briefly reported (Lind & Samueloff, 1957). that the durations of submaximal sustained contractions are profoundly
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1 162 J. Physiol. (I959) I27, I62-I7I MUSCLE FATIGUE AND RECOVERY FROM FATIGUE INDUCED BY SUSTAINED CONTRACTIONS BY A. R. LIND From the Medical Research Council Unit for Research in Climate and Working Efficiency, Department of Human Anatomy, University of Oxford (Received 21 January 1959) Previously reported experiments (Clarke, Hellon & Lind, 1958) have disclosed that the durations of submaximal sustained contractions are profoundly influenced by the temperature of the contracting muscles. Contractions are held longest when the muscle temperature, measured half way between the skin and the centre of the arm, was about 270 C (i.e. after 30 min immersion in water at 180 C), above and below which temperature the durations of contractions fall. In those experiments, the forearm was immersed in water throughout the experiments and the interval between the five successive, sustained contractions remained constant at 20 min. In all experiments where the muscle temperature was 270 C or above, the durations of the successive contractions fell from the initial value to a lower, steady level by the fourth and fifth contractions. Clearly, even though 20 min were allowed between contractions, this period was insufficient to allow full recovery of the function of the muscles. It is well known (e.g. Vernon, 1929) that changes in the interval between successive contractions or successive bouts of rhythmic contractions vary the tension that can be exerted and the duration of such contractions. Nothing, however, is known about the effect that variations of the muscle temperature have on these changes. One of the aims of the present experiments was to determine whether the influence of muscle temperature, in reducing the duration of sustained contractions previously demonstrated at muscle temperatures of 270 C and above (Clarke et al. 1958), is maintained when the interval between contractions is varied. This experimental intention, where the intervals between contractions were varied between 3 and 40 min when the forearm was immersed in water at two temperatures, seemed additionally to offer the opportunity of studying the inter-relationship of these variables on the process of recovery. Some of these experiments have already been briefly reported (Lind & Samueloff, 1957).
2 RECOVERY AFTER MUSCULAR FATIGUE 163 METHODS The apparatus comprised a simple hand-grip, strain-gauge dynamometer, previously described (Clarke et al. 1958), mounted on a rigid pillar which ran on castors to prevent the effective use of muscles other than the flexors of the forearm in making the contractions. The upper arm was held at an angle of approximately 90 to the forearm in all contractions. Four healthy young men acted as subjects; they were fully trained in the use of the apparatus and accustomed to holding sustained submaximal contractions to the agreed end-point, which was the failure to maintain the required tension. Some discomfort was experienced towards the end of such contractions but experiments repeated in the same conditions yielded results with a coefficient of variation of 3-64 %; this was considered to be satisfactory evidence that the subjects maintained the contractions to the agreed end-point, and were not influenced by accompanying ischaemic discomforts, which varied in intensity from experiment to experiment. No subject performed more than one experiment in any 24-hr period. At the start of each experiment two maximal contractions were made, and subsequent sustained contractions were held at 1/3 of the average of these contractions. After making the maximal contractions the forearm was immersed in a water-bath at 18 or 340 C, maintained to ± 0-.5 C, for the remainder of the experiment. Thirty minutes after immersion, the first of five successive sustained contractions was made. The remaining four contractions followed, with an interval from the end of one contraction to the beginning of the next of 40, 20, 7 or 3 min; this interval remained constant in any one experiment. Since the required submaximal tension can no longer be held at the end of a sustained contraction, at this time the ability of the muscle to exert maximum tension has decreased to this value. To estimate the rate of recovery of the ability to exert maximum tension, another series of experiments was carried out, where two brief maximum efforts (each < 3 sec, with a 15 sec interval between the two) were made at 3, 7, 20 or 40 min after each of five successive sustained contractions at 1/3 maximum tension; the