Stretch-induced Force Enhancement Research Articles

The effect of stretch\u2013shortening magnitude and muscle\u2013tendon unit length on performance enhancement in a stretch\u2013shortening cycle

Stretch-induced residual force enhancement (rFE) is associated with increased performance in a stretch–shortening cycle (SSC). Although the influence of different range of motions and muscle–tendon unit lengths has been investigated in pure stretch-hold experiments in vivo, the contribution to a SSC movement in human muscles remains unclear. In two sessions, 25 healthy participants performed isometric reference (ISO), shortening hold (SHO) and SSC contractions on an isokinetic dynamometer. We measured the net knee-joint torque, rotational mechanical work, knee kinematics and fascicle behavior (m. vastus lateralis) of the upper right leg. In session 1 the SHO- and SSC-magnitude was changed respectively (SHO: 50°–20°, 80°–20° and 110°–20°; SSC: 20°–50°–20°, 20°–80°–20° and 20°–110°–20°) and in session 2 the muscle–tendon unit length (SHO: 50°–20°, 80°–50° and 110°–80°; SSC: 20°–50°–20°, 50°–80°–50° and 80°–110°–80°; straight leg = 0°). In both sessions, rotational work was significantly (p < 0.05) increased in the SSC compared to the SHO contractions (in the range of 8.1–17.9%). No significant difference of joint torque was found in the steady-state for all SSC-magnitudes compared to the corresponding SHO contractions in session 1. In session 2, we found only significantly (p < 0.05) less depressed joint torque in the SSC at the longest muscle–tendon unit length compared to the corresponding SHO condition, without any differences in knee kinematics and fascicle behavior. Therefore, the physiological relevance of rFE might be particularly important for movements at greater muscle–tendon unit lengths.

Contribution of Stretch-Induced Force Enhancement to Increased Performance in Maximal Voluntary and Submaximal Artificially Activated Stretch-Shortening Muscle Action.

In everyday muscle action or exercises, a stretch-shortening cycle (SSC) is performed under different levels of intensity. Thereby, compared to a pure shortening contraction, the shortening phase in a SSC shows increased force, work, and power. One mechanism to explain this performance enhancement in the SSC shortening phase is, besides others, referred to the phenomenon of stretch-induced increase in muscle force (known as residual force enhancement; rFE). It is unclear to what extent the intensity of muscle action influences the contribution of rFE to the SSC performance enhancement. Therefore, we examined the knee torque, knee kinematics, m. vastus lateralis fascicle length, and pennation angle changes of 30 healthy adults during isometric, shortening (CON) and stretch-shortening (SSC) conditions of the quadriceps femoris. We conducted maximal voluntary contractions (MVC) and submaximal electrically stimulated contractions at 20%, 35%, and 50% of MVC. Isometric trials were performed at 20° knee flexion (straight leg: 0°), and dynamic trials followed dynamometer-driven ramp profiles of 80°–20° (CON) and 20°–80°–20° (SSC), at an angular velocity set to 60°/s. Joint mechanical work during shortening was significantly (p < 0.05) enhanced by up to 21% for all SSC conditions compared to pure CON contractions at the same intensity. Regarding the steady-state torque after the dynamic phase, we found significant torque depression for all submaximal SSCs compared to the isometric reference contractions. There was no difference in the steady-state torque after the shortening phases between CON and SSC conditions at all submaximal intensities, indicating no stretch-induced rFE that persisted throughout the shortening. In contrast, during MVC efforts, the steady-state torque after SSC was significantly less depressed compared to the steady-state torque after the CON condition (p = 0.034), without significant differences in the m. vastus lateralis fascicle length and pennation angle. From these results, we concluded that the contribution of the potential enhancing factors in SSCs of the m. quadriceps femoris is dependent on the contraction intensity and the type of activation.

Pre-activation affects the effect of stretch-shortening cycle by modulating fascicle behavior.

