Proximal versus distal control of two-joint planar reaching movements in the presence of neuromuscular noise

Determining how the human nervous system contends with neuro-motor noise is vital to understanding how humans achieve accurate goal-directed movements. Experimentally, people learning skilled tasks tend to reduce variability in distal joint movements more than in proximal joint movements. This suggests that they might be imposing greater control over distal joints than proximal joints. However, the reasons for this remain unclear, largely because it is not experimentally possible to directly manipulate either the noise or the control at each joint independently. Therefore, this study used a 2 degree-of-freedom torque driven arm model to determine how different combinations of noise and/or control independently applied at each joint affected the reaching accuracy and the total work required to make the movement. Signal-dependent noise was simultaneously and independently added to the shoulder and elbow torques to induce endpoint errors during planar reaching. Feedback control was then applied, independently and jointly, at each joint to reduce endpoint error due to the added neuromuscular noise. Movement direction and the inertia distribution along the arm were varied to quantify how these biomechanical variations affected the system performance. Endpoint error and total net work were computed as dependent measures. When each joint was independently subjected to noise in the absence of control, endpoint errors were more sensitive to distal (elbow) noise than to proximal (shoulder) noise for nearly all combinations of reaching direction and inertia ratio. The effects of distal noise on endpoint errors were more pronounced when inertia was distributed more toward the forearm. In contrast, the total net work decreased as mass was shifted to the upper arm for reaching movements in all directions. When noise was present at both joints and joint control was implemented, controlling the distal joint alone reduced endpoint errors more than controlling the proximal joint alone for nearly all combinations of reaching direction and inertia ratio. Applying control only at the distal joint was more effective at reducing endpoint errors when more of the mass was more proximally distributed. Likewise, controlling the distal joint alone required less total net work than controlling the proximal joint alone for nearly all combinations of reaching distance and inertia ratio. It is more efficient to reduce endpoint error and energetic cost by selectively applying control to reduce variability in the distal joint than the proximal joint. The reasons for this arise from the biomechanical configuration of the arm itself.     

Effect of Tendon Vibration on Hemiparetic Arm Stability in Unstable Workspaces

Sensory stimulation of wrist musculature can enhance stability in the proximal arm and may be a useful therapy aimed at improving arm control post-stroke. Specifically, our prior research indicates tendon vibration can enhance stability during point-to-point arm movements and in tracking tasks. The goal of the present study was to investigate the influence of forearm tendon vibration on endpoint stability, measured at the hand, immediately following forward arm movements in an unstable environment. Both proximal and distal workspaces were tested. Ten hemiparetic stroke subjects and 5 healthy controls made forward arm movements while grasping the handle of a two-joint robotic arm. At the end of each movement, the robot applied destabilizing forces. During some trials, 70 Hz vibration was applied to the forearm flexor muscle tendons. 70 Hz was used as the stimulus frequency as it lies within the range of optimal frequencies that activate the muscle spindles at the highest response rate. Endpoint position, velocity, muscle activity and grip force data were compared before, during and after vibration. Stability at the endpoint was quantified as the magnitude of oscillation about the target position, calculated from the power of the tangential velocity data. Prior to vibration, subjects produced unstable, oscillating hand movements about the target location due to the applied force field. Stability increased during vibration, as evidenced by decreased oscillation in hand tangential velocity.     

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     

A method for measuring endpoint stiffness during multi-joint arm movements

Current methods for measuring stiffness during human arm movements are either limited to one-joint motions, or lead to systematic errors. The technique presented here enables a simple, accurate and unbiased measurement of endpoint stiffness during multi-joint movements. Using a computer-controlled mechanical interface, the hand is displaced relative to a prediction of the undisturbed trajectory. Stiffness is then computed as the ratio of restoring force to displacement amplitude. Because of the accuracy of the prediction (< 1 cm error after 200 ms) and the quality of the implementation, the movement is not disrupted by the perturbation. This technique requires only 13 as many trials to identify stiffness as the method of Gomi and Kawato (1997, Biological Cybernetics 76, 163-171) and may, therefore, be used to investigate the evolution of stiffness during motor adaptation.     

