Elastic energy storage and release in white muscle from dogfish scyliorhinus canicula

1999 ◽  
Vol 202 (2) ◽  
pp. 135-142 ◽  
Author(s):  
F. Lou ◽  
N.A. Curtin ◽  
R.C. Woledge

The production of work by the contractile component (CC) and the storage and release of work in the elastic structures that act in series (the series elastic component, SEC) with the contractile component were measured using white muscle fibres from the dogfish Scyliorhinus canicula. Heat production was also measured because the sum of work and heat is equivalent to the energy cost of the contraction (ATP used). These energy fluxes were evaluated in contractions with constant-velocity shortening either during stimulation or during relaxation. The muscle preparation was tetanized for 0.6 s and shortened by 1 mm (approximately 15 % of L0) at 3.5 or 7.0 mm s-1 (approximately 15 or 30 % of V0), where L0 is the muscle length at which isometric force is greatest and V0 is the maximum velocity of shortening. In separate experiments, the stiffness of the SEC was characterized from measurements of force responses to step changes in the length of contracting muscle. Using the values of SEC stiffness, we evaluated separately the work and heat associated with the CC and with the SEC. The major findings were (1) that work stored in the SEC could be completely recovered as external work when shortening occurred during relaxation (none of the stored work being degraded into heat) and (2) that, when shortening occurred progressively later during the contraction, the total energy cost of the contraction declined towards that of an isometric contraction.

1997 ◽  
Vol 200 (3) ◽  
pp. 495-501 ◽  
Author(s):  
F Lou ◽  
N Curtin ◽  
R Woledge

The energetic cost of activation was measured during an isometric tetanus of white muscle fibres from the dogfish Scyliorhinus canicula. The total heat production by the fibres was taken as a measure of the total energetic cost. This energy consists of two parts. One is due to crossbridge interaction which produces isometric force, and this part varies linearly with the degree of filament overlap in the fibres. The other part of the energy is that associated with activation of the crossbridges by Ca2+, mainly with uptake of Ca2+ into the sarcoplasmic reticulum by the ATP-driven Ca2+ pump. Total heat production was measured at various degrees of filament overlap beyond the optimum for force development. Extrapolation of heat versus force production data to evaluate the heat remaining at zero force gave a value of 34±5 % (mean ± s.e.m., N=24) for activation heat as a percentage of total heat production in a 2.0 s isometric tetanus. Values for 0.4 and 1.0 s of stimulation were similar. Comparison with values in the literature shows that the energetic cost of activation in dogfish muscle is very similar to that of frog skeletal muscle and it cannot explain the lower maximum efficiency of dogfish muscle compared with frog muscle. The proportion of energy for activation (Ca2+ turnover) is similar to that expected from a simple model in which Ca2+ turnover was varied to minimize the total energy cost for a contraction plus relaxation cycle.


2002 ◽  
Vol 205 (11) ◽  
pp. 1585-1595 ◽  
Author(s):  
F. Lou ◽  
N. A. Curtin ◽  
R. C. Woledge

SUMMARYMaximum isometric tetanic force produced by bundles of red muscle fibres from dogfish, Scyliorhinus canicula (L.), was 142.4±10.3 kN m-2 (N=35 fibre bundles); this was significantly less than that produced by white fibres 289.2±8.4 kN m-2(N=25 fibre bundles) (means ± S.E.M.). Part, but not all, of the difference is due to mitochondrial content. The maximum unloaded shortening velocity, 1.693±0.108 L0 s-1(N=6 fibre bundles), was measured by the slack-test method. L0 is the length giving maximum isometric force. The force/velocity relationship was investigated using a step-and-ramp protocol in seven red fibre bundles. The following equation was fitted to the data:[(P/P0)+(a/P0)](V+b)=[(P0*/P0)+(a/P0)]b,where P is force during shortening at velocity V,P0 is the isometric force before shortening, and a, band P0* are fitted constants. The fitted values were P0*/P0=1.228±0.053, Vmax=1.814±0.071 L0s-1, a/P0=0.269±0.024 and b=0.404±0.041 L0 s-1(N=7 for all values). The maximum power was 0.107±0.005P0Vmax and was produced during shortening at 0.297±0.012Vmax. Compared with white fibres from dogfish, the red fibres have a lower P0 (49%) and Vmax (48%), but the shapes of the force/velocity curves are similar. Thus, the white and red fibres have equal capacities to produce power within the limits set by the isometric force and maximum velocity of shortening of each fibre type. A step shortening of 0.050±0.003L0 (N=7) reduced the maximum isometric force in the red fibres' series elasticity to zero. The series elasticity includes all elastic structures acting in series with the attached cross-bridges. Three red fibre bundles were stretched at a constant velocity, and force (measured when length reached L0) was 1.519±0.032P0. In the range of velocities used here, -0.28 to -0.63Vmax, force varied little with the velocity.


2012 ◽  
Vol 590 (8) ◽  
pp. 1973-1988 ◽  
Author(s):  
S. Park‐Holohan ◽  
M. Linari ◽  
M. Reconditi ◽  
L. Fusi ◽  
E. Brunello ◽  
...  