ABSTRACTThe torque attained during active shortening is enhanced after an active stretch (stretch-shortening cycle, SSC). This study examined the influence of pre-activation on fascicle behavior and the SSC effect. Subjects exhibited the following three conditions by electrically induced plantar flexions. In the isometric-concentric (ISO-CON) condition, subjects exhibited active shortening from dorsiflexion of 15° to 0° after isometric pre-activation. In the eccentric-concentric (ECC-CON) condition, subjects exhibited the above active shortening immediately after the eccentric pre-activation. In the isometric-eccentric-concentric (ISO-ECC-CON) condition, isometric pre-activation was conducted before exhibiting the ECC-CON maneuver. Joint torque and fascicle length of the medial gastrocnemius were compared. The joint torque at the onset and end of shortening was larger in the ISO-ECC-CON than in the ISO-CON or ECC-CON conditions, while no differences were found between ISO-CON and ECC-CON conditions. The magnitude of fascicle elongation attained during the active stretch was larger in the ISO-ECC-CON than in the ECC-CON condition. This could be caused by the shorter fascicle length at the onset of active stretch due to isometric pre-activation. This shorter fascicle length could lead to larger fascicle elongation during the subsequent active stretch, which should emphasize the effect of active stretch-induced force enhancement mechanism.

Muscles as Motors and Muscles as Brakes

During normal daily activities, muscles are required to lengthen as frequently as they shorten to produce movement. Lengthening muscle actions are associated with high forces and low energy consumption, but can often result in muscle injury. These unique features are not explained adequately by current (cross-bridge) theories of muscle contraction. Using specific myosin inhibitors and different temperatures the author has examined the molecular mechanisms of stretch-induced force enhancement. The results, which suggest that lengthening force arises from the strain of both cross-bridge and non-cross-bridge components of the sarcomere, help to refine understanding of the molecular mechanisms of muscle contraction.

Force produced after stretch in sarcomeres and half-sarcomeres isolated from skeletal muscles

The goal of this study was to evaluate if isolated sarcomeres and half-sarcomeres produce a long-lasting increase in force after a stretch is imposed during activation. Single and half-sarcomeres were isolated from myofibrils using micro-needles, which were also used for force measurements. After full force development, both preparations were stretched by different magnitudes. The sarcomere length (SL) or half-sarcomere length variations (HSL) were extracted by measuring the initial and final distances from the Z-line to the adjacent Z-line or to a region externally adjacent to the M-line of the sarcomere, respectively. Half-sarcomeres generated approximately the same amount of isometric force (29.0 ± SD 15.5 nN·μm−2) as single sarcomeres (32.1 ± SD 15.3 nN·μm−2) when activated. In both cases, the steady-state forces after stretch were higher than the forces during isometric contractions at similar conditions. The results suggest that stretch-induced force enhancement is partly caused by proteins within the half-sarcomere.

Contractile Properties of Half-Sarcomeres Mechanically Isolated from Skeletal Muscle Myofibrils

The goal of this study was to develop a system to experiment with half-sarcomeres mechanically isolated from skeletal muscle. Single myofibrils from rabbit psoas were transferred into a temperature-controlled (10°C) bath. Half-sarcomeres were isolated using two pre-calibrated glass microneedles; the first pierced externally adjacent to the Z-line, and the second internally, adjacent to the M-line. The force produced during activation of the half-sarcomere was measured by tracking the displacement of the microneedles. The half-sarcomere length (HSL) was obtained by interpolating the displacement of the needles from the initial to the final distances measured from the Z-line to the center of the sarcomere. Half-sarcomeres (n=12) produced a stress of 24.0 ±3.7 nN/um2 at HSL between 1.0 and 1.4µm. The result was comparable to that observed in isolated sarcomeres (25.5 ±3.1 nN/um2, at SL between 1.8 and 3.0µm). Preliminary trials in which we imposed stretches (ranging from 12 to 33% of the initial HSL/SL, at a speeds of 1.35-3.15 μm·s−1·HSL−1) (n = 6 half-sarcomeres; n = 13 single sarcomeres) during activation show an increase in force during and after stretch, which was long lasting (i.e. residual force enhancement). Despite a high variability, half-sarcomeres showed a tendency to produce a smaller level of residual force enhancement when compared to single sarcomeres. Our results show that half-sarcomeres generate levels of isometric force that are similar to those observed in sarcomeres and myofibrils. However, half-sarcomeres produced a lower level of stretch-induced force enhancement when compared to sarcomeres.

