Motor control and learning in altered dynamic environments

Dynamic perturbations of reaching movements are an important technique for studying motor learning and adaptation. Adaptation to non-contacting, velocity-dependent inertial Coriolis forces generated by arm movements during passive body rotation is very rapid, and when complete the Coriolis forces are no longer sensed. Adaptation to velocity-dependent forces delivered by a robotic manipulandum takes longer and the perturbations continue to be perceived even when adaptation is complete. These differences reflect adaptive self-calibration of motor control versus learning the behavior of an external object or 'tool'. Velocity-dependent inertial Coriolis forces also arise in everyday behavior during voluntary turn and reach movements but because of anticipatory feedforward motor compensations do not affect movement accuracy despite being larger than the velocity-dependent forces typically used in experimental studies. Progress has been made in understanding: the common features that determine adaptive responses to velocity-dependent perturbations of jaw and limb movements; the transfer of adaptation to mechanical perturbations across different contact sites on a limb; and the parcellation and separate representation of the static and dynamic components of multiforce perturbations.     

Mechanisms of Motor Adaptation in Reactive Balance Control

Balance control must be rapidly modified to provide stability in the face of environmental challenges. Although changes in reactive balance over repeated perturbations have been observed previously, only anticipatory postural adjustments preceding voluntary movements have been studied in the framework of motor adaptation and learning theory. Here, we hypothesized that adaptation occurs in task-level balance control during responses to perturbations due to central changes in the control of both anticipatory and reactive components of balance. Our adaptation paradigm consisted of a Training set of forward support-surface perturbations, a Reversal set of novel countermanding perturbations that reversed direction, and a Washout set identical to the Training set. Adaptation was characterized by a change in a motor variable from the beginning to the end of each set, the presence of aftereffects at the beginning of the Washout set when the novel perturbations were removed, and a return of the variable at the end of the Washout to a level comparable to the end of the Training set. Task-level balance performance was characterized by peak center of mass (CoM) excursion and velocity, which showed adaptive changes with repetitive trials. Only small changes in anticipatory postural control, characterized by body lean and background muscle activity were observed. Adaptation was found in the evoked long-latency muscular response, and also in the sensorimotor transformation mediating that response. Finally, in each set, temporal patterns of muscle activity converged towards an optimum predicted by a trade-off between maximizing motor performance and minimizing muscle activity. Our results suggest that adaptation in balance, as well as other motor tasks, is mediated by altering central sensitivity to perturbations and may be driven by energetic considerations.     

Limb Dominance Results from Asymmetries in Predictive and Impedance Control Mechanisms

Handedness is a pronounced feature of human motor behavior, yet the underlying neural mechanisms remain unclear. We hypothesize that motor lateralization results from asymmetries in predictive control of task dynamics and in control of limb impedance. To test this hypothesis, we present an experiment with two different force field environments, a field with a predictable magnitude that varies with the square of velocity, and a field with a less predictable magnitude that varies linearly with velocity. These fields were designed to be compatible with controllers that are specialized in predicting limb and task dynamics, and modulating position and velocity dependent impedance, respectively. Because the velocity square field does not change the form of the equations of motion for the reaching arm, we reasoned that a forward dynamic-type controller should perform well in this field, while control of linear damping and stiffness terms should be less effective. In contrast, the unpredictable linear field should be most compatible with impedance control, but incompatible with predictive dynamics control. We measured steady state final position accuracy and 3 trajectory features during exposure to these fields: Mean squared jerk, Straightness, and Movement time. Our results confirmed that each arm made straighter, smoother, and quicker movements in its compatible field. Both arms showed similar final position accuracies, which were achieved using more extensive corrective sub-movements when either arm performed in its incompatible field. Finally, each arm showed limited adaptation to its incompatible field. Analysis of the dependence of trajectory errors on field magnitude suggested that dominant arm adaptation occurred by prediction of the mean field, thus exploiting predictive mechanisms for adaptation to the unpredictable field. Overall, our results support the hypothesis that motor lateralization reflects asymmetries in specific motor control mechanisms associated with predictive control of limb and task dynamics, and modulation of limb impedance.     

