Maximal force, voluntary activation and muscle soreness after eccentric damage to human elbow flexor muscles
1 Prince of Wales Medical Research Institute, University of New South Wales, Sydney, Australia
2 School of Biomedical Sciences, Faculty of Health Sciences, The University of Sydney, Sydney, Australia
Abstract
Muscle damage reduces voluntary force after eccentric exercise but impaired neural drive to the muscle may also contribute. To determine whether the delayed-onset muscle soreness, which develops 1 day after exercise, reduces voluntary activation and to identify the possible site for any reduction, voluntary activation of elbow flexor muscles was examined with both motor cortex and motor nerve stimulation. We measured maximal voluntary isometric torque (MVC), twitch torque, muscle soreness and voluntary activation in eight subjects before, immediately after, 2 h after, 1, 2, 4 and 8 days after eccentric exercise. Motor nerve stimulation and motor cortex stimulation were used to derive twitch torques and measures of voluntary activation. Eccentric exercise immediately reduced the MVC by 38 ± 3% (mean ± S.D., n = 8). The resting twitch produced by motor nerve stimulation fell by 82 ± 6%, and the estimated resting twitch by cortical stimulation fell by 47 ± 15%. While voluntary torque recovered after 8 days, both measures of the resting twitch remained depressed. Muscle tenderness occurred 1–2 days after exercise, and pain during contractions on days 1–4, but changes in voluntary activation did not follow this time course. Voluntary activation assessed with nerve stimulation fell 19 ± 6% immediately after exercise but was not different from control values after 2 days. Voluntary activation assessed by motor cortex stimulation was unchanged by eccentric exercise. During MVCs, absolute increments in torque evoked by nerve and cortical stimulation behaved differently. Those to cortical stimulation decreased whereas those to nerve stimulation tended to increase. These findings suggest that reduced voluntary activation contributes to the early force loss after eccentric exercise, but that it is not due to muscle soreness. The impairment of voluntary activation to nerve stimulation but not motor cortical stimulation suggests that the activation deficit lies in the motor cortex or at a spinal level.
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Introduction
Eccentric exercise lengthens muscle during contraction and damages its muscle fibres. A prolonged reduction in force occurs in animal (e.g. Faulkner et al. 1993; Friden, 2002) and human studies (e.g. Newham et al. 1983, 1987; Howell et al. 1993). Eccentric exercise also leads to muscle soreness and tenderness. Because this develops over many hours and is maximal one to two days after the exercise, it is commonly termed delayed-onset muscle soreness (e.g. Schwane et al. 1983; Ebbeling & Clarkson, 1989; Jones et al. 1989; Clarkson et al. 1992; Cleak & Eston, 1992). This muscle pain is believed to reflect activity in group III and IV muscle afferents (O'Connor & Cook, 1999), although a contribution from muscle spindle afferents has been postulated (Weerakkody et al. 2003). The reduction in maximal force is thought to be secondary to sarcomere ‘popping’ and disorganization (Morgan, 1990), as well as damage to components of the excitation–contraction coupling process (e.g. Warren et al. 1993; Balnave et al. 1997). Under some circumstances sarcolemmal function is affected (Yeung et al. 2003). These peripheral mechanisms have been reviewed (Proske & Morgan, 2001; Warren et al. 2001; Clarkson & Hubal, 2002; Lieber et al. 2002).
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With some forms of exercise, impaired voluntary activation or an inadequate drive to muscle fibres occurs, and such a mechanism could contribute to the prolonged reduction in voluntary force after eccentric exercise (for review see Gandevia, 2001). If interpolation of a stimulus to the motor nerve in a maximal voluntary contraction evokes a twitch-like increment in force, then voluntary activation of the muscle is less than complete. During muscle fatigue produced by sustained or intermittent maximal isometric contractions (e.g. Gandevia et al. 1996; Taylor et al. 2000), and submaximal isometric contractions (e.g. Lloyd et al. 1991; Lscher et al. 1996; Norregaard et al. 1997), interpolated stimuli reveal impaired voluntary activation. In theory, this deficit may reflect net inhibition of motoneurones due to afferent activity, but there may also be a failure to generate sufficient output from the motor cortex (e.g. Gandevia et al. 1996; Herbert & Gandevia, 1996). Under appropriate conditions, transcranial magnetic stimulation of the motor cortex generates superimposed force increments which decline linearly with increasing levels of background voluntary force. This relationship can be used to estimate reliably the size of a ‘resting’ twitch of the elbow flexors, and to assess the amount of extra output available from the motor cortex to increase force (Todd et al. 2003, 2004).
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After eccentric muscle damage, voluntary activation (and hence muscle force) may be reduced as a result of muscle pain and tenderness. Saxton & Donnelly (1996) used a type of twitch interpolation with nerve stimulation during isometric contraction of the elbow flexors in the days after eccentric exercise. They found inconsistent changes in the force added by tetanic stimulation. Using motor cortical stimulation to evoke force increments Lscher & Nordlund (2002) found some impairment of voluntary activation immediately after eccentric exercise, but this recovered within 5 min. Twitch interpolation using nerve stimulation after eccentric exercise of the elbow flexors also revealed an immediate reduction in voluntary activation (Michaut et al. 2002). In the latter two studies it was not possible to separate an acute effect of muscle fatigue from a longer-term effect related to muscle damage.
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Hence, in the present study we aimed to damage the elbow flexor muscles with fatiguing eccentric exercise and generate muscle soreness, and then to follow recovery of maximal voluntary force and voluntary activation over a week. We measured voluntary activation in brief maximal contractions throughout recovery using conventional twitch interpolation with motor nerve stimulation (e.g. Merton, 1954; Herbert & Gandevia, 1996), and we also measured voluntary activation using a new method based on motor cortical stimulation (Todd et al. 2003, 2004). These two types of stimulation provide different information about the limits to voluntary drive to the muscles. However, during fatigue, both forms of stimulation reveal impairments of voluntary activation. This indicates that some of the impairment is due to inadequate cortical output. In the current study, we hypothesized that any impairment in voluntary activation to the muscle would be maximal when muscle soreness peaked, as muscle pain has been reported to reduce cortical excitability (Le Pera et al. 2001). Furthermore, we expected impairment to be evident with both forms of stimulation.