succeeding sustained contraction followed one minute after these two maximum efforts were made. Muscle temperatures were measured by inserting a 40 S.W.G. copper-constantan thermocouple obliquely in a distal direction through the brachioradialis muscle just below the elbow, leaving the thermocouple junction at a point approximately half way between the skin and the centre of the arm. Muscle temperatures, as described in this paper, refer to this 'representative' muscle temperature. RESULTS Effect of water temperature and recovery interval on duration of contractions Figure 1 shows the duration of the five successive contractions for each subject in each of the eight experimental conditions. While considerable individual variation is evident in the recorded durations of contractions in any given experimental condition, the response followed a similar general pattern for each subject. It is clear from Fig. 1 that it is necessary in all experimental conditions to consider the durations of the first contractions separately from those of subsequent contractions, since at the time of the first contractions the experimental procedure was always the same except for immersion of the arm in water at two temperatures. Consequently, it is to be expected that for a given water temperature the first contraction in all experiments would be of similar duration for each subject. In fact the similarity may be observed in Fig. 1, and serves to demonstrate the repeatability of the results. The 11-2
3 164 A. R. LIND x x x m dif 40emi 20smin 7e mi 3 min duration of the first contraction in water at 340 C was only about 70% of that found in water at 180 C. This agrees with previous findings (Nukada, 1955; Clarke et al. 1958) and this comparison can be seen more clearly in Fig. 2, which shows the average results for the four subjects. The durations of the subsequent four contractions were profoundly affected both by water temperature and by the interval allowed between the contractions. In all experiments the durations of these contractions fell from the initial value to a lower, steady level by the last two contractions and in any ~ C. x x x -~~~~~~~~~~Scesv cotrcton Successive contractions Fig. 1. Durations of five successive contractions for four individual subjects (represented by different symbols) when their arms were immersed in water at 180 C (upper diagrams) or 340 C. of the eight experimental conditions the durations of these last two contractions were not significantly different. When the interval between contractions was 20 or 40 min, the duration of all five contractions remained much greater in water at 180 C than at 340 C. But when the interval between the contractions was 7 or 3 min, the difference found between the durations of the first contractions in the two water temperatures was not maintained and the curves tended to converge (see Fig. 2) although the durations of the last two contractions in water at 180 C were always greater than those obtained in water at 340 C when the interval between the contractions was held constant at 3 or 7 min (P < 0 001). In both water temperatures, the shorter the interval between the contractions, the shorter was the duration of the last two contractions. Reduction of the interval between contractions from 40 to 3 min in water at 180 C resulted
4 RECOVERY AFTER MUSCULAR FATIGUE 165 in a fall in duration (mean for 4 men: see Fig. 2) from 210 to 103 sec, a fall of 107 sec. The corresponding figures in water at 340 C were 132 to 76 see, a fall of only 56 see, or about half that found in cool water. Muscle temperature changes Previous work (Clarke et al. 1958) showed that after a sustained contraction in water at 18 or 340 C there was a sudden rise of muscle temperature, presumably due to the post-exercise hyperaemia. This rise of temperature usually reached a peak about 5 min after the end of the contraction, and thereafter the muscle temperature fell slowly to approximate its initial level in about 20 min. This transient rise in temperature was about 10 C when the forearm was in water at 34 C, but was much greater, about 40 C, in water at 180 C, presumably owing to the much greater temperature gradient existing between the incoming blood and the tissues of the forearm in the cooler water. It 200 E Successive contractions Fig. 2. The average durations of successive, sustained contractions in water at 180 C (on left) and 340 C, when the interval between contractions was 40 (-), 20 (+), 7 (A) or 3 (-) min. remained possible that in the present experiments, when the interval between contractions was reduced to 7 or 3 min, the muscle temperature would rise progressively owing to succeeding contractions occurring during the period when the muscle temperature was raised by the post-exercise hyperaemia resulting from the preceding contractions. This rise would be expected to be greater in water at 180 C, and the changes in durations of contractions shown in Figs. 1 and 2 when the interval was 7 or 3 min might be attributable to such muscle temperature changes throughout the experiments. Figure 3 shows the muscle temperatures (mean of three subjects) measured at the start of each contraction in the eight experimental conditions. As postulated above, a rise of muscle temperature occurred when the interval between contractions was reduced, and a greater rise was found in water
