research Articles

Changes in corticospinal drive to spinal motoneurones following visuo‐motor skill learning in humans

We have previously demonstrated an increase in the excitability of the leg motor cortical area in relation to acquisition of a visuo-motor task in healthy humans. It remains unknown whether the interaction between corticospinal drive and spinal motoneurones is also modulated following motor skill learning. Here we investigated the effect of visuo-motor skill training involving the ankle muscles on the coupling between electroencephalographic (EEG) activity recorded from the motor cortex (Cz) and electromyographic (EMG) activity recorded from the left tibialis anterior (TA) muscle in 11 volunteers. Coupling in the time (cumulant density function) and frequency domains (coherence) between EEG-EMG and EMG-EMG activity were calculated during tonic isometric dorsiflexion before and after 32 min of training a visuo-motor tracking task involving the ankle muscles or performing alternating dorsi- and plantarflexion movements without visual feedback. A significant increase in EEG-EMG coherence around 15-35 Hz was observed following the visuo-motor skill session in nine subjects and in only one subject after the control task. Changes in coherence were specific to the trained muscle as coherence for the untrained contralateral TA muscle was unchanged. EEG and EMG power were unchanged following the training. Our results suggest that visuo-motor skill training is associated with changes in the corticospinal drive to spinal motorneurones. Possibly these changes reflect sensorimotor integration processes between cortex and muscle as part of the motor learning process.

Cognition, schizophrénie et effet des antipsychotiques : le point de vue d’un laboratoire de recherche clinique

Cognition, schizophrénie et effet des antipsychotiques : le point de vue d’un laboratoire de recherche clinique

Transcranial DC stimulation (tDCS): A tool for double-blind sham-controlled clinical studies in brain stimulation

Objective Brain polarization in the form of transcranial direct current stimulation (tDCS), which influences motor function and learning processes, has been proposed as an adjuvant strategy to enhance training effects in Neurorehabilitation. Proper testing in Neurorehabilitation requires double-blind sham-controlled study designs. Here, we evaluated the effects of tDCS and sham stimulation (SHAM) on healthy subjects and stroke patients' self-report measures of attention, fatigue, duration of elicited sensations and discomfort. Methods tDCS or SHAM was in all cases applied over the motor cortex. Attention, fatigue, and discomfort were self rated by study participants using visual analog scales. Duration of perceived sensations and the ability to distinguish tDCS from Sham sessions were determined. Investigators questioning the patients were blind to the intervention type. Results tDCS and SHAM elicited comparably minimal discomfort and duration of sensations in the absence of differences in attention or fatigue, and could not be distinguished from SHAM by study participants nor investigators. Conclusions Successful blinding of subjects and investigators and ease of application simultaneously with training protocols supports the feasibility of using tDCS in double-blind, sham-controlled randomized trials in clinical Neurorehabilitation. Significance tDCS could evolve into a useful tool, in addition to TMS, to modulate cortical activity in Neurorehabilitation.

Analysis of Muscle Activity Patterns between Two Different Walking Exercise Programs-Qualitative Analysis of Walking Exercise for the Amputee

While many studies have investigated muscle activity in amputated legs while walking, in physical therapy and other fields, few studies have examined muscle activity in the healthy legs of amputees. Furthermore, to the best of our knowledge, no previous investigations have examined the motor learning processes in leg amputees or efficient exercise programs for walking with a leg prosthesis. Our previous study clarified the function of the non-amputated legs of amputees while walking with a prosthetic leg by measuring muscle activity patterns using surface electromyography and ground reaction force plates. In the present study, healthy volunteers were asked to wear a pseudo-prosthetic leg and participate in either a basic or applied exercise program using clearly different exercises. Differences in muscle activity patterns between the programs were then analyzed. After 2 weeks of exercises, the exercise program allowing legs without a pseudo-prosthesis to function more like the non-amputated legs of amputees who were skilled at walking with their prosthesis was ascertained. Muscle activity patterns of volunteers on the applied exercise program tended to more closely resemble those of amputees.

