A Linked Muscular Activation Model for Movement Generation and Control

A new model for movement control is presented which incorporates characteristics of impulse-variability and mass-spring models. Movements in the model were controlled with phasic torque impulses in agonist and antagonist muscles and a tonic agonist torque.

Characteristics of the phasic agonist and antagonist torque profiles were based on observed properties of movement-related EMGs and muscle isometric torques. Variability of the phasic impulses depended on impulse magnitude as in impulse-variability models. The model therefore predicted a speed-accuracy tradeoff for limb movement. The time of onset and magnitude of the antagonist torque depended on the magnitude of the preceding agonist torque as indicated in studies of movement-related EMGs. This led to the new concept of linkage between the agonist and antagonist muscle forces which was shown to be important for reducing variability of fast movements. Progressive development of linkage during practice could explain the previous findings of decreased movement variability with practice coupled with increased variability of movement-related EMGs.

It was concluded that an inherently variable motor system deals with the variability associated with generation of large muscle forces by linking the forces produced by opposing muscles. In this way, variability in net joint torques and in movements can be decreased without the need for the nervous system to closely regulate the individual torques.     

Movement Related EMGs Become More Variable During Learning of Fast Accurate Movements

Human subjects performed simple flexion and extension movements about the elbow in a visual step-tracking paradigm. Movements were self-terminated. Subjects were instructed to increase movement velocity while maintaining end-point accuracy during practice. The effects of practice on the pattern and variability of EMG activity of the biceps and triceps muscles were studied. Initial movements were performed using reciprocal phasic activation of agonist and antagonist muscles as indicated by surface EMGs. With practice, increases in movement speed were associated with larger agonist and antagonist bursts and an earlier onset of the antagonist burst. Decreased duration of the premovement antagonist silence was also observed during practice.

Decreases in variability of movements during practice were not accompanied by equivalent decreases in variability of the associated EMGs. Surprisingly, both agonist and antagonist EMGs were more variable in faster, practiced movements. The combined agonist-antagonist EMG variability depended on both movement speed and trajectory variability. Lower variability in movements in the presence of greater variability in the related EMGs occurred because of linked variations in agonist and antagonist muscle activities. Variations in the first agonist burst were often compensated for by associated variations in the antagonist and late agonist bursts. These linked variations maintained the limb trajectory relatively constant in spite of large variations in the first agonist burst. Modifications to impulse-variability models are therefore needed to explain compensations for variability in accelerative impulses (produced by the first agonist burst) by linked variations in impulses for deceleration (produced by the antagonist and late agonist bursts).     

Movement related EMGs become more variable during learning of fast accurate movements

Human subjects performed simple flexion and extension movements about the elbow in a visual step-tracking paradigm. Movements were self-terminated. Subjects were instructed to increase movement velocity while maintaining end-point accuracy during practice. The effects of practice on the pattern and variability of EMG activity of the biceps and triceps muscles were studied. Initial movements were performed using reciprocal phasic activation of agonist and antagonist muscles as indicated by surface EMGs. With practice, increases in movement speed were associated with larger agonist and antagonist bursts and an earlier onset of the antagonist burst. Decreased duration of the premovement antagonist silence was also observed during practice. Decreases in variability of movements during practice were not accompanied by equivalent decreases in variability of the associated EMGs. Surprisingly, both agonist and antagonist EMGs were more variable in faster, practiced movements. The combined agonist-antagonist EMG variability depended on both movement speed and trajectory variability. Lower variability in movements in the presence of greater variability in the related EMGs occurred because of linked variations in agonist and antagonist muscle activities. Variations in the first agonist burst were often compensated for by associated variations in the antagonist and late agonist bursts. These linked variations maintained the limb trajectory relatively constant in spite of large variations in the first agonist burst. Modifications to impulse-variability models are therefore needed to explain compensations for variability in accelerative impulses (produced by the first agonist burst) by linked variations in impulses for deceleration (produced by the antagonist and late agonist bursts).     

