Co-activation alters the linear versus non-linear impression of the EMG-torque relationship of trunk muscles

The use of electromyographic signals in the modeling of muscle forces and joint loads requires an assumption of the relationship between EMG and muscle force. This relationship has been studied for the trunk musculature and been shown to be predominantly non-linear, with more EMG producing less torque output at higher levels of activation. However, agonist-antagonist muscle co-activation is often substantial during trunk exertions, yet has not been adequately accounted for in determining such relationships. The purpose of this study was to revisit the EMG-moment relationship of the trunk recognizing the additional moment requirements necessitated due to antagonist muscle activity. Eight participants generated a series of isometric ramped trunk flexor and extensor moment contractions. EMG was recorded from 14 torso muscles, and the externally resisted moment was calculated. Agonist muscle moments (either flexor or extensor) were estimated from an anatomically detailed biomechanical model of the spine and fit to: the externally calculated moment alone; the externally calculated moment combined with the antagonist muscle moment. When antagonist activity was ignored, the EMG-moment relationship was found to be non-linear, similar to previous work. However, when accounting for the additional muscle torque generated by the antagonist muscle groups, the relationships became, in three of the four conditions, more linear. Therefore, it was concluded that antagonist muscle co-activation must be included when determining the EMG-moment relationship of trunk muscles and that previous impressions of non-linear EMG-force relationships should be revisited.     

Muscular synergism--I. On criteria for load sharing between synergistic muscles

The use of optimization techniques to predict individual muscle forces in redundant biomechanical systems implies the formulation of a criterion for load sharing between the muscles. In part I of this paper, the characteristics and performance of several linear and non-linear criteria reported in the literature have been compared for static-isometric knee flexion. The results show that linear criteria inherently predict discrete muscle action (orderly recruitment of muscles) whereas non-linear criteria can predict synergistic action. All criteria predict that relatively more force is allocated to muscles with large moment arms. When muscle stresses (or ratios of muscle force to maximum muscle force) are used as the decision variables in the objective function, then relatively more force is allocated to muscles with large maximum possible force as well. Future formulations of the optimization should consider the differences in fiber type composition among the muscles. Such an approach is presented in part II of the paper.     

Analytic analysis of the force sharing among synergistic muscles in one- and two-degree-of-freedom models

Mathematical optimization of specific cost functions has been used in theoretical models to calculate individual muscle forces. Measurements of individual muscle forces and force sharing among individual muscles show an intensity-dependent, non-linear behavior. It has been demonstrated that the force sharing between the cat Gastrocnemius, Plantaris and Soleus shows distinct loops that change orientation systematically depending on the intensity of the movement. The purpose of this study was to prove whether or not static, non-linear optimization could inherently predict force sharing loops between agonistic muscles. Using joint moment data from a step cycle of cat locomotion, the forces in three cat ankle plantar flexors (Gastrocnemius, Plantaris and Soleus) were calculated using two popular optimization algorithms and two musculo-skeletal models. The two musculo-skeletal models included a one-degree-of-freedom model that considered the ankle joint exclusively and a two-degree-of-freedom model that included the ankle and the knee joint. The main conclusion of this study was that solutions of the one-degree-of-freedom model do not guarantee force-sharing loops, but the two-degree-of-freedom model predicts force-sharing loops independent of the specific values of the input parameters for the muscles and the musculo-skeletal geometry. The predicted force-sharing loops were found to be a direct result of the loops formed by the knee and ankle moments in a moment-moment graph.     

A mathematical analysis of the force-stiffness characteristics of muscles in control of a single joint system

