Motor Learning Studies Research Articles

Transcranial magnetic stimulation has no placebo effect on motor learning

ObjectiveMotor learning is the core cognitive function in neurorehabilitation and in various other skill-training activities (e.g. sport, music). Therefore, there is an increasing interest in the use of transcranial magnetic stimulation (TMS) methods for its enhancement. However, although usually assumed, a potential placebo effect of TMS methods on motor learning has never been systematically investigated. MethodsImprovement of performance on the Purdue Pegboard Task over three test-blocks (T0, T1, and T2), separated by >20min, was used to evaluate motor learning. In Experiment-1, two groups of 10 participants each were compared: one group immediately before T1 received a sham intermittent theta burst stimulation procedure (P-iTBS group), while another did not have any intervention at all (control – CON group). In Experiment-2, a third group of participants (six subjects) who received sham high-frequency repetitive TMS procedure before T1 (P-rTMS group) was compared with P-iTBS group. ResultsAll three groups showed significant learning over time, but without any difference between them, either in Experiment-1 between P-iTBS and CON, or in Experiment-2 between P-rTMS and P-iTBS. ConclusionThe results suggest lack of any placebo effect of TMS on motor learning. SignificanceThe results may help in designing further TMS–motor learning studies and in interpreting their results.

Separate Contributions of Kinematic and Kinetic Errors to Trajectory and Grip Force Adaptation When Transporting Novel Hand-Held Loads

Numerous studies of motor learning have examined the adaptation of hand trajectories and grip forces when moving grasped objects with novel dynamics. Such objects initially result in both kinematic and kinetic errors; i.e., mismatches between predicted and actual trajectories and between predicted and actual load forces. Here we investigated the contribution of these errors to both trajectory and grip force adaptation. Participants grasped an object with novel dynamics using a precision grip and moved it between two targets. Kinematic errors could be effectively removed using a force channel to constrain hand motion to a straight line. When moving in the channel, participants learned to modulate grip force in synchrony with load force and this learning generalized when movement speed in the channel was doubled. When the channel was removed, these participants continued to effectively modulate grip force but exhibited substantial kinematic errors, equivalent to those seen in participants who did not previously experience the object in the channel. We also found that the rate of grip force adaptation did not depend on whether the object was initially moved with or without a channel. These results indicate that kinematic errors are necessary for trajectory but not grip force adaptation, and that kinetic errors are sufficient for grip force but not trajectory adaptation. Thus, participants can learn a component of the object's dynamics, used to control grip force, based solely on kinetic errors. However, this knowledge is apparently not accessible or usable for controlling the movement trajectory when the channel is removed.

Complexity in Neurobiology: Perspectives from the study of noise in human motor systems

This article serves as an introduction to the themed special issue on "Complex Systems in Neurobiology." The study of complexity in neurobiology has been sensitive to the stochastic processes that dominate the micro-level architecture of neurobiological systems and the deterministic processes that govern the macroscopic behavior of these systems. A large body of research has traversed these scales of interest, seeking to determine how noise at one spatial or temporal scale influences the activity of the system at another scale. In introducing this special issue, we pay special attention to the history of inquiry in complex systems and why scientists have tended to favor linear, causally driven, reductionist approaches in Neurobiology. We follow this with an elaboration of how an alternative approach might be formulated. To illustrate our position on how the sciences of complexity and the study of noise can inform neurobiology, we use three systematic examples from the study of human motor control and learning: 1) phase transitions in bimanual coordination; 2) balance, intermittency, and discontinuous control; and 3) sensorimotor synchronization and timing. Using these examples and showing that noise is adaptively utilized by the nervous system, we make the case for the studying complexity with a perspective of understanding the macroscopic stability in biological systems by focusing on component processes at extended spatial and temporal scales. This special issue continues this theme with contributions in topics as diverse as neural network models, physical biology, motor learning, and statistical physics.

