Positive force feedback in bouncing gaits?

During bouncing gaits (running, hopping, trotting), passive compliant structures (e.g. tendons, ligaments) store and release part of the stride energy. Here, active muscles must provide the required force to withstand the developing tendon strain and to compensate for the inevitable energy losses. This requires an appropriate control of muscle activation. In this study, for hopping, the potential involvement of afferent information from muscle receptors (muscle spindles, Golgi tendon organs) is investigated using a two-segment leg model with one extensor muscle. It is found that: (i) positive feedbacks of muscle-fibre length and muscle force can result in periodic bouncing; (ii) positive force feedback (F+) stabilizes bouncing patterns within a large range of stride energies (maximum hopping height of 16.3 cm, almost twofold higher than the length feedback); and (iii) when employing this reflex scheme, for moderate hopping heights (up to 8.8 cm), an overall elastic leg behaviour is predicted (hopping frequency of 1.4-3 Hz, leg stiffness of 9-27 kN m(-1)). Furthermore, F+ could stabilize running. It is suggested that, during the stance phase of bouncing tasks, the reflex-generated motor control based on feedbacks might be an efficient and reliable alternative to central motor commands.     

Muscle power attenuation by tendon during energy dissipation

An important function of skeletal muscle is deceleration via active muscle fascicle lengthening, which dissipates movement energy. The mechanical interplay between muscle contraction and tendon elasticity is critical when muscles produce energy. However, the role of tendon elasticity during muscular energy dissipation remains unknown. We tested the hypothesis that tendon elasticity functions as a mechanical buffer, preventing high (and probably damaging) velocities and powers during active muscle fascicle lengthening. We directly measured lateral gastrocnemius muscle force and length in wild turkeys during controlled landings requiring rapid energy dissipation. Muscle-tendon unit (MTU) strain was measured via video kinematics, independent of muscle fascicle strain (measured via sonomicrometry). We found that rapid MTU lengthening immediately following impact involved little or no muscle fascicle lengthening. Therefore, joint flexion had to be accommodated by tendon stretch. After the early contact period, muscle fascicles lengthened and absorbed energy. This late lengthening occurred after most of the joint flexion, and was thus mainly driven by tendon recoil. Temporary tendon energy storage led to a significant reduction in muscle fascicle lengthening velocity and the rate of energy absorption. We conclude that tendons function as power attenuators that probably protect muscles against damage from rapid and forceful lengthening during energy dissipation.     

Changes in shear wave propagation within skeletal muscle during active and passive force generation

Muscle force can be generated actively through changes in neural excitation, and passively through externally imposed changes in muscle length. Disease and injury can disrupt force generation, but it can be challenging to separate passive from active contributions to these changes. Ultrasound elastography is a promising tool for characterizing the mechanical properties of muscles and the forces that they generate. Most prior work using ultrasound elastography in muscle has focused on the group velocity of shear waves, which increases with increasing muscle force. Few studies have quantified the phase velocity, which depends on the viscoelastic properties of muscle. Since passive and active forces within muscle involve different structures for force transmission, we hypothesized that measures of phase velocity could detect changes in shear wave propagation during active and passive conditions that cannot be detected when considering only group velocity. We measured phase and group velocity in the human biceps brachii during active and passive force generation and quantified the differences in estimates of shear elasticity obtained from each of these measurements. We found that measures of group velocity consistently overestimate the shear elasticity of muscle. We used a Voigt model to characterize the phase velocity and found that the estimated time constant for the Voigt model provided a way to distinguish between passive and active force generation. Our results demonstrate that shear wave elastography can be used to distinguish between passive and active force generation when it is used to characterize the phase velocity of shear waves propagating in muscle.     