Feldman (1966) has proposed that a muscle endowed with its spinal reflex system behaves as a non-linear spring with an adjustable resting length. In contrast, because of the length-tension properties of muscles, many researchers have modeled them as non-linear springs with adjustable stiffness. Here we test the merits of each approach: Initially, it is proven that the adjustable stiffness model predicts that isometric muscle force and stiffness are linearly related. We show that this prediction is not supported by data on the static stiffness-force characteristics of reflexive muscles, where stiffness grows non-linearly with force. Therefore, an intact muscle-reflex system does not behave as a non-linear spring with an adjustable stiffness. However, when the same muscle is devoid of its reflexes, the data shows that stiffness grows linearly with force. We aim to understand the functional advantage of the non-linear stiffness-force relationship present in the reflexive muscle. Control of an inverted pendulum with a pair of antagonist muscles is considered. Using an active-state muscle model we describe force development in an areflexive muscle. From the data on the relationship of stiffness and force in the intact muscle we derive the length-tension properties of a reflexive muscle. It is shown that a muscle under the control of its spinal reflexes resembles a non-linear spring with an adjustable resting length. This provides independent evidence in support of the Feldman hypothesis of an adjustable resting length as the control parameter of a reflexive muscle, but it disagrees with his particular formulation. In order to maintain stability of the single joint system, we prove that a necessary condition is that muscle stiffness must grow at least linearly with force at isometric conditions. This shows that co-contraction of antagonist muscles may actually destabilize the limb if the slope of this stiffness-force relationship is less than an amount specified by the change in the moment arm of the muscle as a function of joint configuration. In a reflexive muscle where stiffness grows faster than linearly with force, co-contraction will always lead to an increase in stiffness. Furthermore, with the reflexive muscles, the same level of joint stiffness can be produced by much smaller muscle forces because of the non-linear stiffness-force relationship. This allows the joint to remain stable at a fraction of the metabolic energy cost associated with maintaining stability with areflexive muscles.This work was supported in part by grant no. 1R01 NS 24926 from the NIH (Michael Arbib, PI). R.S. was supported by an IBM Graduate Fellowship in Computer Science     

Sensitivity of predicted muscle forces to parameters of the optimization-based human leg model revealed by analytical and numerical analyses

There are different opinions in the literature on whether the cost functions: the sum of muscle stresses squared and the sum of muscle stresses cubed, can reasonably predict muscle forces in humans. One potential reason for the discrepancy in the results could be that different authors use different sets of model parameters which could substantially affect forces predicted by optimization-based models. In this study, the sensitivity of the optimal solution obtained by minimizing the above cost functions for a planar three degrees-of-freedom (DOF) model of the leg with nine muscles was investigated analytically for the quadratic function and numerically for the cubic function. Analytical results revealed that, generally, the non-zero optimal force of each muscle depends in a very complex non-linear way on moments at all three joints and moment arms and physiological cross-sectional areas (PCSAs) of all muscles. Deviations of the model parameters (moment arms and PCSAs) from their nominal values within a physiologically feasible range affected not only the magnitude of the forces predicted by both criteria, but also the number of non-zero forces in the optimal solution and the combination of muscles with non-zero predicted forces. Muscle force magnitudes calculated by both criteria were similar. They could change several times as model parameters changed, whereas patterns of muscle forces were typically not as sensitive. It is concluded that different opinions in the literature about the behavior of optimization-based models can be potentially explained by differences in employed model parameters.     

Are skeletal muscles independent actuators? Force transmission from soleus muscle in the cat

It is unclear if skeletal muscles act mechanically as independent actuators. The purpose of the present study was to investigate force transmission from soleus (SO) muscle for physiological lengths as well as relative positions in the intact cat hindlimb. We hypothesized that force transmission from SO fibers will be affected by length changes of its two-joint synergists. Ankle plantar flexor moment on excitation of the SO was measured for various knee angles (70-140 degrees ). This involved substantial length changes of gastrocnemius and plantaris muscles. Ankle angle was kept constant (80 degrees -90 degrees ). However, SO ankle moment was not significantly affected by changes in knee angle; neither were half-relaxation time and the maximal rate of relaxation (P > 0.05). Following tenotomy, SO ankle moment decreased substantially (55 +/- 16%) but did not reach zero, indicating force transmission via connective tissues to the Achilles tendon (i.e., epimuscular myofascial force transmission). During contraction SO muscle shortened to a much greater extent than in the intact case (16.0 +/- 0.6 vs. 1.0 +/- 0.1 mm), which resulted in a major position shift relative to its synergists. If the SO was moved back to its position corresponding to the intact condition, SO ankle moment approached zero, and most muscle force was exerted at the distal SO tendon. Our results also suggested that in vivo the lumped intact tissues linking SO to its synergists are slack or are operating on the toe region of the stress-strain curve. Thus, within the experimental conditions of the present study, the intact cat soleus muscle appears to act mechanically as an independent actuator.     

