skeletal muscle is essentially caused by failure of membrane excitation or by decrease (Received 16 September 1982)

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1 J. Physiol. (1983), 339, pp With 6 text-figures Printed in Great Britain ELECTROMYOGRAM, FORCE AND RELAXATION TIME DURING AND AFTER CONTINUOUS ELECTRICAL STIMULATION OF HUMAN SKELETAL MUSCLE IN SITU BY ERIC HULTMAN AND HANS SJOHOLM From the Department of Clinical Chemi8try II, Karolin8ka In8titutet, Huddinge University Ho8pital, Huddinge, Sweden (Received 16 September 1982) SUMMARY 1. A technique for recording the surface electromyogram (e.m.g.) simultaneously with electrical stimulation of human skeletal muscle is described. 2. During a fatiguing electrical stimulation the e.m.g. amplitude and force decreased in the same proportion. 3. During recovery the e.m.g. was quickly normalized whereas force remained at a reduced level. 4. Relaxation time increased during the stimulation and helps substantially in keeping up tension during a fatiguing contraction. In the recovery phase the rapid normalization of relaxation time counteracts recovery of tension. 5. It is concluded that e.m.g. measurements alone can be misleading as an index of contraction force and that muscular fatigue during electrical stimulation can be attributed to excitation failure only to a lesser extent. INTRODUCTION For many years there has been an interest in determining whether fatigue in human skeletal muscle is essentially caused by failure of membrane excitation or by decrease of contractile strength of working muscle fibres despite adequate activation. Most studies have been concerned with the relation between force during sustained voluntary contractions and the electromyogram (e.m.g.) recorded either from the surface of the muscle or inside the muscle with needle electrodes. The general view is that there is a good correspondence between reduction in e.m.g. amplitude and reduction in force. This is interpreted as excitation failure being the main cause of fatigue (Stephens & Taylor, 1972; Milner-Brown & Stein, 1975; Lind & Petrofsky, 1979). Recently, electrical stimulation of the body of human skeletal muscle with surface electrodes has been used to study the muscle in a standardized way independent of the subject's voluntary effort (Edwards, Young, Hosking & Jones, 1977b; Hultman, Sjoholm, Sahlin & Edstrom, 1981). Bigland-Ritchie, Jones & Woods (1979) studied the relation between force in response to electrical stimulation and e.m.g. activity by intermittent nerve stimulation 2 PHY 339

2 34 E. HULTMAN AND H. SJHHOLM in brief pauses in between periods of direct electrical muscle stimulation. A good correspondence between e.m.g. amplitude and force was found also in this investigation. The present paper describes a method which makes it possible to record the e.m.g. simultaneously with continuous electrical stimulation. The relation between e.m.g. recorded in this way and force during and after continuous electrical stimulation is presented. A stimulation frequency of 20 Hz was used, generating an initial force around 70% of maximum (Edwards et al. 1977b; Hultman et al. 1981) corresponding to the load in many kinds of everyday work. Also the relaxation time during and after continuous electrical stimulation is measured and presented. METHODS The present work is part of a project which has been approved by the Ethical Committee of the Karolinska Institutet. Seventeen volunteers participated in the study: eleven males aged years and six females aged years. The subjects were lying on a bed with the lower legs flexed to 900 over the short end of the bed. One ankle was attached to a strap and the isometric force of the knee extensors was measured by a strain gauge (Bofors) connected to a d.c. amplifier (Medelec AD6). The output of the amplifier was displayed on an oscilloscope (Medelec M) and recorded on moving U.V.-sensitive paper. Electrical stimulation of the body of human skeletal muscle with surface electrodes has been described elsewhere (Hultman et al. 1981). The stimulation was brought about by square-wave pulses of 0-5 ms duration and by voltage in the range of V (Medelec IS/V stimulator). 20 Hz was used throughout. It has been shown by studying curarized patients that this type of stimulation activates the motor nerve endings in the muscle and not the muscle membranes directly (E. Hultman, H. Sjoholm, I. Jaderholm-Ek & J. Krynichi, unpublished results). The e.m.g. was recorded with surface disks (silver/silver chloride cup electrodes) with a diameter of 10 mm. One electrode was placed over the belly of the contracting quadriceps femoris muscle between the stimulating electrodes. The other electrode was placed over the knee. The subject was earthed by an electrode in an indifferent place. The Medelec system was used for recording with a pre-amplifier (PA 6) and a main a.c. amplifier (AA 6). The e.m.g. amplitude was measured as peak-to-peak of the positive and negative waves. In order to make it possible to record the e.m.g. simultaneously with direct electrical stimulation of the muscle a circuit was constructed to balance off the huge stimulating artifact which otherwise would have masked or distorted the e.m.g. recording. The stimulating artifact is essentially an instantaneous charge with a subsequent exponential discharge of the electrode-skin system. The stimulating pulse was fed into a specially made differentiating R-C circuit where the amplitude and time constant could be changed by variable resistors. The output of the circuit was then inverted and fed into the pre-amplifier for the e.m.g. recording. By observing the e.m.g. signal on the oscilloscope screen in response to single shocks and changing the resistors of the circuit, the pulse passing the compensating R-C circuit could be made a mirror image of the stimulating artifact, so allowing the e.m.g. signal to be recorded almost undisturbed. A schematic drawing of the recording system with the compensating circuit is shown in Fig. 1. Relaxation time was measured as time taken for tension to fall from 95 to 50 % of steady plateau tension after the last stimulus in a train of pulses. An alternative way of measuring the relaxation time was used in some experiments. The output from the strain gauge in response to tension was fed into an a.c. amplifier which differentiated the signal. The derivative was then calibrated against the relaxation time measurement as described above. To calculate the relaxation time the value of the derivative had to be divided by the absolute value of the tension in order to compensate for relaxation from different tension levels and different amplifications of tension.

