Plasticity of muscle contractile properties following temperature acclimation in the marine fish Myoxocephalus scorpius

Live fibre bundles were isolated from the fast myotomal muscle of short-horned sculpin (Myoxocephalus scorpius L.) and isometric contractile properties and the forcevelocity (PV) relationship determined at 5, 10 and 15 °C. Experiments were carried out on winter- and summer-caught sculpins and on individuals acclimated for 68 weeks to either 5 or 15 °C (12 h:12 h light:dark). Maximum tetanic tension (P0) in fibres from 15 °C-acclimated fish increased from 125 kN m-2 at 5 °C to 282 kN m-2 at 15 °C (R10=2.3). For 5 °C-acclimated fish, P0 was 139 kN m-2 at 5 °C, but fell to 78 kN m-2 at 15 °C, consistent with a partial failure of excitationcontraction coupling at high temperatures. Peak force at 15 °C was increased 2.2 times following depolarisation with a high-K+ solution, but was unaffected by the addition of caffeine and/or eserine to the Ringer's solution. The results from winter- and summer-caught fish were similar to those from 5 °C- and 15 °C-acclimated sculpins respectively. In 15 °C-acclimated fish, the power output of muscle fibres calculated from the PV relationship was 55 W kg-1 at 5 °C and 206 W kg-1 at 15 °C. The PV relationship at 5 °C was significantly less curved in muscle fibres from 5 °C- than from 15 °C-acclimated fish. After normalizing the curves for P0 and Vmax, it was found that the change in curvature was sufficient to produce a 40 % increase in relative power output at 5 °C in cold-acclimated fish. The maximum contraction speed of muscle fibres at 15 °C was 2.4 times higher in 15 °C- than in 5 °C-acclimated fish. It was concluded that acclimation modifies the contractile properties of fast muscle fibres at both low and high temperatures.

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Temperature and the Force-Velocity Relationship of Live Muscle Fibres from the Teleost Myoxocephalus Scorpius

Journal of Experimental Biology ◽

10.1242/jeb.144.1.437 ◽

1989 ◽

Vol 144 (1) ◽

pp. 437-448 ◽

Cited By ~ 2

Author(s):

KAREN S. LANGFELD ◽

JOHN D. ALTRINGHAM ◽

IAN A. JOHNSTON

Keyword(s):

Power Output ◽

Muscle Power ◽

Muscle Fibres ◽

Velocity Relationship ◽

Force Velocity ◽

Myoxocephalus Scorpius ◽

Relationship Of ◽

Myotomal Muscle ◽

Best Fit ◽

Tetanic Tension

Small bundles of fast fibres were isolated from the myotomal muscle of the teleost Myoxocephalus scorpius. The temperature-dependence of isometric contractile properties and the force-velocity (P-V) relationship were studied. Fibres were found to deteriorate above 18°C, and the force plateau during tetanic stimulation was not maintained above 15°C. Twitch and tetanic tension (P0) showed optima at around 8°C. Force-velocity curves were fitted using either Hill's hyperbolic equation or a hyperbolic-linear equation (hyp-lin). The best fit to the data was provided by the hyp-lin equation, which gave consistently higher values for unloaded contraction velocity (Vmax): 4.3, 8.1 and 9.5 muscle lengths s−1 at 1, 8 and 12°C, respectively. The P-V relationship was found to become progressively more curved at higher temperatures. Muscle power output calculated from the hyp-lin equation was 123 W kg−1 at 1°C and 256 W kg−1 at 8°C. Curves normalized for P0 and Vmax at each temperature show that the change in curvature is sufficient to increase the relative power output of the muscle by around 15% on decreasing the temperature from 8 to 1°C.

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

Journal of Experimental Biology ◽

10.1242/jeb.183.1.137 ◽

1993 ◽

Vol 183 (1) ◽

pp. 137-147 ◽

Cited By ~ 9

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.

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The mechanical properties of polyneuronally innervated, myotomal muscle fibres isolated from a teleost fish (Myoxocephalus scorpius)

Pflügers Archiv - European Journal of Physiology ◽

10.1007/bf00582542 ◽

1988 ◽

Vol 412 (5) ◽

pp. 524-529 ◽

Cited By ~ 21

Author(s):

J. D. Altringham ◽

I. A. Johnston

Keyword(s):

Mechanical Properties ◽

Teleost Fish ◽

Muscle Fibres ◽

Myoxocephalus Scorpius ◽

Myotomal Muscle

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Activation of Multiply Innervated Fast and Slow Myotomal Muscle Fibres of the Teleost Myoxocephalus Scorpius

Journal of Experimental Biology ◽

10.1242/jeb.140.1.313 ◽

1988 ◽

Vol 140 (1) ◽

pp. 313-324 ◽

Cited By ~ 1

Author(s):

J. D. ALTRINGHAM ◽

I. A. JOHNSTON

Keyword(s):

Action Potentials ◽

Spinal Nerve ◽

Resting Potential ◽

Muscle Fibres ◽

Significant Difference ◽

Slow Muscle Fibres ◽

Myoxocephalus Scorpius ◽

Nerve Muscle ◽

Myotomal Muscle ◽

Tetanic Tension

A nerve-muscle preparation from the sculpin Myoxocephalus scorpius was used to study the membrane response of fast and slow muscle fibres to stimulation of the spinal nerves. There was no significant difference between resting potential in fast (−81.9mV) and slow fibres (−80.8mV). Fast fibres responded to a suprathreshold stimulus in the spinal nerve with an action potential. Overshoots of up to +32 mV were recorded. Both junction potentials and overshooting action potentials were observed in the slow fibres. The twitch/tetanus characteristics of myotomal muscle were investigated using isolated bundles of ‘live’ fast and slow fibres. Both fibre types responded to a single stimulus with a mechanical twitch. Fused tetani were obtained at around 50Hz in fast fibres and 20 Hz in slow fibres. In the slow fibres, tetanic tension increased with frequency up to around 50Hz. At frequencies giving maximum tetanic tension, the twitch/tetanus ratio was 0.70 for fast fibres and 0.29 for slow ones. These results are discussed with reference to the polyneuronal/multiterminal innervation pattern of the myotomal muscle in teleost fish and its role in locomotion.

