Influence of muscle shortening on the geometry of gastrocnemius medialis muscle of the rat

For static and dynamic conditions muscle geometry of the musculus gastrocnemius medialis of the rat was compared at different muscle lengths. The dynamic conditions differed with respect to isokinetic shortening velocity (25, 50 and 75 mm/s) of the muscle-tendon complex and in constancy of force (isotonic) and velocity (isokinetic) during shortening. Muscle geometry was characterized by fibre length and angle as well as aponeurosis length and angle. At high isokinetic shortening velocities (50 and 75 mm/s) small differences in geometry were found with respect to isometric conditions: aponeurosis lengths differed maximally by -2%, fibre length only showed a significant increase (+3.2%) at the highest shortening velocity. The isotonic condition only yielded significant differences of fibre angle (-4.5%) in comparison with isometric conditions. No significant differences of muscle geometry were found when comparing isotonic with isokinetic conditions of similar shortening velocity. The small differences of geometry between isometric and dynamic conditions are presumably due to the lower muscle force in the dynamic condition and the elastic behaviour of the aponeurosis. It is concluded that, unless very high velocities of shortening are used, the relationship between muscle geometry and muscle length in the isometric condition may be used to describe muscle geometry in the dynamic condition.     

A phenomenological model for estimating metabolic energy consumption in muscle contraction

A phenomenological model for muscle energy consumption was developed and used in conjunction with a simple Hill-type model for muscle contraction. The model was used to address two questions. First, can an empirical model of muscle energetics accurately represent the total energetic behavior of frog muscle in isometric, isotonic, and isokinetic contractions? And second, how does such a model perform in a large-scale, multiple-muscle model of human walking? Four simulations were conducted with frog sartorius muscle under full excitation: an isometric contraction, a set of isotonic contractions with the muscle shortening a constant distance under various applied loads, a set of isotonic contractions with the muscle shortening over various distances under a constant load, and an isokinetic contraction in lengthening. The model calculations were evaluated against results of similar thermal in vitro experiments performed on frog sartorius muscle. The energetics model was then incorporated into a large-scale, multiple-muscle model of the human body for the purpose of predicting energy consumption during normal walking. The total energy estimated by the model accurately reflected the observed experimental behavior of frog muscle for an isometric contraction. The model also accurately reproduced the experimental behavior of frog muscle heat production under isotonic shortening and isokinetic lengthening conditions. The estimated rate of metabolic energy consumption for walking was 29% higher than the value typically obtained from gait measurements.     

Effects of speed and distance of muscle shortening on force depression during voluntary contractions

The purpose of this study was to determine the influence of speed and distance of muscle shortening on the amount of force depression for voluntary contractions. Two experimental tests were performed. In the first test, subjects performed isometric knee extensor contractions following muscle shortening produced by isokinetic knee extensions over the range 25-50 degrees. In the second test, subjects performed isometric knee extensor contractions following muscle shortening produced by isokinetic knee extensions at two speeds: 20 and 240 degrees /s. Knee extensor moments, surface electromyographical (EMG) signals of quadriceps femoris, and interpolated twitch moments were measured during all contractions and were compared with the corresponding values obtained during purely isometric contractions. Force depression following muscle shortening for the voluntary contractions tested in this study did not depend on the distance or the speed of muscle shortening. These results are in contrast to the corresponding results in the literature obtained using artificial electrical stimulation in which force depression was always found to be directly related to the distance of shortening and inversely related to the speed of shortening. The difference in force depression as a function of the distance and speed of muscle shortening between voluntary and artificial electrical stimulation may be associated with changes in activation following the voluntary shortening contractions, whereas activation is controlled and constant in all artificial stimulation protocols.     

Dynamic performance of a load-moving skeletal muscle

The dynamic response of the tibialis anterior muscle of the cat was determined while it was subjected to sinusoidally varying orderly stimulation of motor units and to different isotonic loads in the range of 14-85% of the maximal isometric force. The dynamic response consisted of three major components: the displacement gain, the displacement attenuation, and a pure time delay. The displacement gain was dependent on the passive load applied to the muscle and the active force generated during contraction, which could be determined from the length-tension relationships and the corresponding shortening velocity. In general, the load displacement decreased as the load mass increased from 25 to 85% of the maximal isometric force. For loads less than 25% of the maximal isometric force, slight decrease in displacement was consistently observed. The displacement attenuation was dependent on the contraction frequency but uniform for all the load masses applied to the muscle. A pure time delay of 5 ms was present and accounted for various physiological processes such as conduction time in nerve and muscle, neuromuscular junction transmission, and excitation-contraction coupling. A quantitative equation was developed to describe the muscle's dynamic response under isotonic conditions and for a wide range of loads for use in various applications.     

