First published online December 3, 2004
Journal of Experimental Biology 207, 4505-4513 (2004)
Published by The Company of Biologists 2004
doi: 10.1242/jeb.01259
Enhancement of twitch force by stretch in a nerve-skeletal muscle preparation of the frog Rana porosa brevipoda and the effects of temperature on it
Yoshiki Ishii,
Takashi Watari and
Teizo Tsuchiya*
Department of Biology, Faculty of Science, Kobe University,
Rokkodai-cho 1-1, Nada-ku, Kobe 657-8501, Japan
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Fig. 1. Schematic illustrations of experimental setup. (A) An experimental bath
containing a muscle preparation. DS, stimulator for direct stimulation; FT,
force transducer; LS, He-Ne laser for monitoring sarcomere length; M, whole
muscle preparation; NS, stimulator for nerve (indirect) stimulation; SC,
screen for monitoring laser diffraction pattern; SM, servo-motor. The
circulation of physiological saline is shown by thick arrows. The path of the
laser light is shown by thin arrows. (B) Diagram of the electronic circuit
used to drive a dual-mode servomotor (SM) for controlling muscle length and
load and for recording muscle force. Force change was also measured by a force
transducer (FT).
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Fig. 2. Typical recordings of twitch and tetanic forces developed by direct or
indirect stimulation at three different temperatures, 4°C, 12°C and
22°C. Twitch and tetanic forces at the different temperatures were
recorded from the same preparations. The duration of the stimulation in
tetanus was 1 s. Forces obtained by indirect stimulation (thick lines) are
expressed relative values to those obtained by direct stimulation (thin lines)
at each temperature. Temperatures and stimulation frequencies in tetanus are
denoted for each recording.
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Fig. 3. Change in twitch and tetanic force developed by indirect stimulation with a
change in temperature. Twitch (open circles) and tetanic (closed circles)
forces are expressed relative to the respective forces obtained by direct
stimulation. Values are means ± S.D. The figures at each
data point denote the number of samples used. The small letters (a, b and c)
in twitch denote that the differences between points are statistically
significant (P<0.01), while the differences in tetanus are not
significant.
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Fig. 4. Changes in twitch force induced by stretch in directly and indirectly
stimulated muscle. (Top) Length steps applied; (bottom) force changes. The
muscle was stimulated at 5 s intervals at 4°C and stretched by 9.5%
l0 (muscle length) from l0 in the
course of train twitch stimuli. All recordings were obtained from the same
preparation.
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Fig. 7. The influence of stretch velocity on the enhancement of twitch force
induced by indirect stimulation. (A) A quick (4 ms) or slow (8 s) lengthening
step of 6.6% l0 was applied to a muscle (top trace) and
the twitch forces were compared before and after the stretch (lower trace).
(B) The slow-time recordings of the same data as in A. Twitch stimuli were
applied every 12 s. (C) Comparison of the enhanced forces obtained by fast and
slow stretch. The recordings obtained by fast and slow stretches are shown
together in each panel (the second, sixth and tenth records after stretch) but
the two recordings are almost superimposed.
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Fig. 5. Length-force relationships in twitch (A) and tetanus (B) in directly
stimulated muscle. Forces are expressed as values relative to the force at one
muscle length (l0). In A, each symbol shows the data
obtained at three different temperatures; open circles, 4°C
(N=5); filled triangles, 12°C (N=4); open squares,
22°C (N=4). The thick line shows the least-squares regression
curve calculated from the total data in twitch. In B, the data were obtained
from three different preparations all at 4°C. The thin line is the
regression curve obtained from three preparations. The thick line is the same
regression curve as in A.
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Fig. 6. The effects of temperature on stretch-induced enhancement of twitch force
in indirectly stimulated muscle. Twitch forces are expressed as values
relative to the force obtained by direct stimulation at one muscle length
(l0). The thick line is the same regression curve as shown
in Fig. 5A. Forces were
measured 2 min after stretching each preparation from l0
to the length indicated on the abscissa at three different temperatures; open
circles, 4°C (N=5); filled triangles, 12°C (N=4);
open squares, 22°C (N=4). All animals had been kept for more than
2 months at room temperature before the experiment.
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Fig. 8. The influence of maintenance temperature of frogs on the enhancement of
twitch force by stretch. Frogs were kept at room temperature (22°C, open
circles) or at 4°C (filled circles) for more than 2 months and twitch
forces were measured at low temperature (4°C) in both cases. Forces were
measured 2 min after stretching a muscle from l0 to the
length indicated on the abscissa. The data points (open circles) are the same
as those shown in Fig. 6.
Twitch forces are expressed as values relative to the force at resting length
(l0) by direct stimulation. The thick line shows the
regression curve of the twitch force induced by direct stimulation as shown in
Fig. 5A.
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Fig. 9. The thermal acclimation of twitch force by indirect stimulation. Frogs were
kept for 0, 1, 2 or 3 months at 4°C and twitch forces were measured at
resting muscle length (l0) at 4°C. Twitch forces are
expressed as values relative to those obtained by direct stimulation at
l0 at 4°C. The numbers at data points indicate the
number of preparations used. *Differences between two data points
marked by horizontal lines are statistically significant by
P<0.01.
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Fig. 10. Typical action potentials recorded by suction electrodes from nerve (A) and
muscle (B) in a nerve-iliofibularis muscle preparation. All recordings shown
are the average of eight action potentials. (A) Nerve action potentials were
recorded by a bipolar lead from the nerve innervating the muscle at 4°C at
the resting muscle length (thin line) and at the stretched length by 7.7%
above resting length (thick line). Both lines are almost superimposed and
cannot be distinguished. (B) Muscle action potentials were recorded by a
monopolar lead from the surface of the muscle at 4°C at the resting muscle
length (thin line) and at the stretched length (7.7% above resting length;
thick line). The artifact from electrical stimulation was superimposed at the
beginning of the recordings in A.
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© The Company of Biologists Ltd 2004