Mental Representation of Arm Motion Dynamics in Children and Adolescents

Motor imagery, i.e., a mental state during which an individual internally represents an action without any overt motor output, is a potential tool to investigate action representation during development. Here, we took advantage of the inertial anisotropy phenomenon to investigate whether children can generate accurate motor predictions for movements with varying dynamics. Children (9 and 11 years), adolescents (14 years) and young adults (21 years) carried-out actual and mental arm movements in two different directions in the horizontal plane: rightwards (low inertia) and leftwards (high inertia). We recorded and compared actual and mental movement times. We found that actual movement times were greater for leftward than rightward arm movements in all groups. For mental movements, differences between leftward versus rightward movements were observed in the adults and adolescents, but not among the children. Furthermore, significant differences between actual and mental times were found at 9 and 11 years of age in the leftward direction. The ratio R/L (rightward direction/leftward direction), which indicates temporal differences between low inertia and high inertia movements, was inferior to 1 at all ages, except for the mental movements at 9 years of age, indicating than actual and mental movements were shorter for the rightward than leftward direction. Interestingly, while the ratio R/L of actual movements was constant across ages, it gradually decreased with age for mental movements. The ratio A/M (actual movement/mental movement), which indicates temporal differences between actual and mental movements, was near to 1 in the adults'' groups, denoting accurate mental timing. In children and adolescents, an underestimation of mental movement times appeared for the leftward movements only. However, this overestimation gradually decreased with age. Our results showed a refinement in the motor imagery ability during development. Action representation reached maturation at adolescence, during which mental actions were tightly related to their actual production.     

Arm-plane representation of shoulder compensation during pointing movements in patients with stroke

Improvements in functional motor activities are often accompanied by motor compensations to overcome persistent motor impairment in the upper limb. Kinematic analysis is used to objectively quantify movement patterns including common motor compensations such as excessive trunk displacement during reaching. However, a common motor compensation to assist reaching, shoulder abduction, is not adequately characterized by current motion analysis approaches. We apply the arm-plane representation that accounts for the co-variation between movements of the whole arm, and investigate its ability to identify and quantify compensatory arm movements in stroke subjects when making forward arm reaches. This method has not been previously applied to the analysis of motion deficits. Sixteen adults with right post-stroke hemiparesis and eight healthy age-matched controls reached in three target directions (14 trials/target; sampling rate: 100 Hz). Arm-plane movement was validated against endpoint, joint, and trunk kinematics and compared between groups. In stroke subjects, arm-plane measures were correlated with arm impairment (Fugl-Meyer Assessment) and ability (Box and Blocks) scores and were more sensitive than clinical measures to detect mild motor impairment. Arm-plane motion analysis provides new information about motor compensations involving the co-variation of shoulder and elbow movements that may help to understand the underlying motor deficits in patients with stroke.     

Using voluntary motor commands to inhibit involuntary arm movements

A hallmark of voluntary motor control is the ability to stop an ongoing movement. Is voluntary motor inhibition a general neural mechanism that can be focused on any movement, including involuntary movements, or is it mere termination of a positive voluntary motor command? The involuntary arm lift, or ‘floating arm trick’, is a distinctive long-lasting reflex of the deltoid muscle. We investigated how a voluntary motor network inhibits this form of involuntary motor control. Transcranial magnetic stimulation of the motor cortex during the floating arm trick produced a silent period in the reflexively contracting deltoid muscle, followed by a rebound of muscle activity. This pattern suggests a persistent generator of involuntary motor commands. Instructions to bring the arm down voluntarily reduced activity of deltoid muscle. When this voluntary effort was withdrawn, the involuntary arm lift resumed. Further, voluntary motor inhibition produced a strange illusion of physical resistance to bringing the arm down, as if ongoing involuntarily generated commands were located in a ‘sensory blind-spot’, inaccessible to conscious perception. Our results suggest that voluntary motor inhibition may be a specific neural function, distinct from absence of positive voluntary motor commands.     