Rapid Plastic Changes of Human Primary Motor Cortex with Repetitive Motor Practice and Transcranial Magnetic Stimulation

Excitability changes of human primary motor cortex are assumed to be associated with motor learning processes. To examine motor behavioral and neural mechanisms in these processes, the adaptive motor learning processes of the index finger abduction were investigated using motor evoked potential (MEP) elicited from the first dorsal interosseous and extensor carpi radialis muscles. Practice effects were examined on changes of MEP amplitudes elicited from these muscles during motor imagery. Given general consensus that the MEP amplitude change during motor imagery is a useful parameter reflecting changes in excitability of the human primary motor cortex, the present results, that MEP amplitudes of both muscles increased with repeated practice by the index finger abduction and that magnitudes of MEP amplitudes of both muscles (motor learning curves) were clearly different, suggested that participation of the muscles performing the index finger abduction gradually changed with practice. Short-term plastic changes of human primary motor cortex occur with repetitive practice and such adaptive change in human primary motor cortex is expressed in human voluntary movement that becomes more automatic.

Functional imaging of changes in cerebellar activity related to learning during a novel eye–hand tracking task

Coordination between the eyes and the hand is likely to be based on a process of motor learning, so that the interactions between the two systems can be accurately controlled. By using an unusual tracking task we measured the change in brain activation levels, as recorded with 3T functional magnetic resonance imaging (fMRI), between naïve human subjects and the same subjects after a period of extended training. Initially the performance of the two groups was similar. One subject group was then trained in a synchronous, coordinated, eye-hand task; the other group trained with a 304 ms temporal offset between hand and eye tracking movements. After training, different patterns of performance were observed for the groups, and different functional activation profiles. Significant change in the relationship between functional activation levels and eye-hand task conditions was predominantly restricted to visuo-motor areas of the lateral and vermal cerebellum. In an additional test with one of the subject groups, we show that there was increased cerebellar activation after learning, irrespective of change in performance error. These results suggest that two factors contribute to the measured blood oxygen level-dependent (BOLD) signal. One declined with training and may be directly related to performance error. The other increased after training, in the test conditions nearest to the training condition, and may therefore be related to acquisition of experience in the task. The loci of activity changes suggest that improved performance is because of selective modified processing of ocular and manual control signals within the cerebellum. These results support the suggestion that coordination between eye and hand movement is based on an internal model acquired by the cerebellum that provides predictive signals linking the control of the two effectors.

Associative conditioning with leg cycling and inspiratory resistance enhances the early exercise ventilatory response in humans.

Repeated trials of hypercapnic exercise [deltaPET CO2 = 7 (1) mmHg] augment the increase in inspired minute ventilation and tidal volume (V(T)) in the early phase of subsequent trials of unencumbered exercise alone. The increase in V(T) in the first 20 s of exercise was correlated to the increase in V(T) evoked during hypercapnic exercise trials, suggesting that the evoked increase in V(T) during conditioning may be a factor in mediating associative conditioning. To test this hypothesis, inspiratory resistive loading (IRL) was employed to evoke an increase in V(T) [deltaV(T) = 0.4 (0.1) I(BTPS)] during conditioning exercise trials [IRL + EX; deltaP(ET)CO2 = 2 (l) mmHg]. IRL + EX associative conditioning elicited a significant augmentation of the early minute ventilation (+46%) and V(T) (+100%) responses to subsequent unencumbered exercise. The latter was correlated to the evoked increase in V(T) during associative conditioning with IRL + EX. The results support the hypothesis that an evoked increase in V(T) during associative conditioning could be a factor in eliciting long-term modulation of minute ventilation in subsequent unencumbered exercise. The results further indicated that the modulation of ventilation early in exercise is not due to sensitisation to repeated trials of either IRL or exercise alone. Associative conditioning may shape the ventilatory response to exercise through a process of motor learning. Data are presented as mean (SEM) unless otherwise stated.