On the possibility of linear modelling the human arm neuromuscular apparatus

It has been widely claimed that linear models of the neuromuscular apparatus give very inaccurate approximations of human arm reaching movements. The present paper examines this claim by quantifying the contributions of the various non-linear effects of muscle force generation on the accuracy of linear approximation. We performed computer simulations of a model of a two-joint arm with six monarticular and biarticular muscles. The global actions of individual muscles resulted in a linear dependence of the joint torques on the joint angles and angular velocities, despite the great non-linearity of the muscle properties. The effect of time delay in force generation is much more important for model accuracy than all the non-linear effects, while ignoring this time delay in linear approximation results in large errors. Thus, the viscosity coefficients are rather underestimated and some of them can even be paradoxically estimated to be negative. Similarly, our computation showed that ignoring the time delay resulted in large errors in the estimation of the hand equilibrium trajectory. This could explain why experimentally estimated hand equilibrium trajectories may be complex, even during a simple reaching movement. The hand equilibrium trajectory estimated by a linear model becomes simple when the time delay is taken into account, and it is close to that actually used in the non-linear model. The results therefore provide a theoretical basis for estimating the hand equilibrium trajectory during arm reaching movements and hence for estimating the time course of the motor control signals associated with this trajectory, as set out in the equilibrium point hypothesis. Received: 17 February 1999 / Accepted in revised form: 22 October 1999     

Predicted pattern of human muscle activity during clenching derived from a computer assisted model: symmetric vertical bite forces

A computer assisted three-dimensional model of the jaw, based on linear programming, is presented. The upper and lower attachments of the muscles of mastication have been measured on a single human skull and divided into thirteen independent units on each side--a total of 26 muscle elements. The direction (in three dimensions) and maximum forces that could be developed by each muscle element, the bite reaction and two joint reactions are included in the model. It is shown for symmetrical biting that a model which minimizes the sum of the muscle forces used to produce a given bite force activates muscles in a way which corresponds well with previous observations on human subjects. A model which minimizes the joint reactions behaves differently and is rejected. An analysis of the way the chosen model operates suggests that there are two types of jaw muscles, power muscles and control muscles. Power muscles (superficial masseter, medial pterygoid and some of temporalis) produce the bite force but tend to displace the condyle up or down the articular eminence. This displacement is prevented by control muscles (oblique temporalis and lateral pterygoid) which have very poor moment arms for generating usual bite forces, but are efficient for preventing condylar slide. The model incorporates the concept that muscles consist of elements which can contract independently. It predicts that those muscle elements with longer moment arms relative to the joint are the first to be activated and, as the bite force increases, a ripple of activity spreads into elements with shorter moment arms. In general, the model can be used to study the three-dimensional activity in any system of joints and muscles.     

Longer moment arm results in smaller joint moment development, power and work outputs in fast motions

Effects of moment arm length on kinetic outputs of a musculoskeletal system (muscle force development, joint moment development, joint power output and joint work output) were evaluated using computer simulation. A skeletal system of the human ankle joint was constructed: a lower leg segment and a foot segment were connected with a hinge joint. A Hill-type model of the musculus soleus (m. soleus), consisting of a contractile element and a series elastic element, was attached to the skeletal system. The model of the m. soleus was maximally activated, while the ankle joint was plantarflexed/dorsiflexed at a variation of constant angular velocities, simulating isokinetic exercises on a muscle testing machine. Profiles of the kinetic outputs (muscle force development, joint moment development, joint power output and joint work output) were obtained. Thereafter, the location of the insertion of the m. soleus was shifted toward the dorsal/ventral direction by 1cm, which had an effect of lengthening/shortening the moment arm length, respectively. The kinetic outputs of the musculoskeletal system during the simulated isokinetic exercises were evaluated with these longer/shorter moment arm lengths. It was found that longer moment arm resulted in smaller joint moment development, smaller joint power output and smaller joint work output in the larger plantarflexion angular velocity region (>120 degrees/s). This is because larger muscle shortening velocity was required with longer moment arm to achieve a certain joint angular velocity. Larger muscle shortening velocity resulted in smaller muscle force development because of the force-velocity relation of the muscle. It was suggested that this phenomenon should be taken into consideration when investigating the joint moment-joint angle and/or joint moment-joint angular velocity characteristics of experimental data.     