Effect of muscle fatigue on internal model formation and retention during reaching with the arm.

The motor system adapts to novel dynamic environments by forming internal models that predict the muscle forces needed to move skillfully. The goal of this study was to determine how muscle fatigue affects internal model formation during arm movement and whether an internal model acquired while fatigued could be recalled accurately after rest. Twelve subjects adapted to a viscous force field applied by a lightweight robot as they reached to a target. They then reached while being resisted by elastic bands until they could no longer touch the target. This protocol reduced the strength of the muscles used to resist the force field by approximately 20%. The bands were removed, and subjects adapted again to the viscous force field. Their adaptive ability, quantified by the amount and time constant of adaptation, was not significantly impaired following fatigue. The subjects then rested, recovering approximately 70% of their lost force-generation ability. When they reached in the force field again, their prediction of the force field strength was different than in a nonfatigued state. This alteration was consistent with the use of a higher level of effort than normally used to counteract the force field. These results suggest that recovery from fatigue can affect recall of an internal model, even when the fatigue did not substantially affect the motor system's ability to form the model. Recovery from fatigue apparently affects recall because the motor system represents internal models as a mapping between effort and movement and relies on practice to recalibrate this mapping.     

Learning the dynamics of reaching movements results in the modification of arm impedance and long-latency perturbation responses

 Some characteristics of arm movements that humans exhibit during learning the dynamics of reaching are consistent with a theoretical framework where training results in motor commands that are gradually modified to predict and compensate for novel forces that may act on the hand. As a first approximation, the motor control system behaves as an adapting controller that learns an internal model of the dynamics of the task. It approximates inverse dynamics and predicts motor commands that are appropriate for a desired limb trajectory. However, we had previously noted that subtle motion characteristics observed during changes in task dynamics challenged this simple model and raised the possibility that adaptation also involved sensory–motor feedback pathways. These pathways reacted to sensory feedback during the course of the movement. Here we hypothesize that adaptation to dynamics might also involve a modification of how the CNS responds to sensory feedback. We tested this through experiments that quantified how the motor system's response to errors during voluntary movements changed as it adapted to dynamics of a force field. We describe a nonlinear approach that approximates the impedance of the arm, i.e., force response as a function of arm displacement trajectory. We observe that after adaptation, the impedance function changes in a way that closely matches and counters the effect of the force field. This is particularly prominent in the long-latency (>100 ms) component of response to perturbations. Therefore, it appears that practice not only modifies the internal model with which the brain generates motor commands that initiate a movement, but also the internal model with which sensory feedback is integrated with the ongoing descending commands in order to respond to error during the movement. Received: 10 January 2001 / Accepted in revised form: 30 May 2001     

Correlations in state space can cause sub-optimal adaptation of optimal feedback control models

Control of our movements is apparently facilitated by an adaptive internal model in the cerebellum. It was long thought that this internal model implemented an adaptive inverse model and generated motor commands, but recently many reject that idea in favor of a forward model hypothesis. In theory, the forward model predicts upcoming state during reaching movements so the motor cortex can generate appropriate motor commands. Recent computational models of this process rely on the optimal feedback control (OFC) framework of control theory. OFC is a powerful tool for describing motor control, it does not describe adaptation. Some assume that adaptation of the forward model alone could explain motor adaptation, but this is widely understood to be overly simplistic. However, an adaptive optimal controller is difficult to implement. A reasonable alternative is to allow forward model adaptation to ‘re-tune’ the controller. Our simulations show that, as expected, forward model adaptation alone does not produce optimal trajectories during reaching movements perturbed by force fields. However, they also show that re-optimizing the controller from the forward model can be sub-optimal. This is because, in a system with state correlations or redundancies, accurate prediction requires different information than optimal control. We find that adding noise to the movements that matches noise found in human data is enough to overcome this problem. However, since the state space for control of real movements is far more complex than in our simple simulations, the effects of correlations on re-adaptation of the controller from the forward model cannot be overlooked.     