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Power Output and Force-Velocity Relationship of Live Fibres from White Myotomal Muscle of the Dogfish, Scyliorhinus Canicula

Journal of Experimental Biology ◽

10.1242/jeb.140.1.187 ◽

1988 ◽

Vol 140 (1) ◽

pp. 187-197 ◽

Cited By ~ 9

Author(s):

N. A. CURTIN ◽

R. C. WOLEDGE

Keyword(s):

Power Output ◽

Maximum Velocity ◽

Muscle Fibres ◽

Fish Length ◽

Skinned Fibres ◽

Step Method ◽

Velocity Relationship ◽

Velocity Of Shortening ◽

Force Velocity ◽

Myotomal Muscle

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.

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Modelling Muscle Power Output in a Swimming Fish

Journal of Experimental Biology ◽

10.1242/jeb.148.1.395 ◽

1990 ◽

Vol 148 (1) ◽

pp. 395-402 ◽

Cited By ~ 15

Author(s):

JOHN D. ALTRINGHAM ◽

IAN A. JOHNSTON

Keyword(s):

Power Output ◽

Muscle Power ◽

Fish Swimming ◽

Active Muscle ◽

Cycle Frequency ◽

Fibre Bundles ◽

Length Changes ◽

Myoxocephalus Scorpius ◽

Myotomal Muscle ◽

Muscle Power Output

Intact, electrically excitable fibre bundles were isolated from the fast and slow myotomal muscle of the bullrout (Myoxocephalus scorpius L.). Power output was measured under conditions simulating their activity in a fish swimming at different speeds. Preparations were subjected to sinusoidal length changes of ±5% of resting length, and stimulated briefly during each cycle. The number and timing of stimuli were adjusted at each cycle frequency to maximise power output. Maximum power was produced at 5–7 Hz for fast fibres (25–35 W kg−1) and 2 Hz for slow fibres (5–8 Wkg−1). Under these conditions, pre-stretch of active muscle provides an important mechanism for storing potential energy for release during the shortening part of the cycle.

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How fish power predation fast-starts

Journal of Experimental Biology ◽

10.1242/jeb.198.9.1851 ◽

1995 ◽

Vol 198 (9) ◽

pp. 1851-1861 ◽

Cited By ~ 17

Author(s):

I A Johnston ◽

J L van Leeuwen ◽

M L F Davies ◽

T Beddow

Keyword(s):

Tensile Stress ◽

Muscle Mass ◽

Power Output ◽

Average Power ◽

Temperature Acclimation ◽

The Body ◽

Fast Muscle ◽

Muscle Fibres ◽

Fast Start ◽

Tail Beat

Short-horned sculpin (Myoxocephalus scorpius L.) were acclimated for 68 weeks to either 5 °C or 15 °C (12 h dark: 12 h light). Fast-starts elicited by prey capture were filmed from above in silhouette using a high-speed video camera (200 frames s-1). Outlines of the body in successive frames were digitised and changes in strain for the dorsal fast muscle calculated from a knowledge of backbone curvature and the geometrical arrangement of fibres. For 15 °C-acclimated fish at 15 °C, muscle strain amplitude (peak-to-peak) during the first tail-beat was approximately 0.16 at 0.32L, 0.19 at 0.52L and 0.15 at 0.77L, where L is the total length of the fish. Fast muscle fibres were isolated and subjected to the strains calculated for the first tail-beat of the fast-start (abstracted cycle). Preparations were electrically stimulated at various times after the initiation of the fast-start using an in vivo value of duty cycle (27 %). Prior to shortening, muscle fibres at 0.52L and 0.77L were subjected to a pre-stretch of 0.055l0 and 0.085l0 respectively (where l0 is resting muscle length). The net work per cycle was calculated from plots of fibre length and tensile stress. For realistic values of stimulus onset, the average power output per abstracted cycle was similar at different points along the body and was in the range 2431 W kg-1 wet muscle mass. During shortening, the instantaneous power output reached 175265 W kg-1 wet muscle mass in middle and caudal myotomes. At the most posterior position examined, the muscle fibres produced significant tensile stresses whilst being stretched, resulting in an initially negative power output. The fibres half-way down the trunk produced their maximum power at around the same time that caudal muscle fibres generated significant tensile stress. Fast muscle fibres at 0.370.66L produced 76 % of the total work done during the first tail-beat compared with only 14 % for fibres at 0.670.86L, largely reflecting differences in muscle mass. The effect of temperature acclimation on muscle power was determined using the strain fluctuations calculated for 0.52L. For 5 °C-acclimated fish, the average power per cycle (± s.e.m.; W kg-1 wet muscle mass) was 21.8±3.4 at 5 °C, falling to 6.3±1.8 at 15 °C. Following acclimation to 15 °C, average power per cycle increased to 23.8±2.8 W kg-1 wet muscle mass at 15 °C. The results indicate near-perfect compensation of muscle performance with temperature acclimation.

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