Analysis of an optimal control model of multi-joint arm movements

 In this paper, we propose a model of biological motor control for generation of goal-directed multi-joint arm movements, and study the formation of muscle control inputs and invariant kinematic features of movements. The model has a hierarchical structure that can determine the control inputs for a set of redundant muscles without any inverse computation. Calculation of motor commands is divided into two stages, each of which performs a transformation of motor commands from one coordinate system to another. At the first level, a central controller in the brain accepts instructions from higher centers, which represent the motor goal in the Cartesian space. The controller computes joint equilibrium trajectories and excitation signals according to a minimum effort criterion. At the second level, a neural network in the spinal cord translates the excitation signals and equilibrium trajectories into control commands to three pairs of antagonist muscles which are redundant for a two-joint arm. No inverse computation is required in the determination of individual muscle commands. The minimum effort controller can produce arm movements whose dynamic and kinematic features are similar to those of voluntary arm movements. For fast movements, the hand approaches a target position along a near-straight path with a smooth bell-shaped velocity. The equilibrium trajectories in X and Y show an ‘N’ shape, but the end-point equilibrium path zigzags around the hand path. Joint movements are not always smooth. Joint reversal is found in movements in some directions. The excitation signals have a triphasic (or biphasic) pulse pattern, which leads to stereotyped triphasic (or biphasic) bursts in muscle control inputs, and a dynamically modulated joint stiffness. There is a fixed sequence of muscle activation from proximal muscles to distal muscles. The order is preserved in all movements. For slow movements, it is shown that a constant joint stiffness is necessary to produce a smooth movement with a bell-shaped velocity. Scaled movements can be reproduced by varying the constraints on the maximal level of excitation signals according to the speed of movement. When the inertial parameters of the arm are altered, movement trajectories can be kept invariant by adjusting the pulse height values, showing the ability to adapt to load changes. These results agree with a wide range of experimental observations on human voluntary movements. Received: 4 December 1995 / Accepted in revised form: 17 September 1996     

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.     

Learning to predict the future: the cerebellum adapts feedforward movement control

The role of the cerebellum in motor control and learning has been largely inferred from the effects of cerebellar damage. Recent work shows that cerebellar damage produces greater impairment of movements that require predictive as opposed to reactive control. This dissociation is consistent across many different types of movement. Predictive control is crucial for fast and ballistic movements, but impaired prediction can also affect slow movements, because of increased reliance on time-delayed feedback signals. The new findings are compatible with theories of cerebellar function, but still do not resolve whether the cerebellum operates by predicting the optimal motor commands or future sensory states. Prediction mechanisms must be learned and maintained through comparisons between predicted and observed outcomes. New results show that not all such error information is equivalent in driving cerebellar learning.     

Jerk-cost modulations during the practice of rapid arm movements

We examined how hand-trajectory smoothness changed during the practice of a motor task where smoothness was quantified by jerk-cost. Four human subjects each moved his nondominant arm between an upper target and a lower target, while circumnavigating a barrier that extended outward from the vertical plane of the targets. The two targets and the barrier placed boundary constraints on hand trajectories, but the motion was not restrained in any other way. Arm movements were recorded on high-speed ciné film, and linear and angular kinematical data were obtained for all arm segments. In each of 100 practice trials, subjects attempted to minimize movement time. After the practice trials, subjects repeated the same motor task but at movement times corresponding to the slowest, mid-range and fastest motion that had occurred during practice. Thus, jerk-cost could be compared for movements of different speeds during practice and after practice. Because the movement task contained several changes in hand-path direction, the changes in the vector characteristics of the hand accelerations were expected to be important for explaining the modulations in jerk-cost with practice. Total jerk-cost, therefore, was calculated as well as the separate magnitudinal and directional jerk-cost components. During practice, total movement time decreased, hand paths became more parabolic in shape, and significant changes occurred in hand acceleration magnitude, direction, and timing. Total jerk-cost and the magnitudinal and directional jerk-cost components were significantly less when slowest hand movements were compared after practice versus during practice. The decrease in jerk-cost indicated an increased smoothness of the practiced movements.K. Schneider was supported by the German Research Association (Deutsche Forschungsgemeinschaft)     

Octopuses use a human-like strategy to control precise point-to-point arm movements