The role of memory consolidation in motor learning: a positron emission tomography study

While it has been well documented that the process of motor learning is accompanied by a shift in cortical processing regions, there has been little investigation into the effects of memory consolidation. The present study builds on earlier work and aims to investigate changes in the functional anatomy of motor learning that occur when the process of motor memory consolidation is disrupted. Ten healthy, right-handed males took part in the new experimental protocol. A star shape was presented to the subject on a computer monitor positioned above the PET gantry. During each trial, the subject used a ‘Felix’ computer-pointing device to guide a small red dot around the star shape in an anticlockwise direction. Subjects were instructed to perform the trace as quickly and accurately as possible using their left hand. After the 10th trial, the Felix was reconfigured so that hand movements were ‘mirrored’ on the computer screen. In the original study, subjects performed the mirror task 15 times while in the second study a distracter task was inserted between each mirror trial in order to disrupt memory consolidation. PET images were recorded during the seventh trial and then every other trial, culminating in 10 images. The resulting images were analysed using the Minoshima analysis package and the two groups were compared to determine the effects of disrupting memory consolidation. The results showed that there was less transfer from frontal and parietal areas to the occipital and primary motor cortices in the second study. This suggests that interference with motor memory consolidation disrupts the shifts in cortical activation normally seen in motor learning.

Motor processing after movement execution as revealed by evoked and induced activity

Event-related synchronization (ERS) in the beta frequency band following movement execution has shown that motor processing is not completed yet when a movement ends. It is known that induced and evoked activities reflect different aspects of cortical processing which may result in different time courses. In the current study, we analyzed topography of postimperative negative variation (PINV) in 39 healthy right-handed adolescents in an acoustic forewarned reaction time (contingent negative variation, CNV) task using a 64-electrode high-density sensor array. We dissociated different PINV components in their time course from postmovement beta ERS in order to provide fundamental knowledge about evoked and induced EEG components after movement execution as a basis for further analysis of postmovement processing. A postmovement negativity occurred from about 500 to 1200 ms after the imperative stimulus (peaking about 600 ms after a right-hand button press) at central electrodes, contralateral to the response movement side. Current source density (CSD) analysis confirmed the current sinks over motor areas [contralateral primary motor/premotor and supplementary/cingulate motor area]. The described DC component (motor PINV, mPINV) differed in time course and localization from later “classical” PINV (cPINV) which is thought to reflect contingency reappraisal. mPINV could also be distinguished topographically from a mere delayed CNV resolution. When mPINV and ERS at the same left central electrode were compared, both parameters showed different time courses. Left central mPINV rather paralleled ERS at midcentral electrodes. Therefore, we suggest that the topography of mPINV provides first hints towards an involvement of contralateral primary motor cortex in postmovement processing beyond a mere idling state as reflected by later beta ERS. mPINV could be a useful tool to investigate the role of primary motor cortex in motor-learning processes. The combined analysis of induced and evoked activities seems to be able to elucidate different aspects of cortical connectivity and motor processes following movement.

Motor processing after movement execution as revealed by evoked and induced activity

Event-related synchronization (ERS) in the beta frequency band following movement execution has shown that motor processing is not completed yet when a movement ends. It is known that induced and evoked activities reflect different aspects of cortical processing which may result in different time courses. In the current study, we analyzed topography of postimperative negative variation (PINV) in 39 healthy right-handed adolescents in an acoustic forewarned reaction time (contingent negative variation, CNV) task using a 64-electrode high-density sensor array. We dissociated different PINV components in their time course from postmovement beta ERS in order to provide fundamental knowledge about evoked and induced EEG components after movement execution as a basis for further analysis of postmovement processing. A postmovement negativity occurred from about 500 to 1200 ms after the imperative stimulus (peaking about 600 ms after a right-hand button press) at central electrodes, contralateral to the response movement side. Current source density (CSD) analysis confirmed the current sinks over motor areas [contralateral primary motor/premotor and supplementary/cingulate motor area]. The described DC component (motor PINV, mPINV) differed in time course and localization from later “classical” PINV (cPINV) which is thought to reflect contingency reappraisal. mPINV could also be distinguished topographically from a mere delayed CNV resolution. When mPINV and ERS at the same left central electrode were compared, both parameters showed different time courses. Left central mPINV rather paralleled ERS at midcentral electrodes. Therefore, we suggest that the topography of mPINV provides first hints towards an involvement of contralateral primary motor cortex in postmovement processing beyond a mere idling state as reflected by later beta ERS. mPINV could be a useful tool to investigate the role of primary motor cortex in motor-learning processes. The combined analysis of induced and evoked activities seems to be able to elucidate different aspects of cortical connectivity and motor processes following movement.

