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Passive tension and stiffness of vertebrate skeletal and insect flight muscles: the contribution of weak cross-bridges and elastic filaments.

Tension and dynamic stiffness of passive rabbit psoas, rabbit semitendinosus, and waterbug indirect flight muscles were investigated to study the contribution of weak-binding cross-bridges and elastic filaments (titin and minititin) to the passive mechanical behavior of these muscles. Experimentally, a functional dissection of the relative contribution of actomyosin cross-bridges and titin and minititin was achieved by 1) comparing mechanically skinned muscle fibers before and after selective removal of actin filaments with a noncalcium-requiring gelsolin fragment (FX-45), and 2) studying passive tension and stiffness as a function of sarcomere length, ionic strength, temperature, and the inhibitory effect of a carboxyl-terminal fragment of smooth muscle caldesmon. Our data show that weak bridges exist in both rabbit skeletal muscle and insect flight muscle at physiological ionic strength and room temperature. In rabbit psoas fibers, weak bridge stiffness appears to vary with both thin-thick filament overlap and with the magnitude of passive tension. Plots of passive tension versus passive stiffness are multiphasic and strikingly similar for these three muscles of distinct sarcomere proportions and elastic proteins. The tension-stiffness plot appears to be a powerful tool in discerning changes in the mechanical behavior of the elastic filaments. The stress-strain and stiffness-strain curves of all three muscles can be merged into one, by normalizing strain rate and strain amplitude of the extensible segment of titin and minititin, further supporting the segmental extension model of resting tension development.

Actins↗

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.

Animals↗

Slow passive stretch and release characteristics of the calf muscles of older women with limited dorsiflexion range of motion.

OBJECTIVE: Examine the slow passive stretch and release characteristics of the calf muscles of older women with limited dorsiflexion range of motion. DESIGN: A cross-sectional comparative design. BACKGROUND: The passive stretch and release characteristics of the calf muscles of older women with limited dorsiflexion range of motion have not been studied. METHODS: Fifteen older women (mean 79 years) with active dorsiflexion < or =10 degrees and 15 younger women (mean 24 years) without limited dorsiflexion were tested. The right ankle was stretched from plantarflexion to maximal dorsiflexion and released into plantarflexion at 5 degrees /s with minimal surface EMG activity in the soleus, gastrocnemius, and tibialis anterior muscles. Length, passive-elastic stiffness and stored passive-elastic energy were examined. RESULTS: The older women had less maximal passive dorsiflexion, a greater initial stretch angle, and less angular change than the younger women (P < 0.05). The maximal passive resistive force (Newtons) of the stretch phase, and the stored passive-elastic energy ( degrees N) during both stretch and release phases were also less (P < 0.001). The older women had greater passive-elastic stiffness at 0 degrees and 5 degrees of dorsiflexion (P < 0.001). CONCLUSIONS: The older women had decreased calf muscle length, extensibility, maximal passive resistive force, stored passive-elastic energy, but greater angle-specific-stiffness at 0 and 5 degrees of passive dorsiflexion. RELEVANCE: Older women with limited dorsiflexion range of motion have decreased calf muscle length, passive resistive forces and stored passive-elastic energy that may impact static and dynamic standing balance activities. Greater passive-elastic stiffness within their ambulatory dorsiflexion range of motion may partially compensate for the deficits.

Adult↗

Mechanisms of disturbed motor control in ankle weakness during gait after stroke.

This study investigated the role of paresis, excessive antagonist coactivation, increased muscle-tendon passive stiffness and spasticity in the reduced stance phase plantarflexor moment (Mmax) and swing phase dorsiflexion during gait (DFmax) in subjects with a recent (<6 months post-stroke) hemiparesis (patients). The gait pattern of the paretic and non-paretic sides was evaluated in 30 patients (aged 57.8+/-10.8 years), whereas only one side was evaluated in 15 healthy controls (aged 59.1+/-9.8 years) while walking at natural and very slow speeds. Peak plantarflexor moment (Mmax) and peak medial gastrocnemius (MG) activation during the stance phase, as well as peak dorsiflexion angle (Dfmax) and peak tibialis anterior (TA) activation during the swing phase, were retained for analysis. In addition, a coactivation index and a plantarflexor spasticity index were calculated for both the stance and the swing phase, and plantarflexor passive stiffness was evaluated on an isokinetic dynamometer. The results showed that Mmax on the paretic and non-paretic sides were both reduced compared with control values at natural speed. This reduction was combined to a low MG activation (paresis) on the paretic side. On the non-paretic side, the reduced plantarflexor moment was related to excessive coactivation levels. The swing phase Dfmax tended to be reduced (not significantly) on the paretic side of the patients compared with control values. This reduction was neither associated with excessive antagonist coactivation nor to plantarflexor hyperactive stretch reflexes, but rather to an increased plantarflexor passive stiffness. In some of the patients, however, an increased TA activation that overcame the plantarflexor passive stiffness allowed for normal DFmax values. The functional consequences of the disturbed mechanisms of motor control observed in both the paretic and non-paretic sides are discussed.