Relationships between individual isometric muscle forces, EMG activity and joint torque in monkeys

The aim of the present work was to determine the EMG activity and the moment of force developed by the main elbow flexor muscles, and to establish on this basis the degree of their participation in isometric contractions performed at various positions of the elbow. This was achieved by recording the following biomechanical parameters: EMG and tensile stress (or force) from biceps brachii (BB) and brachioradialis (BR); EMG from brachialis; external resultant force (FE). There was: a linear or quadratic relationship between the integrated EMG from each muscle and FE; a linear relationship between the force produced by BB or BR and FE. The slope of these relationships depended on the elbow angle, except for that between BB force and FE. It is proposed that iEMG changes compensate for those of the force lever arm. It has been calculated that the contribution of BR to external torque decreased from the extension to flexion while that of BB increased from 70 degrees to 90 degrees and then decreased. How far these data can be extrapolated to man is a matter of discussion based on iEMG and anthropometrical data.     

In vivo moment arm determination using B-mode ultrasonography

The tendon excursion of the tibialis anterior (TA) muscle was measured in vivo using B-mode ultrasonography in seven subjects under three force levels (0, 30 and 60% maximal voluntary contraction, MVC). For each force level, the TA moment arm (m) was determined by calculating the derivative of the tendon excursion relative to the ankle angle (a). A dynamometer controlled the ankle angle while force levels were monitored. The parametric model proposed by Miller and Dennis (1996), m = R sin(a + delta), where R is the largest moment arm and delta represents the offset angle of R from 90 degrees, was used in a least-squares fit of the relationship between moment arm and ankle angle. The R values at 0% MVC were significantly smaller than those at 30 and 60% MVC. The values of calculated moment arm at 0% MVC were not considered adequate estimates of the TA moment arm because of the possible confounding effect of the slackness of the relaxed muscle-tendon unit in more dorsiflexed positions. The moment arm values at 30 and 60% MVC were believed to provide reliable estimates of those of TA since the application of tension probably reduced the effects of the slackness of the muscle-tendon unit and tendon elongation on tendon excursion measurement at these force levels. Since the ultrasonographic technique is an in vivo application of the tendon excursion technique and therefore takes the functional meaning into consideration, it can yield more significant moment arms than other in vivo or cadaver techniques.     

Passive force characteristics of an architecturally complex muscle

In architecturally complex muscles with large attachment areas, it can be expected that during movement different muscle regions undergo different amounts of length excursions. As a consequence, the amount of passive force produced by the regions will differ. Therefore, we tested the hypothesis that during movement the vector of the passive force of such a muscle, which defines the magnitude, position and orientation of the resultant force of the various regions, has no fixed position, between the muscle's center of origin and insertion. As a model for an architecturally complex muscle we used the masseter muscle. It was expected that during jaw opening anterior muscle regions are more stretched than posterior regions, leading to an anterior shift of the passive force vector. A three-component force transducer was used to measure both the position and magnitude of passive force in the masseter muscle of 9 rabbits. Forces were recorded during repeated cycles of stepwise opening and closure of the jaw. The muscle exhibited a clear hysteresis: passive force measured during jaw opening was larger than that during jaw closing. With an increase of the jaw gape there was an approximately exponential increase of the magnitude of the passive muscle force, while simultaneously the passive force vector shifted anteriorly. Moment arm length of passive force increased by about 100%. This anterior shift contributed substantially to the increase of the passive muscle moment generated during jaw opening. It can be concluded that in architecturally complex muscles the increase of the passive resistance moment which is associated with muscle lengthening might not only be due to an increase of the magnitude of passive muscle force but also to an increase of the moment arm of this force.     

Twitch interpolation technique in testing of maximal muscle strength: Influence of potentiation, force level, stimulus intensity and preload

The aim was to study the methodological aspects of the muscle twitch interpolation technique in estimating the maximal force of contraction in the quadriceps muscle utilizing commercial muscle testing equipment. Six healthy subjects participated in seven sets of experiments testing the effects on twitch size of potentiation, time lag after potentiation, magnitude of voluntary force, stimulus amplitude, stimulus duration, angle of the knee, and angle of the hip. In addition, the consequences of submaximal potentiation on the estimation of maximal force from twitch sizes were studied in five healthy subjects. We found an increase in twitch size with increasing levels of potentiation and twitch size decreased exponentially following potentiation. We found a curvilinear relationship between twitch size and voluntary force, and these properties were more obvious when the stimulation intensity of the preload was reduced. The relationship between twitch size and force was only linear, for force levels greater than 25% of maximum. It was concluded that to achieve an accurate estimate of true maximal force of muscle contraction, it would be necessary for the subject to be able to perform at least 75% of the true maximal force.     

