ascending phases began to diverge was taken to mark the onset of decay in the
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1 605 J. Physiol. (I954) I24, 605-6I2 THE DURATION OF THE PLATEAU OF FULL ACTIVITY IN FROG MUSCLE BY J. M. RITCHIE From the National Institute for Medical Research, Mill Hill, London, N.W. 7 (Received 26 January 1954) When a muscle is stimulated there is an abrupt change from rest to activity (Hill, 1949). Because of the series-elastic component in muscle, the tension rises slowly, and in a twitch the tension developed is usually only a fraction of that developed in a tetanus; but Hill (1949, 1951) has shown that the intrinsic response of the contractile material is of the same magnitude in a twitch as in a tetanus and that it reaches its full extent immediately after the end of the latent period. Once elicited by a single stimulus, the active state of the muscle remains constant for a period, on a plateau,-befre it begins to decay. The theoretical interest in the duration of this platea-iuhas been discussed by Hill (1953b). The quick stretch technique which he used in his earlier experiments (Hill, 1949) did not allow him to assign any accurate value to the duration of this plateau. In his paper Hill (1949) gives a diagram where the time courses, in a single twitch, of the active state and the recorded isometric tension of the whole muscle are plotted together. The plateau of the active state curve seems to last for a little less than half the time taken by the muscle to reach its maximum tension; since the relaxation of the tension of the whole sartorius at 00 C in a single twitch can be taken to occur about 250 msec after the stimulus, the active state would have begun to subside by about 100 msec. The difference between these two times is another result of the presence of the series-elastic component, which causes a time-lag between the internal response and its external sign, the recorded twitch tension. When other more sensitive techniques were used, decay in the active state could be detected at msec (Hill, 1953 a): indeed, signs of it appeared at about 60 msec (Hill & Macpherson, unpublished). Recently, Macpherson & Wilkie (1953a) have measured the start of this decay by yet another method. They superimposed the isometric tension curves of a twitch and of a tetanus, and the moment at which the ascending phases began to diverge was taken to mark the onset of decay in the active state. This was found to occur at msec after the stimulus and, in later experiments, at 44 msec (Macpherson & Wilkie, 1953 b).
2 606 J. M. RITCHIE In the present experiments the duration of the plateau at the end of a brief tetanus has been measured by recording the tension changes in a muscle near the end of the tetanus. For a tetanus, the effect of the series-elastic component is not to cause a difference between the time of the start of decay of the active state and the time at which the tension in the muscle begins to fall, as in a single twitch, but only to slow the rate of tension fall. As the sensitivity of the tension recorder used was extremely high, the time at which tension was first observed to fall after the cessation of stimulation was taken to reflect the onset of decay of the active state; this was found to occur at about 35 msec after the stimulus. METHODS The muscle used was the frog's sartorius. It was mounted on a multi-electrode stimulating assembly (Hill, 1949), and bathed throughout the experiment in Ringer's solution (NaCl 0-675%, KCI 0-015%, CaCI %, w/v) containing 1/50,000 tubocurarine chloride (w/v). The Ringer's solution was continuously aerated and kept at constant temperature, usually 00 C, by means of a DewariLask. The muscle was stimulated directly, and simultaneously at many points on its surface, 'withmiaiimalshocks derived from the charge and discharge currents of a condenser, each successive element of the stimulus being equal in magnitude, but of opposite sign to the preceding one. This method of stimulation minimized polarization effects at the electrodes and was found to lead to a better maintained muscle response. The muscle was connected by a fine copper wire, previously straightened, by drawing beyond its elastic limit, to a rochelle salt piezo-electric crystal. This crystal, of the bender type, gave an output of 0-1 V for a force of 1 g suddenly applied. The crystal output was fed directly to a cathode follower (grid current <IpA), amplified, displayed on a cathode-ray tube and photographed. This provided an extremely sensitive method of recording tension, a change of