Adult↗

Investigation into the relationship between the passive flexibility and active stiffness of the ankle plantar-flexor muscles.

OBJECTIVE: The purpose of the study was to investigate the relationship between measurements of passive flexibility and active stiffness of the ankle plantar-flexor muscles. DESIGN: The study was a correlation design. BACKGROUND: Flexibility has passive and active components. Little information is available regarding the relationship of these measurements in terms of the information that they yield on the state of the muscle-tendon unit. METHODS: Free oscillation data representing active stiffness was obtained using applied masses equivalent to 30%, 60% and 90% of the subject's maximal voluntary contraction. The angle of dorsiflexion, representing passive flexibility, was measured in standing using computer digitisation to obtain the angle.Results. Mean active stiffness values were 14280 N/m (30% maximal voluntary contraction), 22260 N/m (60% maximal voluntary contraction) and 28010 N/m (90% maximal voluntary contraction). Dorsiflexion measurement gave a mean of 34.3 degrees (S.D. 4.8). Correlation's obtained for the association between range of motion and active stiffness were r=0.01 (30% maximal voluntary contraction), r=0.09 (60% maximal voluntary contraction) and r=0.04 (90% maximal voluntary contraction). Moderate reliability coefficients of 0.71 (30% maximal voluntary contraction), 0.78 (60% maximal voluntary contraction) and 0.68 (90% maximal voluntary contraction) were obtained. CONCLUSIONS: The results imply that measurements of passive flexibility and active stiffness of the lower leg musculature are independent measures of components of muscle-tendon unit flexibility. RELEVANCE: Flexibility is a construct with different components of measurement. Etiological studies typically relate static flexibility measurements to injury with conflicting outcomes. This study suggests that static and active flexibility measures yield different information about the muscle tendon unit of the ankle plantar flexors, and that researchers should consider this point in the design of etiological studies.

Adult↗

Dynamic and static stretch responses in muscle spindle receptors in fatigued muscle.

Dynamic and static stretch responses in muscle spindles were investigated in fatigued muscle to determine if acute adaptations do occur in receptor discharge as has been shown after contractions of short duration. Fatigue to 60-50% maximum tetanic tension was induced in the isolated gastrocnemius muscle in 16 cats by sustained, 7 X threshold electrical stimulation (100 Hz) of the cut L7 ventral root and S1 ventral root. Group Ia and II afferent fiber responses to slow ramp stretches (5 mm X s-1) and vibration (100 Hz) applied to the Achilles tendon were monitored before and immediately after muscle tetany to fatigue. Changes in firing characteristics were similar when results from faster (25-30 mm X s-1) ramp stretches were contrasted. During muscle fatigue, decreases in response latency to displacement and increases in resting discharge, mean frequency during stretch, and frequency of firing to vibration were predominant in both afferent fiber types. Static responses were generally lower, indicating a decrease in position sensitivity. Resting muscle force and passive peak muscle stiffness were consistently higher following contraction. The sum effects of these proprioceptive afferent and mechanical muscle responses would be to increase muscle stiffness and thus resist yield in muscle length to perturbations at lower muscle forces. The magnitude of these adaptations in proprioceptive discharge appears dependent on intrafusal muscle fiber activation.

Adaptation, Physiological↗

Relationship between muscle swelling and stiffness after eccentric exercise.