Mechanical effect of rat flexor carpi ulnaris muscle after tendon transfer: does it generate a wrist extension moment?

The mechanical effect of a muscle following agonist-to-antagonist tendon transfers does not always meet the surgeon's expectations. We tested the hypothesis that after flexor carpi ulnaris (FCU) to extensor carpi radialis (ECR) tendon transfer in the rat, the direction (flexion or extension) of the muscle's joint moment is dependent on joint angle. Five weeks after recovery from surgery (tendon transfer group) and in a control group, wrist angle-moment characteristics of selectively activated FCU muscle were assessed for progressive stages of dissection: 1) with minimally disrupted connective tissues, 2) after distal tenotomy, and 3) after maximal tendon and muscle belly dissection, but leaving blood supply and innervations intact. In addition, force transmission from active FCU onto the distal tendon of passive palmaris longus (PL) muscle (a wrist flexor) was assessed. Excitation of control FCU yielded flexion moments at all wrist angles tested. Tenotomy decreased peak FCU moment substantially (by 93%) but not fully. Only after maximal dissection, FCU wrist moment became negligible. The mechanical effect of transferred FCU was bidirectional: extension moments in flexed wrist positions and flexion moments in extended wrist positions. Tenotomy decreased peak extension moment (by 33%) and increased peak flexion moment of transferred FCU (by 41%). Following subsequent maximal FCU dissection, FCU moments decreased to near zero at all wrist angles tested. We confirmed that, after transfer of FCU towards a wrist extensor insertion, force can be transmitted from active FCU to the distal tendon of passive PL. We conclude that mechanical effects of a muscle after tendon transfer to an antagonistic site can be quite different from those predicted based solely on the sign of the new moment arm at the joint.     

Inversion–eversion moment arms of gastrocnemius and tibialis anterior measured in vivo

In this study, the frontal plane moment arms of tibialis anterior (TA) and the lateral and medial heads of gastrocnemius (LG and MG) were determined using ultrasonography of ten healthy subjects. Analysis of variance was performed to investigate the effects of frontal plane angle, muscle activity, and plantarflexion angle on inversion–eversion moment arm for each muscle. The moment arms of each muscle were found to vary with frontal plane angle (all p<0.001). TA and LG exhibited eversion moment arms when the foot was everted, but MG was found to have a slight inversion moment arm in this position. As the ankle rotated from 0° to 20° inversion, the inversion moment arm of each increased, indicating that the three muscles became increasingly effective inverters. In neutral position, the inverter moment arm of MG was greater than that of LG (p=0.001). Muscle activity had a significant effect on both LG and MG moment arm at all frontal plane positions (all p0.005). These results demonstrate the manner in which frontal plane moment arms of gastrocnemius and TA differ across the frontal plane range of motion in healthy subjects. This method for assessing muscle action in vivo used in this study may prove useful for subject-specific planning of surgical treatments for frontal plane foot and ankle deformities.     

Measurement of human Gracilis muscle isometric forces as a function of knee angle,intraoperatively

The goals of the present study were (1) to measure the previously unstudied isometric forces of activated human Gracilis (G) muscle as a function of knee joint angle and (2) to test whether length history effects are important also for human muscle. Experiments were conducted intraoperatively during anterior cruciate ligament (ACL) reconstruction surgery (n=8). Mean peak G muscle force, mean peak G tendon stress and mean optimal knee angle equals 178.5±270.3 N, 24.4±20.6 MPa and 67.5±41.7°, respectively. The substantial inter-subject variability found (e.g., peak G force ranges between 17.2 and 490.5 N) indicate that the contribution of the G muscle to knee flexion moment may vary considerably among subjects. Moreover, typical subject anthropometrics did not appear to provide a sound estimate of the peak G force: only a limited insignificant correlation was found between peak G force and subject mass as well as mid-thigh perimeter and no correlation was found between peak G force and thigh length. The functional joint range of motion for human G muscle was determined to be at least as wide as full knee extension to 120° of knee flexion. However; the portion of the knee angle–muscle force relationship operationalized is not unique but individual specific: our data suggest for most subjects that G muscle operates in both ascending and descending limbs of its length–force characteristics whereas, for the remainder of the subjects, its function is limited to the descending limb, exclusively. Previous activity of G muscle at high muscle length attained during collection of a complete set of knee angle–force data showed for the first time that such length history effects are important also for human muscles: a significant correlation was found between optimal knee angle and absolute value of % force change. Except for two of the subjects, G muscle force measured at low length was lower than that measured during collection of knee joint–force data (maximally by 42.3%).     

