European Journal o f
Applied
Eur. J. Appl. Physiol. 41, 17-25 (1979)
Physiology
and Occupationa[ Physiology 9 Springer-Ver[ag 1979
Muscular Fatigue and Rate of Tension Development M. Boulang~, J. C. Cnockaert, G. Lensel, E. Pertuzon, and B. Vigreux Laboratoire de PhysiologieNeuromusculaire, Universit+ des Sciences et Techniques de Lille, B.P. 36, F-59650, ViUeneuved'Ascq, France Summary. The effects of long-term fatigue upon maximal force and peak rate of tension development (PRTD) (dF/dt max) are studied in man (elbow flexors), in the rat (pseudo-isolated gastrocnemius muscle) and in the frog (isolated sartorius muscle). The muscles are fatigued by voluntary anisometric anisotonic contractions against an elastic resistance in man, and by maximal tetanic contractions in the frog and the rat. In man, the excitation level of the muscle is controlled by the integrated surface EMG of the biceps brachii. In the animals, the muscles are stimulated by a neurostimulator. The PRTD and the maximal isometric force are measured during fatigue tests. In man, frog and rat, the maximal voluntary isometric torque or the maximal force and the PRTD decrease initially more or less rapidly according to the power developed during the fatigue process, and then less rapidly. The relationship between PRTD and maximal force is linear in the animals and curvilinear in man. The variations of maximal force and PRTD are discussed in relation to the level of excitation of the muscles and of the composition in different motor units types and their spatio-temporal recruitment. From a biomechanical point of view, it seems necessary to study the behavior of the series elastic component during the evolution of long term fatigue. Key words: Fatigue -- Maximal force - Peak rate of tension development (dF/dt max)
Fatigue is usually defined as a decrease (reversible during rest) in the force developed during contraction, the level of excitation being constant. The simplest way of studying fatigue is to examine the fall in performance during successive maximal contractions, in which excitation levels are easily controllable. Long-term fatigue arising and Offprint requests to: Prof. E. Pertuzon (address see above)
0301-5548/79/0041/0017/$ 01.80
18
M. Boulang6 et al.
growing during successive contractions is classically distinguished from short-term fatigue arising during a prolonged contraction (Marechal and Aubert, 1958). There are numerous works that show the influence of fatigue on maximal isometric force but the evolution of the rate of tension development (RTD) has rarely been studied in man. A maximal isometric contraction can be divided into three stages: a stage where the force grows, a plateau and a stage where the force decreases. During the first stage, the increasing force presents an inflection point where the slope is maximal. At this point, the slope o f the force defines the peak rate of tension development (PRTD), i.e., d F / d t max. The aim o f this work is to measure the evolution of maximal voluntary isometric force and P R T D of the elbow flexors during the setting in of long-term fatigue in m a n placed under electromyographic control. O n e of the factors that can make the R T D vary is a possible variation in the speed of recruitment of motor units. To verify the influence of this factor, the same study was carried out on the isolated sartorius muscle of the frog and on the gastrocnemius muscle of the rat in situ and with maximal synchronous electrical stimulation.
Material and Methods
1. Elbow Flexors in Man The subjects are seated on, and firmly attached to, a seat. The right arm is horizontal. The right forearm is fixed in a moulded splint supported by a horizontal bar. The vertical axis of rotation of the bar coincides with that of the elbow. The extremity of the bar is connected to a dynamometer by an inextensiblecable. This apparatus allows flexor torque to be measured. The electromyographic activity (EMG) of the biceps brachii is registered by means of surface electrodes (Pertuzon and Lestienne, 1973), the potentials being amplified and either directly recorded, or recorded after rectifying and filtering. The subjects make to-and-fro movements continuously. An elastic resistance is opposed to the flexion movement. In a first experimental series, the power developed against the elastic resistance is 24.3 W. In a second experimentalseries the power developedis 16.2 W. Every 45 s, the work is stopped for 10 s during which a fatigue test is performed. During this test the bar is connected to the dynamometer and the subject is asked to make a maximal effort of flexion as fast as possible and maintains it for 1 s. For these tests, the articulation angle is set at 75 degrees. The work is continued until 10 tests are recorded during the first experimental series and 20 tests during the second. The peak values of the isometric flexion torque and the RTD are also determined at the beginning of each bout of work. Ten subjects were examined once in each series.
