Effects of fatigue on the series elastic component of human muscle

on the Series Elastic Component of Human Muscle ... calculation method of the length and force is explained in detail by Pertuzon (1972) and Bouisset. (i973).
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European Journal of

Applied

Eur J Appl Physiol 45, 11-17 (1980)

Physiology and Occupational Physiology 9 Springer-Varlag 1980

Effects of Fatigue on the Series Elastic Component of Human Muscle B. Vigreux, J. C. Cnockaert, and E. Pertuzon Laboratoire de Physiologic Neuromusculaire, LA n ~ 308 CNRS,

Universit6 des Sciences et Techniques, B.P. 36, F-59655 Villeneuve D'Ascq Cedex, France

Summary.The effects of fatigue on the muscular series elastic component were studied in man. The compliance-force relationship (K-F) of the fatigued muscle was compared with that of the unfatigued muscle. The K-F relationships were established under electromyographic control in two cases: 1. The F variation came from the decrease in maximum voluntary force appearing in fatigue which was produced by rhythmic flexions against an elastic resistance. The compliance was measured at regular intervals as fatigue developed. 2. The compliance was measured at different predetermined levels of force (maximal and submaximal) without the appearance of fatigue. The K-F relationship is curved whether the muscle is fatigued or not: the compliance increases as the force decreases. However, for the same value of force, the fatigued muscle is more compliant than the non-fatigued muscle. These results are discussed in relation to mechanical muscular properties and to the two-component muscle model of Hill. Key words: Fatigue - Series compliance - Maximal force

The prolonged or repeated voluntary contraction of a muscle or a muscular group induces a decrease in mechanical performance which is characteristic of fatigue. In a previous paper (Boulang6 et al. 1979), we showed that fatigue modifies the characteristics of the tension developed during isometric contractions. The purpose of the present work was to study the effects of fatigue on another mechanical property, the compliance of the series elastic component of human muscle. For this purpose, the compliance-force (K-F) relationship of the Offprint requests to." Prof. Dr. E. Pertuzon (address see above)

0301-5548/80/0045/0011/$ 01.40

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B. Vigreux et al.

elbow flexors when fatigued was compared with that of the same muscles when not fatigued. Fatigue was the long-term fatigue which arises progressively in a series of successive contractions (Mar6chal and Aubert 1958).

Material and Methods The techniques have been described previously (Goubel and Pertuzon 1973). In short, the subjects were fixed to a seat. The right arm and forearm were horizontal. The forearm was fixed to the iron bar of a mechanical device whose vertical axis of rotation was aligned with that of the elbow. The hand was semi-pronated and not clenched. The angular position of the elbow was measured on the bar by means of a potentiometric goniometer. The angular acceleration of the forearm was also measured by means of an accelerometer fixed to the bar. Furthermore, the bar could be connected, by means of an electromagnet, to a force transducer to measure the isometric torque of flexion. The breaking of the connection was controlled by the experimenter. Surface electromyograms (EMG) were recorded by means of bipolar electrodes placed on the biceps brachii muscle and the long head of triceps brachii muscle. The E M G of the biceps brachii was also rectified and filtered. The kinematic and electromyographic variables were recorded on a polygraphic recorder with a frequency band of 0 - 7 0 0 Hz. There are three principal flexor muscles. The force and the length of each muscle cannot easily be measured. The problem is solved satisfactorily with the utilization of the "equivalent flexor" concept (Pertuzon 1972). The equivalent flexor has the dimensions of the biceps brachii muscle. The calculation method of the length and force is explained in detail by Pertuzon (1972) and Bouisset (i973). In short, the length (I) is given by the formula I = ~/a2 + b 2 + 2ab cos 0 (1) where a and b are respectively the distances from the axis of the elbow to the distal and proximal insertions of the biceps brachii muscle and 0, the elbow angle, measured from full extension. The force (F) is given by the formula F = I 01/a b sin 0 (2), where 0 is the angular acceleration and I the inertia of the whole limb and bar. For each subject, the inertia (expressed in kg- m z) of the limb (forearm plus hand) was calculated by means of the formula: Inertia = 44 x 10-4 BW x (1FA)2 given by Cnockaert (1976) where BW is the body weight (in kg) and 1FAis the length of the forearm (in m) measured between the lower part of the external epicondylus of the humerus and the distal extremity of the radius.