A phenomenological muscle model to assess history dependent effects in human movement

Most musculoskeletal models used to analyze human movement utilize Hill-type muscle models that account for state dependent intrinsic muscle properties (e.g., force–length–velocity relationships), but rarely do these models include history dependent effects (e.g., force depression or enhancement). While the relationship between muscle shortening and force depression can be well characterized by muscle mechanical work, the relationship between muscle stretch and force enhancement is more complex. Further, it is not well known how these properties influence dynamic movements. Therefore, the goal of this study was to develop a modified Hill-type muscle model that incorporated stretch-induced force enhancement into a previously described model that included shortening-induced force depression. The modified muscle model was based on experimental data from isolated cat soleus muscles. Simulations of in situ muscle experiments were used to validate the model and simulations of a simple human movement task (counter-movement jumping) were used to examine the interactions of the history dependent effects. The phenomenological model of stretch-induced force enhancement was dependent on both the magnitude of stretch and relative length of the muscle fiber. Simulations of the in situ muscle experiments showed that the model could accurately reproduce force enhancement and force depression, as well as the complex additive relationship between these effects. Simulations of counter-movement jumping showed that a similar jump pattern could be achieved with and without history dependent effects and that a relatively minor change in muscle activation could mitigate the impact of these effects.

The mechanisms of the residual force enhancement after stretch of skeletal muscle: non-uniformity in half-sarcomeres and stiffness of titin

When activated skeletal muscles are stretched, the force increases significantly. After the stretch, the force decreases and reaches a steady-state level that is higher than the force produced at the corresponding length during purely isometric contractions. This phenomenon, referred to as residual force enhancement, has been observed for more than 50 years, but the mechanism remains elusive, generating considerable debate in the literature. This paper reviews studies performed with single muscle fibres, myofibrils and sarcomeres to investigate the mechanisms of the stretch-induced force enhancement. First, the paper summarizes the characteristics of force enhancement and early hypotheses associated with non-uniformity of sarcomere length. Then, it reviews new evidence suggesting that force enhancement can also be associated with sarcomeric structures. Finally, this paper proposes that force enhancement is caused by: (i) half-sarcomere non-uniformities that will affect the levels of passive forces and overlap between myosin and actin filaments, and (ii) a Ca(2+)-induced stiffness of titin molecules. These mechanisms are compatible with most observations in the literature, and can be tested directly with emerging technologies in the near future.

Activation-induced force enhancement in human adductor pollicis

It has been known for a long time that the steady-state isometric force after muscle stretch is bigger than the corresponding force obtained in a purely isometric contraction for electrically stimulated and maximal voluntary contractions (MVC). Recent studies using sub-maximal voluntary contractions showed that force enhancement only occurred in a sub-group of subjects suggesting that force enhancement for sub-maximal voluntary contractions has properties different from those of electrically-induced and maximal voluntary contractions. Specifically, force enhancement for sub-maximal voluntary contractions may contain an activation-dependent component that is independent of muscle stretching. To address this hypothesis, we tested for force enhancement using (i) sub-maximal electrically-induced contractions and stretch and (ii) using various activation levels preceding an isometric reference contraction at 30% of MVC (no stretch). All tests were performed on human adductor pollicis muscles. Force enhancement following stretching was found for all subjects ( n = 10) and all activation levels (10%, 30%, and 60% of MVC) for electrically-induced contractions. In contrast, force enhancement at 30% of MVC, preceded by 6 s of 10%, 60%, and 100% of MVC was only found in a sub-set of the subjects and only for the 60% and 100% conditions. This result suggests that there is an activation-dependent force enhancement for some subjects for sub-maximal voluntary contractions. This activation-dependent force enhancement was always smaller than the stretch-induced force enhancement obtained at the corresponding activation levels. Active muscle stretching increased the force enhancement in all subjects, independent whether they showed activation dependence or not. It appears that post-activation potentiation, and the associated phosphorylation of the myosin light chains, might account for the stretch-independent force enhancement observed here.