3 E.M.G. AND CONTRACTION FORCE 35 Voltage Leg stimulator Differential e.m.g. + pre-amplifier Stimulation artifact Compensating Compensating pulse circuit Fig. 1. A schematic drawing ofthe recording system with a compensating circuit generating a compensating pulse with variable amplitude and time constant. Fig. 2. E.m.g. recorded without (top) and with (bottom) the compensatory circuit in response to single direct electrical stimuli to the quadriceps femoris muscle. Vertical and horizontal bars, 5 mv and 10 ms respectively. RESULTS The e.m.g. could be recorded without artifacts from the high-voltage signal by use of the compensating circuit (see Fig. 2). The balance of the circuit had to be adjusted when the voltage of the stimulating impulses was changed. It was observed that the e.m.g. during a continuous electrical stimulation (duration 75 s) of the quadriceps femoris muscle changed continuously, giving a reduction in e.m.g. applitude, a broadening of the signal and a loss of high-frequency components. The changes were progressive during the contraction (see Fig. 3). The force exerted by the quadriceps muscle, measured as knee extension by a strain gauge technique during the 75 s of continuous electrical stimulation at 20 Hz, increased slightly during the first 20 s and decreased thereafter continuously to the 2-2

4 36 E. HULTMAN AND H. SJcHOLM end of the stimulation period. The decrease was parallel with a decrease of the e.m.g. amplitude. In the recovery period the force increased slowly (20% in 30 s) but the e.m.g. signal had already returned to normal within this period. The measurements in the recovery period were based on short tetani lasting 3 s (see Fig. 4). In two subjects it was checked that the reduction in e.m.g. amplitude was not an Y (!IlI pi IVIVI V Fig. 3. E.m.g. at 5, 40 and 75 s during continuous electrical stimulation at 20 Hz of the quadriceps femoris muscle. Vertical and horizontal bars, 5 mv and 50 ms respectively. E.m.g. 08 Force E E x co Time (s) Time (min) Fig. 4. Force and e.m.g. amplitude during and after electrical stimulation for 75 s at 20 Hz of the quadriceps femoris muscle of ten volunteers. Mean +S.D. effect of anoxia as such. Circulatory occlusion was applied for 2 min and e.m.g. was measured during short 3 s tetani at 20 Hz at the beginning and end of the occlusion. In both cases the e.m.g. was unchanged. The measurements of relaxation time were made in two ways. In a first series of experiments relaxation time was measured after progressively longer stimulations of the two legs in four subjects. In a second series of experiments relaxation time was measured during a series of intermittent stimulations each one lasting 6-5 s every 10 s.

5 E.M.G. AND CONTRACTION FORCE Circulatory occlusion was maintained during the whole series of stimulations. The time course of the relaxation time prolongation was the same in the two experimental situations. The relaxation time increased from 40 ms at rest to 130 ms at the end of the stimulation period (Fig. 5). The relation between the restitutions in e.m.g. amplitude, force and relaxation time E aw 80- \ 0 u I Time (s) Fig. 5. Relaxation time of the quadriceps femoris muscle measured after progressively longer stimulation at 20 Hz of the two legs offour volunteers (continuous line). Relaxation time of the quadriceps femoris muscle measured during a series ofintermittent stimulations at 20 Hz, each one lasting 6-5 s, every 10 s. Seven volunteers (interrupted line). Means + S.D. E.m.g. 80- A d Relaxation time 80 c 60/ 40 i Force 1 2 Time (min) Fig. 6. Mean restitutions of e.m.g. amplitude, force and relaxation time in percent after 75 s continuous electrical stimulation at 20 Hz of the quadriceps femoris muscle.