PURPOSE: The time courses of muscle compartmental swelling and passive stiffness change were measured to determine whether muscle compartmental swelling accounted for increased stiffness. METHODS: Eleven untrained female college students exercised eccentrically by lowering a weight with their elbow flexors. Measurements of muscle compartment volume, stiffness, relaxed elbow angle, circumference, and pain were recorded before exercise, immediately after exercise, and 1-5, 7, 9, and 11 d after exercise. Muscle compartment volume was calculated from cross-sectional ultrasound images taken along the upper arm. Stiffness was measured using a device that extended the elbow and recorded the torque required to hold the forearm at successive angles. RESULTS: Elbow flexor volume increased gradually to peak on the fourth day (26.1 +/- 4.3%, P < 0.05) and then decreased to baseline values over days 7-11. Stiffness increased immediately after exercise (59.9 +/- 14.1%, P < 0.05) and remained at or above this level until decreasing to pre-exercise levels over days 7-11. CONCLUSIONS: This suggests that muscle swelling does not account for the sudden increase in stiffness of the elbow flexor muscles within the first 48 h after exercise but may play a role in the subsequent time course of stiffness.

Adult↗

Influence of age on length and passive elastic stiffness characteristics of the calf muscle-tendon unit of women.

BACKGROUND AND PURPOSE: Therapeutic stretching of the calf muscle-tendon unit is used to increase its length and to ameliorate decreased dorsiflexion range of motion (ROM), but the influence of age on the passive properties of the calf muscle-tendon unit has not been studied adequately The purpose of this study was to examine the influence of age on length and passive elastic stiffness (PES) characteristics of the calf muscle-tendon unit when stretched through the full, available dorsiflexion ROM. SUBJECTS: Twenty-four younger women (aged 20-39 years), 24 middle-aged women (aged 40-59 years), and 33 older women (aged 60-84 years) participated. METHODS: An isokinetic dynamometer was used to passively stretch the right calf muscle-tendon unit from relaxed plantar flexion to the maximal angle of available dorsiflexion at 5(ús-1. The maximal passive resistive torque was measured, and passive angle-torque curves were constructed for a full ROM from an initial angle of passive resistive torque to the maximal dorsiflexion angle. The full ROM represented length extensibility. The average PES was calculated for this full stretch ROM and for the first half and the last half of this stretch ROM. The maximal passive dorsiflexion angle, maximal passive resistive torque, angular change for the full stretch ROM, and average PES for the full stretch ROM and the first half and the last half of the full stretch ROM were examined for group differences and their relationships with age. RESULTS: The maximal passive dorsiflexion angle, maximal passive resistive torque, angular change for the full stretch ROM, and average PES within the last half of the full stretch ROM were less for the older women than for the younger women. Age was negatively associated with these variables. CONCLUSION AND DISCUSSION: Decreased maximal passive dorsiflexion ROM in older women was associated with decreased maximal passive resistive torque, decreased calf muscle-tendon unit length extensibility, and decreased average PES within the last half of their available passive dorsiflexion ROM.

Adult↗

The effect of regional myocardial ischemia on series elastic and contractile elements of glycerinated heart muscle in dogs.

The response of the contractile and the series elastic elements to ischemia was studied with isometric contraction and quick release methods after measuring the passive length-tension relationship in glycerinated heart muscle fibers of dogs at resting state. Myocardial infarction was induced by ligating left coronary artery. Muscle fibers taken from the ischemic area three hours after ligation demonstrated reduction in maximal developed tension (P0), the maximal rate of tension development (dp/dtmax) and Vmax. The time to peak tension (t0) was increased. As in fresh papillary muscle the modulus of elasticity of active glycerinated muscle increased in proportion to load. The stiffness of the series elastic element elevated significantly in ischemic muscle fibers. The passive stiffness in resting state showed a decrease in the slope accompanied by an increase in the intercept in ischemic heart muscle. Therefore, increased stiffness of the series elastic element and diminished contractility are present following acute myocardial infarction.

Animals↗

Model and in vivo studies on human trunk load partitioning and stability in isometric forward flexions.