Force enhancement and relaxation rates after stretch of activated muscle fibres

The residual force enhancement following muscle stretch might be associated with an increase in the proportion of attached cross-bridges, as supported by stiffness measurements. In this case, it could be caused by an increase in the attachment or a decrease in the detachment rate of cross-bridges, or a combination of the two. The purpose of this study was to investigate if the stretch-induced force enhancement is related to cross-bridge attachment/detachment kinetics. Single muscle fibres dissected from the lumbrical muscle of frog were place at a length approximately 20% longer than the plateau of the force-length relationship; they were maximally activated, and after full isometric force was reached, ramp stretches were imposed with amplitudes of 5 and 10% fibre length, at a speed of 40% fibre length s(-1). Experiments were performed in Ringer's solution, and with the addition of 2, 5 and 10 nM of 2,3-butanedione monoxime (BDM), a drug that places cross-bridges in a pre-power-stroke, state, inhibiting force production. The total force following stretch was higher than the corresponding force measured after isometric contraction at the corresponding length. This residual force enhancement was accompanied by an increase relaxation time. BDM, which decreases force production during isometric contractions, considerably increased the relative levels of force enhancement. BDM also increased relaxation times after stretch, beyond the levels observed during reference contractions in Ringer's solution, and beyond isometric control tests at the corresponding BDM concentrations. Together, these results support the idea that force enhancement is caused, at least in part, by a decrease in cross-bridge detachment rates, as manifested by the increased relaxation times following fibre stretch.

Enhancement of twitch force by stretch in a nerve-skeletal muscle preparation of the frogRana porosa brevipodaand the effects of temperature on it

We investigated the mechanism of the enhancement of twitch force by stretch and the effects of temperature on it in nerve-skeletal muscle preparations of whole iliofibularis muscles isolated from the frog Rana brevipoda. When a preparation was stimulated indirectly and stretched, the twitch force after the stretch was enhanced remarkably in comparison to that observed before a stretch at low temperature. The enhanced force obtained by a stretch of 20% resting muscle length (l0) at low temperature was as high as the force obtained by direct stimulation. The phenomenon was not dependent on the velocity but on the amplitude of stretch. The enhanced force obeyed the length-force relationship when a stretch was long enough. The above results were observed when the frogs were kept at room temperature (20-22 degrees C). Measurements were also taken at low temperature (4 degrees C); when frogs were kept at low temperature for more than 2 months, twitch force obtained without stretch was considerably higher at l0. The amplitude of the action potential recorded extracellularly from the muscle surface increased remarkably after a stretch, but was same before and after a stretch when recorded from the nerve innervating muscle. The effects of temperature on twitch and tetanic force by direct or indirect stimulation without stretch were also studied as basic data of the stretch experiment. The results from this study suggest that stretch-induced force enhancement in a nerve-muscle preparation is caused by an increase in the transmission rate between nerve and muscle, and the amplitude of the enhanced force is determined by the length-force relationship of the muscle. The phenomenon is also strongly affected by the temperature at which the frogs are kept.

A new motor model representing the stretch-induced force enhancement and shortening-induced force depression in skeletal muscle

A motor model that consists of two Maxwell elements with a force generator and one Voigt element is proposed in this paper. The motor model can achieve a hyperbolic force–velocity relation when we alter weight functions applied to the Maxwell elements and the force generator. Rate coefficients are introduced to determine the weight function and to improve the motor performance and the time course of the motor force. The weight functions are used as a controller of the motor. We assume that the mechanical impulse applied to the motor affects the rate coefficients and found that the amount of the mechanical impulse is related to the amount of force depression following motor shortening and to the amount of force enhancement following motor stretching. The time courses of the motor force following shortening and stretching quantitatively resemble those in other muscle experiments. The maximum energy efficiency of the motor that we obtained was 50% with an ATP hydrolysis type and 25% with an AC–DC motor type.

Active force inhibition and stretch-induced force enhancement in frog muscle treated with BDM.