Active and passive components in the length-dependent stiffness of tracheal smooth muscle during isotonic shortening.

Contraction of smooth muscle tissue involves interactions between active and passive structures within the cells and in the extracellular matrix. This study focused on a defined mechanical behavior (shortening-dependent stiffness) of canine tracheal smooth muscle tissues to evaluate active and passive contributions to tissue behavior. Two approaches were used. In one, mechanical measurements were made over a range of temperatures to identify those functions whose temperature sensitivity (Q(10)) identified them as either active or passive. Isotonic shortening velocity and rate of isometric force development had high Q(10) values (2.54 and 2.13, respectively); isometric stiffness showed Q(10) values near unity. The shape of the curve relating stiffness to isotonic shortening lengths was unchanged by temperature. In the other approach, muscle contractility was reduced by applying a sudden shortening step during the rise of isometric tension. Control contractions began with the muscle at the stepped length so that properties were measured over comparable length ranges. Under isometric conditions, redeveloped isometric force was reduced, but the ratio between force and stiffness did not change. Under isotonic conditions beginning during force redevelopment at the stepped length, initial shortening velocity and the extent of shortening were reduced, whereas the rate of relaxation was increased. The shape of the curve relating stiffness to isotonic shortening lengths was unchanged, despite the step-induced changes in muscle contractility. Both sets of findings were analyzed in the context of a quasi-structural model describing the shortening-dependent stiffness of lightly loaded tracheal muscle strips.     

In vivo and in vitro correlation of trachealis muscle contraction in dogs.

Maximal trachealis muscle shortening in vivo was compared with that in vitro in seven anesthetized dogs. In addition, the effect of graded elastic loads on the muscle was evaluated in vitro. In vivo trachealis muscle shortening, as measured using sonomicrometry, revealed maximal active shortening to be 28.8 +/- 11.7% (SD) of initial length. Trachealis muscle preparations from the same animals were studied in vitro to evaluate isometric force generation, isotonic shortening, and the effect of applying linear elastic loads to the trachealis muscle during contraction from optimal length. Maximal isotonic shortening was 66.8 +/- 8.4% of optimal length in vitro. Increasing elastic loads decreased active shortening and velocity of shortening in vitro in a hyperbolic manner. The elastic load required to decrease in vitro shortening to the extent of the shortening observed in vivo was similar to the estimated load provided by the tracheal cartilage. We conclude that decreased active shortening in vivo is primarily due to the elastic afterload provided by cartilage.     

Isokinetic plantar flexion: experimental results and model calculations

In isokinetic experiments on human subjects, conducted to determine moments that can be exerted about a joint at different angular velocities, joint rotation starts as soon as the moment increases above the resting level. This contraction history differs from the one in experiments on isolated muscle, where the force is allowed to increase to an isometric level before shortening is initiated. The purpose of the present study was to determine the influence of contraction history on plantar flexing moments found during maximal voluntary plantar flexion on an isokinetic dynamometer. In ten subjects, plantar flexing moments were measured as a function of ankle angle at different angular velocities. They were also calculated using a model of the muscle-tendon complex of the human triceps surae. The model incorporates elastic tendinous tissue in series with muscle fibers. The input of the model consists of time histories of active state (the force generating capacity of contractile elements) and shortening velocity of the muscle-tendon complex. Different time courses of active state were offered at fixed length of the muscle-tendon complex. The time course yielding a close match between the calculated rise of plantar flexing moment and the rise measured during fixed angle contractions was used to calculate moment-angle curves for isokinetic plantar flexion. The active state value reached when a peak occurred in calculated moment-angle curves was found to be lower if the angular velocity was made higher. Comparing measured and calculated results, it was concluded that moment-angular velocity diagrams determined in studies of isokinetic plantar flexion in human subjects reflect not only the influence of shortening velocity of contractile elements on the force which can be produced by plantar flexors.     