Adaptation to visual feedback delay influences visuomotor learning

Computational theory of motor control suggests that the brain continuously monitors motor commands, to predict their sensory consequences before actual sensory feedback becomes available. Such prediction error is a driving force of motor learning, and therefore appropriate associations between motor commands and delayed sensory feedback signals are crucial. Indeed, artificially introduced delays in visual feedback have been reported to degrade motor learning. However, considering our perceptual ability to causally bind our own actions with sensory feedback, demonstrated by the decrease in the perceived time delay following repeated exposure to an artificial delay, we hypothesized that such perceptual binding might alleviate deficits of motor learning associated with delayed visual feedback. Here, we evaluated this hypothesis by investigating the ability of human participants to adapt their reaching movements in response to a novel visuomotor environment with 3 visual feedback conditions--no-delay, sudden-delay, and adapted-delay. To introduce novelty into the trials, the cursor position, which originally indicated the hand position in baseline trials, was rotated around the starting position. In contrast to the no-delay condition, a 200-ms delay was artificially introduced between the cursor and hand positions during the presence of visual rotation (sudden-delay condition), or before the application of visual rotation (adapted-delay condition). We compared the learning rate (representing how the movement error modifies the movement direction in the subsequent trial) between the 3 conditions. In comparison with the no-delay condition, the learning rate was significantly degraded for the sudden-delay condition. However, this degradation was significantly alleviated by prior exposure to the delay (adapted-delay condition). Our data indicate the importance of appropriate temporal associations between motor commands and sensory feedback in visuomotor learning. Moreover, they suggest that the brain is able to account for such temporal associations in a flexible manner.     

Adjustment of the human arm viscoelastic properties to the direction of reaching

The viscoelastic properties of the human arm were measured by means of short force perturbations during fast reaching movements in two orthogonal directions. A linear spring model with time delay described the neuromuscular system of the human arm. The obtained viscoelastic parameters ensured movement stability in spite of the time delay of 50 ms. The stiffness and viscosity ellipses appeared to be predominantly orthogonal to the movement direction, which reduced the effect of force perturbation in the direction orthogonal to the reaching movement. Thus, it can be argued that the viscoelastic properties of the neuromuscular system of the human arm are adjusted to the direction of movement according to a “path preserving” strategy, which minimizes the deviation of the movement path from a straight line, when exposed to an unexpected external force.     

Movement Preparation and Bilateral Modulation of Beta Activity in Aging and Parkinson’s Disease

In previous studies of young subjects performing a reaction-time reaching task, we found that faster reaction times are associated with increased suppression of beta power over primary sensorimotor areas just before target presentation. Here we ascertain whether such beta decrease similarly occurs in normally aging subjects and also in patients with Parkinson’s disease (PD), where deficits in movement execution and abnormalities of beta power are usually present. We found that in both groups, beta power decreased during the motor task in the electrodes over the two primary sensorimotor areas. However, before target presentation, beta decreases in PD were significantly smaller over the right than over the left areas, while they were symmetrical in controls. In both groups, functional connectivity between the two regions, measured with imaginary coherence, increased before the target appearance; however, in PD, it decreased immediately after, while in controls, it remained elevated throughout motor planning. As in previous studies with young subjects, the degree of beta power before target appearance correlated with reaction time. The values of coherence during motor planning, instead, correlated with movement time, peak velocity and acceleration. We conclude that planning of prompt and fast movements partially depends on coordinated beta activity of both sensorimotor areas, already at the time of target presentation. The delayed onset of beta decreases over the right region observed in PD is possibly related to a decreased functional connectivity between the two areas, and this might account for deficits in force programming, movement duration and velocity modulation.     

The effect of six weeks endurance training on dynamic muscular control of the knee following fatiguing exercise

