Deactivation rate and shortening velocity as determinants of contractile frequency

1990 ◽  
Vol 259 (2) ◽  
pp. R223-R230 ◽  
Author(s):  
R. L. Marsh

The kinetic properties of muscle that could influence locomotor frequency include rate of activation, rate of cross-bridge "attachment", intrinsic shortening velocity, and rate of deactivation. The latter two mechanisms are examined using examples from high-speed running in lizards and escape swimming in scallops. During running, inertial loading and elastic energy storage probably mitigate the effects of thermal alterations in intrinsic muscle shortening velocity. The result is a rather low thermal dependence of stride frequency over a 15-20 degree C temperature range. However, at lower temperatures, the longer times required for deactivation cause the thermal dependence of frequency to increase greatly. Scallops use a single muscle to swim by jet propulsion. In vivo shortening velocity in these animals also shows a low thermal dependence. As with high-speed running, the mechanics of jet propulsion may limit the effects of thermally induced changes in intrinsic shortening velocity. The largest thermal effect during swimming is on the initial phase of valve opening. The effects of temperature on the rate of deactivation of the adductor muscle could play an important role in limiting reextension of the muscle, which is dependent on elastic energy storage in the hinge ligament. These examples illustrate that the relative importance of various intrinsic contractile properties in controlling locomotor performance depends on the mechanics of the movements.

1995 ◽  
Vol 198 (9) ◽  
pp. 1829-1841 ◽  
Author(s):  
A Biewener ◽  
R Baudinette

In order to evaluate the role of elastic energy recovery in the hopping of macropodids, in vivo measurements of muscle­tendon forces using buckle force transducers attached to the tendons of the gastrocnemius (G), plantaris (PL) and flexor digitorum longus (FDL) of tammar wallabies were made as the animals hopped on a treadmill at speeds ranging from 2.1 to 6.3 m s-1. These muscles and tendons constitute the main structures that are most important in energy storage and recovery. Electromyographic recordings from the lateral gastrocnemius and plantaris muscles, together with high-speed films (200 frames s-1) and video (60 fields s-1), were also used to correlate muscle activation and kinematic patterns of limb movement with force development. On the basis of in situ calibrations of the buckle transducers, we found that muscle forces and elastic energy storage increased with increased hopping speed in all three muscle­tendon units. Elastic energy recovery reached a maximum of 25 % of metabolic energy expenditure at 6.3 m s-1 and is probably greater than this at higher speeds. Force sharing among the three muscles was consistently maintained over this range of speeds in terms of recruitment. Although forces and stresses were generally comparable within the gastrocnemius and plantaris muscles, maximal tendon stresses were considerably greater in the gastrocnemius, because of its smaller cross-sectional area (peak muscle stress: 227 versus 262 kPa; peak tendon stress: 36 versus 32 MPa, G versus PL). As a result, energy storage was greatest in the gastrocnemius tendon despite its much shorter length, which limits its volume and, hence, energy storage capacity, compared with PL and FDL tendons. Forces and stresses (17 MPa maximum) developed within the FDL tendon were consistently much lower than those for the other two tendons. Peak stresses in these three tendons indicated safety factors of 3.0 for G, 3.3 for PL and 6.0 for FDL. The lower stresses developed within the tendons of the plantaris and, especially, the flexor digitorum longus may indicate the need to maintain sufficient stiffness for phalangeal control of foot placement, at the expense of reduced strain energy recovery.


2011 ◽  
Vol 8 (3) ◽  
pp. 386-389 ◽  
Author(s):  
Henry C. Astley ◽  
Thomas J. Roberts

Anuran jumping is one of the most powerful accelerations in vertebrate locomotion. Several species are hypothesized to use a catapult-like mechanism to store and rapidly release elastic energy, producing power outputs far beyond the capability of muscle. Most evidence for this mechanism comes from measurements of whole-body power output; the decoupling of joint motion and muscle shortening expected in a catapult-like mechanism has not been demonstrated. We used high-speed marker-based biplanar X-ray cinefluoroscopy to quantify plantaris muscle fascicle strain and ankle joint motion in frogs in order to test for two hallmarks of a catapult mechanism: (i) shortening of fascicles prior to joint movement (during tendon stretch), and (ii) rapid joint movement during the jump without rapid muscle-shortening (during tendon recoil). During all jumps, muscle fascicles shortened by an average of 7.8 per cent (54% of total strain) prior to joint movement, stretching the tendon. The subsequent period of initial joint movement and high joint angular acceleration occurred with minimal muscle fascicle length change, consistent with the recoil of the elastic tendon. These data support the plantaris longus tendon as a site of elastic energy storage during frog jumping, and demonstrate that catapult mechanisms may be employed even in sub-maximal jumps.