2. Gastrocnemius Muscle of the Rat The rats are adult Wistar rats weighing 250-300 g. The animal is anesthetized with an intraperitoneal injection of Nembutal and then placed on a table. The femur and the ankle are firmly fixed on the table. The gastrocnemius muscle is dissected free from surrounding tissue; its distal tendon is cut and connected to a strain gauge force transducer. The sciatic nerve is dissected and all the nerves innervating muscles other than the gastrocnemius are divided.The sciatic nerve is then cut close to the sacral plexus and placed on silver electrodes. A neurostimulator stimulates the nerve at a frequency of 100 Hz.
Muscular Fatigue and Tension Development
19
J I] C Jo Qo Co
.75
,5
.25
o
~
,;
~
1'o
n -~ test
a J
0
Jo
0o Co
c
I-
.75-
.50-
.25-
0
~'o
~
;o n~ test
b Fig. 1. Evolution of isometric voluntary torque of flexion of the elbow (C/Co; 9 of the peak rate of tension development (J/Jo; 0) and of the recruitment speed of motor units of the biceps brachii (Q/Q0; I ) during fatigue in man. Each point represents the mean value (and standard deviation) of the ten subjects, a series I: work power = 24.3 W, b series II: work power = 16.2 W
20
M. Boulange et al.
The muscle is ifatigued by a series of tetanic isometric contractions lasting 2 s separated by a rest period of 10s. The ,test of fatigue consists of recording one tetanic contraction after four others have been performed. During the test of fatigue, the maximal force and the PRTD are measured. During each bout of work, "15 tests were carried out.
3. Sartorius Muscle of the Frog The techniques have been described elsewhere (Lensel, 1976). In short, the sartorius muscle is dissected leaving its proximal tendon attached to the pelvis. The muscle is then placed into a bath of circulating oxygenated physiological solution at 0 ~ C. The muscle is left for 1 h to obtain thermal equilibrium. Then the pelvis is fixed ~ a force transducer made with strain gauges. The tibial tendon is attached to a fixed point. The all-over transverse stimulation of the muscle is performed by a neurostimulator at a frequency of 3 0 - 4 0 Hz. The muscle is fatigued by series of tetanic contractions lasting 1 s each separated by rests of 1 s. The level of fatigue is determined by measuring the isometric tension developed. For predetermined submaximal values of tetanic tension the PRTD is measured.
Results
In each experimental series, each variables is expressed as a percentage of the maximal value and then in man, rat and frog taken separately the interindividual means
J Jo
I EMG I EMGo
F Fo
1-
.75-
.5-
.25 -
o
~
~
~
8
lb
12
n ~ test
Fig. 2. Evolution of the isometric tetanic force (FIFo; 0), of the peak rate of tension development (J/Jo; O) and of the integrated EMG measured during the plateau of force (IEMG/IEMG0; I ) during fatigue of the gastrocnemius muscle of the rat. Each point represents the mean value (and standard deviation) of five rats, except for the IEMG (one rat)
Muscular Fatigue and Tension Development
21
are calculated. It should be noted that, in man, maximal values were not obtained for every fatigue test. Therefore, as the results correspond to means calculated for the ten subjects, the theoretical maximal value (100% or 1) may not be reached, as can be seen in Figure lb. The voluntary isometric maximal flexor torque and the P R T D are shown for each successive fatigue test. Furthermore, in man, the maximal speed of recruitment of motor units of biceps brachii, defined as the maximal slope of the rectified and filtered EMG, is examined at each test of fatigue. Figure 1 shows that, during the two experimental series performed in man, the maximal voluntary flexor torque decreases, showing the development of fatigue. For a power of 24.3 W (Fig. la) the torque decreases sharply at first, and then more slowly. For a power of 16.2 W (Fig. lb), the decrease is slower and more regular. In each case, the P R T D decreases in a manner parallel to that of the maximal torque. The results obtained on the gastrocnemius muscle of the rat stimulated maximally (Fig. 2) parallel those obtained in man, especially in the first experimental series (Fig. la). Figure 3 shows that the shape of the relationship between the maximal speed of contraction and the maximal torque in man, is relatively constant whatever the power of the work may be. In the two experimental series, this relationship seems to be curvilinear. On the other hand, in the gastrocnemius muscle of the rat (Fig. 4a) and the sartorius muscle of the frog (Fig. 4b) the relationship is practically linear.