Muscle activation is different when the same muscle acts as an agonist or an antagonist during voluntary movement

During movement, the intrinsic muscle force-velocity property decreases the net force for the shortening muscle (agonist) and increases it for the lengthening muscle (antagonist). The authors present a quantitative analysis of the effect of that muscle property on activation and force output of the same muscle acting as agonist and antagonist in fast and medium speed goal-oriented movements. They compared biceps activation and force output when that muscle was the agonist in a series of elbow flexions and when it was the antagonist in a series of elbow extensions. They performed the same analysis for the lateral, long, and medial heads of the triceps muscle. Muscle EMG was about 2 times larger and the angular impulse developed by the modeled contractile torque was up to 3 times larger when the muscle or muscles acted as the agonist than when the same muscle or muscles acted as the antagonist in movements with similar kinematics. The large effect of the muscle force-velocity property strongly suggests that the neural controller must account for intrinsic muscle properties to generate movements with a commonly observed bell-shaped velocity profile.     

Understanding movement control in infants through the analysis of limb intersegmental dynamics

One important component in the understanding of the control of limb movements is the way in which the central nervous system accounts for joint forces and torques that may be generated not only by muscle actions but by gravity and by passive reactions related to the movements of limb segments. In this study, we asked how the neuromotor system of young infants controls a range of active and passive forces to produce a stereotypic, nonintentional movement. We specifically analyzed limb intersegmental dynamics in spontaneous, cyclic leg movements (kicking) of varying intensity in supine 3-month-old human infants. Using inverse dynamics, we calculated the contributions of active (muscular) and passive (motion-dependent and gravitational) torque components at the hip, knee, and ankle joints from three-dimensional limb kinematics. To calculate joint torques, accurate estimates were needed of the limb's anthropometric parameters, which we determined using a model of the human body. Our analysis of limb intersegmental dynamics explicitly quantified the complex interplay of active and passive forces producing the simple, involuntary kicking movements commonly seen in 3-month-old infants. our results revealed that in nonvigorous kicks, hip joint reversal was the result of an extensor torque due to gravity, opposed by the combined flexor effect of the muscle torque and the total motion-dependent torque. The total motion-dependent torque increased as a hip flexor torque in more vigorous kicks; an extensor muscle torque was necessary to counteract the flexor influences of the total motion-dependent torque and, in the case of large ranges of motion, a flexor gravity torque as well. Thus, with changing passive torque influences due to motions of the linked segments, the muscle torques were adjusted to produce a net torque to reverse the kicking motion. As a consequence, despite considerable heterogeneity in the intensity, range of motion, coordination, and movement context of each kick, smooth trajectories resulted from the muscle torque, counteracting and complementing not only gravity but also the motion-dependent torques generated by movement of the linked segments.     

Impulse-variability theory: implications for ballistic, multijoint motor skill performance

Impulse-variability theory (R. A. Schmidt, H. N. Zelaznik, B. Hawkins, J. S. Frank, & J. T. Quinn, 1979) accounts for the curvilinear relationship between the magnitude and resulting variability of the muscular forces that influence the success of goal-directed limb movements. The historical roots of impulse-variability theory are reviewed in the 1st part of this article, including the relationship between movement speed and spatial error. The authors then address the relevance of impulse-variability theory for the control of ballistic, multijoint skills, such as throwing, striking, and kicking. These types of skills provide a stark contrast to the relatively simple, minimal degrees of freedom movements that characterized early research. However, the inherent demand for ballistic force generation is a strong parallel between these simple laboratory tasks and multijoint motor skills. Therefore, the authors conclude by recommending experimental procedures for evaluating the adequacy of impulse variability as a theoretical model within the context of ballistic, multijoint motor skill performance.     

The organization of spontaneous leg movements in newborn infants

Spontaneous, supine kicking in newborn (2- and 4-week-old) infants is described in terms of its temporal structure, interjoint coordination, and muscle activation characteristics as measured by surface electromyography. Phasic kick movements shoed a constrained temporal organization in the movement, but not the pause phases. Hip, knee, and ankle joints moved in temporal and spatial synchrony, and all three joints showed a rhythmical or periodic organization over time. EMGs revealed antagonist coactivation at the initiation of the flexor movement, but little or not extensor activity. The dorsal muscles, the gastrocnemius and hamstrings, showed less activity than the ventral pair, tibialis anterior and quadriceps. Burst and onset-to-peak durations were also constrained. As a result of neural mechanisms and biomechanical forces, newborn leg movements are structured muscle synergies. This organization has implications both for newborn functioning and for later development.     