5 166 A. R. LIND at 180 C than in water at 340 C. The temperature, however, did not rise progressively throughout the experiments when the intervals between contractions were 3 or 7 min; the rise occurred after the first two or three contractions, and thereafter the temperature remained steady or fell slightly to a steady level for the last two contractions. This is presumably owing to smaller rises of temperature following progressively shorter contractions. Reduction of the interval from 40 to 3 min resulted in a rise of muscle temperature for the last two contractions of about 0.60 C in water at 34 C, but at 18 C the corresponding rise amounted to about 50 C s Successive contractions Fig. 3. Muscle temperatures (means for three subjects) measured at the start of five successive, sustained contractions when the forearm was immersed in water at 180 C (lower traces) or 340 C and when the interval between the contractions was 40 (0), 20 (-), 7 (A) or 3 (0) min. Recovery of muscle function It has been noted that in any experimental condition the durations of the last two contractions were not different. If it is then assumed that this fact demonstrates the existence of a 'steady state' between the metabolic requirements of the muscle to perform sustained contractions at the required tension and the time allowed for recovery of muscle function between successive contractions, then the durations of these contractions may be considered to be a measure of the recovery of muscle function after fatigue. In Fig. 4 the zero point on the abscissa represents the point at which a contraction ended (i.e. the point of fatigue for the maintenance of a contraction of 1/3 maximum tension) and thereafter the interval between contractions represents the 'recovery time'. Against 'recovery time' is plotted the duration of contractions in the 'steady state' (the average of the durations of the last two contractions) expressed as a percentage of the duration of the initial
6 RECOVERY AFTER MUSCULAR FATIGUE 167 contractions. The points shown in Fig. 4 represent the average for four subjects for each of the eight experimental conditions. It is evident from Fig. 4 that there were two phases in the recovery of the ability of the muscle to maintain submaximal contractions. An initial, fast rate of recovery occurred within about the first 10 min after fatigue, when more than 50 % of the total recovery occurred. This was followed by a slower rate of recovery, during 30 min of which only a further 20-25% of the total recovery was achieved. After 40 min the muscle was able to maintain contractions at the required tension for only 70-75% of the initial maximum duration at either water temperature. The rate of recovery in the 7 min period following fatigue was found to be just significantly faster in water at 340 C than in water at 180 C (P < 0.5). There was no difference due to water temperature 75- C~~~~~~~~~~ 0 so Recovery time (min) Fig. 4. The duration of sustained contractions after different lengths of time allowed for recovery from fatigue in water at 18 C (0) or 340 C ( x). in the rate of recovery in the period from 7 to 40 min after fatigue. If this second, slower rate of recovery did not become further slowed, then extrapolation suggests that an interval of more than 90 min would be necessary for complete recovery. For the second series of experiments where the greatest tension that could be exerted was determined at various intervals after the muscle had been fatigued by sustained contractions at 1/3 maximum tension, the tension that could be exerted has been plotted (Fig. 5) as a percentage of the initial maximum value, against the time allowed for recovery following fatigue. In these experiments the point of fatigue represents the moment when the maximum tension that can be exerted had fallen to 1/3 maximum. It is clear from Fig. 5 that the recovery of the ability to exert maximum tension is complete within 20 min after fatigue, and after 7 min is more than 90% complete.