There is evidence that the stretch-induced residual force enhancement observed in skeletal muscles is associated with 1) cross-bridge dynamics and 2) an increase in passive force. The purpose of this study was to characterize the total and passive force enhancement and to evaluate whether these phenomena may be associated with a slow detachment of cross bridges. Single fibers from frog lumbrical muscles were placed at a length 20% longer than the plateau of the force-length relationship, and active and passive stretches (amplitudes of 5 and 10% of fiber length and at a speed of 40% fiber length/s) were performed. Experiments were conducted in Ringer solution and with the addition of 2, 5, and 10 mM of 2,3-butanedione monoxime (BDM), a cross-bridge inhibitor. The steady-state active and passive isometric forces after stretch of an activated fiber were higher than the corresponding forces measured after isometric contractions or passive stretches. BDM decreased the absolute isometric force and increased the total force enhancement in all conditions investigated. These results suggest that total force enhancement is directly associated with cross-bridge kinetics. Addition of 2 mM BDM did not change the passive force enhancement after 5 and 10% stretches. Addition of 5 and 10 mM did not change (5% stretches) or increased (10% stretches) the passive force enhancement. Increasing stretch amplitudes and increasing concentrations of BDM caused relaxation after stretch to be slower, and because passive force enhancement is increased at the greatest stretch amplitudes and the highest BDM concentrations, it appears that passive force enhancement may be related to slow-detaching cross bridges.

Effects of shortening on stretch-induced force enhancement in single skeletal muscle fibers

The main purpose of this study was to evaluate the effects of shortening on the stretch-induced force enhancement in single muscle fibers, and indirectly test the hypothesis that force enhancement may be associated with the engagement of a passive element upon activation. Fibers were placed on the descending limb of the force–length relationship, and stretch and shortening contractions were performed. Fibers underwent two sets of shortening–stretch cycles. First, fibers were shortened by a fixed amplitude and speed (10% fiber length, and at 40% fiber length/s), and then were stretched (10% fiber length, and at 40% fiber length/s) immediately following shortening, or 500 or 1000 ms following the shortening. Second, fibers were shortened by varying amounts (5%, 10% and 15% fiber length) and at a constant speed (40% fiber length/s) immediately preceding a given fiber stretch (10% fiber length, and at 40% fiber length/s). When stretching was immediately preceded by shortening, force enhancement was decreased proportionally with the shortening magnitude. When intervals were introduced between shortening and stretch, the effects of shortening on the stretch-induced force enhancement became less prominent. We concluded that, in contrast to published suggestions, shortening affects the stretch-induced force enhancement in an amplitude-dependent manner in single fibers, as it does in whole muscles, but this effect is diminished by increasing the time period between the shortening and stretch phases.

Stretch-induced, steady-state force enhancement in single skeletal muscle fibers exceeds the isometric force at optimum fiber length

Stretch-induced force enhancement has been observed in a variety of muscle preparations and on structural levels ranging from single fibers to in vivo human muscles. It is a well-accepted property of skeletal muscle. However, the mechanism causing force enhancement has not been elucidated, although the sarcomere-length non-uniformity theory has received wide support. The purpose of this paper was to re-investigate stretch-induced force enhancement in frog single fibers by testing specific hypotheses arising from the sarcomere-length non-uniformity theory. Single fibers dissected from frog tibialis anterior (TA) and lumbricals ( n=12 and 22, respectively) were mounted in an experimental chamber with physiological Ringer's solution (pH=7.5) between a force transducer and a servomotor length controller. The tetantic force–length relationship was determined. Isometric reference forces were determined at optimum length (corresponding to the maximal, active, isometric force), and at the initial and final lengths of the stretch experiments. Stretch experiments were performed on the descending limb of the force–length relationship after maximal tetanic force was reached. Stretches of 2.5–10% (TA) and 5–15% lumbricals of fiber length were performed at 0.1–1.5 fiber lengths/s. The stretch-induced, steady-state, active isometric force was always equal or greater than the purely isometric force at the muscle length from which the stretch was initiated. Moreover, for stretches of 5% fiber length or greater, and initiated near the optimum length of the fiber, the stretch-enhanced active force always exceeded the maximal active isometric force at optimum length. Finally, we observed a stretch-induced enhancement of passive force. We conclude from these results that the sarcomere length non-uniformity theory alone cannot explain the observed force enhancement, and that part of the force enhancement is associated with a passive force that is substantially greater after active compared to passive muscle stretch.

Stretch-induced force enhancement and stability of skeletal muscle myofibrils.