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Methods
Eight healthy subjects (three female and five male) took part in this study. Each gave written informed consent prior to the study that was approved by the institutional ethics committee and conducted according to the Declaration of Helsinki. Subjects had a mean age of 38 ± 12 years, height of 171 ± 9 cm and weight of 69 ± 13 kg. Six subjects were not involved in any kind of exercise of their arm muscles for at least 6 months before the experiment. Two subjects undertook regular weight training.
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A number of measurements were performed before, immediately after, 2 h after, and 1, 2, 4 and 8 days after eccentric exercise. The main assessments included maximal voluntary isometric torque (MVC), and voluntary activation assessed with transcranial magnetic stimulation (TMS) (Todd et al. 2003, 2004) and with nerve stimulation (e.g. Merton, 1954; Herbert & Gandevia, 1996). In addition, we measured the relaxed elbow angle and degree of muscle soreness.
Eccentric exercise
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A bout of controlled eccentric exercise with the elbow flexors of the non-dominant arm was used to reduce maximal voluntary isometric torque by 40%. Subjects sat with the elbow joint aligned with the axis of rotation of a wheel. Subjects lowered a weight attached to the wheel (13–30 kg) from about 130 deg flexion to full extension by eccentric contraction of the elbow flexors. The experimenter lifted the load while subjects relaxed. The load was set at 30% of the predicted maximal eccentric contraction which was estimated as 1.4 times the maximal isometric contraction at 90 deg flexion (see force–velocity relation, Katz, 1939). The exercise consisted of a series of five sets of ten repetitions. After each five sets, subjects performed an isometric MVC. One subject completed only four sets (40 repetitions). The other seven subjects completed between 50 and 350 repetitions before the isometric MVC dropped by 40%. Each eccentric contraction lasted 2 s with 6 s rest between repetitions and 30 s rest between sets. An electronic metronome provided timing clicks to assist subjects to perform each lengthening contraction over 2 s. Before the exercise, subjects practised the timing of contractions with the dominant arm.
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Stimulation and recording
Motor nerve stimulation. For stimulation of the motor nerve, single electrical stimuli (100 μs duration, constant current, DS7, Digitimer) were delivered to intramuscular nerve fibres innervating the biceps brachii via a surface cathode located midway between the anterior edge of the deltoid and the elbow crease, and a surface anode positioned over the distal biceps tendon. The stimulation intensity (77–275 mA) was set at 10% above the level required to produce a resting twitch of maximal amplitude. The stimulus intensity was set at each measurement session. The sites of stimulation were marked on the skin to ensure consistent placement throughout the seven testing sessions.
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Brachial plexus stimulation. For stimulation of the brachial plexus, single stimuli (100 μs duration, constant current, DS7, Digitimer) were delivered to the brachial plexus via a cathode in the supraclavicular fossa, with an anode over the acromion. The stimulation intensity (90–285 mA) was at least 50% above the level required to produce a resting maximal compound muscle action potential (Mmax) in the biceps, brachioradialis and triceps muscles. The stimulus sites were marked on the skin.
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Cortical stimulation. For TMS of the motor cortex, a circular coil (13.5 cm outside diameter, Magstim 200, Magstim Co., Dyfed, UK) was positioned over the vertex to evoke EMG responses (motor evoked potentials, MEPs) and twitch-like increments in torque. The direction of current in the coil preferentially activated the appropriate motor cortex. The stimulator output was set at 45–90% of maximum to produce a large MEP in the biceps of at least 50% of Mmax and only a small MEP in the triceps (maximum amplitude 15% of Mmax) during brief MVCs of the elbow flexor muscles. This stimulus intensity remained constant for all measurements in an individual subject. Before eccentric exercise, the area of MEPs in the biceps during an MVC was 83.8 ± 18.1% of Mmax and in the triceps, 16.2 ± 9.0% of Mmax.
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EMG recording. Electromyographic (EMG) recordings were obtained from pairs of surface electrodes positioned along the middle portion of the muscle belly of the biceps brachii, brachioradialis and triceps brachii. All recording positions were marked on the skin to ensure consistent electrode placement throughout the study. EMG was filtered (16–1000 Hz) and amplified (CED 1902, Cambridge Electronic Design) before sampling (2000 Hz) to computer through a laboratory interface (CED 1401 with Spike 2 software). Flexion torque about the elbow was measured with a myograph (force transducer Xtran linear to 2 kN).
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Maximal isometric flexion torques, voluntary activations, twitch properties and evoked EMG responses
Subjects sat with the arm in a myograph which measured maximal isometric flexion torque at 90 deg of elbow flexion. In each session, subjects performed a series of contractions which included 15 maximal isometric voluntary contractions of 2 s duration with 1–1.5 min rest between MVCs. The sequence of contractions and stimuli depicted in Fig. 1A was repeated five times. Thus, motor nerve stimuli were delivered during and after five MVCs. TMS was delivered during five MVCs and subsequent contractions of 75% and 50% of MVC. Brachial plexus stimulation was delivered during and after the remaining five MVCs and also during contractions of 75% and 50% of MVC. The increments in torque evoked by motor nerve stimulation and by TMS were used to quantify voluntary activation. In addition, EMG responses to TMS (MEPs) and the following inhibition of EMG (silent period) were recorded. As well, the EMG responses to brachial plexus stimuli (Mmax) were measured in the biceps, brachioradialis and triceps.
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A, first, electrical stimulation was delivered to the motor nerve during a 2 s MVC and then after 4 s of rest. Second, transcranial magnetic stimulation of the motor cortex was delivered during a sequence of three contractions: 100% MVC, 75% MVC and 50% MVC. Third, supramaximal stimulation of the brachial plexus was delivered during a similar sequence of three contractions, and also at rest after the MVC. In each session, this measurement sequence was repeated 5 times with rest intervals of 1–1.5 min between all MVCs. Stimulus timing is indicated by the arrows. B, typical twitch torques evoked by motor cortical stimulation during contraction at 100% MVC, 75% MVC and 50% MVC from the control session in a typical subject. C, data from this subject to show linear regression between the twitch torques evoked by motor cortical stimulation and voluntary torque from the control day () and for day 1 after eccentric exercise (). Extrapolation was used to estimate the resting twitch (r2 = 0.98 for the control day and r2 = 0.95 for day 1).