Elastic energy savings and active energy cost in a simple model of running

The energetic economy of running benefits from tendon and other tissues that store and return elastic energy, thus saving muscles from costly mechanical work. The classic “Spring-mass” computational model successfully explains the forces, displacements and mechanical power of running, as the outcome of dynamical interactions between the body center of mass and a purely elastic spring for the leg. However, the Spring-mass model does not include active muscles and cannot explain the metabolic energy cost of running, whether on level ground or on a slope. Here we add explicit actuation and dissipation to the Spring-mass model, and show how they explain substantial active (and thus costly) work during human running, and much of the associated energetic cost. Dissipation is modeled as modest energy losses (5% of total mechanical energy for running at 3 m s^-1) from hysteresis and foot-ground collisions, that must be restored by active work each step. Even with substantial elastic energy return (59% of positive work, comparable to empirical observations), the active work could account for most of the metabolic cost of human running (about 68%, assuming human-like muscle efficiency). We also introduce a previously unappreciated energetic cost for rapid production of force, that helps explain the relatively smooth ground reaction forces of running, and why muscles might also actively perform negative work. With both work and rapid force costs, the model reproduces the energetics of human running at a range of speeds on level ground and on slopes. Although elastic return is key to energy savings, there are still losses that require restorative muscle work, which can cost substantial energy during running.     

The series elastic shock absorber: tendon elasticity modulates energy dissipation by muscle during burst deceleration

During downhill running, manoeuvring, negotiation of obstacles and landings from a jump, mechanical energy is dissipated via active lengthening of limb muscles. Tendon compliance provides a ‘shock-absorber’ mechanism that rapidly absorbs mechanical energy and releases it more slowly as the recoil of the tendon does work to stretch muscle fascicles. By lowering the rate of muscular energy dissipation, tendon compliance likely reduces the risk of muscle injury that can result from rapid and forceful muscle lengthening. Here, we examine how muscle–tendon mechanics are modulated in response to changes in demand for energy dissipation. We measured lateral gastrocnemius (LG) muscle activity, force and fascicle length, as well as leg joint kinematics and ground-reaction force, as turkeys performed drop-landings from three heights (0.5–1.5 m centre-of-mass elevation). Negative work by the LG muscle–tendon unit during landing increased with drop height, mainly owing to greater muscle recruitment and force as drop height increased. Although muscle strain did not increase with landing height, ankle flexion increased owing to increased tendon strain at higher muscle forces. Measurements of the length–tension relationship of the muscle indicated that the muscle reached peak force at shorter and likely safer operating lengths as drop height increased. Our results indicate that tendon compliance is important to the modulation of energy dissipation by active muscle with changes in demand and may provide a mechanism for rapid adjustment of function during deceleration tasks of unpredictable intensity.     

Muscle Function in vivo: A Comparison of Muscles used for Elastic Energy Savings versus Muscles Used to Generate Mechanical Power1

SYNOPSIS. The function of muscles used to generate force economicallyand facilitate elastic energy savings in their tendons is comparedwith muscles that function to produce mechanical power. Theunderlying architectural design of the muscle and its tendon(if present) dictate much of their functional capacity and rolein animal locomotion. Using methods that allow direct recordingsof muscle force and fiber length change, the functional designof muscle-tendon systems can now be investigated in vivo. Thesestudies reveal that, in the case of wallaby hindleg muscles,the fibers can maintain sufficient stiffness during tendon stretchand recoil to ensure useful elastic energy recovery and savingsof metabolic energy. In the case of the pectoralis muscle ofpigeons, although isometric or active lengthening of the muscle'sfibers may occur late in the upstroke of the wing beat cycleto enhance force development, the fibers shorten extensivelyduring the downstroke (up to 35% of their resting length) toproduce mechanical power for aerodynamic lift and thrust. Oscillatorylength change, with force enhancement during active lengtheningmay be a general feature of muscles that power aerial and aquaticlocomotion. Similarly, force enhancement by active lengtheningis likely to be important to the design and function of musclesthat primarily generate force to minimize energy expenditure/unitforce generated, as well as for elastic energy savings withina long tendon. Architectural features of muscle-tendon unitsfor effective elastic energy savings, however, are likely toconstrain locomotor performance when mechanical work is required,as when an animal accelerates, either limiting performance orrequiring the recruitment of functional agonists with greatermechanical power generating capability (i.e., longer fibers)     

Energetics of rat papillary muscle during contractions with sinusoidal length changes