An impulse-timing theory for reciprocal control of muscular activity in rapid, discrete movements

Much remains to be learned about how agonist and antagonist muscles are controlled during the production of rapid, voluntary movements. In an effort to summarize a wide body of existing knowledge and stimulate future research on this subject, an impulse-timing theory is presented which attempts to predict the activity of reciprocal muscles based on certain characteristics of a movement. The basic tenet of the theory is that variables of movement time, movement distance and inertial load have fairly predictable effects on the underlying muscular activity of the agonist and antagonist muscles during the production of rapid and discrete, voluntary movements. The theory is derived from the kinematic work of Schmidt, Zelaznik, Hawkins, Frank and Quinn (1979) and supporting evidence from studies which have used electromyographic (EMG) recordings of agonist and antagonist muscles during rapid movements. Issues related to synergistic muscle control, central and peripheral control of reciprocal muscle activity, muscle control, and neurological disorder and the relationship between impulse-timing and mass-spring control are discussed in the final section.     

An Impulse-Timing Theory for Reciprocal Control of Muscular Activity in Rapid,Discrete Movements

Much remains to be learned about how agonist and antagonist muscles are controlled during the production of rapid, voluntary movements. In an effort to summarize a wide body of existing knowledge and stimulate future research on this subject, an impulse-timing theory is presented which attempts to predict the activity of reciprocal muscles based on certain characteristics of a movement. The basic tenet of the theory is that variables of movement time, movement distance, and inertial load have fairly predictable effects on the underlying muscular activity of the agonist and antagonist muscles during the production of rapid and discrete, voluntary movements. The theory is derived from the kinematic work of Schmidt, Zelaznik, Hawkins, Frank, and Quinn (1979) and supporting evidence from studies which have used electromyographic (EMG) recordings of agonist and antagonist muscles during rapid movements. Issues related to synergistic muscle control, central and peripheral control of reciprocal muscle activity, muscle control, and neurological disorder and the relationship between impulse-timing and mass-spring control are discussed in the final section.     

Effect of Age and Gender in the Control of Elbow Flexion Movements

In previous studies of rapid elbow movements in young healthy men, characteristic task-dependent changes in the patterns of muscle activation when movement speed or distance was varied have been reported. In the present study, the authors investigated whether age or gender is associated with changes in the patterns of muscle activity previously reported in young men. Arm movements of 10 healthy older and 10 healthy younger participants (5 men and 5 women in each group) were studied. Surface electromyograms (EMGs) from agonist (biceps) and antagonist (triceps) muscles, kinematic and kinetic parameters, as well as anthropometric and strength measures were recorded. All 4 groups of participants showed similar task- (distance or speed) dependent changes in biphasic EMG activity. Similar modulation of the initial rate of rise of the EMG, integrated agonist and antagonist EMG activity, as well as their relative timing were observed in all 4 groups. Those results suggest that older individuals of both genders retain the control strategies for elbow movements used by young individuals. Despite the qualitative similarities in the patterns of muscle activation, the men moved more quickly than the women, and younger participants moved more quickly than older participants. Those performance differences could not be explained in terms of differences in body size and strength alone.     

Effect of age and gender in the control of elbow flexion movements

In previous studies of rapid elbow movements in young healthy men, characteristic task-dependent changes in the patterns of muscle activation when movement speed or distance was varied have been reported. In the present study, the authors investigated whether age or gender is associated with changes in the patterns of muscle activity previously reported in young men. Arm movements of 10 healthy older and 10 healthy younger participants (5 men and 5 women in each group) were studied. Surface electromyograms (EMGs) from agonist (biceps) and antagonist (triceps) muscles, kinematic and kinetic parameters, as well as anthropometric and strength measures were recorded. All 4 groups of participants showed similar task- (distance or speed) dependent changes in biphasic EMG activity. Similar modulation of the initial rate of rise of the EMG, integrated agonist and antagonist EMG activity, as well as their relative timing were observed in all 4 groups. Those results suggest that older individuals of both genders retain the control strategies for elbow movements used by young individuals. Despite the qualitative similarities in the patterns of muscle activation, the men moved more quickly than the women, and younger participants moved more quickly than older participants. Those performance differences could not be explained in terms of differences in body size and strength alone.     