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Maximal voluntary torque was measured during all MVCs, and mean EMG levels were measured prior to the stimuli during the three levels of muscle contraction. For twitch responses, the amplitude, time-to-peak and half-relaxation time were measured.
For electrical stimulation of the motor nerve, any increment in elbow flexion torque evoked during a MVC (‘superimposed twitch’) was expressed as a fraction of the amplitude of the maximal response evoked by the same stimulus in the relaxed muscle immediately after an MVC (‘resting twitch’). Voluntary activation was then quantified as a percentage using the formula:
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Voluntary activation (%) = (1 – a/b) x 100 where a is the superimposed twitch and b is the resting twitch (see Herbert & Gandevia, 1996).
For TMS, the same formula was used to quantify voluntary activation except that the resting twitch was estimated by linear extrapolation of the regression between the superimposed twitch and voluntary torque at 100%, 75% and 50% of MVC (see Todd et al. 2003; Todd et al. 2004). The intercept of the regression with the y axis was taken as the estimated resting twitch (Fig. 1B). The mean values for r2 remained acceptably high at all time points (control, r2 = 0.93; following exercise, r2 ranged from 0.78 to 0.92).
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Relaxed elbow angle
Relaxed elbow angle was recorded at the start of each measurement session while subjects stood with the arm hanging vertically. To ensure that subjects were relaxed, the surface EMG signals were monitored at high gain. In the initial session, points over the middle of the upper third of the humerus, over the lateral epicondyle and over the ulnar styloid process were marked on the skin. In each session, three measurements of the angle made by these points were recorded by using a goniometer.
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Muscle soreness
Muscle soreness and tenderness were measured in two ways. Before any contractions were performed in each session, a force transducer with a circular disc (15 mm-diameter) was applied perpendicular to the skin over four reference parts of the biceps to measure the force at which subjects reported any discomfort or pain. The four marked spots were over the medial and lateral aspects of the middle and distal portions of the muscle. Subjects also located an additional spot that was sore 24 h after the exercise, and it was used for subsequent assessments. For the second method, subjects rated the soreness in their elbow flexor muscles during the final 50% and 100% MVC in each session. They gave a value out of 10 using a modified Borg scale, where ‘0’ represented ‘absolutely no soreness’ and ‘10’ corresponded to ‘the most muscle soreness they could possibly bear’.
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Data analysis
Mean values were derived for all key measurements within each session. Measurements included maximal voluntary isometric torque, resting twitches to nerve stimulation, superimposed twitches from both nerve and cortical stimulation, and evoked EMG responses. Maximal voluntary isometric torque for each subject in each session was normalized to the initial MVC torque before eccentric exercise. The area of MEPs evoked by cortical stimulation was analysed. To account for any activity-dependent changes in muscle fibre action potentials (e.g. Cupido et al. 1996), the area of each MEP was normalized to the average area of Mmax elicited during contractions of the same strength. The silent period (SP) was measured in the biceps muscle by cursor and was taken as the interval from the stimulus to the return of ongoing EMG. Throughout the text, results are given as mean ± S.D. Mean ± S.E.M. is depicted in the figures, except where data from a single subject or all data points are presented. Statistical analysis involved one-way repeated-measures analysis of variance (ANOVA). Post hoc discrimination between means was made with the Student–Newman–Keuls procedure. Statistical significance was set at the 5% level.
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Results
The eccentric exercise protocol reduced the force produced by the elbow flexors, changed the relaxed elbow angle and induced muscle soreness. These changes followed different time courses over the 8 days after the exercise. Twitches evoked by motor nerve stimulation and by motor cortical stimulation were used to assess voluntary activation. Voluntary EMG and EMG responses evoked by supramaximal brachial plexus stimulation (Mmax) and by motor cortex stimulation (MEP) were also measured. Examples are given in Fig. 2.
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A, typical traces from one subject of the resting twitch (longer twitch) and superimposed twitch evoked by motor nerve stimulation (overlaid in upper panels) and superimposed twitch evoked by motor cortical stimulation (lower panels) in the control session (left panels) and day 1 after eccentric exercise (right panels). Calibration bars for the superimposed twitches represent 1 Nm and 20 ms (i.e. these traces are amplified two fold). When the maximal voluntary torque decreased to 60% at day 1, impaired voluntary activation from motor nerve stimulation was decreased as indicated by the twitch responses during MVCs and a marked decrease in the resting twitches. B, traces of motor evoked potentials (MEP, upper panels) evoked by motor cortical stimulation and maximal M-wave (Mmax, lower panels) evoked by brachial plexus stimulation during 100% MVC (left panel). Stimulus timing indicated by arrows. There were no changes in the EMG responses to cortical stimulation or brachial plexus stimulation after eccentric exercise.
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Deficit in force production and changes in relaxed elbow angle
Following eccentric exercise, the maximal voluntary isometric torques dropped to 62 ± 3% (mean ± S.D.) of the initial value (from 54.7 ± 15.5 to 34 ± 8.4 Nm as required by the protocol; see Methods) and gradually improved in the subsequent 8 days (Fig. 3A). The angle of the elbow measured with the arm hanging relaxed changed in the direction of flexion immediately after eccentric exercise, and then gradually returned to normal (Fig. 3B). This involuntary flexion at the elbow was not accompanied by EMG. The maximal change in angle was 12.6 ± 8 deg immediately after exercise.
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Maximal voluntary torque and elbow angle were measured under control conditions (C), immediately after (0), 2 h after (2 h), and days 1, 2, 4 and 8 after eccentric exercise for the group of subjects. The time scale from day 1 is linear. In this and subsequent figures, the vertical hatched area shows the period of exercise, the horizontal line indicates a baseline value, and * indicates a statistically significant difference from control values (P < 0.05). Mean ± S.E.M. (n = 8) is plotted in this and subsequent figures. A, maximal isometric voluntary torque decreased to 60% of the control value immediately after eccentric exercise (as required by the protocol), and then improved gradually over the subsequent 8 days. B, relaxed elbow angle became more flexed immediately after exercise and recovered over 8 days.