less than 2 mg could be easily detected. The crystal, when used with the cathode follower, had a time constant of about 25 sec. Because the object of the present experiments was to record changes of tension at a time when tension was already high, the amplifiers were capacity coupled: limiting diodes across the grids of the valves prevented blocking. By the end of a tetanus of 1 sec duration, the amplifier had recovered from the voltages produced in the initial stages when tetanic tension was being developed: subsequent tension changes could be then recorded through an amplifier whose effective time constant was 100 msec. Because of the high sensitivity of the tension recorder, care had to be taken to shield the system from mechanical disturbances. Stability was achieved by standing the Dewar flask which carried the muscle assembly on a very solid base. Anti-vibration mountings were not necessary because of the solidness of the particular room where the experiments were made. The procedure during an experiment was to stimulate the muscle with a series of stimuli at a frequency depending on the particular experiment. The third or fourth stimulus from the end of the tetanus (in early experiments the last stimulus) was arranged to trigger the time base of the cathode-ray oscilloscope. Photographic records of the tension-time curve during and after the last three or four stimuli were then made, and the time after the last stimulus at which the tension began to fall was measured. RESULTS In the earliest experiments the muscle was kept at 20 C and stimulated at a frequency of between 20 and 35 shocks/sec, and the tension changes after the last stimulus recorded: the lower frequency limit was chosen because this was given by Abbott & Wilkie (1953) as the frequency which provided com-
3 DURATION OF THE ACTIVE STATE 607 plete fusion in a frog's sartorius at 00 C. In these records there were nearly always marked oscillations or humps in the tension curves, as shown in Fig. 1A. These were not caused by external sources of vibration, as was shown by the record (Fig. 1B) which was made under the same conditions as existed for Fig. 1A, except that the muscle stimulating electrodes were short-circuited. It appeared that these oscillations resulted from the stimulation frequency being too small to produce a fused response. On general grounds, the minimum stimulation frequency to produce a fused response should be such that the interval between each element of the stimulus and the preceding one should be equal to the duration of the active state. Fusion frequency was determined experimentally. In a sartorius at 00 C, 40 shocks/sec produced a response which was just fused and 30 shocks/sec a response which was just not. There fore, in subsequent experiments at 00 C, frequencies of stimulation of between A J 40 dynes (LIBRA B _ Fig. 1. A: onset of tension decline in frog's sartorius at 2 C after tetanus of 1 sec duration at 35 shocks/sec. Record is begun by last stimulus. B: baseline, see text. Upper trace: time calibration, 300 c/s, with pips at same frequency as that of the previous stimuli. The vertical bar gives the deflexion for a tension change of 40 dynes. 33 and 55 shocks/sec were used; oscillations of the type found in Fig. 1 A were then absent. Fig. 2 shows an experiment similar to that just described but at a temperature of 16 C where, of course, higher frequencies of stimulation were used. The records at different frequencies have been so aligned that the last stimuli in the various tetani lie on the solid line. The interval between this line and the broken line is 12 msec which was the time, as judged from the records at 125 and 150 shocks/sec, at which relaxation of tension began; fusion occurred at some frequency between these two. Fig. 3 shows the type of record obtained in four experiments at 00 C, each on a different muscle. The times at which relaxation set in have been marked by vertical bars, although, as in all latency experiments, there must be some doubt as to the precise time at which this occurred. In such experiments several records were made, usually at 15 min intervals, and the mean relaxation time for each muscle found. Twenty-seven experiments in which a stimulus frequency between 33 and 55 shocks/sec was used showed that relaxa-