In vivo moment arm lengths for hip extensor muscles at different angles of hip flexion

Moment arm lengths of three hip extensor muscles, the gluteus maximus, the hamstrings and the adductor magnus, were determined at hip flexion angles from 0 degrees to 90 degrees by combining data from ten autopsy specimens and from twenty patients, the latter examined by computed tomography. A straight-line muscle model for muscle force was used for the hamstrings and adductor magnus, and for the gluteus maximus a two-segment straight-line muscle force model was used. With the joint in its anatomical position the moment arm of the gluteus maximus to the bilateral motion axis averaged 79 mm, for the hamstrings 61 mm and for the adductor magnus 15 mm. The moment arm of gluteus maximus decreased with increasing hip flexion angle. The hamstrings showed an increase in moment arm length up to an average of 35 degrees hip flexion and then a decrease with increasing hip flexion angle. The corresponding figures for the adductor magnus moment arm showed an increase up to 75 degrees and then a decrease. Statistical analysis revealed significant differences in moment arm length between men and women.     

A parametric model of muscle moment arm as a function of joint angle: Application to the dorsiflexor muscle group in mice

A parametric model was developed to describe the relationship between muscle moment arm and joint angle. The model was applied to the dorsiflexor muscle group in mice, for which the moment arm was determined as a function of ankle angle. The moment arm was calculated from the torque measured about the ankle upon application of a known force along the line of action of the dorsiflexor muscle group. The dependence of the dorsiflexor moment arm on ankle angle was modeled as r=R sin(a+Δ), where r is the moment arm calculated from the measured torque and a is the joint angle. A least-squares curve fit yielded values for R, the maximum moment arm, and Δ, the angle at which the maximum moment arm occurs as offset from 90°. Parametric models were developed for two strains of mice, and no differences were found between the moment arms determined for each strain. Values for the maximum moment arm, R, for the two different strains were 0.99 and 1.14 mm, in agreement with the limited data available from the literature. While in some cases moment arm data may be better fitted by a polynomial, use of the parametric model provides a moment arm relationship with meaningful anatomical constants, allowing for the direct comparison of moment arm characteristics between different strains and species.     

Torso flexion modulates stiffness and reflex response.

Neuromuscular factors that contribute to spinal stability include trunk stiffness from passive and active tissues as well as active feedback from reflex response in the paraspinal muscles. Trunk flexion postures are a recognized risk factor for occupational low-back pain and may influence these stabilizing control factors. Sixteen healthy adult subjects participated in an experiment to record trunk stiffness and paraspinal muscle reflex gain during voluntary isometric trunk extension exertions. The protocol was designed to achieve trunk flexion without concomitant influences of external gravitational moment, i.e., decouple the effects of trunk flexion posture from trunk moment. Systems identification analyses identified reflex gain by quantifying the relation between applied force disturbances and time-dependent EMG response in the lumbar paraspinal muscles. Trunk stiffness was characterized from a second order model describing the dynamic relation between the force disturbances versus the kinematic response of the torso. Trunk stiffness increased significantly with flexion angle and exertion level. This was attributed to passive tissue contributions to stiffness. Reflex gain declined significantly with trunk flexion angle but increased with exertion level. These trends were attributed to correlated changes in baseline EMG recruitment in the lumbar paraspinal muscles. Female subjects demonstrated greater reflex gain than males and the decline in reflex gain with flexion angle was greater in females than in males. Results reveal that torso flexion influences neuromuscular factors that control spinal stability and suggest that posture may contribute to the risk of instability injury.