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Muscle soreness
A sensitive region to palpation of the muscle was identifiable by day 1 in each subject and checked on subsequent days. The force required to elicit pain at this point was low on days 1 and 2 and gradually recovered (Fig. 4A). This change was focal and not evident uniformly over the muscle. When muscle pain was assessed during voluntary contraction at different intensities (50% and 100% of MVC) with a Borg scale, pain scores were not elevated immediately after exercise but were highest 1–4 days after exercise (Fig. 4B).
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A, group data for the external force required to elicit local pain in the muscle. Data for one spot () identified as tender on day 1 and studied on subsequent days. Pain was prominent on days 1 and 2. The horizontal continuous line and broken lines indicate the mean and 95% confidence interval for the force required to elicit pain at the reference points on the muscle before exercise. B, subjective pain induced in the muscle by voluntary contractions at 50% MVC () and 100%MVC (). Across contraction intensities from 50% to 100% MVC, muscle pain was most intense 1–4 days after the exercise and recovered after 8 days. A score of 2 is described as ‘mild’.
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Changes in twitch properties
While maximal voluntary isometric torque had dropped by 38% immediately after exercise (Fig. 3A), the resting twitch produced by motor nerve stimulation had decreased by 82% (from 6.1 ± 1.5 to 1.1 ± 0.3 Nm; Figs 2A and 5A). After 8 days, the resting twitch remained depressed by 43% (3.3 ± 0.7 Nm, P < 0.001).
A, group data for twitch torque for biceps measured from motor nerve stimulation under resting conditions (resting twitch, ). Twitch torque from elbow flexor muscles estimated using TMS (; see Methods). Twitch torques produced by nerve stimulation were depressed more than the MVC after eccentric exercise (compare Fig. 3A). S.E.M.s are smaller than the symbol size for some . B, time-to peak value for the resting potentiated twitch of biceps evoked by nerve stimulation () increased slightly at day 2–8 and the half-relaxation time () decreased immediately after exercise.
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Changes in the time course of the twitch following eccentric exercise were small. Immediately after exercise the half-relaxation time declined significantly by 39% (from 68 ± 17.7 to 41.3 ± 22.2 ms) (Fig. 5B) but then recovered. However, the time to peak was slightly, but significantly, longer on day 2 and remained lengthened thereafter.
The size of the ‘resting’ twitch for all elbow flexor muscles was estimated using TMS of the motor cortex (see Methods). This technique provides an estimate of the force-generating capacity of all the elbow flexor muscles (Todd et al. 2003). This decreased by 47% from 12 ± 3 to 6.2 ± 2 Nm immediately after eccentric exercise, and was not completely recovered at day 8 (Fig. 5A). Changes in the estimated resting twitch paralleled changes in the maximal voluntary torque (Fig. 3A).
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Voluntary activation
When assessed the conventional way using motor nerve stimulation, voluntary activation of the elbow flexors decreased by 19% (from 97.3 ± 1.4 to 78.5 ± 6.5%) immediately after exercise, with some recovery at 2 and 24 h (P < 0.001, Fig. 6). However, when assessed with TMS of the motor cortex and using the usual equation (see Methods), there was a trend for voluntary activation to decline immediately after exercise, but this was not statistically significant. Comparison of the two measures of voluntary activation should be made with care (Todd et al. 2003), because the resting twitch to which the superimposed twitches are normalized (see Methods) behaved differently after exercise (Fig. 5A). The resting twitch to nerve stimulation was depressed by eccentric exercise more than maximal voluntary torque (Fig. 3A), and more than the twitch response estimated with motor cortical stimulation during voluntary contractions. Thus, the force generated by a single stimulus is differentially impaired compared to that generated by repetitive activation of the muscle. This may make the resting twitch to motor nerve stimulation inappropriate for normalization. To circumvent this difficulty, the absolute sizes of the responses to motor nerve stimulation and to motor cortical stimulation during MVC are plotted in Fig. 7A. After eccentric exercise, the superimposed responses to motor nerve stimulation did not significantly change, whereas the superimposed responses to motor cortical stimulation showed some depression (P = 0.002 at 2 h and P = 0.006 at day 8). The size of superimposed twitches from motor nerve stimulation did not correlate with the size of superimposed twitches from motor cortical stimulation (r2 = 0.01). Relative to their initial control sizes, responses to cortical stimulation were small compared to those to nerve stimulation (Fig. 7B). Hence, after exercise, superimposed twitches to nerve stimulation clustered to the right of the line of identity (sign test P < 0.01).
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Voluntary activation calculated from motor nerve stimulation () decreased by 23% immediately after eccentric exercise, and remained significantly decreased for 24 h. The time course of this reduction differed from the time course of muscle pain and tenderness, which peaked at day 1–2 (see Fig. 4). Voluntary activation calculated from motor cortex stimulation () did not change significantly after eccentric exercise.
A, group data for superimposed responses to motor nerve stimulation during MVCs () and for superimposed responses to cortical stimulation during MVCs (). Superimposed twitch torques evoked by nerve stimulation during MVCs did not significantly change after eccentric exercise. Superimposed twitch torques evoked by motor cortex stimulation during MVCs were larger and decreased significantly at 2 h after exercise and at day 8. B, for each subject, the mean of sizes of superimposed twitches evoked by nerve stimulation are plotted against those evoked by motor cortical stimulation in the same measurement sessions. Data for different times are shown using different symbols. Values are expressed relative to control data obtained before exercise. A line of identity is shown.
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EMG responses to brachial plexus and motor cortical stimulation
The area of the maximal compound muscle action potential (Mmax) measured in the relaxed biceps (0.10 ± 0.05 mVs), brachioradialis (0.06 ± 0.03 mVs) and triceps (0.07 ± 0.03 mVs) was unchanged by exercise. The amplitude of Mmax was also unchanged (13.1 ± 13.6 mV for the biceps). The area of the MEPs evoked during 50%, 75% and 100% MVC and expressed relative to Mmax in the biceps and brachioradialis did not change after eccentric exercise. There was no change in the MEP of the antagonist muscle, triceps. The length of the silent periods after cortical stimulation during MVCs was 110 ms in the biceps and brachioradialis. There were no changes in the duration of silent periods in either muscle at any level of contraction after exercise.
