Power at the expense of efficiency in contraction of white muscle fibres from dogfish Scyliorhinus canicula

1996 ◽  
Vol 199 (3) ◽  
pp. 593-601 ◽  
Author(s):  
N Curtin ◽  
R Woledge
Keyword(s):  
Duty Cycle ◽  
White Muscle ◽  
Fibre Length ◽  
Energy Output ◽  
Muscle Fibres ◽  
Cycle Duration ◽  
Scyliorhinus Canicula ◽  
Stimulus Timing ◽  
High Level ◽  
Myotomal Muscle

Work and heat production of white myotomal muscle fibres from dogfish were measured during sinusoidal movement (0.71-5.0 Hz) at 12 C. Stimulus phase (stimulus timing relative to movement) and duty cycle (stimulus duration as a fraction of movement cycle duration) were varied to determine the parameters optimal for power output and for efficiency (work/total energy output). Movements of 0.067 and 0.120L0 were used, where L0 is the muscle fibre length giving maximum force in an isometric tetanus. At each frequency of movement and duty cycle, the stimulus phase giving the highest power was the same as that giving the highest efficiency. In contrast, at each frequency and optimal stimulus phase, the dependence of power on duty cycle was very different from the dependence of efficiency on duty cycle. Power generally increased with increasing duty cycle, whereas efficiency decreased. Thus, high power can be achieved at the expense of efficiency by adjusting stimulus duty cycle. When stimulus phase and duty cycle were optimized, efficiency was always higher for the larger distance of movement. The efficiency of energy conversion can be maintained at a high level as the frequency of movement increases from 1.25 to 5.0 Hz.

EFFICIENCY OF ENERGY CONVERSION DURING SINUSOIDAL MOVEMENT OF WHITE MUSCLE FIBRES FROM THE DOGFISH SCYLIORHINUS CANICULA

1993 ◽  
Vol 183 (1) ◽  
pp. 137-147 ◽  
Author(s):  
N. A. Curtin ◽  
R. C. Woledge
Keyword(s):  
Power Output ◽  
High Efficiency ◽  
Fibre Length ◽  
Dry Mass ◽  
Energy Output ◽  
Maximum Efficiency ◽  
Muscle Fibres ◽  
Work Output ◽  
Sinusoidal Movement ◽  
Myotomal Muscle

Net work output and heat production of white myotomal muscle fibres from the dogfish were measured during complete cycles of sinusoidal movement at 12°C. The peak-to-peak movement was about 9 % of the muscle fibre length; three stimuli at 32 ms intervals were given in each mechanical cycle. The frequency of movement and the timing of the stimulation were varied for each preparation to find the optimal conditions for power output and those optimal for efficiency (the ratio of net work output to total energy output as heat+work). To achieve either maximum power or maximum efficiency, the tetanus must start while the muscle fibres are being stretched, before the beginning of the shortening part of the mechanical cycle. The highest power output, averaged over one cycle, was 0.23+/−0.014 W g-1 dry mass (+/−s.e.m., N=9, 46.9+/−2.8 mW g-1 wet mass) and was produced during movement at 3.5 Hz. The highest efficiency, 0.41+/−0.02 (+/−s.e.m., N=13), occurred during movements at 2.0-2.5 Hz. This value is higher than the efficiency previously measured during isovelocity shortening of these fibres. The implications of the high efficiency for crossbridge models of muscle contraction are discussed.

EFFICIENCY OF ENERGY CONVERSION DURING SINUSOIDAL MOVEMENT OF RED MUSCLE FIBRES FROM THE DOGFISH SCYLIORHINUS CANICULA

1993 ◽  
Vol 185 (1) ◽  
pp. 195-206 ◽  
Author(s):  
N. A. Curtin ◽  
R. C. Woledge
Keyword(s):  
Power Output ◽  
Fibre Length ◽  
Stimulus Frequency ◽  
Energy Output ◽  
Maximum Efficiency ◽  
Muscle Fibres ◽  
Work Output ◽  
Sinusoidal Movement ◽  
The Difference ◽  
Myotomal Muscle

Bundles of red myotomal muscle fibres isolated from dogfish were electrically stimulated at 12 sC. Peak twitch force was 54 % of that produced by a brief isometric tetanus. Relaxation was slower than in white fibres, but much faster than would be expected for the tonic fibres found in amphibian muscle. These two results indicate that the red fibres in dogfish are slow, but not tonic, in their behaviour. Net work output and heat production were measured during complete cycles of sinusoidal movement. The following variables were kept constant: peak-to-peak movement, about 7 % of the muscle fibre length; tetanus duration, 33 % of the mechanical cycle time; stimulus frequency, 40 Hz. The frequency of movement and the timing of the stimulation were varied for each preparation to find the conditions optimal for power output and those optimal for efficiency (the ratio of net work output to total energy output as heat+work). To achieve either maximum power or maximum efficiency, the tetanus must start while the muscle fibres are being stretched, before the beginning of the shortening part of the mechanical cycle. The highest power output was produced during movement at 1.02 Hz. The highest efficiency, 0.507+/−0.045 (+/−s.e.m., N=9), was at 0.61-0.95 Hz. The efficiency is higher than that previously measured during sinusoidal movement of white fibres; the difference, 0.095+/− 0.045 (+/−s.e.m. of the difference, d.f. 20), is statistically significant at the 5 % level.