The aim of the study was to examine whether six weeks of endurance training minimizes the effects of fatigue on postural control during dynamic postural perturbations. Eighteen healthy volunteers were assigned to either a 6-week progressive endurance training program on a cycle ergometer or a control group. At week 0 and 7, dynamic exercise was performed on an ergometer until exhaustion and immediately after, the anterior–posterior centre of pressure (COP) sway was analyzed during full body perturbations. Maximal voluntary contractions (MVC) of the knee flexors and extensors, muscle fiber conduction velocity (MFCV) of the vastus lateralis and medialis during sustained isometric knee extension contractions, and power output were measured. Following the training protocol, maximum knee extensor and flexor force and power output increased significantly for the training group with no changes observed for the control group. Moreover, the reduction of MFCV due to fatigue changed for the training group only (from 8.6% to 3.4%). At baseline, the fatiguing exercise induced an increase in the centre of pressure sway during the perturbations in both groups (>10%). The fatiguing protocol also impaired postural control in the control group when measured at week 7. However, for the training group, sway was not altered after the fatiguing exercise when assessed at week 7. In summary, six weeks of endurance training delayed the onset of muscle fatigue and improved the ability to control balance in response to postural perturbations in the presence of muscle fatigue. Results implicate that endurance training should be included in any injury prevention program.     

Adaptation of reflexive feedback during arm posture to different environments

 In this study we have examined the ability of the central nervous system (CNS) to use spinal reflexes to minimize displacements during postural control while continuous force perturbations were applied at the hand. The subjects were instructed to minimize the displacements of the hand from a reference position that resulted from the force perturbations. The perturbations were imposed in one direction by means of a hydraulic manipulator of which the virtual mass and damping were varied. Resistance to the perturbations came from intrinsic and reflexive stiffness, and from the virtual environment. It is hypothesized that reflexive feedback during posture maintenance is optimally adjusted such that position deviations are minimal for a given virtual environment. Frequency response functions were estimated, capturing all mechanical properties of the arm at the end point (hand) level. Intrinsic and reflexive parameters were quantified by fitting a linear neuromuscular model to the frequency responses. The reflexive length feedback gain increased strongly with damping and little with the eigenfrequency of the total combined system (i.e. arm plus environment). The reflexive velocity feedback gain decreased slightly with relative damping at the largest eigenfrequency and more markedly at smaller eigenfrequencies. In the case of highest reflex gains, the total system remained stable and sufficiently damped while the responses of only the arm were severely underdamped and sometimes even unstable. To further analyse these results, a model optimization was performed. Intrinsic and reflexive parameters were optimized such that two criterion functions were minimized. The first concerns performance and penalized hand displacements from a reference point. The second one weights afferent control effort to avoid inefficient feedback. The simulations showed good similarities with the estimated values. Length feedback was adequately predicted by the model for all conditions. The predicted velocity feedback gains were larger in all cases, probably indicating a mutual gain limiting relation between length and velocity afferent signals. The results suggest that both reflex gains seem to be adjusted by the CNS, where in particular the length feedback gain was optimal so as to maximize performance at minimum control effort. Received: 23 July 2001 / Accepted in revised form: 15 January 2002     

Coordinate Representations for Interference Reduction in Motor Learning

When opposing force fields are presented alternately or randomly across trials for identical reaching movements, subjects learn neither force field, a behavior termed ‘interference’. Studies have shown that a small difference in the endpoint posture of the limb reduces this interference. However, any difference in the limb’s endpoint location typically changes the hand position, joint angles and the hand orientation making it ambiguous as to which of these changes underlies the ability to learn dynamics that normally interfere. Here we examine the extent to which each of these three possible coordinate systems—Cartesian hand position, shoulder and elbow joint angles, or hand orientation—underlies the reduction in interference. Subjects performed goal-directed reaching movements in five different limb configurations designed so that different pairs of these configurations involved a change in only one coordinate system. By specifically assigning clockwise and counter-clockwise force fields to the configurations we could create three different conditions in which the direction of the force field could only be uniquely distinguished in one of the three coordinate systems. We examined the ability to learn the two fields based on each of the coordinate systems. The largest reduction of interference was observed when the field direction was linked to the hand orientation with smaller reductions in the other two conditions. This result demonstrates that the strongest reduction in interference occurred with changes in the hand orientation, suggesting that hand orientation may have a privileged role in reducing motor interference for changes in the endpoint posture of the limb.     