The mechanical efficiency of rat cardiac muscle was determined using a contraction protocol involving cyclical, sinusoidal length changes and phasic stimulation at physiological frequencies (1-4 Hz). Experiments were performed in vitro (27 degrees C) using rat left ventricular papillary muscles. Efficiency was determined from measurements of the net work performed and enthalpy produced by muscles during a series of 40 contractions. Net mechanical efficiency was defined as the percentage of the total, suprabasal enthalpy output that appeared as mechanical work. Maximum efficiency was approximately 15% at contraction frequencies between 2 and 2.5 Hz. At lower and higher frequencies, efficiency was approximately 10%. Enthalpy output per cycle was independent of cycle frequency at all but the highest frequency used. The basis of the high efficiency between 2 and 2.5 Hz was that work output was also greatest at these frequencies. At these frequencies, the duration of the applied length change was well matched to the kinetics of force generation, and active force generation occurred throughout the shortening period.     

Exploring Muscle Activation during Nordic Walking: A Comparison between Conventional and Uphill Walking

Nordic Walking (NW) owes much of its popularity to the benefits of greater energy expenditure and upper body engagement than found in conventional walking (W). Muscle activation during NW is still understudied, however. The aim of the present study was to assess differences in muscle activation and physiological responses between NW and W in level and uphill walking conditions. Nine expert Nordic Walkers (mean age 36.8±11.9 years; BMI 24.2±1.8 kg/m²) performed 5-minute treadmill trials of W and NW at 4 km/h on inclines of 0% and 15%. The electromyographic activity of seven upper body and five leg muscles and oxygen consumption (VO₂) were recorded and pole force during NW was measured. VO₂ during NW was 22.3% higher at 0% and only 6.9% higher at 15% than during W, while upper body muscle activation was 2- to 15-fold higher under both conditions. Lower body muscle activation was similarly increased during NW and W in the uphill condition, whereas the increase in erector spinae muscle activity was lower during NW than W. The lack of a significant increase in pole force during uphill walking may explain the lower extra energy expenditure of NW, indicating less upper body muscle activation to lift the body against gravity. NW seemed to reduce lower back muscle contraction in the uphill condition, suggesting that walking with poles may reduce effort to control trunk oscillations and could contribute to work production during NW. Although the difference in extra energy expenditure between NW and W was smaller in the uphill walking condition, the increased upper body muscle involvement during exercising with NW may confer additional benefit compared to conventional walking also on uphill terrains. Furthermore, people with low back pain may gain benefit from pole use when walking uphill.     

The bounce of the body in hopping,running and trotting: different machines with the same motor

The bouncing mechanism of human running is characterized by a shorter duration of the brake after ‘landing’ compared with a longer duration of the push before ‘takeoff’. This landing–takeoff asymmetry has been thought to be a consequence of the force–velocity relation of the muscle, resulting in a greater force exerted during stretching after landing and a lower force developed during shortening before takeoff. However, the asymmetric lever system of the human foot during stance may also be the cause. Here, we measure the landing–takeoff asymmetry in bouncing steps of running, hopping and trotting animals using diverse lever systems. We find that the duration of the push exceeds that of the brake in all the animals, indicating that the different lever systems comply with the basic property of muscle to resist stretching with a force greater than that developed during shortening. In addition, results show both the landing–takeoff asymmetry and the mass-specific vertical stiffness to be greater in small animals than in large animals. We suggest that the landing–takeoff asymmetry is an index of a lack of elasticity, which increases with increasing the role of muscle relative to that of tendon within muscle–tendon units.     

Influence of static stretching on viscoelastic properties of human tendon structures in vivo.

The purpose of this study was to investigate the influences of static stretching on the viscoelastic properties of human tendon structures in vivo. Seven male subjects performed static stretching in which the ankle was passively flexed to 35 degrees of dorsiflexion and remained stationary for 10 min. Before and after the stretching, the elongation of the tendon and aponeurosis of medial gastrocnemius muscle (MG) was directly measured by ultrasonography while the subjects performed ramp isometric plantar flexion up to the maximum voluntary contraction (MVC), followed by a ramp relaxation. The relationship between the estimated muscle force (Fm) of MG and tendon elongation (L) during the ascending phase was fitted to a linear regression, the slope of which was defined as stiffness of the tendon structures. The percentage of the area within the Fm-L loop to the area beneath the curve during the ascending phase was calculated as an index representing hysteresis. Stretching produced no significant change in MVC but significantly decreased stiffness and hysteresis from 22.9 +/- 5.8 to 20.6 +/- 4.6 N/mm and from 20.6 +/- 8.8 to 13.5 +/- 7.6%, respectively. The present results suggest that stretching decreased the viscosity of tendon structures but increased the elasticity.     