Saccade adaptation improves in response to a gradually introduced stimulus perturbation

A major goal in the study of motor learning is to improve the extent to which subjects adapt their movements in response to errors. Recent attention has focused on the gradual-adaptation paradigm, in which an adaptive stimulus is introduced incrementally, rather than all at once as in conventional adaptation paradigms. However, there is disagreement – even among studies involving the same sensorimotor-learning task – as to the robustness of this approach. In particular, although all studies confirm that retention of learning is improved, not all agree that exposure to a gradual-adaptation paradigm can improve the extent of adaptation that takes place. Also, the paradigm has not previously been studied with saccadic eye movements, which are unique in that they typically lack online error feedback during each movement. To determine the effectiveness of gradual adaptation in this system, we compared saccadic adaptation performed with gradual and conventional adaptation paradigms. We find evidence consistent with more robust adaptation – in the sense of greater extent of adaptation as well as greater retention of learning (larger aftereffects) – in response to a gradual adaptation stimulus. The results suggest the need to develop alternative models of motor learning, as current error-based modeling efforts are unable to account for the increased extent of adaptation when subjects are only exposed to the full adaptive stimulus for a brief time.

Effectiveness of automated locomotor training in patients with acute incomplete spinal cord injury: A randomized controlled multicenter trial

BackgroundA large proportion of patients with spinal cord injury (SCI) regain ambulatory function. However, during the first 3 months most of the patients are not able to walk unsupported. To enable ambulatory training at such an early stage the body weight is partially relieved and the leg movements are assisted by two therapists. A more recent approach is the application of robotic based assistance which allows for longer training duration. From motor learning science and studies including patients with stroke, it is known that training effects depend on the duration of the training. Longer trainings result in a better walking function. The aim of the present study is to evaluate if prolonged robot assisted walking training leads to a better walking outcome in patients with incomplete SCI and whether such training is feasible or has undesirable effects.Methods/DesignPatients from multiple sites with a subacute incomplete SCI and who are not able to walk independently will be randomized to either standard training (3-5 sessions per week, session duration maximum 25 minutes) or an intensive training (3-5 sessions per week, session duration minimum 50 minutes). After 8 weeks of training and 4 months later the walking ability, the occurrence of adverse events and the perceived rate of exertion as well as the patients' impression of change will be compared between groups.Trial registrationThis study is registered at clinicaltrials.gov, identifier: NCT01147185.

Effectiveness of injury prevention programs in female youth soccer: a systematic review

IntroductionThere is growing evidence on the higher vulnerability of the knee in young female soccer players. In adult female soccer populations injury prevention programs had demonstrated positive effects on injury...

Self-Control of Feedback During Motor Learning: Accounting for the Absolute Amount of Feedback Using a Yoked Group With Self-Control Over Feedback

ABSTRACT A traditional control group yoked to a group that self-controls their reception of feedback receives feedback in the same relative and absolute manner. This traditional control group typically does not learn the task as well as the self-control group. Although the groups are matched for the amount of feedback they receive, the information is provided on trials in which the individual may not request feedback if he or she were provided the opportunity. Similarly, individuals may not receive feedback on trials for which it would be a beneficial learning experience. Subsequently, the mismatch between the provision of feedback and the potential learning opportunity leads to a decrement in retention. The present study was designed to examine motor learning for a yoked group with the same absolute amount of feedback, but who could self-control when they received feedback. Increased mental processing of error detection and correction was expected for the participants in the yoked self-control group because of their choice to employ a limited resource in the form of a decreasing amount of feedback opportunities. Participants in the yoked with self-control group committed fewer errors than the self-control group in retention and the traditional yoked group in both the retention and time transfer blocks. The results suggest that the yoked with self-control group was able to produce efficient learning effects and can be a viable control group for further motor learning studies.

Cortical Activation Changes During Simple Motor Task over Repeated Sessions -A Functional Near-infrared Spectroscopy Study-

Recent fMRI studies of human motor function and learning have reported that the magnitude of brain activity involves a decreasing trend over repeated tasks in the absence of improvements in task performance, probably suggesting the effect of habituation. Here we show that similar effect can be detected by NIRS. In experiments, oxygenated hemoglobin (HbO) changes were monitored during a finger tapping task over repeated sessions. Results showed that task-related brain activity exhibited a decreasing trend on motor-related areas over the sessions. These suggest that measurements of NIRS may exhibit the brain-induced trends over repetition of simple motor tasks.