The Effect of Load on Torques in Point-to-Point Arm Movements: A 3D Model

A dynamic, 3-dimensional model was developed to simulate slightly restricted (pronation-supination was not allowed) point-to-point movements of the upper limb under different external loads, which were modeled using 3 objects of distinct masses held in the hand. The model considered structural and biomechanical properties of the arm and measured coordinates of joint positions. The model predicted muscle torques generated by muscles and needed to produce the measured rotations in the shoulder and elbow joints. The effect of different object masses on torque profiles, magnitudes, and directions were studied. Correlation analysis has shown that torque profiles in the shoulder and elbow joints are load invariant. The shape of the torque magnitude-time curve is load invariant but it is scaled with the mass of the load. Objects with larger masses are associated with a lower deflection of the elbow torque with respect to the sagittal plane. Torque direction–time curve is load invariant scaled with the mass of the load. The authors propose that the load invariance of the torque magnitude–time curve and torque direction–time curve holds for object transporting arm movements not restricted to a plane.     

Simulation Studies of Descending and Reflex Control of Fast Movements

Several neurological control strategies for fast head movements are considered using computer simulations of a stretch reflex model. Each control strategy incorporates a different amount of proprioceptive feedback contributing to braking and/or clamping the movement. The model behavior for each control strategy is qualitatively compared to experimental data that includes the agonist and antagonist EMGs, and the head position, velocity, and acceleration. Significance of the study is discussed with respect to the characteristic tri-phasic EMG pattern for fast voluntary movements and the possible roles that the stretch reflex may have in contributing to this pattern of activation.     

Impulse Characteristics in Rapid Movement

Three untested assumptions of the impulse-variability model were examined in two experiments utilizing rapid, uni-planar limb movements. Experiment 1 varied movement distance (A) and movement time (MT) in a rapid-timing paradigm where the subject moved a lever through a certain distance in a certain time. Experiment 2 varied A in a reversal response where the S made a rapid elbow flexion and extension in a given MT. Displacement recordings were made on every trial. KR (knowledge of results) about MT was given after every trial. The results can be summarized as follows: (a) As predicted by the model, variations in impulse size and velocity were directly related to the impulses size; (b) There was no correlation between the accelerative and decelerative impulse durations recorded during the reversal response supporting the notion that the impulses might be independent; (c) Negative correlations (–.20 to –.50) were demonstrated between peak acceleration and impulse duration for both experiments, counter to the predictions of the model; and (d) Counter to the predictions of the model, timing error (VEt) increased as A decreased for rapid-timing responses. When the correlational results are taken into account, the model has the capacity to account for curvilinear relationships between relative timing error and movement speed. Overall, the results suggest that the impulse variability model requires some restructuring before it can be considered a viable model for the control of rapid limb movements.     

Impulse characteristics in rapid movement: implications for impulse-variability models

Three untested assumptions of the impulse-variability model were examined in two experiments utilizing rapid, uni-planar limb movements. Experiment 1 varied movement distance (A) and movement time (MT) in a rapid-timing paradigm where the subject moved a lever through a certain distance in a certain time. Experiment 2 varied A in a reversal response where the S made a rapid elbow flexion and extension in a given MT. Displacement recordings were made on every trial. KR (knowledge of results) about MT was given after every trial. The results can be summarized as follows: (a) As predicted by the model, variations in impulse size and velocity were directly related to the impulses size; (b) There was no correlation between the accelerative and decelerative impulse durations recorded during the reversal response supporting the notion that the impulses might be independent; (c) Negative correlations (-.20 to -.50) were demonstrated between peak acceleration and impulse duration for both experiments, counter to the predictions of the model; and (d) Counter to the predictions of the model, timing error (VEt) increased as A decreased for rapid-timing responses. When the correlational results are taken into account, the model has the capacity to account for curvilinear relationships between relative timing error and movement speed. Overall, the results suggest that the impulse variability model requires some restructuring before it can be considered a viable model for the control of rapid limb movements.     

Time-dependence between upper arm muscles activity during rapid movements: Observation of the proportional effects predicted by the kinematic theory

Rapid human movements can be assimilated to the output of a neuromuscular system with an impulse response modeled by a Delta-Lognormal equation. In such a model, the main assumption concerns the cumulative time delays of the response as it propagates toward the effector following a command. To verify the validity of this assumption, delays between bursts in electromyographic (EMG) signals of agonist and antagonist muscles activated during a rapid hand movement were investigated. Delays were measured between the surface EMG signals of six muscles of the upper limb during single rapid handwriting strokes. From EMG envelopes, regressions were obtained between the timing of the burst of activity produced by each monitored muscle. High correlation coefficients were obtained supporting the proportionality of the cumulative time delays, the basic hypothesis of the Delta-Lognormal model. A paradigm governing the sequence of muscle activities in a rapid movement could, in the long run, be useful for applications dealing with the analysis and synthesis of human movements.     