J Jo
.75-
.5-
.25 -
o
";
i
C
Co
Fig. 3. Peak rate of tension development(J/Jo) of elbow flexors versus isometric flexion torque (C/Co) during fatigue in man. SeriesI: A, SeriesII: *. Each point represents the mean value (and standard deviation) of ten subjects
J Jo 10
8~ o
9
El
o O
.75-
O
I
O
O
O
0
Cil
0 o
.5-
B
9 o OC3
.25-
9
o 9
A9
F F0
Et Jo
9
lio ,A
.9 ,tA
.8 E]
.7'
& 0 ,I
.5 A
.4
L3
A
.3 A
el:]
.2 ta
,
o
.i
.2
I
.~
.4
9
,
t
,
,
,
.5
.6
.z
.8
:9
F
i
F0
b Fig. 4. Peak rate of tension development (J/Jo) and isometric tetanus force (F/Fo) during fatigue in the gastrocnemius muscle of the rat (a) and in the sartorius muscle of the frog (b). The symbols correspond to the different preparations
Muscular Fatigue and Tension Development
23
Discussion
This study has been limited to biomeehanical aspects of m u s c a t fatigue and PKTD. Furthermore, the study has been limited to the problem of long term fatigue induced by repeated isometric maximal contractions of isolated muscle~(sartorius) or pseudo-isolated muscle (gastrocnemius). In man, it was impossible to ask the subjects to perform repeated maximal isometric contractions. Indeed, two problems were set, 1) these sort of contractions became rapidly painfully, 2) these contractions induced ischemia in the muscle (Humphreys and Lind, I963). So, in man, the duration of the isometric tests of fatigue were limited to one second, i.e:, a duration largely lower than the "limit-time" of maximal voluntary isometric contraction (Barcroft and Millen, 1939; Scherrer and Monod, 1960). Fatigue was induced by dynamic contractions, which maintain a normal blood supply to the muscle (Walder, 1955). However, it was necessary to control the level of excitation of the muscle during the first stage of contraction. This control is easy in an isolated muscle; but in man it is necessary to ensure that the level of excitation does not vary too much. In other words, it is necessary to ensure that a modification of the PRTD is not simply due to a modification in the spatiotemporal recruitment of motor units. It has been Verified that, in man, during the stage of increasing force where J and Q are measured, the integrated EMG (speed of recruitment) remains approximately constant (Fig. 1). For the gastrocnemius muscle of the rat, recruitment is immediately maximal, but it can be seen that fatigue does not involve an important decrease in the integrated EMG during the tetanus plateau (Fig. 2). This means that, in these experimental conditions, decreasing performance of the muscle would be related only to diminution in mechanical performance and not to failure of the mechanisms of excitation. These conclusions agree with those of Mashima et ai. (1962), Eberstein and Sandow (1963), Nilson et al. (1977). If the power at work during the development of the fatigue (voluntary movements) is sufficiently high, the force decreases in two stages, as it does in isolated muscle. Our results agree with those of Nilson et al. (1977) in man, those of Fitts and Holloszy (1977) on the rat soleus muscle and those of Marechal and Aubert (1959) and Aljure and Borrero (1968) in the sartorius muscle of the frog or toad. As for the PRTD, it is necessary to cheek if the level of excitation remains constant during the experiment. The level of excitation which remains constant for the isolated muscle (Fig. 2) does so in man during long term fatigue (Merton, 1954; Nilsson et al., 1977) whereas Stephens and Taylor (1972) showed that the level of excitation decreases during short-term fatigue. It could be supposed that contraction time remains constant because the PRTD and the maximal force decrease in parallel. This point is not entirely verified in the isolated muscle (i.e., when the level of excitation is immediately maximal). For all the contractions recorded on the sartorius muscle of the frog, the mean contraction time is 589 ms (SD = 112). It seems, however, that a rather narrow relationship exists between tetanic tension and the PRTD, but that contraction time: is more weakly related to tetanic tension (Goslow et al., i977a). It has been shown elsewhere that, in man, PRTD is directly proportional to the mean value of RTD (Pertuzon, 1972). In these conditions, the decrease in PRTD and maximal force can be partly explained