The measurement of force/velocity relationships of fresh and fatigued human adductor pollicis muscle

The purpose of the study was to obtain force/velocity relationships for electrically stimulated (80 Hz) human adductor pollicis muscle (n = 6) and to quantify the effects of fatigue. There are two major problems of studying human muscle in situ; the first is the contribution of the series elastic component, and the second is a loss of force consequent upon the extent of loaded shortening. These problems were tackled in two ways. Records obtained from isokinetic releases from maximal isometric tetani showed a late linear phase of force decline, and this was extrapolated back to the time of release to obtain measures of instantaneous force. This method gave usable data up to velocities of shortening equivalent to approximately one-third of maximal velocity. An alternative procedure (short activation, SA) allowed the muscle to begin shortening when isometric force reached a value that could be sustained during shortening (essentially an isotonic protocol). At low velocities both protocols gave very similar data (r2 = 0.96), but for high velocities only the SA procedure could be used. Results obtained using the SA protocol in fresh muscle were compared to those for muscle that had been fatigued by 25 s of ischaemic isometric contractions, induced by electrical stimulation at the ulnar nerve. Fatigue resulted in a decrease of isometric force [to 69 (3)%], an increase in half-relaxation time [to 431 (10)%], and decreases in maximal shortening velocity [to 77 (8)%] and power [to 42 (5)%]. These are the first data for human skeletal muscle to show convincingly that during acute fatigue, power is reduced as a consequence of both the loss of force and slowing of the contractile speed.     

Behavior of human muscle fascicles during shortening and lengthening contractions in vivo.

The aim of the present study was to investigate the behavior of human muscle fascicles during dynamic contractions. Eight subjects performed maximal isometric dorsiflexion contractions at six ankle joint angles and maximal isokinetic concentric and eccentric contractions at five angular velocities. Tibialis anterior muscle architecture was measured in vivo by use of B-mode ultrasonography. During maximal isometric contraction, fascicle length was shorter and pennation angle larger compared with values at rest (P < 0.01). During isokinetic concentric contractions from 0 to 4.36 rad/s, fascicle length measured at a constant ankle joint angle increased curvilinearly from 49.5 to 69.7 mm (41%; P < 0.01), whereas pennation angle decreased curvilinearly from 14.8 to 9.8 degrees (34%; P < 0.01). During eccentric muscle actions, fascicles contracted quasi-isometrically, independent of angular velocity. The behavior of muscle fascicles during shortening contractions was believed to reflect the degree of stretch applied to the series elastic component, which decreases with increasing contraction velocity. The quasi-isometric behavior of fascicles during eccentric muscle actions suggests that the series elastic component acts as a mechanical buffer during active lengthening.     

Velocity transients and viscoelastic resistance to active shortening in cat papillary muscle.

When isotonic force steps were applied to activated papillary muscles, the velocity was almost never constant. Early rapid shortening associated with the step persisted for 2-7 ms after the step ends. The early rapid shortening is attributed to lightly damped series elastic recoil and velocity transients of the contractile elements. In most steps, the subsequent velocity declines progressively with shortening, and most of the decline in velocity can be accounted for by compression of a viscoelastic element in parallel with the contractile elements. To demonstrate this, the time course of isotonic velocity was compared with a model in which the force-velocity characteristics of the contractile element were assumed to be constant, and the decline in velocity was due to increasing compression of the viscoelastic element. This model predicted the observed results except that the predicted velocities rose progressively above the measured values for steps to light loads applied late in the twitch, and fell below the velocity trace for heavy loads applied early in the twitch. These deviations would occur if rapid shortening caused deactivation late in the twitch, and if activation were rising early in the twitch. A conditioning step applied to the muscle during the rise of force depressed both isometric force and maximum velocity measured at the peak of force; isometric force was more depressed with later conditioning steps than with earlier steps, while maximum velocity was depressed by about the same extent with both early and late steps. This difference between the effects on isometric force and maximum velocity are explained by a combination of deactivation and viscoelastic load.     