Compliance Measurements The measurement of the compliance K = A1/AF of the equivalent flexor was made during the relaxation of the series elastic component in quick-release movements (Wilkie 1956). In Fig. 1, the recording of a K measurement is presented. The flexion torque increases in parallel with the biceps brachii E M G at first, and then becomes constant. The contraction is strictly isometric in this period as can be seen from the angular position (0 = 75~ The excitation level of the biceps brachii is approximately constant. The activity of the triceps brachii can be neglected. The start of the quick-release movement is expressed by the sudden rise of the tracing of the torque. At the same time, the angular acceleration increases to a maximum value, after which it decreases. The angle of the elbow increases as the flexors shorten. On the biceps brachii EMG, an electric silence corresponding to the unloading reflex can be noted. On the triceps brachii EMG, a burst of E M G corresponding to the stretch reflex can be noted. AI and AF are calculated from Eqs. (1) and (2) just after the release and just before the stretch reflex. This period corresponds to the relaxation of the series elastic component as postulated by Goubel and Pertuzon (1973). For each subject, the K and F values were normalized in the classical manner. The length variations (A1) were divided by 1o, length of the equivalent flexor at the equilibrium position of the elbow (0 = 75~ (Pertuzon and Lestienne 1973). The force variations were divided by Fo, isometric maximal voluntary force measured at 1o without fatigue. The normalized compliance is then expressed by A1/AF x Fo/lo. The normalization does not change the shape of the K-F relationships and the results of the different subjects may be collated.

Muscular Fatigue and Series Compliance

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Fig.

1. Recording of an isometric contraction and a quick-release movement. From top to bottom: 0: Angular position of the elbow joint; E M G B: Surface electromyogram of biceps brachii; C: Isometric torque of flexion; EMG T: Surface electrom.y.ogram of triceps brachii; 0: Angular acceleration; Q: Rectified and filtered EMG of biceps brachii. The isometric contraction is performed at 75~

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Procedure Five subjects were examined during three experimental series with a lapse of 1 week between each examination. In the first two series, the K-F relationships were established during the development of long-term fatigue. In the first experimental series, each subject first performed a maximal isometric flexion lasting less than 2 s. As soon as the flexion torque was constant the electromagnet current was cut off by the experimenter without the knowledge of the subject, causing a quick-release movement (Fig. 1). Then the subject performed rhythmic flexion movements lasting 45 s against an elastic resistance. In these movements, the power developed was 30 W. At the end of these movements, the compliance was measured again. The same sequence was repeated until 11 measurements of K had been performed. Each K measurement lasted less than 10 s. In the second experimentals series, the procedure was the same but the power was cut by half and 21 measurements of K were carried out. In the third experimental series, the K-F relationship was established without fatigue. The experimenter started quick-release movements during predetermined isometric maximal and submaximal efforts. The K measurements were separated by rests of sufficient duration to avoid fatigue. The predetermined isometric torque values were presented twice, first in an increasing order and then decreasing. The results obtained in each case were not significantly different.

Results

The results presented in Fig. 2 show the changes of the torque of elbow flexion (C) and of the compliance of the series elastic component (K) of the elbow flexors as fatigue develops, for one subject (power of work = 30 W). The force of the elbow flexors being proportional to the torque (Eq. 2), it ensues that the force decreases and the compfiance increases as fatigue develops. The decrease in force and the increase in compliance are faster at 30 W than at 15 W. It is well known that compliance is a function of the force developed by the muscle (Joyce and Rack 1969). From our results, the rapid appearance of fatigue does not modify the K-F relationship. Therefore, the results obtained on the five