One of the key problems in motor control is mastering or reducing the number of degrees of freedom (DOFs) through coordination. This problem is especially prominent with hyper-redundant limbs such as the extremely flexible arm of the octopus. Several strategies for simplifying these control problems have been suggested for human point-to-point arm movements. Despite the evolutionary gap and morphological differences, humans and octopuses evolved similar strategies when fetching food to the mouth. To achieve this precise point-to-point-task, octopus arms generate a quasi-articulated structure based on three dynamic joints. A rotational movement around these joints brings the object to the mouth . Here, we describe a peripheral neural mechanism-two waves of muscle activation propagate toward each other, and their collision point sets the medial-joint location. This is a remarkably simple mechanism for adjusting the length of the segments according to where the object is grasped. Furthermore, similar to certain human arm movements, kinematic invariants were observed at the joint level rather than at the end-effector level, suggesting intrinsic control coordination. The evolutionary convergence to similar geometrical and kinematic features suggests that a kinematically constrained articulated limb controlled at the level of joint space is the optimal solution for precise point-to-point movements.     

Conclusions on motor control depend on the type of model used to represent the periphery

Within the field of motor control, there is no consensus on which kinematic and kinetic aspects of movements are planned or controlled. Perturbing goal-directed movements is a frequently used tool to answer this question. To be able to draw conclusions about motor control from kinematic responses to perturbations, a model of the periphery (i.e., the skeleton, muscle–tendon complexes, and spinal reflex circuitry) is required. The purpose of the present study was to determine to what extent such conclusions depend on the level of simplification with which the dynamical properties of the periphery are modeled. For this purpose, we simulated fast goal-directed single-joint movement with four existing types of models. We tested how three types of perturbations affected movement trajectory if motor commands remained unchanged. We found that the four types of models of the periphery showed different robustness to the perturbations, leading to different predictions on how accurate motor commands need to be, i.e., how accurate the knowledge of external conditions needs to be. This means that when interpreting kinematic responses obtained in perturbation experiments the level of error correction attributed to adaptation of motor commands depends on the type of model used to describe the periphery.     

Changes in limb dynamics during the practice of rapid arm movements

In our study we examined Bernstein's hypothesis that practice alters the motor coordination among the muscular and passive joint moments. In particular, we conducted dynamical analyses of a human multisegmental movement during the practice of a task involving the upper extremity. Seven male human volunteers performed maximal-speed, unrestrained vertical arm movements whose upward and downward trajectories between two target endpoints required the hand to round a barrier, resulting in complex shoulder, elbow, and wrist joint movements. These movements were recorded by high-speed ciné film, and myopotentials from selected upper-extremity muscles were recorded. The arm was modeled as interconnected rigid bodies, so that dynamical interactions among the upper arm, forearm, and hand could be calculated. With practice, subjects achieved significantly shorter movement times. As movement times decreased, all joint-moment components (except gravity) increased, and the moment-time and EMG profiles were changed significantly. Particularly during reversals in movement direction, the changes in moment-time and EMG profiles were consistent with Bernstein's hypothesis relating practice effects and intralimb coordination: with practice, motor coordination was altered so that individuals employed reactive phenomena in such a way as to use muscular moments to counterbalance passive-interactive moments created by segment movements.     

Activation of the Shoulder-Belt and Shoulder Muscles in Two-Joint Arm Movements Performed in Humans with the Action of Opposite Loadings

In tests on four volunteers, we examined coordination of central motor commands (CMCs) controlling slow two-joint movements of the arm within the horizontal plane. Current amplitudes of EMGs recorded from six muscles of the shoulder belt and shoulder and subjected to full-wave rectifying and low-frequency filtration were considered correlates of these commands. In particular, we studied the dependence of coordination of CMCs on the direction of an external force applied to the distal forearm part. As was found, coordination of CMCs significantly depends on the direction of the force flexing the elbow joint. According to our observations, EMGs of definite muscles in the case of performance of a two-joint movement can, in a first approximation, be presented as linear combinations of the EMGs recorded in the course of separate sequential single-joint movements under conditions of shifting the reference point of the hand toward the same point of the operational space as that in the two-joint movement. These data can be interpreted as confirmation of the principle of superposition of elementary CMCs in the performance of complex movements of the extremity.     