A comparison of muscle energy models for simulating human walking in three dimensions

The popular Hill model for muscle activation and contractile dynamics has been extended with several different formulations for predicting the metabolic energy expenditure of human muscle actions. These extended models differ considerably in their approach to computing energy expenditure, particularly in their treatment of active lengthening and eccentric work, but their predictive abilities have never been compared. In this study, we compared the predictions of five different Hill-based muscle energy models in 3D forward dynamics simulations of normal human walking. In a data-tracking simulation that minimized muscle fatigue, the energy models predicted metabolic costs that varied over a three-fold range (2.45–7.15 J/m/kg), with the distinction arising from whether or not eccentric work was subtracted from the net heat rate in the calculation of the muscle metabolic rate. In predictive simulations that optimized neuromuscular control to minimize the metabolic cost, all five models predicted similar speeds, step lengths, and stance phase durations. However, some of the models predicted a hip circumduction strategy to minimize metabolic cost, while others did not, and the accuracy of the predicted knee and ankle angles and ground reaction forces also depended on the energy model used. The results highlights the need to clarify how eccentric work should be treated when calculating muscle energy expenditure, the difficulty in predicting realistic metabolic costs in simulated walking even with a detailed 3D musculoskeletal model, the potential for using such models to predict energetically-optimal gait modifications, and the room for improvement in existing muscle energy models and locomotion simulation frameworks.     

The weak link: do muscle properties determine locomotor performance in frogs?

Muscles power movement, yet the conceptual link between muscle performance and locomotor performance is poorly developed. Frog jumping provides an ideal system to probe the relationship between muscle capacity and locomotor performance, because a jump is a single discrete event and mechanical power output is a critical determinant of jump distance. We tested the hypothesis that interspecific variation in jump performance could be explained by variability in available muscle power. We used force plate ergometry to measure power produced during jumping in Cuban tree frogs (Osteopilus septentrionalis), leopard frogs (Rana pipiens) and cane toads (Bufo marinus). We also measured peak isotonic power output in isolated plantaris muscles for each species. As expected, jump performance varied widely. Osteopilus septentrionalis developed peak power outputs of 1047.0 ± 119.7 W kg(-1) hindlimb muscle mass, about five times that of B. marinus (198.5 ± 54.5 W kg(-1)). Values for R. pipiens were intermediate (543.9 ± 96.2 W kg(-1)). These differences in jump power were not matched by differences in available muscle power, which were 312.7 ± 28.9, 321.8 ± 48.5 and 262.8 ± 23.2 W kg(-1) muscle mass for O. septentrionalis, R. pipiens and B. marinus, respectively. The lack of correlation between available muscle power and jump power suggests that non-muscular mechanisms (e.g. elastic energy storage) can obscure the link between muscle mechanical performance and locomotor performance.     

Making muscle elastic: the structural basis of myomesin stretching

Skeletal and cardiac muscles are remarkable biological machines that support and move our bodies and power the rhythmic work of our lungs and hearts. As well as producing active contractile force, muscles are also passively elastic, which is essential to their performance. The origins of both active contractile and passive elastic forces can be traced to the individual proteins that make up the highly ordered structure of muscle. In this Primer, we describe the organization of sarcomeres--the structural units that produce contraction--and the nature of the proteins that make muscle elastic. In particular, we focus on an elastic protein called myomesin, whose novel modular architecture helps explain elasticity.     