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Fig. 2. Evolution of torque and compliance of the Equivalent Flexor in relation to fatigue (one subject) (30 W). C: Isometric torque (N.m); K: Compliance (m.N-I); N ~ test: Number of the isometric contraction and the quick-release movement during the development of fatigue

subjects during the first two experimental series were grouped together. In Fig. 3, the K-F relationships of the fatigued muscle as in the first two experimental series, and of the non-fatigued muscle as in the third experimental series, are presented. At neither 15 W nor 30 W were the fatigue sequences continued to exhaustion. This point will be discussed later. For this particular reason, the highest values of compliance, during the tests of fatigue, were reached in only a few cases. In addition, on the upper curve (tests with fatigue) the highest value of force does not reach F/Fo = 1, because this mean value is calculated on F values obtained before the fatigue test (Fo) and in the early stages of fatigue (F I> 0.9

Fo). The shape of the K-F relationships is similar to those described previously by Goubel and Pertuzon (1973) on the elbow flexors and by Cnockaert and Pertuzon (1974) on the elbow extensors. The shape of the K-F relationship of the non-fatigued muscle is similar to that of the fatigued muscle. However, for each value of force, the fatigued muscle compliance is significantly higher than that of the non-fatigued muscle (P < 0.001) except for the lower values of compliance, i.e., near the maximal force of the elbow flexors.

Muscular Fatigue and Series Compliance

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Fig. 3. Compliance-force relationships with and without fatigue (normalized values) (five subjects). K Fo/lo: Normalized compliance; F/Fo: Normalized force; O: without fatigue; 0: with fatigue. Forces have been put into classes of 0.10 F/Fo. In each class, the mean and the standard deviation have been calculated (horizontal bars). For each mean value of force, the mean and the standard deviation of the corresponding compliance have been calculated (vertical bars)

Discussion

The compliance of non-fatigued muscle increases as the developed tension decreases, particularly when the tension is lower than 50% maximal. In these conditions, the decrease in tension arises from a decrease in the excitation level. If fatigue specifically affects the K-F relationship, this effect can only be observed when the excitation "factor" is avoided, i.e., when the excitation level remains constant. Several mechanisms can modify the level of excitation of a fatigued muscle. Several authors (Scherrer and Monod 1960) have distinguished fatigue which develops during isometric (static) contractions from fatigue which develops during anisometric (dynamic) contractions. In the present work, we have chosen to fatigue the muscles by means of successive anisometric contractions, and to follow the development of fatigue by the decrease in maximum isometric voluntary force. This was done to avoid pain which is caused by prolonged or repeated maximum isometric contractions. The excitation level is probably reduced by inhibitory reflexes under the latter conditions.

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B. Vigreux et at.

Furthermore, when the force is higher than 20% maximal, the blood flow in the muscles is strongly reduced (Barcroft and Millen 1939); this involves anoxia and consequently pain. To avoid this, fatigue has been provoked by repeated anisometric contractions. Under the conditions of our experiments, as in the previous one (Boulang6 et al. 1979), fatigue did not lead to any appreciable decrease in the excitation level of the muscles as determined from the integrated EMG of the biceps brachii muscle. This agrees with the results of Mashima et al. (1962) and Nilsson et al. (1977). In turn, our experimental conditions are probably responsible for the fact that the maximal forces in fatigued muscle are rarely less than 50% of the same non-fatigued muscle. If the contraction is sustained for a relatively long time (1 min), the surface EMG is modified (Stephens and Taylor 1972). So all our measurements have been carried out after the first phase of contraction and the contraction was too short to involve a modification in the EMG. The decrease in force in the non-fatigued muscle is due to a decrease in the number of active motor units, while in the fatigued muscle, the number of active motor units, i.e., the excitation level, seems to remain the same judging from the EMG constancy throughout the experiments. Thus, it follows that the excitation level can only be considered as a criterion of tension and compliance when there is no fatigue. Indeed, in this case (Fig. 3, lower curve), the K-F relationship corresponds to different excitation levels. On the contrary, the excitation level of the fatigued muscle is constant, though the compliance increases and the tension decreases through a relationship similar to that of the non-fatigued muscle (Fig. 3, upper curve). Thus, the apposite criterion of tension and compliance would not be the excitation level but the activation level, i.e., the activity of the contractile material. Hill (1938) described active muscle as being composed of two separate components, an elastic component, undamped and uncontrolled by the activation, in series with a contractile component, controlled by the activation. These two components were often improperly considered as two different structures. In point of fact, the more recent models of muscle, such as that of Huxley (1974), are compatible with that of Hill, and Huxley says that: "each cross-bridge seems to contain an instantaneous elastic element and, in series with it, an element which can maintain tension". On this basis it is obvious that the double property of muscle cross-bridges requires that any change in muscle tension is linked with a change in muscle compliance. Thus, the shape of the K-F relationship could be explained. However, this reasoning fails to explain why the compliance of fatigued muscle is higher than the compliance without fatigue, and the question arises as to whether the series elastic component is damped or not. Numerous authors have questionned this point of view (Bahler 1967) and considered that the series compliance is damped. Thus, if it is assumed that fatigue increases viscous damping of muscle, it follows that: (a) the viscous damping does not affect the isometric force; (b) the viscous forces oppose relaxation of the series elastic component. Thus, the variation of the force (AF) measured during relaxation is minimized and compliance is then overestimated.