Infant grasp learning: a computational model.

This paper presents ILGM (the Infant Learning to Grasp Model), the first computational model of infant grasp learning that is constrained by the infant motor development literature. By grasp learning we mean learning how to make motor plans in response to sensory stimuli such that open-loop execution of the plan leads to a successful grasp. The open-loop assumption is justified by the behavioral evidence that early grasping is based on open-loop control rather than on-line visual feedback. Key elements of the infancy period, namely elementary motor schemas, the exploratory nature of infant motor interaction, and inherent motor variability are captured in the model. In particular we show, through computational modeling, how an existing behavior (reaching) yields a more complex behavior (grasping) through interactive goal-directed trial and error learning. Our study focuses on how the infant learns to generate grasps that match the affordances presented by objects in the environment. ILGM was designed to learn execution parameters for controlling the hand movement as well as for modulating the reach to provide a successful grasp matching the target object affordance. Moreover, ILGM produces testable predictions regarding infant motor learning processes and poses new questions to experimentalists.

Facilitative effect of high frequency subthreshold repetitive transcranial magnetic stimulation on complex sequential motor learning in humans

We investigated the effect of repetitive transcranial magnetic stimulation (rTMS) applied to the motor cortex, on the motor learning of sequential finger movements. Fifteen healthy subjects were trained to perform seven sequential finger movements of the left hand. Ten Hertz or sham rTMS with a resting motor threshold of 80% was applied to each subject during the task period. Stimulation with 10 Hz rTMS produced a better learning performance in terms of target score and execution time than sham stimulation. We conclude that high-frequency rTMS may modulate the excitability of the motor cortex and facilitate the sequential motor learning process in normal subjects. These findings may provide a basis for the development of therapeutic applications of rTMS in patients with impaired motor skill.

Cerebellar activation during leg withdrawal reflex conditioning: an fMRI study.

The aim of the present study was to examine cerebellar areas related to conditioning of the nociceptive leg withdrawal reflex using event-related functional magnetic resonance imaging (fMRI). Because of the aversive nature of the unconditioned stimulus effects of accompanying fear conditioning were expected. In 20 healthy adult subjects leg withdrawal reflex conditioning was performed using a standard delay protocol during MR-scanning. Electromyographic recordings from the anterior tibial and biceps femoris muscles were used to quantify conditioned responses. Fear-related changes of heart rate were assessed. In the group of all subjects a significant increase of cerebellar activation was found in the anterior and posterior vermis. In the group of subjects (n=9) who showed conditioned leg withdrawal responses cerebellar activation was more pronounced in parts of the anterior vermis, which correspond to the known leg representation. In the group of subjects (n=11) who did not develop conditioned responses cerebellar activation was more pronounced in the posterolateral hemispheres. Changes of heart rate, however, did not significantly differ between groups. Results suggest that areas within the anterior vermis are involved in conditioning of the leg withdrawal response. The present results, however, do not allow to differentiate between motor performance, learning or timing-related processes. Areas in the posterior vermis and cerebellar hemispheres may be related to concomitant fear conditioning. Results of the present event-related fMRI study suggest involvement of the human cerebellum in conditioning of the nociceptive leg withdrawal response.