24
M. Boulang6 et al.
by a decrease in the number of m o t o r units mechanically active, and b y the type of m o t o r units which remain active as the fatigue develops. Indeed, it has been shown (Burke et ai., 1971; Stephens and Taylor, 1972; Stephens and Usherwood, 1975) that the m o t o r units which are less sensitive to fatigue are the slow ones, i.e., the m o t o r units which have a lower R T D and a weaker tetanic force. However, G o s l o w et al. (1977a and b) have pointed out that fast m o t o r units can be subdivided into several categories with regard to their degree o f fatiguability. F r o m a purely biomechanical point o f view and on the basis of the two-component muscle model of Hill (1938), P R T D depends on the force-velocity relationship o f the contractile component and on the compliance of the series-elastic component (Wilkie, 1950). Fatigue involves a modification of the force-velocity relationship, and an increase in the series-elastic compliance (Lensel, 1978). A detailed study of the evolution o f the series elastic compliance during fatigue in m a n would permit a more precise analysis of the mechanisms. Finally, it appears that the relationship between P R T D and maximal force, which is fairly linear in isolated muscle (Fig. 4), seems to be curvilinear in m a n (Fig. 3). This difference could be due to the fact that fatigue in m a n develops in a different manner in the three principal flexors of the elbow either because the distribution o f the c o m m a n d between the three muscles o f the group is modified or because the composition of m o t o r unit types differs from one muscle to another.
Acknowledgements. We should like to thank Mr. J. Rembowski of the specialized language service of the CUEEP. Universit~ de Lille I. for translation of the manuscript, Mrs. Le Bec for technical assistance, and Mrs. Coisne for typing the manuscript.
References Aljure, E. F., Borrero, L. M.: Influence of muscle length on the development of fatigue in toad sartorius. J. Physiol. (Lond.) 199, 241-252 (1968) Barcroft, H., Millen, J. L. E.: The blood flow through muscle during sustained contraction. J. Physiol. (Lond.) 97, 17-31 (1939) Burke, R. E., Levine, D. N., Zajac, F. E., Tsairis, P., Engel, W. K.: Mammalian motor units: physiological-histochemical correlation in three types in cat gastrocnemius. Science 174, 709-712 (1971) Eberstein, A., Sandow, A.: Fatigue mechanisms in muscle fibres. In: The effect of use and disuse on neuromuscular functions. Gutman, E. (ed.), pp. 515--526. Prague: Czechoslovack Acad. Sci. 1963 Fitts, R. H., Holloszy, J. O.: Contractile properties of rat soleus muscle: effects of training and fatigue. Am. J. Physiol. 233, C86--C91 (1977) Goslow, G. E., Jr., Cameron, W. E., Stuart, D. G.: The fast twitch motor units of cat ankle flexors. I. Tripartite classification on basis of fatigability. Brain Res. 134, 35--46 (1977a) Goslow, G. E., Jr., Cameron, W. E., Stuart, D. G.: The fast twitch motor units of cat ankle flexors. II. Speed-force relations and recruitment order. Brain Res. 134, 47--57 (1977b) Hill, A. V.: The heat of shortening and the dynamic constants of muscle. Proc. R. Soc. Lond. [Biol.] 126, 136--195 (1938) Humphreys, P. W., Lind, A. R.: Blood flow through active and inactive muscles of the forearm during sustained handgrip contraction. J. Physiol. (Lond.) 166, 120-135 (1963) Lensel, G.: Comparaison de la compliance du muscle au repos et en contraction. Arch. Int. Physiol. Biochim. 84, 699-711 (1976) Lensel, G.: Evolution de la compliance s~rie du muscle isol6 en fonction de la fatigue. C.R. Soc. Biol, 172, 485--493 (1978)
Muscular Fatigue and Tension Development
25