Differences in Context and Feedback Result in Different Trajectories and Adaptation Strategies in Reaching

Computational models of motor control have often explained the straightness of horizontal planar reaching movements as a consequence of optimal control. Departure from rectilinearity is thus regarded as sub-optimal. Here we examine if subjects may instead select to make curved trajectories following adaptation to force fields and visuomotor rotations. Separate subjects adapted to force fields with or without visual feedback of their hand trajectory and were retested after 24 hours. Following adaptation, comparable accuracies were achieved in two ways: with visual feedback, adapted trajectories in force fields were straight whereas without it, they remained curved. The results suggest that trajectory shape is not always straight, but is also influenced by the calibration of available feedback signals for the state estimation required by the task. In a follow-up experiment, where additional subjects learned a visuomotor rotation immediately after force field, the trajectories learned in force fields (straight or curved) were transferred when directions of the perturbations were similar but not when directions were opposing. This demonstrates a strong bias by prior experience to keep using a recently acquired control policy that continues to produce successful performance inspite of differences in tasks and feedback conditions. On relearning of force fields on the second day, facilitation by intervening visuomotor rotations occurred only when required motor adjustments and calibration of feedback signals were similar in both tasks. These results suggest that both the available feedback signals and prior history of learning influence the choice and maintenance of control policy during adaptations.     

A gain-field encoding of limb position and velocity in the internal model of arm dynamics

Adaptability of reaching movements depends on a computation in the brain that transforms sensory cues, such as those that indicate the position and velocity of the arm, into motor commands. Theoretical consideration shows that the encoding properties of neural elements implementing this transformation dictate how errors should generalize from one limb position and velocity to another. To estimate how sensory cues are encoded by these neural elements, we designed experiments that quantified spatial generalization in environments where forces depended on both position and velocity of the limb. The patterns of error generalization suggest that the neural elements that compute the transformation encode limb position and velocity in intrinsic coordinates via a gain-field; i.e., the elements have directionally dependent tuning that is modulated monotonically with limb position. The gain-field encoding makes the counterintuitive prediction of hypergeneralization: there should be growing extrapolation beyond the trained workspace. Furthermore, nonmonotonic force patterns should be more difficult to learn than monotonic ones. We confirmed these predictions experimentally.     

Anticipatory synergy adjustments in preparation to self-triggered perturbations in elderly individuals

We tested the ability of healthy elderly persons to use anticipatory synergy adjustments (ASAs) prior to a self-triggered perturbation of one of the fingers during a multifinger force production task. An index of a force-stabilizing synergy was computed reflecting covariation of commands to fingers. The subjects produced constant force by pressing with the four fingers of the dominant hand on force sensors against constant upwardly directed forces. The middle finger could be unloaded either by the subject pressing the trigger or unexpectedly by the experimenter. In the former condition, the synergy index showed a drop (interpreted as ASA) prior to the time of unloading. This drop started later and was smaller in magnitude as compared with ASAs reported in an earlier study of younger subjects. At the new steady state, a new sharing pattern of the force was reached. We conclude that aging is associated with a preserved ability to explore the flexibility of the mechanically redundant multifinger system but a decreased ability to use feedforward adjustments to self-triggered perturbations. These changes may contribute to the documented drop in manual dexterity with age.     

The effect of fast and slow motor unit activation on whole-muscle mechanical performance: the size principle may not pose a mechanical paradox

The output of skeletal muscle can be varied by selectively recruiting different motor units. However, our knowledge of muscle function is largely derived from muscle in which all motor units are activated. This discrepancy may limit our understanding of in vivo muscle function. Hence, this study aimed to characterize the mechanical properties of muscle with different motor unit activation. We determined the isometric properties and isotonic force–velocity relationship of rat plantaris muscles in situ with all of the muscle active, 30% of the muscle containing predominately slower motor units active or 20% of the muscle containing predominately faster motor units active. There was a significant effect of active motor unit type on isometric force rise time (p < 0.001) and the force–velocity relationship (p < 0.001). Surprisingly, force rise time was longer and maximum shortening velocity higher when all motor units were active than when either fast or slow motor units were selectively activated. We propose this is due to the greater relative effects of factors such as series compliance and muscle resistance to shortening during sub-maximal contractions. The findings presented here suggest that recruitment according to the size principle, where slow motor units are activated first and faster ones recruited as demand increases, may not pose a mechanical paradox, as has been previously suggested.     