Science ◽  
2013 ◽  
Vol 340 (6137) ◽  
pp. 1217-1220 ◽  
Author(s):  
N. T. George ◽  
T. C. Irving ◽  
C. D. Williams ◽  
T. L. Daniel

Muscles not only generate force. They may act as springs, providing energy storage to drive locomotion. Although extensible myofilaments are implicated as sites of energy storage, we show that intramuscular temperature gradients may enable molecular motors (cross-bridges) to store elastic strain energy. By using time-resolved small-angle x-ray diffraction paired with in situ measurements of mechanical energy exchange in flight muscles of Manduca sexta, we produced high-speed movies of x-ray equatorial reflections, indicating cross-bridge association with myofilaments. A temperature gradient within the flight muscle leads to lower cross-bridge cycling in the cooler regions. Those cross-bridges could elastically return energy at the extrema of muscle lengthening and shortening, helping drive cyclic wing motions. These results suggest that cross-bridges can perform functions other than contraction, acting as molecular links for elastic energy storage.


Nature ◽  
2013 ◽  
Vol 498 (7455) ◽  
pp. 483-486 ◽  
Author(s):  
Neil T. Roach ◽  
Madhusudhan Venkadesan ◽  
Michael J. Rainbow ◽  
Daniel E. Lieberman

1990 ◽  
Vol 152 (1) ◽  
pp. 333-351 ◽  
Author(s):  
G. J. Ettema ◽  
P. A. Huijing ◽  
G. J. van Ingen Schenau ◽  
A. de Haan

Work output of rat gastrocnemius medialis (GM) muscle (N = 5) was measured for stretch-shortening contractions, in which initiation of stretch occurred prior to the onset of activation, and for contractions with an isometric prephase. Duration of the active prephase (prestretch and pre-isometric) varied from 20 to 200 ms. Subsequent shortening (from optimum length + 4 mm to optimum length −2mm) lasted 150 ms. Stretch velocities of 5, 10 and 20 mm s-1 were used, and the shortening velocity was 40 mm s-1. The effects of several combinations of active stretch duration and active stretch amplitude were compared. Using force-compliance characteristics, the work of the contractile element (CE), elastic energy storage and release of the undamped series elastic component (SEC) were distinguished. During shortening, an extra amount of work output was produced, induced by active stretch, of which the largest contribution (70–80%) was due to higher elastic energy release. Enhancement of the storage and utilization of elastic energy during the stretch-shortening cycle, caused by higher transition-point forces (i.e. force at onset of shortening), increased with active stretch amplitude and was associated with a net loss of work, probably due to cross-bridge detachment during active stretch. Net work over the stretch-shortening cycle remained positive for all prestretch contractions, indicating that when a muscle performs this type of contraction, it is able to contribute to work performance on body segments. It is concluded that, in stretch-shortening movements of rat GM muscle, maximal positive work output is incompatible with maximal net work output. Consequences for complex movements in vivo are discussed.


1990 ◽  
Vol 68 (3) ◽  
pp. 1033-1040 ◽  
Author(s):  
R. E. Shadwick

We investigated the possibility that tendons that normally experience relatively high stresses and function as springs during locomotion, such as digital flexors, might develop different mechanical properties from those that experience only relatively low stresses, such as digital extensors. At birth the digital flexor and extensor tendons of pigs have identical mechanical properties, exhibiting higher extensibility and mechanical hysteresis and lower elastic modulus, tensile strength, and elastic energy storage capability than adult tendons. With growth and aging these tendons become much stronger, stiffer, less extensible, and more resilient than at birth. Furthermore, these alterations in elastic properties occur to a significantly greater degree in the high-load-bearing flexors than in the low-stress extensors. At maturity the pig digital flexor tendons have twice the tensile strength and elastic modulus but only half the strain energy dissipation of the corresponding extensor tendons. A morphometric analysis of the digital muscles provides an estimate of maximal in vivo tendon stresses and suggests that the muscle-tendon unit of the digital flexor is designed to function as an elastic energy storage element whereas that of the digital extensor is not. Thus the differences in material properties between mature flexor and extensor tendons are correlated with their physiological functions, i.e., the flexor is much better suited to act as an effective biological spring than is the extensor.