4 608 J. M. RITCHIE tion occurred at an average time of about 35 msec after the last stimulus (the standard deviation about the mean being 3-0 msec) v.w. I 40 dynes Fig. 2. Tension/time curves of frog's sartorius at 160 C, during and after terminal stages of tetanus of about 1 sec duration at different frequencies of stimulation. Frequency is given in shocks/sec by the numbers opposite each record. The last stimulus in each record falls on the unbroken line. Interval between the broken and unbroken lines is 12 msec. Upper trace: time calibration, 300 c/s: the pips indicate the stimuli given to the muscle in the first record only. The vertical bar gives the deflexion for a tension change of 40 dynes. The length of the muscle was usually the standard length, i.e. the greatest in the body. When a series of records was taken at various muscle lengths from 8 mm greater to 8 mm smaller than this length, no systematic change was
5 DURATION OF THE ACTIVE STATE 609 observed in the time at which relaxation set in. Thus, in a typical experiment on a muscle at 0 C whose standard length was 40 mm, the times at lengths 44, 36, 32, 40 and 48 mm were 30, 33, 33, 31 and 32 msec respectively: the records were taken in this order and at half-hourly intervals _-4 \ 50 dynes Fig. 3. Tension/time curves of four frog's sartorii at 0 C during and after terminal stages of tetanus at stimulation frequency of about 55 shocks/sec. The numbers on each record are the times, in msec after the last stimulus, at which tension begins to fall (indicated by vertical bars). Upper trace in each record: 300 c/s time calibration, with pips indicating the stimuli given to the muscle. The vertical bar at the side gives the deflexion for a tension change of 50 dynes. The time at which relaxation set in was measured in some experiments at a series of temperatures from 0 to 160 C. The logarithm of this time proved to be a linear function of temperature, thus justifying a calculation of the Q1o of this process for this temperature range. Five experiments gave an average Qlo of 2x20, the standard deviation about the mean being The latent period PH. CXXIV. 39
6 610 J. M. RITCHIB of contraction was measured in these experiments, the muscle length being reduced by about 1 mm to get rid of the latency relaxation (Abbott & Ritchie, 1951). It was found that, for any given muscle, the interval between the last stimulus of a tetanus and the onset of relaxation bore a constant ratio to the latent period and this ratio was independent of temperature; in five muscles, for a temperature range from 0 to 160 C, the ratio varied between 3-1 and 3 9, the mean being 3'4. In fourteen muscles at 00 C, the average ratio was 3-4 and the standard deviation about the mean An attempt was made to assess the effect of fatigue and of previous activity on the duration of the plateau. In one experiment three tetani of just over 1 sec duration were given at 30 min intervals: these were followed by three 5 sec tetani at 2 min intervals. The relaxation times for the short tetani were 31, 35 and 35 msec: for the 5 sec tetani they were 36, 38 and 35 msec. The duration of the plateau may therefore have increased slightly. In other experiments greater increases were observed. A similar result was found to follow previous activity in muscles not deliberately fatigued. In a series of experiments on sixteen sartorii at 00 C, with 1 sec tetani from 5 to 30 min apart, the average time at which relaxation set in was 32 msec for the first tetanus applied to the fresh muscle and 34 msec for the third tetanus. The standard error of the mean difference between the first and third measurements, 2 msec, was 0 5 msec. Therefore, previous activity apparently increased the duration of the active state. However, these longer times have been no more than a reflexion of the observed slowing of the rate of decline of tension consequent on previous activity. DISCUSSION The quantity measured in these experiments was the time, after the last stimulus of a tetanus, at which a decline in tension could be detected. On the current explanation of events in muscular contraction (Hill, 1949, 1953 a), the time at which this decline can be measured must occur after the onset of decay of the active state, the more sensitive the recording apparatus the shorter the delay between them. It would be difficult, however, to employ usefully much more sensitive techniques than those used here: a change of less than 2 dynes, i.e % of the total tension developed by the muscle, can easily be detected. The conclusion has therefore been drawn that at about 35 msec after a stimulus, at the time when tension after the end of a tetanus begins to fall, the active state of muscle begins to decline. Before this time muscle tension remains constant, as far as can be seen with the present method: for the next few msec after this time tension begins to fall at an ever-increasing rate. There does seem, therefore, to be a true plateau on the active state curve. To calculate the actual duration of the plateau of the active state curve, the ordinary latent period of contraction must be known. This was measured in