Marechal, G., Aubert, X.: Composantes multiples de la fatigue du muscle isol~ r6v+lees par l'analyse m6canique et thermique de la contraction. J. Physiol. (Paris) 50, 404-406 (1958) Marechal, G., Aubert, X.: Analyse de la contraction isom6trique du muscle isol+ stri~ dans diff+rents types d'6preuves de fatigue. J. Physiol. (Paris) 51, 527 (1959) Mashima, H., Matsumura, M., Nakayama, Y.: On the coupling relation between action potential and mechanical response during repetitive stimulation in frog sartorius muscle. Jpn. J. Physiol. 12, 324-336 (1962) Merton, P. A.: Voluntary strength and fatigue. J. Physiol. (Lond.) 123, 553-564 (1954) Nilsson, J., Tesch, P., Thorstensson, A.: Fatigue and I~MG of repeated fast voluntary contractions in man. Acta Physiol. Scand. 101, 194-198 (1977) Pertuzon, E.: La contraction musculaire dans le mouvement volontaire maximal. Th~se Doctorat d'Etat, Univ. Lille 1, 1 vol., 208 p. (1972) Pertuzon, E., Lestienne, F.: D&ermination dynamique de la position d'6quilibre d'une articulation. Int. Z. Angew. Physiol. 31, 315-325 (1973) Scherrer, J., Monod, H.: Le travail musculaire local et la fatigue chez l'homme. J. Physiol. (Paris) 52, 419-501 (1960) Stephens, J. A., Taylor, A.: Fatigue of maintained voluntary muscle contraction in man. J. Physiol. (Lond.) 220, 1-18 (1972) Stephens, J. A., Usherwood, T. P.: The fatigability of human motor units. J. Physiol. (Lond.) 250, 37P--38P (1975) Walder, D. N.: The relationship between blood flow capillary surface area and sodium clearance in muscle. Clin. Sci. Mol. Med. 14, 303--315 (1955) Wilkie, D. R.: The relation between force and velocity in human muscle. J. Physiol. (Lond.) 110, 249--280 (1950) Accepted November 2, 1978
Applied
Eur. J. Appl. Physiol. 41, 17-25 (1979)
Physiology
and Occupationa[ Physiology 9 Springer-Ver[ag 1979
Muscular Fatigue and Rate of Tension Development M. Boulang~, J. C. Cnockaert, G. Lensel, E. Pertuzon, and B. Vigreux Laboratoire de PhysiologieNeuromusculaire, Universit+ des Sciences et Techniques de Lille, B.P. 36, F-59650, ViUeneuved'Ascq, France Summary. The effects of long-term fatigue upon maximal force and peak rate of tension development (PRTD) (dF/dt max) are studied in man (elbow flexors), in the rat (pseudo-isolated gastrocnemius muscle) and in the frog (isolated sartorius muscle). The muscles are fatigued by voluntary anisometric anisotonic contractions against an elastic resistance in man, and by maximal tetanic contractions in the frog and the rat. In man, the excitation level of the muscle is controlled by the integrated surface EMG of the biceps brachii. In the animals, the muscles are stimulated by a neurostimulator. The PRTD and the maximal isometric force are measured during fatigue tests. In man, frog and rat, the maximal voluntary isometric torque or the maximal force and the PRTD decrease initially more or less rapidly according to the power developed during the fatigue process, and then less rapidly. The relationship between PRTD and maximal force is linear in the animals and curvilinear in man. The variations of maximal force and PRTD are discussed in relation to the level of excitation of the muscles and of the composition in different motor units types and their spatio-temporal recruitment. From a biomechanical point of view, it seems necessary to study the behavior of the series elastic component during the evolution of long term fatigue. Key words: Fatigue -- Maximal force - Peak rate of tension development (dF/dt max)
Fatigue is usually defined as a decrease (reversible during rest) in the force developed during contraction, the level of excitation being constant. The simplest way of studying fatigue is to examine the fall in performance during successive maximal contractions, in which excitation levels are easily controllable. Long-term fatigue arising and Offprint requests to: Prof. E. Pertuzon (address see above)