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Relationship between EMG and torque
As there were no changes in Mmax, the mean level of EMG was compared for the three contraction levels (50%, 75% and 100%MVC) and is shown in Fig. 8. Prior to eccentric exercise, an EMG level of 54.5 ± 9.3% maximum was required to produce a torque of 50% MVC. Immediately after exercise, this level increased to 88.8 ± 7.2% maximum, and returned to pre-exercise levels after a week.
Mean levels of EMG required to produce 50%, 75% and 100% MVC are shown. Data for different times after exercise are shown using different symbols. As force-generating capacity recovered, there was a gradual reduction in the relative level of EMG required to generate 50% MVC.
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Discussion
Our eccentric exercise produced a target reduction of 40% in MVC of the elbow flexors. Maximal voluntary torque showed little improvement until 48 h after exercise, with slow recovery towards control values over the next week. Such prolonged recovery has been described by others (e.g. Newham et al. 1983; Jones et al. 1986; Howell et al. 1993; Saxton & Donnelly, 1996; Sayers et al. 2003; Weerakkody et al. 2003). The exercised muscles were shortened (i.e. flexed) immediately after exercise (Howell et al. 1993; Weerakkody et al. 2003), and this occurred in the absence of elbow flexor EMG. However, muscle soreness was not present initially, but developed within 24 h, as measured by tenderness in the relaxed muscle (e.g. Schwane et al. 1983; Jones et al. 1986; Ebbeling & Clarkson, 1989; Clarkson et al. 1992; Howell et al. 1993; Weerakkody et al. 2003) and also by pain evoked by voluntary contractions. The pain did not increase with stronger contractions, and was similar for contractions of 50% and 100% MVC. Eccentric exercise produced some profound changes in peripheral force production, and unexpected changes in estimates of voluntary activation of the elbow flexors. These changes will be considered in turn, along with the accompanying EMG changes.
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After eccentric exercise, the resting twitch produced by stimulation of the biceps motor nerve was reduced by more than 75%. This reduction showed little change over the first two hours of recovery, and even after a week, the twitches were less than half their pre-exercise values. The magnitude of this prolonged reduction in twitch force is greater than previously observed (see Table 3 in Sayers et al. 2003). When cortical stimulation was used to estimate the size of the resting twitch of the combined elbow flexor muscles (Todd et al. 2003, 2004), again there was a reduction, but this was of smaller magnitude than when biceps motor nerve stimulation was used. Hence, the changes in the estimated resting twitch more closely matched the changes in maximal voluntary force than the changes in the twitch evoked by nerve stimulation. Altered excitation of the sarcolemma is unlikely to have caused the reduction in twitch amplitude, because the maximal M-wave showed no significant change after exercise (cf. Sayers et al. 2003). A likely explanation for these changes is a rapid and prolonged impairment in excitation–contraction coupling. This is consistent with animal studies. Eccentric exercise disrupts the T-tubule network immediately after downhill running in rats (e.g. Takekura et al. 2001). The increase in intracellular Ca2+ concentration during tetanic stimulation is decreased immediately after eccentric damage (Balnave & Allen, 1995). Furthermore, the maximal Ca2+-activated force is reduced less than the force produced by tetanic stimulation, particularly when the eccentric exercise protocol is severe (Warren et al. 1994; Balnave & Allen, 1995). That is, contraction can occur when Ca2+ is provided, but the link between excitation of the sarcolemma and release of Ca2+ is disrupted.
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A second contribution to the changes in contractile force after exercise may involve changes in the length–tension relation of the elbow flexors. There is an acute shift immediately after eccentric exercise, towards longer lengths for the peak of this relation for a twitch contraction (Saxton & Donnelly, 1996; Jones et al. 1997). This reflects focal lengthening and disruption of occasional sarcomeres (Proske & Morgan, 2001), so that overall muscle length must be increased beyond the original optimum to produce the same myofilament overlap in undamaged sarcomeres. Some studies in animals (Lynn & Morgan, 1994) and humans (Brockett et al. 2001) suggest that incorporation of new sarcomeres in series produces a sustained shift to longer lengths in the length–tension relationship. Presumably changes in both excitation–contraction coupling and the length–tension relation underlie the prolonged reduction in the twitch after eccentric damage in the present study. The relative contribution of the two effects is difficult to determine because we assessed forces only at 90 deg of elbow flexion, an angle close to the usual optimum for maximal voluntary forces. However, a recent study suggests that for voluntary forces the shift in the length–tension relation after eccentric damage of human elbow flexors may explain only a modest part of our observed changes (Philippou et al. 2004).
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Changes in force-generating capacity after eccentric exercise altered neural drive to the elbow flexor muscles during submaximal contractions. The near-linear relation between force and EMG became flatter immediately after eccentric exercise, so that almost 90% of maximal voluntary EMG was needed to generate a 50% MVC. This distortion recovered progressively over the following week. One explanation is that the motor units used to lower the load during the eccentric exercise were damaged so that they generated much less force although their sarcolemmal activation was preserved (i.e. there was EMG but little force). Changes in the length–tension relation for motor units firing at physiological frequencies will also affect this force–EMG relation, as may changes in motor unit synchronization (e.g. Yao et al. 2000). A surprising finding is that MEPs recorded during 50% MVCs did not change in size. In undamaged biceps, MEP size increases with the increasing strength of voluntary contractions up to 50% MVC, and then decreases with stronger contractions (Todd et al. 2003). This decrease probably reflects increased motoneurone firing rates. Thus, after eccentric exercise, the lack of decrease in the MEP suggests that mechanisms other than firing rates may be important in increasing background EMG.