7 DURATION OF THE ACTIVE STATE 611 single twitches, the tension record having the same sensitivity as in the tetanus experiments, and at a muscle length where there was no latency relaxation in the traces to obscure the point at which contraction began. This time, which was about 10 msec, was then subtracted from the time after the last stimulus of a tetanus in the same muscle at which relaxation set in. The duration of the active state, determined in this manner, was about 25 msec, at 00 C: fourteen muscles gave an average of 24 msec, the standard deviation about the mean being 18 msec. This is only about a tenth of the time taken for the maximum tension to be reached in an isometric twitch. There is good agreement between the results of the experiments discussed above and those on fusion frequency at both 00 C and at 160 C. If, as suggested above, the duration of the plateau of the active state is about 25 msec at 00 C, a fusion frequency of 40 shocks/sec would be predicted, and this is very near to that found experimentally. The ratio of the relaxation time after a tetanus to the latent period of contraction was found to be independent of temperature, and the Qlo of the former was 2x20; the Qlo of the duration of the active state is therefore also about 2*20. The disagreement between the present findings and those of Hill (1953a) and Macpherson & Wilkie (1953 a, b) is more apparent than real. The duration of the plateau was measured in their experiments during a single twitch: in the present experiments it was measured at the end of a tetanus. Also, the different sensitivities of the methods used must be considered. Inspection of the four records of Fig. 3 shows that, at 80 msec after the last stimulus of the tetanus, the muscle tension has fallen on the average by about 50 dynes, only 0.1 % of the total tension developed. This fall would be extremely difficult to detect in Hill's (1953 a) records. A similar argument can also be applied to fusion frequency. With a frequency of about 20 c/s (as used by Abbott & Wilkie, 1953), the oscillation would be too small to measure, except when using extremely sensitive recorders. In one muscle at 00 C, with the piezo-electric crystal used to measure tension, 20 shocks/sec produced a tension oscillation of about 0-02 % of the total; even with 10 shocks/sec the oscillation was only about 01%. Therefore, although the results obtained by using these different methods differ slightly in detail, they all emphasize that a plateau of full activity in muscle does exist and that its duration is much smaller than the time during which tension continues to rise in a twitch. SUMMARY 1. The internal activity in muscle elicited by a stimulus remains constant for a time, after which it begins to decay. In frog muscle at 00 C the onset of this decay occurs at about 35 msec after the stimulus and is independent of muscle length. 39-2
8 612 J. M. RITCHIE 2. In frog muscle at 0 C the latent period of contraction is about 10 msec: the duration of the plateau of the active state is therefore about 25 msec. 3. The Qlo of the duration of plateau of the active state curve is about At 00 C fusion frequency in frog muscle is about 40 shocks/sec. REFERENCES ABBOTT, B.C. & RrrCHIE, J. M. (1951). Early tension relaxation duringamuscletwitch. J. Physiol. 113, ABBOTT, B. C. & WrLKIE, D. R. (1953). The relation between velocity of shortening and the tension-length curve of skeletal muscle. J. Physiol. 120, Hni., A. V. (1949). The abrupt transition from rest to activity in muscle. Proc. Roy. Soc. B, 136, HarT, A. V. (1951). The transition from rest to full activity in muscle: the velocity of shortening. Proc. Roy. Soc. B, 138, HuL, A. V. (1953a). The 'plateau' of full activity during a muscle twitch. Proc. Roy. Soc. B, 141, HILL, A. V. (1953b). A re-investigation of two critical points in the energetics of muscular contraction. Proc. Roy. Soc. B, 141, MACPHERSON, L. & WrKuIE, D. R. (1953a). The duration of the active state in a muscle twitch. J. Phy8iol. 122, 20P. MACPHERSON, L. & WILKIE, D. R. (1953b). The duration of the active state in a muscle twitch. J. Phy8iol. 124,
University College, London. (Hill, 1949c) the use of a quick stretch applied shortly after a shock showed
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