Localization and sex-difference of steroid receptor coactivator-1 immunoreactivities in the brain of adult female and male mice

Females and males are different in brain and behaviors. These differences are mediated by steroids and their nuclear receptors which require coactivators to regulate the transcription of target genes. Studies have shown that these coactivators are critical for modulating steroid hormone action in the brain. Steroid receptor coactivator-1 has been implied in the regulation of reproduction, stress, motor learning, and limited studies have reported the sex-specific difference of SRC-1 mRNA or protein expression in specific brain regions, but the expression and differences of SRC-1 immunoreactivities in adult female and male brain remain unclear. In this study we reported that in both sexes, high levels of SRC-1 immunoreactivities were detected in olfactory bulb, cerebral cortex, hippocampus, Purkinje cells, some limited diencephalon and brainstem nuclei. The immunopositive materials were predominantly detected in cell nucleus, but in some regions they were also detected in the processes or fiber-like structures. In most of the brain regions studied, males possessed significantly higher levels of SRC-1 immunoreactivities than that of females. Higher levels of SRC-1 were detected in some nuclei related to learning and memory, motor regulation and reproduction indicated its potential roles in neurodegeneration and sex-dependent behavior and structure; the region- and sex-specific localization of SRC-1 immunoreactivities in agreement with that of some steroid receptors, indicating this coactivator play important roles in these hormone-reactive regions and cell groups related to reproduction, learning and memory, integration of motor and sense.

Rapid Adaptation of Visual Search in Simulated Hemianopia

Patients with homonymous hemianopia have altered visual search patterns, but it is unclear how rapidly this develops and whether it reflects a strategic adaptation to altered perception or plastic changes to tissue damage. To study the temporal dynamics of adaptation alone, we used a gaze-contingent display to simulate left or right hemianopia in 10 healthy individuals as they performed 25 visual search trials. Visual search was slower and less accurate in hemianopic than in full-field viewing. With full-field viewing, there were improvements in search speed, fixation density, and number of fixations over the first 9 trials, then stable performance. With hemianopic viewing, there was a rapid shift of fixation into the blind field over the first 5-7 trials, followed by continuing gradual improvements in completion time, number of fixations, and fixation density over all 25 trials. We conclude that in the first minutes after onset of hemianopia, there is a biphasic pattern of adaptation to altered perception: an early rapid qualitative change that shifts visual search into the blind side, followed by more gradual gains in the efficiency of using this new strategy, a pattern that has parallels in other studies of motor learning.

Contributions of Spatial Working Memory to Visuomotor Learning

Previous studies of motor learning have described the importance of cognitive processes during the early stages of learning; however, the precise nature of these processes and their neural correlates remains unclear. The present study investigated whether spatial working memory (SWM) contributes to visuomotor adaptation depending on the stage of learning. We tested the hypothesis that SWM would contribute early in the adaptation process by measuring (i) the correlation between SWM tasks and the rate of adaptation, and (ii) the overlap between the neural substrates of a SWM mental rotation task and visuomotor adaptation. Participants completed a battery of neuropsychological tests, a visuomotor adaptation task, and an SWM task involving mental rotation, with the latter two tasks performed in a 3.0-T MRI scanner. Performance on a neuropsychological test of SWM (two-dimensional mental rotation) correlated with the rate of early, but not late, visuomotor adaptation. During the early, but not late, adaptation period, participants showed overlapping brain activation with the SWM mental rotation task, in right dorsolateral prefrontal cortex and the bilateral inferior parietal lobules. These findings suggest that the early, but not late, phase of visuomotor adaptation engages SWM processes.

Motor control theories and their applications

We describe several influential hypotheses in the field of motor control including the equilibrium-point (referent configuration) hypothesis, the uncontrolled manifold hypothesis, and the idea of synergies based on the principle of motor abundance. The equilibrium-point hypothesis is based on the idea of control with thresholds for activation of neuronal pools; it provides a framework for analysis of both voluntary and involuntary movements. In particular, control of a single muscle can be adequately described with changes in the threshold of motor unit recruitment during slow muscle stretch (threshold of the tonic stretch reflex). Unlike the ideas of internal models, the equilibrium-point hypothesis does not assume neural computations of mechanical variables. The uncontrolled manifold hypothesis is based on the dynamic system approach to movements; it offers a toolbox to analyze synergic changes within redundant sets of elements related to stabilization of potentially important performance variables. The referent configuration hypothesis and the principle of abundance can be naturally combined into a single coherent scheme of control of multi-element systems. A body of experimental data on healthy persons and patients with movement disorders are reviewed in support of the mentioned hypotheses. In particular, movement disorders associated with spasticity are considered as consequences of an impaired ability to shift threshold of the tonic stretch reflex within the whole normal range. Technical details and applications of the mentioned hypo-theses to studies of motor learning are described. We view the mentioned hypotheses as the most promising ones in the field of motor control, based on a solid physical and neurophysiological foundation.