Sleep and the Time Course of Motor Skill Learning

Growing evidence suggests that sleep plays an important role in the process of procedural learning. Most recently, sleep has been implicated in the continued development of motor-skill learning following initial acquisition. However, the temporal evolution of motor learning before and after sleep, the effects of different training regimens, and the long-term development of motor learning across multiple nights of sleep remain unknown. Here, we report data for subjects trained and retested on a sequential finger-tapping task across multiple days. The findings demonstrate firstly that following initial training, small practice-dependent improvements are possible before, but not following the large practice-independent gains that develop across a night of sleep. Secondly, doubling the quantity of initial training does not alter the amount of subsequent sleep-dependent learning that develops overnight. Thirdly, the amount of sleep-dependent learning does not correlate with the amount of practice-dependent learning achieved during training, suggesting the existence of two discrete motor-learning processes. Finally, whereas the majority of sleep-dependent motor-skill learning develops during the first night of sleep following training, additional nights of sleep still offer continued improvements.

Dissociation of visual associative and motor learning in Drosophila at the flight simulator.

Ever since operant conditioning was studied experimentally, the relationship between associative learning and possible motor learning has become controversial. Although motor learning and its underlying neural substrates have been extensively studied in mammals, it is still poorly understood in invertebrates. The visual discriminative avoidance paradigm of Drosophila at the flight simulator has been widely used to study the flies' visual associative learning and related functions, but it has not been used to study the motor learning process. In this study, newly-designed data analysis was employed to examine the flies' solitary behavioural variable that was recorded at the flight simulator-yaw torque. Analysis was conducted to explore torque distributions of both wild-type and mutant flies in conditioning, with the following results: (1) Wild-type Canton-S flies had motor learning performance in conditioning, which was proved by modifications of the animal's behavioural mode in conditioning. (2) Repetition of training improved the motor learning performance of wild-type Canton-S flies. (3) Although mutant dunce(1) flies were defective in visual associative learning, they showed essentially normal motor learning performance in terms of yaw torque distribution in conditioning. Finally, we tentatively proposed that both visual associative learning and motor learning were involved in the visual operant conditioning of Drosophila at the flight simulator, that the two learning forms could be dissociated and they might have different neural bases.

Case studies of appropriate teacher feedback in gymnastic units at elementary school level

This study examines teacher feedback within the context of students'motor learning process in gymnastic units, with particular foeus on the question of what constitutes appropriate corrective feedback between teacher and students, who are failing in a given task. The study analyzes the contents and outcome of teacher feedback in the motor learning process (with focus on the challenge-level of the task, the point of failure as well as content of feedback for solving the students'problem), and shows that motor skills of students changed according to feedback content and the students'perception of the feedback situation.The study is based on case studies of two gymnastic units (a total of 15 classes), and participants included two elementary school teachers and 63 students from elementary school (sixth grade). Through the case studies various types of data were gathered: verbal interaction between teacherand students was recorded via a microphone attached to the teacher, while nonverbal interaction between teacher and students was recorded with a video camera. In addition, student participants filled out questionnaires concerning teacher feedback received in each class.Our results indicate that when a student attempts tasks at a moderately challenging level but fails, then appropriate and specific feedback from the teacher to solve the problem in most cases causes improvement in the student's motor skills. Feedback of this charactar was generally perceived by students to be “useful advice”, which was also the case among students who failed to improve their motor skills despite having received feedback. Our findings indicate the importance of appropriate and specific feedback when seeking ways of helping students to improve motor skills.

Specific functions of the motor cortex in reorganizing coordinations during motor training in animals and humans.

The involvement of the motor cortex in learning movements has recently attracted much attention. One aspect of motor learning is the inhibition of innate synergies which interfere with performance of the acquired movement. Various models of operant responses in dogs have demonstrated the critical role of the motor cortex in the reorganization and inhibition of interfering synergies during learning. The role of the motor cortex and corticospinal influences in the formation of new coordinations in humans was studied here in patients with organic lesions of the cerebral circulation involving the internal capsule, using postural coordination and movements in a bimanual unloading response as an example. Formation of the forearm stabilization response was deeply lesioned on the afflicted side. Some degree of impairment was also seen on the ipsilateral side, but it was no different from the level of learning impairment in patients with lesions not involving the internal capsule or in patients with parkinsonism. The existence of specific contralateral influences of the motor cortex and non-specific descending influences on the process of motor learning is proposed.