0301-5548/79/0041/0017/$ 01.80
18
M. Boulang6 et al.
growing during successive contractions is classically distinguished from short-term fatigue arising during a prolonged contraction (Marechal and Aubert, 1958). There are numerous works that show the influence of fatigue on maximal isometric force but the evolution of the rate of tension development (RTD) has rarely been studied in man. A maximal isometric contraction can be divided into three stages: a stage where the force grows, a plateau and a stage where the force decreases. During the first stage, the increasing force presents an inflection point where the slope is maximal. At this point, the slope o f the force defines the peak rate of tension development (PRTD), i.e., d F / d t max. The aim o f this work is to measure the evolution of maximal voluntary isometric force and P R T D of the elbow flexors during the setting in of long-term fatigue in m a n placed under electromyographic control. O n e of the factors that can make the R T D vary is a possible variation in the speed of recruitment of motor units. To verify the influence of this factor, the same study was carried out on the isolated sartorius muscle of the frog and on the gastrocnemius muscle of the rat in situ and with maximal synchronous electrical stimulation.
Material and Methods
1. Elbow Flexors in Man The subjects are seated on, and firmly attached to, a seat. The right arm is horizontal. The right forearm is fixed in a moulded splint supported by a horizontal bar. The vertical axis of rotation of the bar coincides with that of the elbow. The extremity of the bar is connected to a dynamometer by an inextensiblecable. This apparatus allows flexor torque to be measured. The electromyographic activity (EMG) of the biceps brachii is registered by means of surface electrodes (Pertuzon and Lestienne, 1973), the potentials being amplified and either directly recorded, or recorded after rectifying and filtering. The subjects make to-and-fro movements continuously. An elastic resistance is opposed to the flexion movement. In a first experimental series, the power developed against the elastic resistance is 24.3 W. In a second experimentalseries the power developedis 16.2 W. Every 45 s, the work is stopped for 10 s during which a fatigue test is performed. During this test the bar is connected to the dynamometer and the subject is asked to make a maximal effort of flexion as fast as possible and maintains it for 1 s. For these tests, the articulation angle is set at 75 degrees. The work is continued until 10 tests are recorded during the first experimental series and 20 tests during the second. The peak values of the isometric flexion torque and the RTD are also determined at the beginning of each bout of work. Ten subjects were examined once in each series.
2. Gastrocnemius Muscle of the Rat The rats are adult Wistar rats weighing 250-300 g. The animal is anesthetized with an intraperitoneal injection of Nembutal and then placed on a table. The femur and the ankle are firmly fixed on the table. The gastrocnemius muscle is dissected free from surrounding tissue; its distal tendon is cut and connected to a strain gauge force transducer. The sciatic nerve is dissected and all the nerves innervating muscles other than the gastrocnemius are divided.The sciatic nerve is then cut close to the sacral plexus and placed on silver electrodes. A neurostimulator stimulates the nerve at a frequency of 100 Hz.
Muscular Fatigue and Tension Development
19
J I] C Jo Qo Co
.75
,5
.25
o
~
,;
~
1'o
n -~ test
a J
0
Jo
0o Co
c
I-
.75-
.50-
.25-
0
~'o
~
;o n~ test
b Fig. 1. Evolution of isometric voluntary torque of flexion of the elbow (C/Co; 9 of the peak rate of tension development (J/Jo; 0) and of the recruitment speed of motor units of the biceps brachii (Q/Q0; I ) during fatigue in man. Each point represents the mean value (and standard deviation) of the ten subjects, a series I: work power = 24.3 W, b series II: work power = 16.2 W
20
M. Boulange et al.
The muscle is ifatigued by a series of tetanic isometric contractions lasting 2 s separated by a rest period of 10s. The ,test of fatigue consists of recording one tetanic contraction after four others have been performed. During the test of fatigue, the maximal force and the PRTD are measured. During each bout of work, "15 tests were carried out.