The energetic cost of activation of white muscle fibres from the dogfish Scyliorhinus canicula

1997 ◽  
Vol 200 (3) ◽  
pp. 495-501 ◽  
Author(s):  
F Lou ◽  
N Curtin ◽  
R Woledge
Keyword(s):  
Heat Production ◽  
White Muscle ◽  
Isometric Force ◽  
Force Production ◽  
Total Heat ◽  
Energetic Cost ◽  
Maximum Efficiency ◽  
Muscle Fibres ◽  
Scyliorhinus Canicula ◽  
A Value

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.

scholarly journals Mechanics of myosin function in white muscle fibres of the dogfish, Scyliorhinus canicula

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

scholarly journals Efficiency of energy conversion during shortening of muscle fibres from the dogfish Scyliorhinus canicula

1991 ◽  
Vol 158 (1) ◽  
pp. 343-353 ◽  
Author(s):  
N. A. Curtin ◽  
R. C. Woledge
Keyword(s):  
Total Energy ◽  
Energy Conversion ◽  
Heat Production ◽  
Mechanical Power ◽  
Energy Output ◽  
Muscle Fibres ◽  
Fibre Bundles ◽  
Velocity Of Shortening ◽  
Myotomal Muscle ◽  
Fibre Preparation

Force and heat production were measured during isovelocity shortening of tetanized white myotomal muscle fibres from the dogfish at 12 degrees C. For each fibre preparation a range of velocities was used. Mechanical power was calculated from force X velocity of shortening. The rate of total energy output during shortening was evaluated as the sum of mechanical power and the rate of heat production. The ratio of mechanical power to total energy rate was taken as a measure of efficiency of energy conversion to mechanical power during shortening. Efficiency was maximal and varied little in the range of shortening velocities 0.42-0.89 fibres lengths s-1 (0.11-0.23 Vmax); maximal efficiency was 0.33 +/− 0.01 (+/− S.E.M., N = 23 measurements on seven fibre bundles). The efficiency of the white fibres from dogfish was less than that measured in the same way in earlier experiments on frog muscle and tortoise muscle.

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
Keyword(s):  
Energy Cost ◽  
White Muscle ◽  
Isometric Force ◽  
Muscle Length ◽  
Maximum Velocity ◽  
Muscle Fibres ◽  
External Work ◽  
Scyliorhinus Canicula ◽  
Velocity Of Shortening ◽  
In Series

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.

Heat production and oxygen consumption during metabolic recovery of white muscle fibres from the dogfish Scyliorhinus canicula

2000 ◽  
Vol 203 (7) ◽  
pp. 1201-1210 ◽  
Author(s):  
F. Lou ◽  
W. J. van Der Laarse ◽  
N.A. Curtin ◽  
R.C. Woledge
Keyword(s):  
Oxygen Consumption ◽  
Heat Production ◽  
White Muscle ◽  
Recovery Period ◽  
Atp Synthesis ◽  
Muscle Fibres ◽  
Scyliorhinus Canicula ◽  
Maximum Value ◽  
The Difference ◽  
Time Courses

Oxygen consumption and heat production were measured during contraction and recovery of isolated, white muscle fibres from dogfish (Scyliorhinus canicula) at 19 degrees C. The contraction period consisted of 20 isometric twitches at 3 Hz; this was followed by a recovery period of 2 h without stimulation. We tested the hypothesis that recovery is wholly oxidative (not glycolytic) in these fibres. The following features support this hypothesis. (i) The ratio of total heat produced to oxygen consumed, 451+/−34 kJ mol(−)(1) (mean +/− s.e.m., N=29), was close to that expected for either the oxidation of carbohydrate, 473 kJ mol(−)(1), or the oxidation of fat, 439 kJ mol(−)(1). Even assuming the maximum value (95 % confidence limit) of the observed heat production, glycolysis could account for resynthesis of at most 18 % of the ATP used during the contractions. (ii) When the difference in rates of diffusion of oxygen and heat within the muscle are taken into account, the time courses of oxygen consumption and heat production match each other well during the entire recovery period. The efficiency of recovery (=energy used for ATP synthesis/energy available for ATP synthesis) was estimated from the results. This value, 84.0+/−20.1 % (mean +/− s.e.m., N=29), is relatively high and represents the first such measurement in functioning muscle.

scholarly journals Sustained performance by red and white muscle fibres from the dogfish Scyliorhinus canicula