To resolve the trunk redundancy to determine muscle forces, spinal loads, and stability margin in isometric forward flexion tasks, combined in vivo-numerical model studies was undertaken. It was hypothesized that the passive resistance of both the ligamentous spine and the trunk musculature plays a crucial role in equilibrium and stability of the system. Fifteen healthy males performed free isometric trunk flexions of approximately 40 degrees and approximately 65 degrees +/- loads in hands while kinematics by skin markers and EMG activity of trunk muscles by surface electrodes were measured. A novel kinematics-based approach along with a nonlinear finite element model were iteratively used to calculate muscle forces and internal loads under prescribed measured postures and loads considered in vivo. Stability margin was investigated using nonlinear, linear buckling, and perturbation analyses under various postures, loads and alterations in ligamentous stiffness. Flexion postures significantly increased activity in extensor muscles when compared with standing postures while no significant change was detected in between flexed postures. Compression at the L5-S1 substantially increased from 570 and 771 N in upright posture, respectively, for +/-180 N, to 1912 and 3308 N at approximately 40 degrees flexion, and furthermore to 2332 and 3850 N at approximately 65 degrees flexion. Passive ligamentous/muscle components resisted up to 77% of the net moment. In flexion postures, the spinal stability substantially improved due both to greater passive stiffness and extensor muscle activities so that, under 180 N, no muscle stiffness was required to maintain stability. The co-activity of abdominal muscles and the muscle stiffness were of lesser concern to maintain stability in forward flexion tasks as compared with upright tasks. An injury to the passive system, on one hand, required a substantial compensatory increase in active muscle forces which further increased passive loads and, hence, the risk of injury and fatigue. On the other hand, it deteriorated the system stability which in turn could require greater additional muscle activation. This chain of events would place the entire trunk active-passive system at higher risks of injury, fatigue and instability.

Abdomen↗

Mechanical properties of the isolated catch apparatus of the sea urchin spine joint: muscle fibers do not contribute to passive stiffness changes.

The catch apparatus (CA) is the collagenous ligament at the spinal joint of sea urchins. It maintains spine posture by stiffening and allows spine movement by softening. A CA preparation, which was isolated from ossicles, was used to test the hypothesis that frictional forces between collagen fibers and ossicles are the source of stiffness changes. Isolated preparations of the CA changed in stiffness, thus falsifying the hypothesis. Another hypothesis proposes that muscle fibers, which represent a relatively small component of the CA, cause stiffening of the CA by contraction. Chemicals that evoked contraction in spine muscles did not always stiffen the CA: the CA of Heterocentrotus mammillatus softened in response to artificial seawater with potassium concentration elevated to 100 mM. This provided evidence against the muscle-based hypothesis. The present results suggest that the stiffness changes of the CA are based on changes in the mechanical properties of the extracellular components of the connective tissue and are therefore related to the connective tissue catch that is widespread in other echinoderms.

Animals↗

The effect of alcohol on active and passive stiffness, and on isometric contractions of glycerinated heart muscle in rats.

The response of the contractile and the series elastic elements to ethanol was studied isometric contraction and quick release methods after measuring the passive length-tension relationship in glycerinated heart muscle fibers of rats at resting state. In rats consuming 30% ethanol for an average of 5 weeks, maximal developed tension (P0), the maximal rate of tension development (dp/dtmax) and Vmax were significantly depressed, the time to peak tension (t0) was not changed. As in fresh papillary muscle the modulus of elasticity of active glycerinated muscle increased in proportion to load. The stiffness of the series elastic element showed significant elevation in rats receiving ethanol. The passive stiffness in resting state revealed no significant difference between control and alcohol exposed rats. Therefore, increased stiffness of the series elastic element and diminished contractility are present following chronic alcohol consumption.

Animals↗

A biomechanical evaluation of cyclic and static stretch in human skeletal muscle.

The short term effect of static and cyclic stretch paradigms on stiffness and maximal joint range of motion was examined in 12 recreational athletes. To assess flexibility, joint range of motion and resistance to stretch were measured using a dynamometer during a passive stretch of the hamstring muscle group to the point of pain. The recorded torque-angle curve allowed for identification of maximal joint range of motion and calculation of passive muscle-tendon stiffness and energy. Three flexibility assessments (stretch 1 - 3), each 10 min apart, were administered to each leg. A 90 s static stretch and 10 cyclic stretches were performed after the second stretch on the left and right side, respectively. Stiffness in a common range for stretch 1 - 3 was unchanged on both the left and right side. However, on the left side (static stretch) there was a significant effect of flexibility assessment (stretch 1 - 3) (p < 0.0001) with an increased maximal joint angle (p < 0.01) and maximal stiffness (p < 0.05) between all three stretches. Similarly, on the right side (cyclic stretches) there was a significant effect of flexibility assessment (p < 0.0001) with an increased maximal joint angle between stretch 1 and 3 (p < 0.01) and maximal stiffness (p < 0.05) between all stretches. During the static stretch passive torque declined 35+/-4% (p < 0.001). During the cyclic stretches passive energy and hysteresis both declined 17% (p < 0.05) while stiffness increased 12% (p < 0.05). The results of the present study demonstrate that static and cyclic stretching, as it is commonly performed by athletes, increases joint range of motion by increasing stretch tolerance while the viscoelastic characteristics of the muscle remain unaltered.