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Maximal voluntary activation assessed using conventional twitch interpolation with motor nerve stimulation was diminished immediately after exercise and had largely, but not completely, recovered after 24 h. This time course did not parallel estimates of muscle pain which peaked 1–2 days after exercise. Maximal voluntary activation assessed with motor cortical stimulation showed little impairment, and did not correlate with measurements of muscle pain. Previous comparative measurements of voluntary activation using motor nerve and cortical stimulation have shown that voluntary activation measured with nerve stimulation was similar to, or higher than, when measured with cortical stimulation (Todd et al. 2003). Furthermore, during fatiguing isometric exercise, progressively impaired voluntary activation (or central fatigue) was demonstrated by both nerve and cortical stimulation (e.g. Gandevia et al. 1996). The findings of Todd et al. (2003) suggest that output from neither the motor cortex nor from the motoneurones is fully engaged during maximal efforts of non-fatigued muscle. That is, some contribution to the failure to drive the muscle fully comes from a failure to drive the motor cortex to generate output. Similarly, during fatiguing isometric exercise some central fatigue is due to impairment ‘upstream’ of motor cortical output. This was not the case after eccentric exercise. We considered whether the disparity in the measurements of voluntary activation with nerve and cortical stimulation might simply reflect differences in the resting twitch contractions used to calculate voluntary activation: the twitch force evoked by nerve stimulation was depressed more than that estimated by cortical stimulation. However, this difference is not the full explanation because superimposed twitches to cortical stimulation declined after eccentric exercise, whereas those to nerve stimulation showed no significant change but tended to increase. Compared to the superimposed twitches during MVCs with fresh muscles, the relative size of superimposed twitches to cortical stimulation was 70% of control after eccentric exercise, whereas that to nerve stimulation increased to 200% of control (Fig. 7B). A possible explanation for this behaviour is that although some motoneurones were not recruited or not firing fast enough to produce maximal muscle force and the axons of these motoneurones could be activated by nerve stimulation, motor cortical stimulation failed to activate them synaptically. One possibility is that TMS did not evoke extra output from the cortex. Another is that any such output failed to activate the motoneurones. This would imply that despite maximal voluntary effort, some inhibition or disfacilitation occurred at the level of motor cortex or motoneurones. Furthermore, in contrast to what happens during muscle fatigue, failure to drive the motor cortex to use all available output did not contribute to poor voluntary activation after eccentric exercise.
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The current study cannot determine the specific mechanism of reduced voluntary activation after eccentric exercise, it can only localize a change in the motor pathway to somewhere between the sites of stimulation at the motor cortex and motor axons. Changes either in afferent discharge or in generation of descending drive could underlie the effects on the motor pathway. We postulated that the muscle soreness that develops after eccentric exercise might impair voluntary activation. As acute muscle pain can reduce the size of MEPs in the resting muscle, pain may inhibit the motor cortex (Le Pera et al. 2001). The firing of group III and IV muscle afferents has also been linked to poor voluntary activation (Gandevia et al. 1996). However, the different time course of muscle soreness after eccentric exercise and changes in voluntary activation make it unlikely that muscle pain directly causes the changes in voluntary drive.
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In summary, eccentric exercise of human elbow flexors produces a marked and long-lasting reduction in voluntary torque. The prolonged decrease in the size of the resting twitch from motor nerve stimulation confirms that much of the loss of force occurs through muscle damage. The lack of change in the maximal M-wave points to major defects in excitation–contraction coupling, although a contribution from altered length–tension characteristics cannot be excluded. When measured with motor nerve stimulation, voluntary activation is impaired and must contribute to the early loss of maximal voluntary torque. However, we failed to show an association between the later muscle soreness and impaired voluntary drive. When measured with motor cortical stimulation, voluntary activation was not impaired. The disparate results of motor nerve and motor cortical stimulation suggest that inhibition at the motor cortex and/or the motoneurones limits voluntary drive to the muscle in the first 24 h after eccentric exercise.
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2 School of Biomedical Sciences, Faculty of Health Sciences, The University of Sydney, Sydney, Australia
Abstract
Muscle damage reduces voluntary force after eccentric exercise but impaired neural drive to the muscle may also contribute. To determine whether the delayed-onset muscle soreness, which develops 1 day after exercise, reduces voluntary activation and to identify the possible site for any reduction, voluntary activation of elbow flexor muscles was examined with both motor cortex and motor nerve stimulation. We measured maximal voluntary isometric torque (MVC), twitch torque, muscle soreness and voluntary activation in eight subjects before, immediately after, 2 h after, 1, 2, 4 and 8 days after eccentric exercise. Motor nerve stimulation and motor cortex stimulation were used to derive twitch torques and measures of voluntary activation. Eccentric exercise immediately reduced the MVC by 38 ± 3% (mean ± S.D., n = 8). The resting twitch produced by motor nerve stimulation fell by 82 ± 6%, and the estimated resting twitch by cortical stimulation fell by 47 ± 15%. While voluntary torque recovered after 8 days, both measures of the resting twitch remained depressed. Muscle tenderness occurred 1–2 days after exercise, and pain during contractions on days 1–4, but changes in voluntary activation did not follow this time course. Voluntary activation assessed with nerve stimulation fell 19 ± 6% immediately after exercise but was not different from control values after 2 days. Voluntary activation assessed by motor cortex stimulation was unchanged by eccentric exercise. During MVCs, absolute increments in torque evoked by nerve and cortical stimulation behaved differently. Those to cortical stimulation decreased whereas those to nerve stimulation tended to increase. These findings suggest that reduced voluntary activation contributes to the early force loss after eccentric exercise, but that it is not due to muscle soreness. The impairment of voluntary activation to nerve stimulation but not motor cortical stimulation suggests that the activation deficit lies in the motor cortex or at a spinal level.
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Introduction
Eccentric exercise lengthens muscle during contraction and damages its muscle fibres. A prolonged reduction in force occurs in animal (e.g. Faulkner et al. 1993; Friden, 2002) and human studies (e.g. Newham et al. 1983, 1987; Howell et al. 1993). Eccentric exercise also leads to muscle soreness and tenderness. Because this develops over many hours and is maximal one to two days after the exercise, it is commonly termed delayed-onset muscle soreness (e.g. Schwane et al. 1983; Ebbeling & Clarkson, 1989; Jones et al. 1989; Clarkson et al. 1992; Cleak & Eston, 1992). This muscle pain is believed to reflect activity in group III and IV muscle afferents (O'Connor & Cook, 1999), although a contribution from muscle spindle afferents has been postulated (Weerakkody et al. 2003). The reduction in maximal force is thought to be secondary to sarcomere ‘popping’ and disorganization (Morgan, 1990), as well as damage to components of the excitation–contraction coupling process (e.g. Warren et al. 1993; Balnave et al. 1997). Under some circumstances sarcolemmal function is affected (Yeung et al. 2003). These peripheral mechanisms have been reviewed (Proske & Morgan, 2001; Warren et al. 2001; Clarkson & Hubal, 2002; Lieber et al. 2002).