Effect of cycle frequency and excursion amplitude on work done by rat diaphragm muscle

Strips of isolated rat diaphragm muscle were attached to a servomotor-transducer apparatus, and the muscle length was cycled in a sinusoidal fashion about the length at which maximum isometric twitch force was developed, Lo. The amplitude of the length displacement (excursion amplitude) and rate of cycling were varied between 3 and 13% Lo and 1-4 Hz respectively. The muscle was tetanically stimulated (100 Hz, supramaximal voltage, stimulus duration (duty cycle) 20% of the length cycle period) during the shortening stage of the imposed length cycle at the phase that yielded maximum net positive work. The force and displacement of the muscle were recorded. Work per cycle was calculated from the area of the loop formed by plotting force against length for one full stretch-shorten cycle. Work per cycle decreased, but power increased, as cycle frequency was increased from 1 to 4 Hz. Maximum work done per cycle was about 12.8 J/kg at a cycle frequency of 1 Hz. Maximum mean power developed was about 27 W/kg and occurred at a cycle frequency of 4 Hz. Work and power were maximum at an excursion amplitude of 13% of Lo (i.e., Lo +/- 6.5%). Measured work and power output are considerably less than values estimated from length-tension and force-velocity curves.     

Evidence that a higher ATP cost of muscular contraction contributes to the lower mechanical efficiency associated with COPD: preliminary findings

Impaired metabolism in peripheral skeletal muscles potentially contributes to exercise intolerance in chronic obstructive pulmonary disease (COPD). We used (31)P-magnetic resonance spectroscopy ((31)P-MRS) to examine the energy cost and skeletal muscle energetics in six patients with COPD during dynamic plantar flexion exercise compared with six well-matched healthy control subjects. Patients with COPD displayed a higher energy cost of muscle contraction compared with the controls (control: 6.1 ± 3.1% of rest·min(-1)·W(-1), COPD: 13.6 ± 8.3% of rest·min(-1)·W(-1), P = 0.01). Although, the initial phosphocreatine resynthesis rate was also significantly attenuated in patients with COPD compared with controls (control: 74 ± 17% of rest/min, COPD: 52 ± 13% of rest/min, P = 0.04), when scaled to power output, oxidative ATP synthesis was similar between groups (6.5 ± 2.3% of rest·min(-1)·W(-1) in control and 7.8 ± 3.9% of rest·min(-1)·W(-1) in COPD, P = 0.52). Therefore, our results reveal, for the first time that in a small subset of patients with COPD a higher ATP cost of muscle contraction may substantially contribute to the lower mechanical efficiency previously reported in this population. In addition, it appears that some patients with COPD have preserved mitochondrial function and normal energy supply in lower limb skeletal muscle.     

Experimental Evidence of the Tonic Vibration Reflex during Whole-Body Vibration of the Loaded and Unloaded Leg

Increased muscle activation during whole-body vibration (WBV) is mainly ascribed to a complex spinal and supraspinal neurophysiological mechanism termed the tonic vibration reflex (TVR). However, TVR has not been experimentally demonstrated during low-frequency WBV, therefore this investigation aimed to determine the expression of TVR during WBV.  Whilst seated, eight healthy males were exposed to either vertical WBV applied to the leg via the plantar-surface of the foot, or Achilles tendon vibration (ATV) at 25Hz and 50Hzfor 70s. Ankle plantar-flexion force, tri-axial accelerations at the shank and vibration source, and surface EMG activity of m. soleus (SOL) and m. tibialis anterior (TA) were recorded from the unloaded and passively loaded leg to simulate body mass supported during standing.  Plantar flexion force was similarly augmented by WBV and ATV and increased over time in a load- and frequency dependent fashion. SOL and TA EMG amplitudes increased over time in all conditions independently of vibration mode. 50Hz WBV and ATV resulted in greater muscle activation than 25Hz in SOL when the shank was loaded and in TA when the shank was unloaded despite the greater transmission of vertical acceleration from source to shank with 25Hz and WBV, especially during loading. Low-amplitude WBV of the unloaded and passively loaded leg produced slow tonic muscle contraction and plantar-flexion force increase of similar magnitudes to those induced by Achilles tendon vibration at the same frequencies. This study provides the first experimental evidence supporting the TVR as a plausible mechanism underlying the neuromuscular response to whole-body vibration.     

The influence of an elastic tendon on the force producing capabilities of a muscle during dynamic movements

With increasing computer power, computer simulation of human movement has become a popular research tool. However, time to complete simulations can still be long even on powerful computers. One possibility for reducing simulation time, with models of musculo-skeletal system, is to simulate the muscle using a rigid tendon rather than the more realistic compliant tendon. This study examines the effect of tendon elasticity on muscle force output under different dynamic conditions. A single muscle, point mass model was used and simulations were performed varying the mass, the tendon length, the initial position, and the task. For simulations for relatively slow motion, as experienced for example in upper limb reaching motions or rising from a chair, tendon properties had little influence on muscle force, in contrast simulations of an explosive task similar to jumping or throwing tendon had a much larger effect.     