6 38 E. HULTMAN AND H. SJ6HOLM is shown in Fig. 6. The restitution curve for relaxation is taken from Hultman et al. (1981). It is apparent from the Figure that the restitution curves have different time courses, the shortest time being for e.m.g. restitution, followed by relaxation time, while the restitution in force is pronouncedly delayed. DISCUSSION In order to record and follow the e.m.g. simultaneously with standardized direct muscle stimulation it was found necessary to construct an electronic circuit that made it possible to balance off the stimulation artifact. The approach was somewhat similar to the technique of Araki & Otani (1955) for micro-electrodes where recordings of action potentials were possible during continuous electrical stimulation. Since the stimulation artifact was a rapid charge with an exponential decay, an inverted pulse of equal shape could be generated. This may be accomplished in many ways but the circuit had to be provided with variable resistors to make it possible to change the amplitude and time constant of the exponential decay of the compensating pulse, since the charge and discharge of the e.m.g. electrodes will vary from subject to subject. In our system we made use of the stimulating pulse in order to tie the compensating pulse to the frequency of stimulation and to make it coincide with the stimulus. By letting the stimulus pulse pass an R-C filter which also inverted the pulse, the stimulation artifact could be cancelled out by trial and error, looking at the oscilloscope screen when single test stimulations were fired off. As soon as the stimulation intensity was changed a new adjustment of the e.m.g. recording had to be made. The shape of the synchronous mass action potential changes considerably during 75 s stimulation with 20 Hz at a constant voltage. Most notably there was a reduction in amplitude, broadening and loss of high-frequency components. The restitution after stimulation was however rapid and in 30 s the original configuration was nearly completely regained. The change in shape of the synchronous e.m.g. may be a combination of several events. At first there may be a drop out of fast units (Stephens & Taylor, 1972). Units may fire more out of phase of one another, damping and broadening the mass action potential. The conduction velocity in the muscle membrane may change (Jones, 1981). The obvious loss of high-frequency components is most likely a reflexion of the mechanisms underlying the well known shift from high to low in the e.m.g. frequency spectrum concomitant with sustained muscular contractions (Kadefors, Kaiser & Petersen, 1968; Lindstr6m, Kadefors & Petersen, 1977). Most studies have so far been concerned with the relation between e.m.g. amplitude and force during sustained contractions (Milner-Brown & Stein, 1975; Lind & Petrofsky, 1979; Bigland-Ritchie et al. 1979). In this study too there was a very good relation between e.m.g. amplitude and force during fatiguing contractions. However, during recovery the relation was completely lost. This shows that e.m.g. measurements alone as an index of fatigue can be very misleading, since a given e.m.g. amplitude can be recorded in a muscle producing quite different force levels. If the relation between e.m.g. amplitude and force had been looked at only during

7 E.M.G. AND CONTRACTION FORCE the continuous 75 s contraction, the conclusion would have been drawn that excitation failure was the cause of fatigue. But when the separation between force and e.m.g. is so clear in the recovery period it seems that excitation failure can only partly contribute to decline in tension, at least in this experimental situation. The results speak instead in favour of the excitation-contraction mechanism or the contractile machinery as main fatigue-sensitive sites. This is in line with the findings of Edwards, Hill, Jones & Merton (1977a) that stimulation at 20 Hz produced a reduced force up to 24 h after preceding fatiguing contraction. However, when they used 80 Hz the maximum contractile force could be attained. There was evidently a selective change in the excitation-contraction mechanism at low frequencies. One important factor in tension regulation is the relaxation time. During a fatiguing contraction relaxation time was prolonged by %, aiding the maintenance of tension. Had the relaxation time been unchanged throughout, contraction force would more or less have collapsed. During recovery relaxation time quickly returned to normal. This contributes substantially to the fact that tension remains reduced. However, in the first 2 min after a 75s continuous contraction tension actually increases somewhat despite the almost normal relaxation time. This must mean that the contractile force per impulse has increased compared to the end of the preceding fatiguing contraction. In conclusion, muscular fatigue seems to be composed of at least one rapidly reversible stage and one long lasting stage operating in parallel during a fatiguing contraction. The rapidly reversible one could be the summed effect of impaired electrical conduction in the T-tubules and decreased release of Ca2+ from the sacroplasmic reticulum, both dependent on electrolyte shifts and ph changes (Endo, 1977; Gonzales-Serratos, Somlyo, McClellan, Schuman, Borrero & Somlyo, 1978; Bianchi & Narayan, 1982). Also the affinity of Ca2+ and the force development of the contractile filaments are affected by changes in electrolyte composition, ph and energy metabolism (Donaldson, Hermansen & Bolles, 1978; Fabiato & Fabiato, 1978). The long lasting fatigue component persists after the recovery of ph and energy stores (Edwards et al. 1977a) and seems to be an effect of an impaired excitationcontraction mechanism at low frequencies. This, then leads to a changed relation between e.m.g. amplitude and force. The work was supported by grants from the Swedish Medical Research Council (92647) and from the Swedish Work Environment Fund ( ). The authors wish to express their gratitude to Mrs Lillemor Karlsson for excellent technical assistance during the study and to Mrs Ann-Christine Adestam for her skilful execution of the Figures. REFERENCES ARAKI, T. & OTANI, T. (1955). Responses of single motoneurons to direct stimulation in toad's spinal cord. J. Neurophysiol. 18, BIANCHI, C. P. & NARAYAN, S. (1982). Muscle fatigue and the role of transverse tubules. Science, N. Y. 215, BIGLAND-RITCHIE, B., JONES, D. A. & WOODS, J. J. (1979). Excitation frequency and muscle fatigue: electrical responses during human voluntary and stimulated contractions. Expl Neurol. 64,

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