7 168 A. R. LIND Fig Recovery time (min) The recovery of the ability to exert maximum tension following fatigue induced by sustained contractions, in water at 180 C (a) or 340 C ( x). DISCUSSION The view is no longer accepted that fatigue induced by sustained contractions or bouts of rhythmic contractions is due mainly to the failure of central nervous pathways (e.g. Reid, 1928). Recent evidence places the site of the fatigue at the periphery, although there are conflicting views on whether the fatigue is due only to chemical changes in the muscle (Merton, 1954) or whether the neuromuscular junction is also involved (Naess & Storm-Mathisen, 1955; Krnjevic & Miledi, 1958). The belief that the neuromuscular junction may be responsible, in part at least, for fatigue induced by muscular contractions results mainly from observations made during experiments when maximum tensions were being exerted. It is doubtful whether in submaximal, sustained contractions of the type investigated here, the neuromuscular junction would be so affected. It has been shown that the frequency of stimulation necessary to elicit maximum tension in healthy human muscle is usually of the order of 35-40/sec (e.g. Bigland & Lippold, 1954) although frequencies as high as 60/sec have been recorded (Seyffarth, 1940). Also, tension has been shown to be almost linearly related to the frequency of stimulation (Bigland & Lippold, 1954) and a tension of 1/3 maximum would be associated with frequencies probably of much less than 20/sec. Smith (1934) observed frequencies of 5-12/sec during sustained contractions of unspecified strength. At such low frequencies no failure of the neuromuscular junction has been demonstrated (e.g. Brown & Burns, 1949; Krnjevic & Miledi, 1958). The balance of evidence
8 RECOVERY AFTER MUSCULAR FATIGUE 169 suggests that neuromuscular failure is probably not responsible for the muscular fatigue induced in the present experiments, where the tension was maintained at 1/3 maximum tension and, in the following discussion, the assumption is made that the muscular fatigue here is due only to chemical changes occurring within the muscle. The results show that the durations of five successive, sustained, submaximal contractions held to the point when the required tension could no longer be maintained, fall from the initial value to a lower, steady duration which is dependent partly on the temperature of the muscle and partly on the amount of time allowed for recovery between the contractions. When the interval between the contractions is kept constant at a given value, the durations of these final contractions are always longer when the forearm is immersed in water at 180 C than in water at 340 C. The reason for this is probably to be found in the faster rate of accumulation of metabolites with increasing muscle temperature (Clarke et al. 1958). When the temperature of the water is kept constant at 180 C, reduction of the interval between the contractions from 40 to 3 min results in a fall, by some 107 sec, in the durations of the final contractions. Part of this fall may be attributed to the concomitant rise of muscle temperature of about 50 C, as is seen in Fig. 3. Evidence from the present and from previous experiments (Clarke et al. 1958), shows that over the range of muscle temperatures involved, the decrease in the duration of sustained contractions (held at 1/3 maximum tension) due only to the change of muscle temperature is about 10 sec per degree C. Of the decrease in duration of 107 sec, about 50 sec is estimated to be due to the rise of muscle temperature, so that the fall due only to the reduction in the interval between contractions must be about 57 sec. In water at 340 C, the corresponding fall in duration was 56 sec, of which about 6 sec is attributable to the rise of muscle temperature, and about 50 sec is due to the reduction of the interval between contractions. The decrease in durations of final contractions estimated in this way to be due only to the reduction of the time allowed for the muscle to recover is in reasonable agreement at both water temperatures. The difference may be due to small differences in siting the thermocouple in the muscle or to differences observed in the rates of recovery (see Fig. 4) in the two water-baths. It is surprising to find that, after contractions lasting only some min, even 40 min after fatigue the durations of sustained contractions are only 70-75% of the initial value. Examination of the curves representing the recovery of the ability of the muscle to maintain submaximal contractions shows that there is a fast rate of recovery during the first 10 min after fatigue, followed by a much slower rate ofrecovery which is not complete within 40 min. Concurrent with the completion of the fast rate of recovery are two events: (1) the full recovery of the ability to exert maximum tension, and (2) the completion of the post-contraction hyperaemia (Clarke et al. 1958). Thus the