The influence of an elastic tendon on the force producing capabilities of a muscle during dynamic movements

With increasing computer power, computer simulation of human movement has become a popular research tool. However, time to complete simulations can still be long even on powerful computers. One possibility for reducing simulation time, with models of musculo-skeletal system, is to simulate the muscle using a rigid tendon rather than the more realistic compliant tendon. This study examines the effect of tendon elasticity on muscle force output under different dynamic conditions. A single muscle, point mass model was used and simulations were performed varying the mass, the tendon length, the initial position, and the task. For simulations for relatively slow motion, as experienced for example in upper limb reaching motions or rising from a chair, tendon properties had little influence on muscle force, in contrast simulations of an explosive task similar to jumping or throwing tendon had a much larger effect.     

The effect of higher ATP cost of contraction on the metabolic response to graded exercise in patients with chronic obstructive pulmonary disease

To better understand the metabolic implications of a higher ATP cost of contraction in chronic obstructive pulmonary disease (COPD), we used (31)P-magnetic resonance spectroscopy ((31)P-MRS) to examine muscle energetics and pH in response to graded exercise. Specifically, in six patients and six well-matched healthy controls, we determined the intracellular threshold for pH (T(pH)) and inorganic phosphate-to-phosphocreatine ratio (T(Pi/PCr)) during progressive dynamic plantar flexion exercise with work rate expressed as both absolute and relative intensity. Patients with COPD displayed a lower peak power output (WRmax) compared with controls (controls 25 ± 4 W, COPD 15 ± 5 W, P = 0.01) while end-exercise pH (controls 6.79 ± 0.15, COPD 6.76 ± 0.21, P = 0.87) and PCr consumption (controls 82 ± 10%, COPD 70 ± 18%, P = 0.26) were similar between groups. Both T(pH) and T(Pi/PCr) occurred at a significantly lower absolute work rate in patients with COPD compared with controls (controls: 14.7 ± 2.4 W for T(pH) and 15.3 ± 2.4 W for T(Pi/PCr); COPD: 9.7 ± 4.5 W for T(pH) and 10.0 ± 4.6 W for T(Pi/PCr), P < 0.05), but these thresholds occurred at the same percentage of WRmax (controls: 63 ± 11% WRmax for T(pH) and 67 ± 18% WRmax for T(Pi/PCr); COPD: 59 ± 9% WRmax for T(pH) and 61 ± 12% WRmax for T(Pi/PCr), P > 0.05). Indexes of mitochondrial function, the PCr recovery time constant (controls 42 ± 7 s, COPD 45 ± 11 s, P = 0.66) and the PCr resynthesis rate (controls 105 ± 21%/min, COPD 91 ± 31%/min, P = 0.43) were similar between groups. In combination, these results reveal that when energy demand is normalized to WRmax, as a consequence of higher ATP cost of contraction, patients with COPD display the same metabolic pattern as healthy subjects, suggesting that skeletal muscle energy production is well preserved in these patients.     

Length-force characteristics of aponeurosis in passive muscle and during isometric and slow dynamic contractions of rat gastrocnemius muscle

Length-force characteristics of aponeurosis of rat gastrocnemius medialis muscle and achilles tendon were studied for passive and active muscle. Active muscle performed isometric as well as slow concentric and eccentric contractions at low velocity. For isometric conditions, different aponeurosis and tendon length-force characteristics were found between passive and active muscle: At comparable low levels of force longer aponeuroses were encountered in passive than in active muscle. Similar results were found for achilles tendon, but the magnitude of the length change involved was smaller than for aponeurosis. For active muscle, no differences of aponeurosis length- force characteristics could be distinguished between the isometric contractions and a slow concentric contraction. Indications that such differences of aponeurosis length-force characteristics may exist between slow concentric and eccentric contractions were found. It is concluded that, for gastrocnemius medialis muscle, aponeurosis and tendon length - force characteristics may be quite variable depending on recent history of muscle length and activity.