Muscular Fatigue and Series Compliance

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References Bahler AS (1967) Series elastic component of mammalian skeletal muscle. Am J Physiol 213:1560-1564 Barcroft H, Millen JLE (1939) The blood flow through muscle during sustained contraction. J Physiol (Lond) 97:17-31 Bouisset S (1973) EMG and muscle force in normal motor activities. In: Desmedt JE (ed) New developments in EMG and clinical neurophysiology, vol 1. Karger, Basel, pp 547-583 Boulang6 M, Cnockaert JC, Lensel G, Pertuzon E, Vigreux B (1979) Muscular fatigue and rate of tension development. Eur J Appl Physiol 41:17-25 Cnockaert JC (1976) Recherche des conditions optimales d'ex6cution de mouvements simples partir de crit6res biomdcaniques et 61ectromyographiques. Th~se Doctorat d'Etat, Universit6 Lille, vol 1, 1, p 276 Cnockaert JC, Pertuzon E (1974) Sur la g6om6trie musculo-squelettique du triceps brachii. Application g la d6termination dynamique de sa compliance. Europ J Appl Physiol 32: 149-158 Goubel F, Pertuzon E (1973) Evaluation de l'61asticit6 du muscle in situ par une m6thode de quick-release. Arch Int Physiol Biochim 81:697-707 Hill AV (1938) The heat of shortening and the dynamic constants of muscle. Proc R Soc Lond [Bioi] 126:136-195 Huxley AF (1974) Review lecture: Muscular contraction. J Physiol (Lond) 243:1-44 Joyce JC, Rack PMH (1969) Isotonic lengthening and shortening movements of cat soleus muscle. J Physiol (Lond) 204:475-491 Mardchal G, Aubert X (1958) Composantes multiples de la fatigue du muscle isol6 r6v616es par l'analyse m6canique et thermique de la contraction. J Physiol (Paris) 50:404-406 Mashima H, Matsumura H, Nakayama Y (1962) On the coupling relation between action potential and mechanical response during repetitive stimulation in frotg sartorius muscle. Jpn J Physiol 12: 324- 336 Nilsson J, Tesch P, Thorstensson A (1977) Fatigue and EMG of repeated fast voluntary contractions in man. Acta Physiol Scand 101:194-198 Pertuzon E (1972) La contraction musculaire dans le mouvement volontaire maximal. Th6se Doctorat d'Etat, Universit6 Lille, vol 1, 1, p 208 Pertuzon E, Lestienne F (1973) Ddtermination dynamique de la position d'6quilibre d'une articulation. Int Z Angew Physiol Einschl Arbeitsphysiol 31:315-325 Scherrer J, Monod H (1960) Le travail musculaire local et la fatigue chez l'homme. J Physiol (Paris) 52 : 419- 501 Stephens JA, Taylor A (1972) Fatigue of maintained voluntary muscle contraction in man. J Physiol (Lond) 220:1-18 Wilkie DR (1956) Measurement of the series elastic component at various times during a single muscle twitch. J Physiol (Lond) 134:527-530 Accepted June 13, 1980