Changes in muscle directional tuning parallel feedforward adaptation to a visuomotor rotation

When people learn to reach in a novel sensorimotor environment, there are changes in the muscle activity required to achieve task goals. Here, we assessed the time course of changes in muscle directional tuning during acquisition of a new mapping between visual information and isometric force production in the absence of feedback-based error corrections. We also measured the influence of visuomotor adaptation on corticospinal excitability, to test whether any changes in muscle directional tuning are associated with adaptations in the final output components of the sensorimotor control system. Nine right-handed subjects performed a ballistic, center-out isometric target acquisition task with the right wrist (16 targets spaced every 22.5 degrees in the joint space). Surface electromyography was recorded from four major wrist muscles, and motor evoked potentials induced by transcranial magnetic stimulation were measured at baseline, after task execution in the absence of the rotation (A1), after adaptation to the rotation (B), and after a final block of trials without rotation (A2). Changes in the directional tuning of muscles closely matched the rotation of the directional error in force, indicating that the functional contribution of muscles remained consistent over the adaptation period. In contrast to previous motor learning studies, we found only minor changes in the amount of muscular activity and no increase in corticospinal excitability. These results suggest that increased muscle co-activation occurs only when the dynamics of the limb are perturbed and/or that online error corrections or altered force requirements are necessary to elicit a component of the adaptation in the final steps of the transformation between motor goal and muscle activation.

How studies of motor learning and effects of brain stimulation in animal and human models may contribute to more effective neurorehabilitative strategies

How studies of motor learning and effects of brain stimulation in animal and human models may contribute to more effective neurorehabilitative strategies

Visual Cues Signaling Object Grasp Reduce Interference in Motor Learning

Recent motor learning studies show that human subjects and nonhuman primates form neural representations of novel mechanical environments and associated forces. Whereas proficient adaptation is seen for a single force field, when faced with multiple novel force environments, movement performance and in particular the ability to switch between different force environments declines. It is difficult to reconcile these findings with the notion that primates can proficiently switch between multiple motor skills. Conceivably, particular kinds of sensory, cognitive, or perceptual contextual cues are required. This study examined the effect of visual feedback on motor learning, in particular, cues that simulated interaction with a virtual object. A robot arm was used to deliver novel patterns of forces (force fields) to the limb during reaching movements. We tested the possibility that subjects transition more easily between novel forces and their sudden absence when they are accompanied by visual cues that relate to object grasp. We used a virtual display system to present subjects with different kinds of visual feedback during reaching, including illusory feedback, indicating grasp of a virtual object during reaching in the force field, and object release in the absence of forces. Throughout the experiment, subjects in fact maintained grasp of the robot. We found that, indeed, the most effective visual cues were those associating the force field with grasp of the virtual object and the absence of the force field with release of the object. Our findings show more broadly that specific visual cues can protect motor skills from interference.

Long-term motor training induced changes in regional cerebral blood flow in both task and resting states.

Neuroimaging studies of functional activation often only reflect differentiated involvement of brain regions compared between task performance and control states. Signals common for both states are typically not revealed. Previous motor learning studies have shown that extensive motor skill training can induce profound changes in regional activity in both task and control states. To address the issue of brain activity changes in the resting-state, we explored long-term motor training induced neuronal and physiological changes in normal human subjects using functional magnetic resonance imaging (fMRI) and positron emission tomography (PET). Ten healthy subjects performed a finger movement task daily for four weeks, during which three sessions of fMRI images and two sessions of PET images were acquired. Using a classical data analysis strategy, we found that the brain activation increased first and then returned to the pre-training, replicating previous findings. Interestingly, we also observed that motor skill training induced significant increases in regional cerebral blood flow (rCBF) in both task and resting states as the practice progressed. The apparent decrease in activation may actually result from a greater increase in activity in the resting state, rather than a decrease in the task state. By showing that training can affect the resting state, our findings have profound implications for the interpretation of functional activations in neuroimaging studies. Combining changes in resting state with activation data should greatly enhance our understanding of the mechanisms of motor-skill learning.