Adult↗

The behaviour of a mammalian muscle during sinusoidal stretching.

1. Tension changes have been recorded in tetanized and passive cat soleus muscles during sinusoidal stretching at frequencies between 0.25 and 12.5 c/s.2. During sinusoidal stretching the muscle tension varied in an approximately sinusoidal manner. The tension record showed an angular advance on muscle length. A method of measuring mean angular advance in nonlinear systems is described.3. In tetanized muscle, resistance to lengthening increased with increasing frequency of stretching. With increasing frequency the elastic stiffness increased more rapidly than the viscous stiffness, so that at the higher frequencies the angular separation between length and tension became smaller.4. With increasing stretch amplitude the elastic stiffness of the tetanized muscle declined, and the mean angular advance of tension became larger.5. In passive muscle the viscous stiffness increased at the higher frequencies, and the mean angular advance of tension on length was correspondingly increased.6. The functional significance of these findings and their relation to the findings of other workers are discussed.

Animals↗

Effects of jump training on passive mechanical stress and stiffness in rabbit skeletal muscle: role of collagen.

AIMS: This study evaluated the effect of a 15-week jump training period on mechanical parameters and collagen concentration of different muscle types in rabbits, at 50, 90 and 140 days of age. METHODS: Trained (T) animals were made to jump over obstacles in order to get food and water. The height of the obstacle was increased according to the animal's age. Control (C) animals were sedentary. Mechanical parameters (force, stress, stiffness) and collagen concentration were measured in Extensor Digitorum Longus (EDL), Rectus Femoris (RF), Semimembranosus Proprius (SMP) and Psoas Major (PSOAS). RESULTS: Both EDL and RF collagen concentrations and passive mechanical parameters increased between 50 and 140 days of age (P<0.001), whereas SMP and PSOAS collagen concentrations decreased (P<0.001). Soluble collagen concentration decreased similarly with age in all muscles and groups. Exercise training at 140 days induced a significant increase in force (EDL 20.4% and RF 15.3%, 0.01<P<0.05), stress (EDL 26.8% and RF 22.6%, P<0.001), and stiffness (EDL 13.2% and RF 16%, 0.001<P<0.05) with a greater collagen concentration (EDL 16.1% and RF 19.1%, 0.001<P<0.05). Finally, stiffness and stress are well correlated with collagen concentration in EDL and RF muscles at 140 days (0.74<r<0.84, P<0.05). CONCLUSION: These results suggest that jump training can increase muscle capabilities of strength and stiffness in fast-twitch mixed muscles with pennate architecture (EDL, RF). This increase is essentially mediated by a rise in cross-linked collagen fraction, coupled with a relative decrease in soluble collagen. The collagen covalent cross-links improve resistance and stability in force transmission processes during stretching.

Aging↗

Influence of muscle cooling on the viscoelastic response of the human ankle to sinusoidal displacements.

The changes in passive mechanical muscle properties due to cooling of the calf in healthy human volunteers were investigated. The technique, using sinusoidal driving of the foot, permitted the separation of muscle stiffness response into its elastic and viscous components. Cooling the calf with ice for 30 minutes increases the rate of change of elastic stiffness with frequency, and it increases the frictional stiffness over a frequency range of 3 to 12Hz. Such cooling would produce an estimated 3% to 10% increase in total stiffness, on average, in a spastic person. This increase in stiffness would counteract reductions in total stiffness achieved during the application of cryotherapy to relieve spasticity. However, one could expect that for a clinically significant reduction of spasticity, the increase in passive stiffness of the muscle generated by cooling would be largely overshadowed by the decrease in reflex reactivity.

Adult↗

Separation of active and passive components of short-range stiffness of muscle.

The short-range stiffness of smoothly but submaximally contracting isometric soleus muscles of anesthetised cats was measured by applying small fast stretches. The ratio of isometric tension to stiffness was plotted against tension over a wide range of muscle lengths and stimulus rates. The results fitted a straight line well, as predicted from crossbridge theory, showing the stiffness to be a function of tension only, independent of the combination of length and stimulus rate used to generate the tension. The major deviation from this line was attributed to incomplete fusion at low frequencies of stimulation. Values believed to be tendon compliance and crossbridge tension per unit of stiffness were found from the graph, and the tendon compliance correlated with the maximum muscle tension. Shortening the tendon by attaching nearer to the muscle changed the results in a manner consistent with the theory, provided that appropriate precautions were taken against slippage.

Animals↗