2010 ◽  
Vol 213 (11) ◽  
pp. 1921-1929 ◽  
Author(s):  
N. A. Curtin ◽  
F. Lou ◽  
R. C. Woledge
Keyword(s):  
White Muscle ◽  
Muscle Fibres ◽  
Scyliorhinus Canicula ◽  
Sustained Performance

scholarly journals Muscle power output during escape responses in an Antarctic fish

1997 ◽  
Vol 200 (4) ◽  
pp. 703-712 ◽  
Author(s):  
C E Franklin ◽  
I A Johnston
Keyword(s):  
Fibre Length ◽  
Antarctic Fish ◽  
Maximum Velocity ◽  
The Body ◽  
Muscle Performance ◽  
Muscle Fibres ◽  
Cycle Duration ◽  
Peak Strain ◽  
Escape Responses

Escape responses (C-shaped fast-starts) were filmed at 500 frames s-1 in the Antarctic rock cod (Notothenia coriiceps) at 0 °C. The activation and strain patterns of the superficial fast myotomal muscle were measured simultaneously using electromyography and sonomicrometry respectively. In order to bend the body into the initial C-shape, the muscle fibres in the rostral myotomes (at 0.35L, where L is total length) shortened by up to 13 % of their resting length at a maximum velocity of 1.68 fibre lengths s-1. During the contralateral contraction, muscle fibres were stretched (by 5 % and 7 % at 0.35L and 0.65L, respectively) and were activated prior to the end of lengthening, before shortening by up to 12 % of resting fibre length (peak-to-peak strain). Representative strain records were digitised to create cyclical events corresponding to the C-bend and contralateral contraction. Isolated fibres were subjected to the abstracted strain cycles and stimulated at the same point and for the same duration as occurs in vivo. During the early phase of shortening, muscle shortening velocity (V) increased dramatically whilst the load was relatively constant and represented a substantial fraction of the maximum isometric stress. Pre-stretch of active muscle was associated with significant force enhancement. For the contralateral contraction, V exceeded that predicted by the steady-state force­velocity relationship for considerable periods during each tailbeat, contributing to relatively high maximum instantaneous power outputs of up to 290 W kg-1 wet muscle mass. In vitro experiments, involving adjusting strain, cycle duration and stimulation parameters, indicated that in vivo muscle fibres produce close to their maximum power. During escape responses, the maximum velocity and acceleration recorded from the centre of gravity of the fish were 0.71±0.03 m s-1 and 17.1±1.4 m s-2, respectively (mean ± s.e.m., N=7 fish). Muscle performance was sufficient to produce maximum velocities and accelerations that were within the lower end of the range reported for temperate-zone fish.

Metabolic biochemistry of water- vs. air-breathing fishes: muscle enzymes and ultrastructure

1978 ◽  
Vol 56 (4) ◽  
pp. 736-750 ◽  
Author(s):  
P. W. Hochachka ◽  
M. Guppy ◽  
H. E. Guderley ◽  
K. B. Storey ◽  
W. C. Hulbert
Keyword(s):  
White Muscle ◽  
Large Diameter ◽  
Oxidative Capacity ◽  
The Body ◽  
Muscle Enzymes ◽  
Air Breathing ◽  
Red Muscle ◽  
Phosphofructokinase Activity ◽  
Metabolic Biochemistry ◽  
Myotomal Muscle

To delineate what modifications in muscle metabolic biochemistry correlate with transition to air breathing in fishes, the myotomal muscles of aruana, an obligate water breather, and Arapaima, a related obligate air breather, were compared using electron microscopy and enzyme methods. White muscle in both species maintained a rather similar ultrastructure, characterized by large-diameter fibers, very few mitochondria, and few capillaries. However, aruana white muscle displayed nearly fivefold higher levels of pyruvate kinase, threefold higher levels of muscle-type lactate dehydrogenase, and a fourfold higher ratio of fructose diphosphatase –phosphofructokinase activity; at the same time, enzymes in aerobic metabolism occurred at about one-half the levels in Arapaima. Red muscle was never found in the myotomal mass of aruana, but in Arapaima, red muscle was present and seemed fueled by glycogen, lipid droplets never being observed. From these and other data, it was concluded that in myotomal muscle two processes correlate with the transition to air breathing in Amazon osteoglossids: firstly, an emphasis in oxidative metabolism, and secondly, a retention of red muscle. However, compared with more active water-breathing species, Arapaima sustains an overall dampening of enzyme activities in its myotomal muscle, which because of the large myotome mass explains why its overall metabolic rate is relatively low. By keeping the oxidative capacity of its myotomal muscle low, Arapaima automatically conserves O2 either for a longer time or for other more O2-requiring organs in the body, a perfectly understandable strategy for an air-breathing, diving fish, comparable with that observed in other diving vertebrates. A similar comparison was also made of two erythrinid fishes, one that skimmed the O2-rich surface layers of water and one that obtained three quarters of its O2 from water, one quarter from air. Ultrastructural and enzyme data led to the unexpected conclusion that the surface skimmer sustained a higher oxidative capacity in its myotomal muscles than did the facultative air breather.

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