Force depression decays during shortening in the medial gastrocnemius of the rat

Force depression due to shortening of activated skeletal muscles has previously been described to be long lasting during isometric contractions following the shortening. In the present study, using the medial gastrocnemius of the rat, effects of force depression have been made apparent during shortening by computationally partially compensating for the direct effect of shortening velocity due to the tension–velocity relation. Evidence was found for the decay and complete disappearance of force depression already during continuation of the shortening contraction to short muscle lengths.     

Force depression following muscle shortening in sub-maximal voluntary contractions of human adductor pollicis

Mechanical properties of skeletal muscles are often studied for controlled, electrically induced, maximal, or supra-maximal contractions. However, many mechanical properties, such as the force-length relationship and force enhancement following active muscle stretching, are quite different for maximal and sub-maximal, or electrically induced and voluntary contractions. Force depression, the loss of force observed following active muscle shortening, has been observed and is well documented for electrically induced and maximal voluntary contractions. Since sub-maximal voluntary contractions are arguably the most important for everyday movement analysis and for biomechanical models of skeletal muscle function, it is important to study force depression properties under these conditions. Therefore, the purpose of this study was to examine force depression following sub-maximal, voluntary contractions. Sets of isometric reference and isometric-shortening-isometric test contractions at 30% of maximal voluntary effort were performed with the adductor pollicis muscle. All reference and test contractions were executed by controlling force or activation using a feedback system. Test contractions included adductor pollicis shortening over 10 degrees, 20 degrees, and 30 degrees of thumb adduction. Force depression was assessed by comparing the steady-state isometric forces (activation control) or average electromyograms (EMGs) (force control) following active muscle shortening with those obtained in the corresponding isometric reference contractions. Force was decreased by 20% and average EMG was increased by 18% in the shortening test contractions compared to the isometric reference contractions. Furthermore, force depression was increased with increasing shortening amplitudes, and the relative magnitudes of force depression were similar to those found in electrically stimulated and maximal contractions. We conclude from these results that force depression occurs in sub-maximal voluntary contractions, and that force depression may play a role in the mechanics of everyday movements, and therefore may have to be considered in biomechanical models of human movement.     

Dynamic and steady state characteristics of the rabbit gastrocnemius muscle determined in series measurements

1. Within the range of the given conditions of measuring static and dynamic properties of the rabbit gastrocnemius muscle the following results were obtained: a) the dependence of the maxima of isotonic shortening upon the relative length of the muscle at constant load is linear; b) the parameters of the non-linear dependence of the passive elastic force of the muscle upon its relative length (measured in series) were identified using asymptotic regression; c) the time course of isotonic contractions (at an interval from 0 to 0.3 s after the beginning of stimulation) could be satisfactorily approximated by responses of a linear system to a step-function; d) the time course of isometric contractions (at an interval from 0 to 0.3 s after the beginning of stimulation) could be closely approximated by responses of a linear system to a step-function. 2. The time constants of isotonic and isometric contractions were determined as the parameters of the corresponding linear systems. 3. The maximum rates of the isometric and isotonic contractions were determined as maxima of the first derivatives of the responses of the corresponding models. 4. The experimental set-up made it possible to compare the values of the parameters concomitantly followed at various muscle lengths and at various loads.     

Force depression in human quadriceps femoris following voluntary shortening contractions.

The purpose of this study was to investigate whether the isometric muscle force, redeveloped following maximal-effort voluntary shortening contractions in human skeletal muscle, is smaller than the purely isometric muscle force at the corresponding length. Isometric knee extensor moments, surface electromyographic (EMG) signals of quadriceps femoris, and interpolated twitch moments (ITMs) were measured while 10 subjects performed purely isometric knee extensor contractions at a 60 degrees knee angle and isometric knee extensor contractions at a 60 degrees knee angle preceded by maximal-effort voluntary shortening of the quadriceps muscles. It was found that the knee extensor moments were significantly decreased for the isometric-shortening-isometric contractions compared with the isometric contractions for the group as a whole, whereas the corresponding EMG and ITM values were the same. This study is the first to demonstrate force depression following muscle shortening for voluntary contractions. We concluded that force depression following muscle shortening is an actual property of skeletal muscle rather than a stimulation artifact and that force depression during voluntary contraction is not accompanied by systematic changes in muscle activation as evaluated by EMG and ITM.     