Directional variability of the isometric force vector produced by the human hand in multijoint planar tasks

Numerous studies have examined control of force magnitude, but relatively little research has considered force direction control. The subjects applied isometric forces to a handle and the authors compared within-trial variability when force is produced in different directions. The standard deviation of the force parallel to the prescribed direction of force production increased linearly with the targeted force level, as did the standard deviation of the force perpendicular to the instructed direction. In contrast, the standard deviation of the angle of force production decreased with increased force level. In the 4 (of 8) instructed force directions where the endpoint force was generated due to a joint torque in only 1 joint (either the shoulder or elbow) the principal component axes in force space were well aligned with the prescribed direction of force production. In the other directions, the variance was approximately equal along the 2 force axes. The variance explained by the first principal component was significantly larger in torque space compared to the force space, and mostly corresponded to positive correlation between the joint torques. Such coordinated changes suggest that the torque variability was mainly due to the variability of the common drive to the muscles serving 2 joints, although this statement needs to be supported by direct studies of muscle activation in the future.     

Directional Variability of the Isometric Force Vector Produced by the Human Hand in Multijoint Planar Tasks

Numerous studies have examined control of force magnitude, but relatively little research has considered force direction control. The subjects applied isometric forces to a handle and the authors compared within-trial variability when force is produced in different directions. The standard deviation of the force parallel to the prescribed direction of force production increased linearly with the targeted force level, as did the standard deviation of the force perpendicular to the instructed direction. In contrast, the standard deviation of the angle of force production decreased with increased force level. In the 4 (of 8) instructed force directions where the endpoint force was generated due to a joint torque in only 1 joint (either the shoulder or elbow) the principal component axes in force space were well aligned with the prescribed direction of force production. In the other directions, the variance was approximately equal along the 2 force axes. The variance explained by the first principal component was significantly larger in torque space compared to the force space, and mostly corresponded to positive correlation between the joint torques. Such coordinated changes suggest that the torque variability was mainly due to the variability of the common drive to the muscles serving 2 joints, although this statement needs to be supported by direct studies of muscle activation in the future.     

Age and gender moderate the effects of localized muscle fatigue on lower extremity joint torques used during quiet stance

This study examined the effects of localized muscle fatigue, age, and gender on lower extremity joint torques used during quiet stance. Thirty-two participants performed exercises designed to fatigue the ankle plantarflexors, knee extensors, torso extensors, or shoulder flexors. Body kinematics and ground reaction forces were obtained both before and after the exercises, and joint torques were derived via inverse dynamics. Single joint fatigue affected torque variability at all lower extremity joints, with similar changes for both age groups. Males and females exhibited increased ankle torque variability after different tasks, with males showing more variability after ankle fatigue and females after shoulder and lumbar fatigue. Correlations between peak torques and torque variability differed between males and females and between age groups in certain cases. The results of this study suggested that both age and gender moderate the effects of fatigue on postural control and should be considered when developing strategies to prevent occupational falls.     

Changes in muscle and joint coordination in learning to direct forces

While it has been suggested that bi-articular muscles have a specialized role in directing external reaction forces, it is unclear how humans learn to coordinate mono- and bi-articular muscles to perform force-directing tasks. Participants were asked to direct pedal forces in a specified target direction during one-legged cycling. We expected that with practice, performance improvement would be associated with specific changes in joint torque patterns and mono- and bi-articular muscular coordination. Nine male participants practiced pedaling an ergometer with only their left leg, and were instructed to always direct their applied pedal force perpendicular to the crank arm (target direction) and to maintain a constant pedaling speed. After a single practice session, the mean error between the applied and target pedal force directions decreased significantly. This improved performance was accompanied by a significant decrease in the amount of ankle angular motion and a smaller increase in knee and hip angular motion. This coincided with a re-organization of lower extremity joint torques, with a decrease in ankle plantarflexor torque and an increase in knee and hip flexor torques. Changes were seen in both mono- and bi-articular muscle activity patterns. The mono-articular muscles exhibited greater alterations, and appeared to contribute to both mechanical work and force-directing. With practice, a loosening of the coupling between bi-articular thigh muscle activation and joint torque co-regulation was observed. The results demonstrated that participants were able to learn a complex and dynamic force-directing task by changing the direction of their applied pedal forces through re-organization of joint torque patterns and mono- and bi-articular muscle coordination.