9 170 A. R. LIND second, slow rate of recovery is not associated with hyperaemia, and occurs after the muscle has recovered its ability to exert maximum tension. These facts suggest that two different processes may occur in the recoveryof the ability of the muscle to sustain submaximal contractions, the first probably involving the removal of metabolites from the muscle during the post-contraction hyperaemia while the second process may well involve the slow replacement in the muscle of reserves of materials necessary for contraction, which are depleted by the sustained contractions. Such a concept would also be compatible with the gradual decrease in duration of successive sustained contractions, possibly by a cumulative depletion of reserves of materials necessary for contraction in the muscle. In considering the events occurring in the muscle immediately after fatigue, an economical hypothesis worth considering is that the substance which accumulates in the muscle to cause fatigue is the same as that which causes the post-exercise hyperaemia. If the arguments above are accepted, the incomplete recovery of the ability of the muscle to sustain contractions at the end of the period of hyperaemia does not invalidate such a hypothesis. Dornhorst & Whelan (1953) and Patterson & Shepherd (1954) considered that the substance causing the post-exercise hyperaemia is removed from the muscle at a rate independent of the rate of blood flow, provided that this is above 'some low level'. In the present experiments, the rate of recovery of muscle function is just significantly faster in the warmer water during the hyperaemia period, and this might be taken, at first sight, to show that the substances causing the fatigue and the hyperaemia are not identical. This phenomenon, however, may be due to the faster replacement of reserves of materials to the muscle during this period, or to the expected faster rate of chemical reactions due solely to the higher muscle temperature (Abramson, Kahn, Tuck, Turman, Rejal & Fleischer, 1957), or to a combination of these two factors. While there is no direct evidence to support the hypothesis that the substance causing fatigue also causes the post-exercise hyperaemia, there is no evidence on which to reject it. SUMMARY 1. Five successive, sustained contractions at a tension of 1/3 maximum tension were held by four subjects when the forearm was immersed in water at 180 C or at 340 C. The intervals between the contractions were 3, 7, 20 or 40 min. 2. The duration of contractions for a given interval between contractions was always greater in water at 180 C than in water at 340 C. 3. The duration of the final contractions fell markedly at both water temperatures when the interval between contractions was reduced from 40 to 3 min. In water at 18 C this fall was nearly twice as great as in water at 340 C; this was attributable to a greater concomitant rise in muscle tempera-
10 RECOVERY AFTER MUSCULAR FATIGUE 171 ture during the experiments, due to the reduction of the interval between contractions, when the arm was in water at 180 C than when in water at 340 C. 4. The recovery of the ability to sustain submaximal contractions after fatigue was only % complete 40 min after fatigue. Recovery occurred at a fast rate immediately after the contraction, and at a much slower rate later. Recovery of the ability to exert maximum tension was completed in 10 min. I wish to express my gratitude to D. E. Lee and E. S. Reeves for invaluable technical help and for their co-operation as subjects in these experiments. REFERENCES ABRAMSON, D. I., KAHN, A., TUCK, S., TURMAN, G. A., REJAL, H. & FLEISCHER, C. S. (1957). Relationship between a range of tissue temperature and local oxygen consumption in the resting forearm. J. Lab. clin. Med. 50, 789. BIGLAND, B. & LIPPOLD, 0. C. J. (1954). Motor unit activity in the voluntary contraction of human muscle. J. Physiol. 125, BROWN, G. L. & BURNS, B. D. (1949). Fatigue and neuromuscular block in mammalian skeletal muscle. Proc. Roy. Soc. B, 136, CLARKE, R. S. J., HELLON, R. F. & LIND, A. R. (1958). The duration of sustained contractions of the human forearm at different muscle temperatures. J. Phy8iol. 143, DORNHORST, A. C. & WHELAN, R. F. (1953). The blood flow in muscle following exercise and circulatory arrest; the influence of reduction in effective local blood pressure, of arterial hypoxia and of adrenaline. Clin. Sci. 12, KRNJEVIC, K. & MILEDI, R. (1958). Failure of neuromuscular propagation in rats. J. Phy8iol. 140, LIND, A. R. & SAMUELOFF, M. (1957). The influence of local temperature on successive, sustained contractions. J. Physsol. 136, 12-13P. MERTON, P. A. (1954). Voluntary strength and fatigue. J. Physiol. 123, NAEss, K. & STORM-MATHISEN, A. (1955). Fatigue of sustained tetanic contractions. Acta physiol. 8cand. 34, NUKADA, A. (1955). Hauttemperatur und Leistungsfahigkeit in Extremitaten bei statischer Haltearbeit. Arbeitsphysiologie, 16, PATTERSON, G. C. & SHEPHERD, J. T. (1954). The effects of continuous infusions into the brachial artery of adenosine triphosphate, histamine and acetylcholine on the amount and rate of blood debt repayment following rhythmic exercise of forearm muscles. Clin. Sci. 13, REID, C. (1928). The mechanism of voluntary muscle fatigue. Quart. J. exp. Physiol. 19, SEYFFARTH, H. (1940). The behaviour of motor-units in voluntary contractions. Skr. nor8ke VidensAkad. 4. Oslo. SMITH, 0. C. (1934). Action potentials from single motor units in voluntary contractions. Amer. J. Physiol. 108, VERNON, H. M. (1929). The influence of rest pauses and changes of posture on the capacity for muscular work. A.R. industr. Fatig. Res. Bd., Lond., No. 54, Part B.
Efficiency, Department of Human Anatomy, University of Oxford
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