Bodily movement – The fundamental dimensions

Bodily movement has become an interesting topic in recent philosophy, both in analytic and phenomenological versions. Philosophy from Descartes to Kant defined the human being as a mental subject in a material body. This mechanistic attitude toward the body still lingers on in many studies of motor learning and control. The article shows how alternative philosophical views can give a better understanding of bodily movement. The article starts with Heidegger's contribution to overcoming the subject-object dichotomy and his new understanding of the primacy of the practical involvement with the surrounding world. Heidegger, however, in many ways neglected the role of the human body. Merleau-Ponty took a huge step forward when he focused on the bodily intentionality of our interaction with the world. The next step was taken by Samuel Todes who presented a better understanding of how we are bodily oriented in space. After having seen how the body is oriented outward towards the environment it is proper that the final part of this article goes inward toward the role of bodily awareness and the role of proprioception in human movement. The goal of the presentation is to contribute to a better understanding of what goes on in sport. The article therefore uses examples from sport, especially football, to show the relevance of the new insights for sport studies.

A novel MR-compatible device for providing forces to the human finger during functional neuroimaging studies

Many motor learning experiments involve subjects performing a task while experiencing external force perturbations. However, it is difficult to transfer these tasks to functional magnetic resonance imaging (fMRI) studies, and much of the technology that currently exists to facilitate this is expensive to produce and difficult to use. Here, we report on the design and construction of a novel device (the ‘force coil’) that is simple and inexpensive, and that uses the static magnetic field inside the scanner to provide forces to the human finger. The coil incorporates a potentiometer in the base to allow the recording of angular position. To test whether the magnetic field generated by the current flowing through the coil would interfere with the functional images collected, we compared images from a phantom during the use of the coil at arm's length in a 7T magnet. There was no noticeable interference from the coil at the levels of current used in this experiment, which produced about 10 N of force in a 7T scanner. In conclusion, the force coil is a cheap, easy to operate device which provides forces to the finger inside the scanner without affecting image quality. Designs based on this principle are likely to prove useful in studies of motor learning using fMRI.

Prehistoric Italian Pottery Production

In this paper, I suggest that studies of motor development, learning and memory may provide important insights into technological change and conservatism in prehistoric craft activities. The physical and mental processes involved in the learning and development of highly skilled motor activities result in strongly rooted changes in an individual’s actions and levels of performance. In terms of craft production, this means that mature, skilled artisans have a selective and efficient array of actions and strategies, which they can draw upon to produce competent products of predictable quality and quantity.The flip side of this degree of specialized physical training is, however, the possibility of ‘negative transfer’ when it comes to learning new skills. The presence within late second millennium bc in Italy of both handmade and wheelmade pottery technologies can be explained in part by the degree of difficulty mature craftspeople may have experienced in learning the radically different physical processes involved in wheel-manufacture.

Neuro-Physiological Adaptations Associated with Cross-Education of Strength

Cross-education of strength is the increase in strength of the untrained contralateral limb after unilateral training of the opposite homologous limb. We investigated central and peripheral neural adaptations associated with cross-education of strength. Twenty-three right-handed females were randomized into a unilateral training group or an imagery group. A sub-sample of eight subjects (four training, four imagery) was assessed with functional magnetic resonance imaging (fMRI) for patterns of cortical activation during exercise. Strength training was 6 weeks of maximal isometric ulnar deviation of the right arm, four times per week. Peak torque, muscle thickness (ultrasound), agonist-antagonist electromyography (EMG), and fMRI were assessed before and after training. Strength training was highly effective for increasing strength in trained (45.3%; P < 0.01) and untrained (47.1%; P < 0.01) limbs. The imagery group showed no increase in strength for either arm. Muscle thickness increased only in the trained arm of the training group (8.4%; P < 0.001). After training, there was an enlarged region of activation in contralateral sensorimotor cortex and left temporal lobe during muscle contractions with the untrained left arm (P < 0.001). Training was associated with a significantly greater change in agonist muscle EMG pooled over both limbs, compared to the imagery group (P < 0.05). These results suggest that cross-education of strength may be partly controlled by adaptations within sensorimotor cortex, consistent with previous studies of motor learning. However, this research demonstrates the involvement of temporal lobe regions that subserve semantic memory for movement, which has not been previously studied in this context. We argue that temporal lobe regions might play a significant role in the cross-education of strength.