The main purpose of the experiments presented in this chapter was to test the hypothesis that the stretch-induced force enhancement commonly observed in skeletal muscle is associated with sarcomere length instability. Single myofibrils isolated from the rabbit psoas muscle were attached to a nanolever pair for force measurement at the one end, and to a glass needle for controlled displacements at the other end. The image of the striation pattern was projected onto a linear 1024-element photodiode array, which was scanned (20 Hz) to produce a dark-light pattern corresponding to the A- and I-bands, respectively. Starting from a mean SL of approximately 2.55 microm, stretches of a nominal amplitude of 4 to 10% of SL, at a nominal speed of 100 nm x sec(-1) were applied to activated myofibrils (pCa2+ = 4.75). Following stretch, the isometric, steady-state force was greater by 10.9% to 45.9% than the force produced before stretch, and was greater than the force predicted at the corresponding final length. Passive force could not account for the force enhancement. Sarcomere lengths along the activated myofibrils were non-uniform, but remained constant before stretch or during the extended isometric period after stretch. Further, sarcomeres never stretched to a length beyond thick and thin filament overlap. It is concluded that sarcomeres are stable, and therefore the increased force observed after stretch must be a sarcomeric property, not associated with continuous length changes of unstable sarcomeres, as had been assumed in the past.

Force enhancement following an active stretch in skeletal muscle

When skeletal muscle is stretched during a tetanic contraction, the resulting force is greater than the purely isometric force obtained at the corresponding final length. Several mechanisms have been proposed to explain this phenomenon, but the most accepted mechanism is the sarcomere length non-uniformity theory. This theory is associated with the notion of instability of sarcomeres on the descending limb of the force–length relationship. However, recent evidence suggests that this theory cannot account solely for the stretch-induced force enhancement. Some of this evidence is presented in this paper, and a new mechanism for force enhancement is proposed: one that is associated with the engagement of a passive force during stretch. We speculate that this passive force enhancement may be caused by titin, a protein associated with passive force production at long sarcomere lengths.

Measured and modeled properties of mammalian skeletal muscle: III. the effects of stimulus frequency on stretch-induced force enhancement and shortening-induced force depression.

Stretch-induced force enhancement and shortening-induced force depression were examined in fast-twitch feline caudofemoralis muscle at 37 degrees C. These phenomena were induced by applying ramp length changes during the first 100--200 ms of an otherwise isometric contraction. The effects of various stimulus frequencies ranging from 30 to 120 pps were investigated over lengths ranging from 0.85 to 1.15 L0. Distributed asynchronous stimulation of bundles of ventral roots was employed to produce smooth contractions at sub-tetanic stimulus frequencies in whole muscle. Of the two components of force enhancement identified by Noble (1992) we observed only the transient component that decays with time; we did not observe residual force enhancement. The force depression that we observed was symmetrical in almost all respects to the transient force enhancement, and was unlike the shortening-induced de-activation and residual force depression identified by Edman (Edman. 1975; Edman et al., 1993). Both transient force enhancement and depression were independent of work, load and activation. Reversals in the direction of ramp length changes following either an initial stretch or initial shortening were shown to cancel the effects of both transient force enhancement and transient force depression. The distances over which these cancellations could be achieved were different for the lengthening and shortening effects. This asymmetry can be reconciled with the predictions of Huxley's original cross-bridge mechanism by incorporating the recent suggestion that myosin heads can interact with multiple actin binding sites during a single 'working' stroke. We conclude that the types of force enhancement/ depression that are most likely to be encountered under physiological conditions are the transient effects observed here, but that even these will have relatively little effect on force production during most natural behaviors.

Electron Microscopic Studies on the Stretch-Induced Disordering of the Myofilament Lattice in Tetanized Frog Skeletal Muscle Fibers

To study the effect of stretch on the hexagonal myofilament lattice in frog skeletal muscle fibers, the fibers were fixed at rest and during the isometric tetanus with or without stretch, and their cross sections were examined electron microscopically. The degree of disorder of the myofilament lattice as estimated by the Fourier transform and rotation methods in the digital image analysis was found to be largest during the isometeric tetanus with stretch and smallest during the isometeric tetanus without stretch, supporting the view that the stretch-induced force enhancement results from the disordering of the myofilament lattice.