Effect of nitric oxide synthase inhibition on the manipulative behaviour of Sepia officinalis

Nitric oxide (NO), produced by nitric oxide synthase (NOS) in brain tissue, is essential for a variety of kinds of learning in vertebrates. In invertebrates, there are clear examples of an association between NO signalling and olfaction, feeding behaviour and learning. The role of NO as a neurotransmitter in the manipulative behaviour of Sepia officinalis was tested. Manipulative behaviour requires extensive chemotactile sensory processing, fine motor control and probably motor learning processes. NADPH-diaphorase activity (a reliable histochemical marker for nitric oxide synthase) was found in sensory epithelia and in the axial nerve cord of the arms. NOS inhibitor injections ( l-NAME) produced an increase in the latency of prey paralysis. By placing mechanical constraints on the base of the fifth periopods of the crab, we prevented the cuttlefish from injecting cephalotoxin and, thus, forced it to change injection sites. We showed that l-NAME pretreatment did not affect the flexibility of the manipulative behaviour. The implications of the involvement of NO in the acquisition of chemo-tactile information and in the programming of the motor skills of the manipulative behaviour is discussed.

Activity of neurons in the pedunculopontine nucleus during a food-related operant conditioned reflex.

The activity of 91 neurons in the compact and diffuse zones of the pedunculopontine nucleus of freely mobile rabbits was studied during performance of a food-related operant conditioned reflex. A total of 37.4% of the neurons recorded showed reactivity to the conditioned stimulus, which is evidence that the pedunculopontine nucleus is involved in operant learning. A significant predominance of excitatory responses to the conditioned stimulus and to food reinforcement was demonstrated. The main patterns of cell responses were identified, these reflecting the nature of the effect of the conditioned stimulus on neuron activity, the structure of the behavioral act, and the properties of the reinforcement, and demonstrating a relationship between the pedunculopontine nucleus and the processes of attention, motor learning, and reinforcement. Differences were seen in the associative reactive properties of the compact and diffuse zones of the pedunculopontine nucleus to the conditioned stimulus and reinforcement, which is evidence for the functional diversity of this formation and suggests a leading role for the cholinergic compact zone in food-related operant learning and reinforcement, the diffuse zone having a leading role in food-related classical conditioned-reflex learning.

Striatal level of regulation of learned forepaw movements in rats.

The role of the striatal adenylyl cyclase (AC) and cholinergic systems in the learning and expression of new forepaw movements (reaching with prolonged pushing on a fixed piston) was studied in male Wistar rats. Motor learning processes, prenatal hypoxia, and cholinergic drugs changed the properties of the AC system in the striatum. After learning, the striatal basal AC activity was decreased compared to untrained control rats. In addition, the AC activity was more decreased in animals with a good ability to learn compared to poor learners (up to 31 % and 51 %, correspondingly; p<0.01). Rats subjected to prenatal hypoxia (13-14th days of embryogenesis) had a lower ability to learn the new movements requiring tactile control and the striatal AC activity in these rats was 1.8 times higher (p<0.001) than controls. In vitro application of the cholinergic agonist carbachol (CARB) 10-5 M (corresponding to ~ 0.3 g), as well as the antagonist scopolomine (SCOP) 10-5 M (~ 0.3 g) decreased AC activity in the synaptosomal fraction of the striatum. In vivo injections of CARB (0.3-3 g/1l) or SCOP (0.3-3 g/1l) into the ventral striatum (nucleus accumbens) modified the newly learned sensorimotor skill. After CARB injections the rats performed slower movements with more prolonged pushing. After SCOP the rats could not retain the learned pushing movement. These in vivo and in vitro data suggest that the cholinergic mediator system of the striatum is involved in learning sensory-controlled forepaw movements as well as the regulation of new motor skills by modulating the AC signal transduction process in the striatum. The data confirmed that modification of the striatal AC system resulted in the modulation of reaching behavior and better expression of the learned reflex.