A review on directional information in neural signals for brain-machine interfaces

Brain-machine interfaces (BMIs) can be characterized by the technique used to measure brain activity and by the way different brain signals are translated into commands that control an effector. We give an overview of different approaches and focus on a particular BMI approach: the movement of an artificial effector (e.g. arm prosthesis to the right) by those motor cortical signals that control the equivalent movement of a corresponding body part (e.g. arm movement to the right). This approach has been successfully applied in monkeys and humans by accurately extracting parameters of movements from the spiking activity of multiple single-units. Here, we review recent findings showing that analog neuronal population signals, ranging from intracortical local field potentials over epicortical ECoG to non-invasive EEG and MEG, can also be used to decode movement direction and continuous movement trajectories. Therefore, these signals might provide additional or alternative control for this BMI approach, with possible advantages due to reduced invasiveness.     

Cerebellar learning of accurate predictive control for fast-reaching movements

Long conduction delays in the nervous system prevent the accurate control of movements by feedback control alone. We present a new, biologically plausible cerebellar model to study how fast arm movements can be executed in spite of these delays. To provide a realistic test-bed of the cerebellar neural model, we embed the cerebellar network in a simulated biological motor system comprising a spinal cord model and a six-muscle two-dimensional arm model. We argue that if the trajectory errors are detected at the spinal cord level, memory traces in the cerebellum can solve the temporal mismatch problem between efferent motor commands and delayed error signals. Moreover, learning is made stable by the inclusion of the cerebello-nucleo-olivary loop in the model. It is shown that the cerebellar network implements a nonlinear predictive regulator by learning part of the inverse dynamics of the plant and spinal circuit. After learning, fast accurate reaching movements can be generated. Received: 8 February 1999 /Accepted in revised form: 7 August 1999     

Activity of pre-entral neurones in conscious monkeys: effects of deafferentation and cerebellar ablation.

After limb deafferentation, there was no gross alteration in the initiation and performance of a sound-triggered ballistic movement. The pattern of neuronal discharge in the arm area of the motor cortex was not significantly modified. In the absence of cerebellum, the reaction time of motor cortex cells was about 150 msec longer than the reaction time observed in normal and deafferented animals. This was associated with an equal retardation in the onset of ENG changes in the limb muscles. This observation is compatible with the idea that the motor cortex is normally situated downstream to the cerebellum in the initiation of some movements. However, the motor cortex is necessary for the initiation and execution of simple sound-triggered movements since its removal results in a permanent inability to perform the task. Finally, in the absence of peripheral feedback, the pattern of motor output to the agonistic and antagonistic muscles was initiated normally and thus appeared to be preprogrammed centrally. The importance of the motor cortex as a "reflex center" in the control of slower movements is obviously not challenged by these observations since the motor task that we have used depends very little or not at all on sensory feedback (Stark, 1968). What these results indicate, however, is that the execution of some voluntary fast ballistic movements can be entirely preprogrammed independently of peripheral and cerebellar influences, and that the program, which is mainly concerned with generating velocity signals, appears to require the integrity of the motor cortex for its execution.     

Modulation of the soleus muscle H reflex caused by ballistic voluntary arm movements in humans

In healthy humans, we studied the influence of conditioning voluntary arm movements on the H reflex induced by transcutaneous stimulation of the tibial nerve and recorded from the soleus muscle. We examined the effects of flexion and extension of the forearm, as well as of finger clenching performed with the maximum rate. Conditioning arm movements were self-induced or realized upon presentation of a visual signal (light flash). We found that the pattern of changes in the H reflex is determined by the position of the subject’s body in the course of tests. The ipsilateral arm flexion in the elbow joint in the standing position resulted in depression of the H reflex lasting about 100 msec from the beginning of the movement, while the effect observed in the lying position (on the couch with the feet hanging free in the air) looked like a facilitation of the reflex lasting about 100 to 200 msec. The direction and dynamics of modifications of the H reflex under conditions of the use of different conditioning movements (forearm flexions/extensions and finger clenching of the ipsilateral arm, as well as contralateral forearm flexions in the elbow joint) were rather similar. We also showed that the observed facilitation of the H reflex began earlier than the voluntary arm movement (40 to 50 msec prior to the beginning). We hypothesize that these conditioning influences result from the action of central motor commands and represent the factor related to anticipatory postural rearrangements. Such rearrangements are directed toward the maintenance of equilibrium of the body in the course of a future movement. These commands depend significantly on the spatial position of the subject’s body. Neirofiziologiya/Neurophysiology, Vol. 40, No. 2, pp. 147–154, March–April, 2008.