Attenuated fatigue in slow twitch skeletal muscle during isotonic exercise in rats with chronic heart failure

During isometric contractions, slow twitch soleus muscles (SOL) from rats with chronic heart failure (chf) are more fatigable than those of sham animals. However, a muscle normally shortens during activity and fatigue development is highly task dependent. Therefore, we examined the development of skeletal muscle fatigue during shortening (isotonic) contractions in chf and sham-operated rats. Six weeks following coronary artery ligation, infarcted animals were classified as failing (chf) if left ventricle end diastolic pressure was >15 mmHg. During isoflurane anaesthesia, SOL with intact blood supply was stimulated (1s on 1s off) at 30 Hz for 15 min and allowed to shorten isotonically against a constant afterload. Muscle temperature was maintained at 37°C. In resting muscle, maximum isometric force (F(max)) and the concentrations of ATP and CrP were not different in the two groups. During stimulation, F(max) and the concentrations declined in parallel sham and chf. Fatigue, which was evident as reduced shortening during stimulation, was also not different in the two groups. The isometric force decline was fitted to a bi-exponential decay equation. Both time constants increased transiently and returned to initial values after approximately 200 s of the fatigue protocol. This resulted in a transient rise in baseline tension between stimulations, although this effect which was less prominent in chf than sham. Myosin light chain 2s phosphorylation declined in both groups after 100 s of isotonic contractions, and remained at this level throughout 15 min of stimulation. In spite of higher energy demand during isotonic than isometric contractions, both shortening capacity and rate of isometric force decline were as well or better preserved in fatigued SOL from chf rats than in sham. This observation is in striking contrast to previous reports which have employed isometric contractions to induce fatigue.     

The biphasic force-velocity relationship in whole rat skeletal muscle in situ.

Edman has reported that the force-velocity relationship (FVR) departs from Hill's classic hyperbola near 0.80 of measured isometric force (J Physiol 404: 301-321, 1988). The purpose of this study was to investigate the biphasic nature of the FVR in the rested state and after some recovery from fatigue in the rat medial gastrocnemius muscle in situ. Force-velocity characteristics were determined before and during recovery from fatigue induced by intermittent stimulation at 170 Hz for 100 ms each second for 6 min. Force-velocity data were obtained for isotonic contractions with 100 ms of 200-Hz stimulation, including several measurements with loads above 0.80 of measured isometric force. The force-velocity data obtained in this study were fit well by a double-hyperbolic equation. A departure from Hill's classic hyperbola was found at 0.88+/-0.01 of measured isometric force, which is higher than the approximately 0.80 reported by Edman et al. for isolated frog fibers. After 45 min of recovery, maximum shortening velocity was 86+/-2% of prefatigue, but neither curvature nor predicted isometric force was significantly different from prefatigue. The location of the departure from Hill's classic hyperbola was not different after this recovery from the fatiguing contractions. Including an isometric point in the data set will not yield the same values for maximal velocity and the degree of curvature as would be obtained using the double hyperbola approach. Data up to 0.88 of measured isometric force can be used to fit data to the Hill equation.     

Residual force enhancement following eccentric induced muscle damage

During lengthening of an activated skeletal muscle, the force maintained following the stretch is greater than the isometric force at the same muscle length. This is termed residual force enhancement (RFE), but it is unknown how muscle damage following repeated eccentric contractions affects RFE. Using the dorsiflexors, we hypothesised muscle damage will impair the force generating sarcomeric structures leading to a reduction in RFE. Following reference maximal voluntary isometric contractions (MVC) in 8 young men (26.5±2.8y) a stretch was performed at 30°/s over a 30° ankle excursion ending at the same muscle length as the reference MVCs (30° plantar flexion). Surface electromyography (EMG) of the tibialis anterior and soleus muscles was recorded during all tasks. The damage protocol involved 4 sets of 25 isokinetic (30°/s) lengthening contractions. The same measures were collected at baseline and immediately post lengthening contractions, and for up to 10min recovery. Following the lengthening contraction task, there was a 30.3±6.4% decrease in eccentric torque (P<0.05) and 36.2±9.7% decrease in MVC (P<0.05) compared to baseline. Voluntary activation using twitch interpolation and RMS EMG amplitude of the tibialis anterior remained near maximal without increased coactivation for MVC. Contrary to our hypothesis, RFE increased (～100-250%) following muscle damage (P<0.05). It appears stretch provided a mechanical strategy for enhanced muscle function compared to isometric actions succeeding damage. Thus, active force of cross-bridges is decreased because of impaired excitation-contraction coupling but force generated during stretch remains intact because force contribution from stretched sarcomeric structures is less impaired.     