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With some forms of exercise, impaired voluntary activation or an inadequate drive to muscle fibres occurs, and such a mechanism could contribute to the prolonged reduction in voluntary force after eccentric exercise (for review see Gandevia, 2001). If interpolation of a stimulus to the motor nerve in a maximal voluntary contraction evokes a twitch-like increment in force, then voluntary activation of the muscle is less than complete. During muscle fatigue produced by sustained or intermittent maximal isometric contractions (e.g. Gandevia et al. 1996; Taylor et al. 2000), and submaximal isometric contractions (e.g. Lloyd et al. 1991; Lscher et al. 1996; Norregaard et al. 1997), interpolated stimuli reveal impaired voluntary activation. In theory, this deficit may reflect net inhibition of motoneurones due to afferent activity, but there may also be a failure to generate sufficient output from the motor cortex (e.g. Gandevia et al. 1996; Herbert & Gandevia, 1996). Under appropriate conditions, transcranial magnetic stimulation of the motor cortex generates superimposed force increments which decline linearly with increasing levels of background voluntary force. This relationship can be used to estimate reliably the size of a ‘resting’ twitch of the elbow flexors, and to assess the amount of extra output available from the motor cortex to increase force (Todd et al. 2003, 2004).
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After eccentric muscle damage, voluntary activation (and hence muscle force) may be reduced as a result of muscle pain and tenderness. Saxton & Donnelly (1996) used a type of twitch interpolation with nerve stimulation during isometric contraction of the elbow flexors in the days after eccentric exercise. They found inconsistent changes in the force added by tetanic stimulation. Using motor cortical stimulation to evoke force increments Lscher & Nordlund (2002) found some impairment of voluntary activation immediately after eccentric exercise, but this recovered within 5 min. Twitch interpolation using nerve stimulation after eccentric exercise of the elbow flexors also revealed an immediate reduction in voluntary activation (Michaut et al. 2002). In the latter two studies it was not possible to separate an acute effect of muscle fatigue from a longer-term effect related to muscle damage.
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Hence, in the present study we aimed to damage the elbow flexor muscles with fatiguing eccentric exercise and generate muscle soreness, and then to follow recovery of maximal voluntary force and voluntary activation over a week. We measured voluntary activation in brief maximal contractions throughout recovery using conventional twitch interpolation with motor nerve stimulation (e.g. Merton, 1954; Herbert & Gandevia, 1996), and we also measured voluntary activation using a new method based on motor cortical stimulation (Todd et al. 2003, 2004). These two types of stimulation provide different information about the limits to voluntary drive to the muscles. However, during fatigue, both forms of stimulation reveal impairments of voluntary activation. This indicates that some of the impairment is due to inadequate cortical output. In the current study, we hypothesized that any impairment in voluntary activation to the muscle would be maximal when muscle soreness peaked, as muscle pain has been reported to reduce cortical excitability (Le Pera et al. 2001). Furthermore, we expected impairment to be evident with both forms of stimulation.
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Methods
Eight healthy subjects (three female and five male) took part in this study. Each gave written informed consent prior to the study that was approved by the institutional ethics committee and conducted according to the Declaration of Helsinki. Subjects had a mean age of 38 ± 12 years, height of 171 ± 9 cm and weight of 69 ± 13 kg. Six subjects were not involved in any kind of exercise of their arm muscles for at least 6 months before the experiment. Two subjects undertook regular weight training.
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A number of measurements were performed before, immediately after, 2 h after, and 1, 2, 4 and 8 days after eccentric exercise. The main assessments included maximal voluntary isometric torque (MVC), and voluntary activation assessed with transcranial magnetic stimulation (TMS) (Todd et al. 2003, 2004) and with nerve stimulation (e.g. Merton, 1954; Herbert & Gandevia, 1996). In addition, we measured the relaxed elbow angle and degree of muscle soreness.
Eccentric exercise
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A bout of controlled eccentric exercise with the elbow flexors of the non-dominant arm was used to reduce maximal voluntary isometric torque by 40%. Subjects sat with the elbow joint aligned with the axis of rotation of a wheel. Subjects lowered a weight attached to the wheel (13–30 kg) from about 130 deg flexion to full extension by eccentric contraction of the elbow flexors. The experimenter lifted the load while subjects relaxed. The load was set at 30% of the predicted maximal eccentric contraction which was estimated as 1.4 times the maximal isometric contraction at 90 deg flexion (see force–velocity relation, Katz, 1939). The exercise consisted of a series of five sets of ten repetitions. After each five sets, subjects performed an isometric MVC. One subject completed only four sets (40 repetitions). The other seven subjects completed between 50 and 350 repetitions before the isometric MVC dropped by 40%. Each eccentric contraction lasted 2 s with 6 s rest between repetitions and 30 s rest between sets. An electronic metronome provided timing clicks to assist subjects to perform each lengthening contraction over 2 s. Before the exercise, subjects practised the timing of contractions with the dominant arm.
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Stimulation and recording
Motor nerve stimulation. For stimulation of the motor nerve, single electrical stimuli (100 μs duration, constant current, DS7, Digitimer) were delivered to intramuscular nerve fibres innervating the biceps brachii via a surface cathode located midway between the anterior edge of the deltoid and the elbow crease, and a surface anode positioned over the distal biceps tendon. The stimulation intensity (77–275 mA) was set at 10% above the level required to produce a resting twitch of maximal amplitude. The stimulus intensity was set at each measurement session. The sites of stimulation were marked on the skin to ensure consistent placement throughout the seven testing sessions.