2019 ◽  
Vol 286 (1900) ◽  
pp. 20182764 ◽  
Author(s):  
Christopher J. Arellano ◽  
Nicolai Konow ◽  
Nicholas J. Gidmark ◽  
Thomas J. Roberts

Tendinous structures are generally thought of as biological springs that operate with a fixed stiffness, yet recent observations on the mechanical behaviour of aponeuroses (broad, sheet-like tendons) have challenged this general assumption. During in situ contractions, aponeuroses undergo changes in both length and width and changes in aponeuroses width can drive changes in longitudinal stiffness. Here, we explore if changes in aponeuroses width can modulate elastic energy (EE) storage in the longitudinal direction. We tested this idea in vivo by quantifying muscle and aponeuroses mechanical behaviour in the turkey lateral gastrocnemius during landing and jumping, activities that require rapid rates of energy dissipation and generation, respectively. We discovered that when aponeurosis width increased (as opposed to decreased), apparent longitudinal stiffness was 34% higher and the capacity of aponeuroses to store EE when stretched in the longitudinal direction was 15% lower. These data reveal that biaxial loading of aponeuroses allows for variation in tendon stiffness and energy storage for different locomotor behaviours.


1994 ◽  
Vol 266 (3) ◽  
pp. R1022-R1031 ◽  
Author(s):  
C. M. Pollock ◽  
R. E. Shadwick

This paper considers the structural properties of muscle-tendon units in the hindlimbs of mammals as a function of body mass. Morphometric analysis of the ankle extensors, digital flexors, and digital extensors from 35 quadrupedal species, ranging in body mass from 0.04 to 545 kg, was carried out. Tendon dimensions scale nearly isometrically, as does muscle mass. The negative allometry of muscle fiber length results in positive allometric scaling of muscle cross-sectional areas in all but digital extensors. Maximum muscle forces are predicted to increase allometrically, with mass exponents as high as 0.91 in the plantaris, but nearly isometrically (0.69) in the digital extensors. Thus the maximum amount of stress a tendon may experience in vivo, as indicated by the ratio of muscle and tendon cross-sectional areas, increases with body mass in digital flexors and ankle extensors. Consequently, the capacity for elastic energy storage scales with positive allometry in these tendons but is isometric in the digital extensors, which probably do not function as springs in normal locomotion. These results suggest that the springlike tendons of large mammals can potentially store more elastic strain energy than those of smaller mammals because their disproportionately stronger muscles can impose higher tendon stresses.


Author(s):  
Brooke A. Christensen ◽  
David C. Lin ◽  
M. Janneke Schwaner ◽  
Craig P. McGowan

Small bipedal hoppers, including kangaroo rats, are thought to not benefit from substantial elastic energy storage and return during hopping. However, recent species-specific material properties research suggests that, despite relative thickness, the ankle extensor tendons of these small hoppers are considerably more compliant than had been assumed. With faster locomotor speeds demanding higher forces, a lower tendon stiffness suggests greater tendon deformation and thus a greater potential for elastic energy storage and return with increasing speed. Using the elastic modulus values specific to kangaroo rat tendons, we sought to determine how much elastic energy is stored and returned during hopping across a range of speeds. In vivo techniques were used to record tendon force in the ankle extensors during steady-speed hopping. Our data support the hypothesis that the ankle extensor tendons of kangaroo rats store and return elastic energy in relation to hopping speed, storing more at faster speeds. Despite storing comparatively less elastic energy than larger hoppers, this relationship between speed and energy storage offer novel evidence of a functionally similar energy storage mechanism, operating irrespective of body size or tendon thickness, across the distal muscle-tendon units of both small and large bipedal hoppers.


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