1992 ◽  
Vol 163 (1) ◽  
pp. 281-295 ◽  
Author(s):  
L. C. Rome ◽  
A. Sosnicki ◽  
I. H. Choi

To understand better how scup can swim twice as fast as carp with its red muscle, we measured the mechanical properties of red muscle bundles in scup. The values of the mean maximum velocity of shortening (Vmax) at 10 degrees C (3.32 muscle lengths s-1) and at 20 degrees C (5.55 muscle lengths s-1; Q10 = 1.69) were nearly the same as those in carp. Isometric force, however, was approximately 50% greater (183 kN m-2; Q10 = 1.08). The maximal power generation was correspondingly about 50% greater in scup than in carp (71 W kg-1 at 10 degrees C and 134 W kg-1 at 20 degrees C; Q10 = 1.88). The larger power output of its muscle may be important in the faster swimming of the scup. In addition, the fact that scup use a less undulatory style of swimming means that, when they are swimming twice as fast, their red muscle shortens at the same velocity (V) and with the same V/Vmax (0.37, i.e. where maximum power is generated) as that of carp. The importance of V/Vmax is further shown by the comparison of scup swimming at different temperatures. The 1.69-fold higher Vmax at 20 degrees C than at 10 degrees C enables scup to swim with a 1.67-fold faster V at 20 degrees C. Thus, at both 10 degrees C and 20 degrees C, red muscle is used only over the same narrow range of V/Vmax (0.17-0.37), where experiments on isolated muscle suggest that power and efficiency are maximal. Therefore, V/Vmax appears to be an important design constraint that limits the range of velocities over which muscle is used in vivo, both at different temperatures and in fast- and slow-locomoting species.


1988 ◽  
Vol 140 (1) ◽  
pp. 187-197 ◽  
Author(s):  
N. A. CURTIN ◽  
R. C. WOLEDGE

The relationship between force and velocity of shortening and between power and velocity were examined for myotomal muscle fibre bundles from the dogfish. The maximum velocity of shortening, mean value 4.8 ± 0.2 μms−1 half sarcomere−1 (±S.E.M., N = 13), was determined by the ‘slack step’ method (Edman, 1979) and was found to be independent of fish length. The force-velocity relationship was hyperbolic, except at the high-force end where the observations were below the hyperbola fitted to the rest of the data. The maximum power output was 91 ± 14 W kg−1 wet mass (±S.E.M., N = 7) at a velocity of shortening of 1.3 ± 0.13μms−1 halfsarcomere−1 (±S.E.M., N = 7). This power output is considerably higher than that previously reported for skinned fibres (Bone et al. 1986). Correspondingly the force-velocity relationship is less curved for intact fibres than for skinned fibres. The maximum swimming speed (normalized for fish length) predicted from the observed power output of the muscle fibres decreased with increasing fish size; it ranged from 12.9 to 7.8 fish lengths s−1 for fish 0155–0.645m in length.


1998 ◽  
Vol 201 (1) ◽  
pp. 103-114 ◽  
Author(s):  
N A Curtin ◽  
A R Gardner-Medwin ◽  
R C Woledge

The aim of this study was to identify the principal factors that determine the time course of force and power output by muscle during patterns of stimulation and movement similar to those during fish swimming. Fully activated, white muscle fibres isolated from dogfish Scyliorhinus canicula were used to characterize the force-velocity relationship of the contractile component (CC) and the stress-strain relationship of the passive, elastic component (SEC) in series with the CC. A simple model of the time course of crossbridge activation during brief contractions was devised. Using the mechanical properties of the CC and SEC and the activation time course, force and power were predicted for brief contractions with constant-velocity movement and also for brief contractions starting at various times during sinusoidal movement. The predicted force and power were compared with observations for these patterns of stimulation and movement. The predictions matched the observations well for the period during stimulation. Matching of force was much less good for some specific conditions during relaxation, the period during which force persists after the end of stimulation. If either the slow rise of activation or the SEC was omitted from the calculation, the predictions were poor, even during stimulation. Additional factors which may influence force are discussed. These include the after-effects of shortening and stretch, the variation of force during constant-velocity stretch and non-uniform behaviour within the muscle.


1975 ◽  
Vol 63 (1) ◽  
pp. 53-83 ◽  
Author(s):  
H. C. Bennet-Clark

The anatomy of the metathoracic leg is redescribed with particular reference to storage of energy in cuticular elements and the way in which the stored energy is used in jumping. The jump of adult male locusts requires an energy of 9 mJ and that of the female requires 11 mJ. The semilunar processes of each metafemur store 4 mJ at a stress of 15 N, and the extensor tibiae apodeme stores a further 3 mJ at the same stress. The total stored energy in both metathoracic legs is 14 mJ. The extensor tibiae muscle produces a maximum isometric force of over 15 N at 30 degrees C and, when loaded with the extensor apodeme and semilunar processes, attains this force in 0.3 sec with a strain of 0.8 mm. The peak power output is 36 mW or 0.45 W.g-1. The peak isometric force is attained when the tibia is fully flexed and the force falls as the tibia extends. The extensor tibiae muscle A band is 5.5 mum long and the peak force is over 0.75 N.m-2. The peak velocity of shortening is 7 mm.sec-1 or about 1.75 lengths/sec at 30 degrees C. The tensile strength of the extensor apodeme is 0.6 kN.mm-2 and Young's modulus is 19 kN.mm-2. The safety factor does not exceed 1.2 and the safety factor of the semilunar processes and tibial cuticle is little higher. The jump impulse lasts 25–30 msec. A velocity of 3.2 m.sec-1 is reached after a peak acceleration of 180 m.sec-2. The peak power output is 0.75 W at close to maximum velocity. Energy losses in rotating the femur and tibia are small and it is shown that the leg is able to extend at 7 times the normal rate with losses of about 20%. Most of the stored energy is converted to kinetic energy as the animal jumps. A model is based on the relaxation of a spring that has the properties of the elastic elements of the locust leg into a lever with the same kinematics as the locust leg produces a force-distance curve similar to that measured for locust jumps. The major part of the jump energy is stored before the jump.


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