Recruitment of single human low-threshold motor units with increasing loads at different muscle lengths.

We investigated the recruitment behaviour of low threshold motor units in flexor digitorum superficialis by altering two biomechanical constraints: the load against which the muscle worked and the initial muscle length. The load was increased using isotonic (low load), loaded dynamic (intermediate load) and isometric (high load) contractions in two studies. The initial muscle position reflected resting muscle length in series A, and a longer length with digit III fully extended in series B. Intramuscular EMG was recorded from 48 single motor units in 10 experiments on five healthy subjects, 21 units in series A and 27 in series B, while subjects performed ramp up, hold and ramp down contractions. Increasing the load on the muscle decreased the force, displacement and firing rate of single motor units at recruitment at shorter muscle lengths (P<0.001, dependent t-test). At longer muscle lengths this recruitment pattern was observed between loaded dynamic and isotonic contractions, but not between isometric and loaded dynamic contractions. Thus, the recruitment properties of single motor units in human flexor digitorum superficialis are sensitive to changes in both imposed external loads and the initial length of the muscle.     

Complex myograph allows the examination of complex muscle contractions for the assessment of muscle force, shortening, velocity, and work in vivo

Background

The devices used for in vivo examination of muscle contractions assess only pure force contractions and the so-called isokinetic contractions. In isokinetic experiments, the extremity and its muscle are artificially moved with constant velocity by the measuring device, while a tetanic contraction is induced in the muscle, either by electrical stimulation or by maximal voluntary activation. With these systems, experiments cannot be performed at pre-defined, constant muscle length, single contractions cannot be evaluated individually and the separate examination of the isometric and the isotonic components of single contractions is not possible.

Methods

The myograph presented in our study has two newly developed technical units, i.e. a). a counterforce unit which can load the muscle with an adjustable, but constant force and b). a length-adjusting unit which allows for both the stretching and the contraction length to be infinitely adjustable independently of one another. The two units support the examination of complex types of contraction and store the counterforce and length-adjusting settings, so that these conditions may be accurately reapplied in later sessions.

Results

The measurement examples presented show that the muscle can be brought to every possible pre-stretching length and that single isotonic or complex isometric-isotonic contractions may be performed at every length. The applied forces act during different phases of contraction, resulting into different pre- and after-loads that can be kept constant - uninfluenced by the contraction. Maximal values for force, shortening, velocity and work may be obtained for individual muscles. This offers the possibility to obtain information on the muscle status and to monitor its changes under non-invasive measurement conditions.

Conclusion

With the Complex Myograph, the whole spectrum of a muscle's mechanical characteristics may be assessed.     

Muscular force production after concentric contraction

The steady-state force following active shortening does not reach the maximum isometric force associated with the final length. Isolated extensor digitorum longus and soleus muscles from mice (NMRI strain) were used to investigate the force produced by a muscle, and some parameters hypothetically influencing this shortening-induced force depression. The muscles were pre-stimulated at fixed length, shortened and then held isometrically to give maximum post-shortening forces, before de-stimulation. The shortening magnitude was 0.18, 0.36 or 0.72mm (about 2-7% of optimal length), time of shortening was chosen as 0.03, 0.06 and 0.12s, and final length as +0.72, 0 and -0.72mm, related to optimal length. The mechanical work during active shortening was evaluated by integrating the product of force and shortening velocity over the shortening period. The results show a positive correlation between the force depression and the mechanical work, whereas the force depression was not correlated to the velocity of shortening. Depression of the passive force component was also observed following all stimulations. Experiments show that the fully stimulated redevelopment of isometric force following concentric contraction follows a time function similar to the creation of force when isometric muscle is initially stimulated. The conclusion is that the isometric force development after active shortening can be well described by an asymptotic force which is decided by the produced work, and the initial isometric time constant.