Direct measurement of power during one single sprint on treadmill

We tested the validity of an instrumented treadmill dynamometer for measuring maximal propulsive power during sprint running, and sought to verify whether this could be done over one single sprint, as shown during sprint cycling. The treadmill dynamometer modified towards sprint use (constant motor torque) allows vertical and horizontal forces to be measured at the same location as velocity, i.e. at the foot, which is novel compared to existing methods in which power is computed as the product of belt velocity and horizontal force measured by transducers placed in the tethering system. Twelve males performed 6 s sprints against default, high and low loads set from the motor torque necessary to overcome the friction due to subjects’ weight on the belt (default load), and 20% higher and lower motor torque values. Horizontal ground reaction force, belt velocity, propulsive power and linear force–velocity relationships were compared between the default load condition and when taking all conditions together. Force and velocity traces and values were reproducible and consistent with the literature, and no significant difference was found between maximal power and force–velocity relationships obtained in the default load condition only vs. adding data from all conditions. The presented method allows one to measure maximal propulsive power and calculate linear force–velocity relationships from one single sprint data. The main novelties are that both force and velocity are measured at the same location, and that instantaneous values are averaged over one contact period, and not over a constant arbitrary time-window.     

Factors that differentiate acceleration ability in field sport athletes

Speed and acceleration are essential for field sport athletes. However, the mechanical factors important for field sport acceleration have not been established in the scientific literature. The purpose of this study was to determine the biomechanical and performance factors that differentiate sprint acceleration ability in field sport athletes. Twenty men completed sprint tests for biomechanical analysis and tests of power, strength, and leg stiffness. The sprint intervals analyzed were 0-5, 5-10, and 0-10 m. The subjects were split into a faster and slower group based on 0- to 10-m velocity. A 1-way analysis of variance determined variables that significantly (p ≤ 0.05) distinguished between faster and slower acceleration. All subject data were then pooled for a correlation analysis to determine factors contributing most to acceleration. The results showed that 0- to 5-m (～16% difference) and 0- to 10-m (～11% difference) contact times for the faster group were significantly lower. Times to peak vertical and horizontal force during ground contact were lower for the faster group. This was associated with the reduced support times achieved by faster accelerators and their ability to generate force quickly. Ground contact force profiles during initial acceleration are useful discriminators of sprint performance in field sport athletes. For the strength and power measures, the faster group demonstrated a 14% greater countermovement jump and 48% greater reactive strength index. Significant correlations were found between velocity (0-5, 5-10, and 0-10 m) and most strength and power measures. The novel finding of this study is that training programs directed toward improving field sport sprint acceleration should aim to reduce contact time and improve ground force efficiency. It is important that even during the short sprints required for field sports, practitioners focus on good technique with short contact times.     

The discontinuous nature of motor execution

Human movement control requires adequate coordination of different movements, which is particularly important when different motor tasks are simultaneously executed by the same effector(s) (e.g. a muscle or a joint). The process of movement execution involves a series of highly nonlinear elements; for instance, a motor unit of a muscle produces force only in the direction of muscle shortening, thus representing a threshold operator that transforms the bipolar (i.e. excitatory or inhibitory) information at its spinal input into a purely unipolar signal (i.e. muscle force). This tripartite research report addresses the contribution of the nonlinearity of neuromuscular elements to the coordination of different motor tasks simultaneously executed by the same limb. In this first part of the series, a new hypothesis for such a single-muscle multiple-task coordination is presented which suggests an essentially threshold-linear coordination mechanism. Control signals generated by the central nervous system for each individual movement independently and feedback information from peripheral receptors are linearly superimposed. This compound control/feedback signal is processed by a nonlinear limiter element reflecting the discontinuous properties of the muscle and its reflex circuitry. It is shown that threshold-linear interaction of descending commands and afferent feedback information can lead to complex interdependent patterns of compound motor action. This includes the possibility of gating (i.e. the ability of one movement pattern to constrain or even impede the execution of another pattern) and of delayed response initiation when simultaneously performing more than one voluntary motor task. A theoretical analysis of the threshold-linear coordination mechanism and an extensive experimental validation of the model is provided in part II and part III of the report. Received: 6 October 1998 / Accepted in revised form: 2 June 1999