3. Sartorius Muscle of the Frog The techniques have been described elsewhere (Lensel, 1976). In short, the sartorius muscle is dissected leaving its proximal tendon attached to the pelvis. The muscle is then placed into a bath of circulating oxygenated physiological solution at 0 ~ C. The muscle is left for 1 h to obtain thermal equilibrium. Then the pelvis is fixed ~ a force transducer made with strain gauges. The tibial tendon is attached to a fixed point. The all-over transverse stimulation of the muscle is performed by a neurostimulator at a frequency of 3 0 - 4 0 Hz. The muscle is fatigued by series of tetanic contractions lasting 1 s each separated by rests of 1 s. The level of fatigue is determined by measuring the isometric tension developed. For predetermined submaximal values of tetanic tension the PRTD is measured.
Results
In each experimental series, each variables is expressed as a percentage of the maximal value and then in man, rat and frog taken separately the interindividual means
J Jo
I EMG I EMGo
F Fo
1-
.75-
.5-
.25 -
o
~
~
~
8
lb
12
n ~ test
Fig. 2. Evolution of the isometric tetanic force (FIFo; 0), of the peak rate of tension development (J/Jo; O) and of the integrated EMG measured during the plateau of force (IEMG/IEMG0; I ) during fatigue of the gastrocnemius muscle of the rat. Each point represents the mean value (and standard deviation) of five rats, except for the IEMG (one rat)
Muscular Fatigue and Tension Development
21
are calculated. It should be noted that, in man, maximal values were not obtained for every fatigue test. Therefore, as the results correspond to means calculated for the ten subjects, the theoretical maximal value (100% or 1) may not be reached, as can be seen in Figure lb. The voluntary isometric maximal flexor torque and the P R T D are shown for each successive fatigue test. Furthermore, in man, the maximal speed of recruitment of motor units of biceps brachii, defined as the maximal slope of the rectified and filtered EMG, is examined at each test of fatigue. Figure 1 shows that, during the two experimental series performed in man, the maximal voluntary flexor torque decreases, showing the development of fatigue. For a power of 24.3 W (Fig. la) the torque decreases sharply at first, and then more slowly. For a power of 16.2 W (Fig. lb), the decrease is slower and more regular. In each case, the P R T D decreases in a manner parallel to that of the maximal torque. The results obtained on the gastrocnemius muscle of the rat stimulated maximally (Fig. 2) parallel those obtained in man, especially in the first experimental series (Fig. la). Figure 3 shows that the shape of the relationship between the maximal speed of contraction and the maximal torque in man, is relatively constant whatever the power of the work may be. In the two experimental series, this relationship seems to be curvilinear. On the other hand, in the gastrocnemius muscle of the rat (Fig. 4a) and the sartorius muscle of the frog (Fig. 4b) the relationship is practically linear.
J Jo
.75-
.5-
.25 -
o
";
i
C
Co
Fig. 3. Peak rate of tension development(J/Jo) of elbow flexors versus isometric flexion torque (C/Co) during fatigue in man. SeriesI: A, SeriesII: *. Each point represents the mean value (and standard deviation) of ten subjects
J Jo 10
8~ o
9
El
o O
.75-
O
I
O
O
O
0
Cil
0 o
.5-
B
9 o OC3
.25-
9
o 9
A9
F F0
Et Jo
9
lio ,A
.9 ,tA
.8 E]
.7'
& 0 ,I
.5 A
.4
L3
A
.3 A
el:]
.2 ta
,
o
.i
.2
I
.~
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9
,
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,
,
,
.5
.6
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.8
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F
i
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b Fig. 4. Peak rate of tension development (J/Jo) and isometric tetanus force (F/Fo) during fatigue in the gastrocnemius muscle of the rat (a) and in the sartorius muscle of the frog (b). The symbols correspond to the different preparations
Muscular Fatigue and Tension Development
23
Discussion
This study has been limited to biomeehanical aspects of m u s c a t fatigue and PKTD. Furthermore, the study has been limited to the problem of long term fatigue induced by repeated isometric maximal contractions of isolated muscle~(sartorius) or pseudo-isolated muscle (gastrocnemius). In man, it was impossible to ask the subjects to perform repeated maximal isometric contractions. Indeed, two problems were set, 1) these sort of contractions became rapidly painfully, 2) these contractions induced ischemia in the muscle (Humphreys and Lind, I963). So, in man, the duration of the isometric tests of fatigue were limited to one second, i.e:, a duration largely lower than the "limit-time" of maximal voluntary isometric contraction (Barcroft and Millen, 1939; Scherrer and Monod, 1960). Fatigue was induced by dynamic contractions, which maintain a normal blood supply to the muscle (Walder, 1955). However, it was necessary to control the level of excitation of the muscle during the first stage of contraction. This control is easy in an isolated muscle; but in man it is necessary to ensure that the level of excitation does not vary too much. In other words, it is necessary to ensure that a modification of the PRTD is not simply due to a modification in the spatiotemporal recruitment of motor units. It has been Verified that, in man, during the stage of increasing force where J and Q are measured, the integrated EMG (speed of recruitment) remains approximately constant (Fig. 1). For the gastrocnemius muscle of the rat, recruitment is immediately maximal, but it can be seen that fatigue does not involve an important decrease in the integrated EMG during the tetanus plateau (Fig. 2). This means that, in these experimental conditions, decreasing performance of the muscle would be related only to diminution in mechanical performance and not to failure of the mechanisms of excitation. These conclusions agree with those of Mashima et ai. (1962), Eberstein and Sandow (1963), Nilson et al. (1977). If the power at work during the development of the fatigue (voluntary movements) is sufficiently high, the force decreases in two stages, as it does in isolated muscle. Our results agree with those of Nilson et al. (1977) in man, those of Fitts and Holloszy (1977) on the rat soleus muscle and those of Marechal and Aubert (1959) and Aljure and Borrero (1968) in the sartorius muscle of the frog or toad. As for the PRTD, it is necessary to cheek if the level of excitation remains constant during the experiment. The level of excitation which remains constant for the isolated muscle (Fig. 2) does so in man during long term fatigue (Merton, 1954; Nilsson et al., 1977) whereas Stephens and Taylor (1972) showed that the level of excitation decreases during short-term fatigue. It could be supposed that contraction time remains constant because the PRTD and the maximal force decrease in parallel. This point is not entirely verified in the isolated muscle (i.e., when the level of excitation is immediately maximal). For all the contractions recorded on the sartorius muscle of the frog, the mean contraction time is 589 ms (SD = 112). It seems, however, that a rather narrow relationship exists between tetanic tension and the PRTD, but that contraction time: is more weakly related to tetanic tension (Goslow et al., i977a). It has been shown elsewhere that, in man, PRTD is directly proportional to the mean value of RTD (Pertuzon, 1972). In these conditions, the decrease in PRTD and maximal force can be partly explained
24
M. Boulang6 et al.
by a decrease in the number of m o t o r units mechanically active, and b y the type of m o t o r units which remain active as the fatigue develops. Indeed, it has been shown (Burke et ai., 1971; Stephens and Taylor, 1972; Stephens and Usherwood, 1975) that the m o t o r units which are less sensitive to fatigue are the slow ones, i.e., the m o t o r units which have a lower R T D and a weaker tetanic force. However, G o s l o w et al. (1977a and b) have pointed out that fast m o t o r units can be subdivided into several categories with regard to their degree o f fatiguability. F r o m a purely biomechanical point o f view and on the basis of the two-component muscle model of Hill (1938), P R T D depends on the force-velocity relationship o f the contractile component and on the compliance of the series-elastic component (Wilkie, 1950). Fatigue involves a modification of the force-velocity relationship, and an increase in the series-elastic compliance (Lensel, 1978). A detailed study of the evolution o f the series elastic compliance during fatigue in m a n would permit a more precise analysis of the mechanisms. Finally, it appears that the relationship between P R T D and maximal force, which is fairly linear in isolated muscle (Fig. 4), seems to be curvilinear in m a n (Fig. 3). This difference could be due to the fact that fatigue in m a n develops in a different manner in the three principal flexors of the elbow either because the distribution o f the c o m m a n d between the three muscles o f the group is modified or because the composition of m o t o r unit types differs from one muscle to another.
Acknowledgements. We should like to thank Mr. J. Rembowski of the specialized language service of the CUEEP. Universit~ de Lille I. for translation of the manuscript, Mrs. Le Bec for technical assistance, and Mrs. Coisne for typing the manuscript.
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