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Brachial plexus stimulation. For stimulation of the brachial plexus, single stimuli (100 μs duration, constant current, DS7, Digitimer) were delivered to the brachial plexus via a cathode in the supraclavicular fossa, with an anode over the acromion. The stimulation intensity (90–285 mA) was at least 50% above the level required to produce a resting maximal compound muscle action potential (Mmax) in the biceps, brachioradialis and triceps muscles. The stimulus sites were marked on the skin.
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Cortical stimulation. For TMS of the motor cortex, a circular coil (13.5 cm outside diameter, Magstim 200, Magstim Co., Dyfed, UK) was positioned over the vertex to evoke EMG responses (motor evoked potentials, MEPs) and twitch-like increments in torque. The direction of current in the coil preferentially activated the appropriate motor cortex. The stimulator output was set at 45–90% of maximum to produce a large MEP in the biceps of at least 50% of Mmax and only a small MEP in the triceps (maximum amplitude 15% of Mmax) during brief MVCs of the elbow flexor muscles. This stimulus intensity remained constant for all measurements in an individual subject. Before eccentric exercise, the area of MEPs in the biceps during an MVC was 83.8 ± 18.1% of Mmax and in the triceps, 16.2 ± 9.0% of Mmax.
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EMG recording. Electromyographic (EMG) recordings were obtained from pairs of surface electrodes positioned along the middle portion of the muscle belly of the biceps brachii, brachioradialis and triceps brachii. All recording positions were marked on the skin to ensure consistent electrode placement throughout the study. EMG was filtered (16–1000 Hz) and amplified (CED 1902, Cambridge Electronic Design) before sampling (2000 Hz) to computer through a laboratory interface (CED 1401 with Spike 2 software). Flexion torque about the elbow was measured with a myograph (force transducer Xtran linear to 2 kN).
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Maximal isometric flexion torques, voluntary activations, twitch properties and evoked EMG responses
Subjects sat with the arm in a myograph which measured maximal isometric flexion torque at 90 deg of elbow flexion. In each session, subjects performed a series of contractions which included 15 maximal isometric voluntary contractions of 2 s duration with 1–1.5 min rest between MVCs. The sequence of contractions and stimuli depicted in Fig. 1A was repeated five times. Thus, motor nerve stimuli were delivered during and after five MVCs. TMS was delivered during five MVCs and subsequent contractions of 75% and 50% of MVC. Brachial plexus stimulation was delivered during and after the remaining five MVCs and also during contractions of 75% and 50% of MVC. The increments in torque evoked by motor nerve stimulation and by TMS were used to quantify voluntary activation. In addition, EMG responses to TMS (MEPs) and the following inhibition of EMG (silent period) were recorded. As well, the EMG responses to brachial plexus stimuli (Mmax) were measured in the biceps, brachioradialis and triceps.
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A, first, electrical stimulation was delivered to the motor nerve during a 2 s MVC and then after 4 s of rest. Second, transcranial magnetic stimulation of the motor cortex was delivered during a sequence of three contractions: 100% MVC, 75% MVC and 50% MVC. Third, supramaximal stimulation of the brachial plexus was delivered during a similar sequence of three contractions, and also at rest after the MVC. In each session, this measurement sequence was repeated 5 times with rest intervals of 1–1.5 min between all MVCs. Stimulus timing is indicated by the arrows. B, typical twitch torques evoked by motor cortical stimulation during contraction at 100% MVC, 75% MVC and 50% MVC from the control session in a typical subject. C, data from this subject to show linear regression between the twitch torques evoked by motor cortical stimulation and voluntary torque from the control day () and for day 1 after eccentric exercise (). Extrapolation was used to estimate the resting twitch (r2 = 0.98 for the control day and r2 = 0.95 for day 1).
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Maximal voluntary torque was measured during all MVCs, and mean EMG levels were measured prior to the stimuli during the three levels of muscle contraction. For twitch responses, the amplitude, time-to-peak and half-relaxation time were measured.
For electrical stimulation of the motor nerve, any increment in elbow flexion torque evoked during a MVC (‘superimposed twitch’) was expressed as a fraction of the amplitude of the maximal response evoked by the same stimulus in the relaxed muscle immediately after an MVC (‘resting twitch’). Voluntary activation was then quantified as a percentage using the formula:
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Voluntary activation (%) = (1 – a/b) x 100 where a is the superimposed twitch and b is the resting twitch (see Herbert & Gandevia, 1996).
For TMS, the same formula was used to quantify voluntary activation except that the resting twitch was estimated by linear extrapolation of the regression between the superimposed twitch and voluntary torque at 100%, 75% and 50% of MVC (see Todd et al. 2003; Todd et al. 2004). The intercept of the regression with the y axis was taken as the estimated resting twitch (Fig. 1B). The mean values for r2 remained acceptably high at all time points (control, r2 = 0.93; following exercise, r2 ranged from 0.78 to 0.92).
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Relaxed elbow angle
Relaxed elbow angle was recorded at the start of each measurement session while subjects stood with the arm hanging vertically. To ensure that subjects were relaxed, the surface EMG signals were monitored at high gain. In the initial session, points over the middle of the upper third of the humerus, over the lateral epicondyle and over the ulnar styloid process were marked on the skin. In each session, three measurements of the angle made by these points were recorded by using a goniometer.
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Muscle soreness
Muscle soreness and tenderness were measured in two ways. Before any contractions were performed in each session, a force transducer with a circular disc (15 mm-diameter) was applied perpendicular to the skin over four reference parts of the biceps to measure the force at which subjects reported any discomfort or pain. The four marked spots were over the medial and lateral aspects of the middle and distal portions of the muscle. Subjects also located an additional spot that was sore 24 h after the exercise, and it was used for subsequent assessments. For the second method, subjects rated the soreness in their elbow flexor muscles during the final 50% and 100% MVC in each session. They gave a value out of 10 using a modified Borg scale, where ‘0’ represented ‘absolutely no soreness’ and ‘10’ corresponded to ‘the most muscle soreness they could possibly bear’.
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Data analysis
Mean values were derived for all key measurements within each session. Measurements included maximal voluntary isometric torque, resting twitches to nerve stimulation, superimposed twitches from both nerve and cortical stimulation, and evoked EMG responses. Maximal voluntary isometric torque for each subject in each session was normalized to the initial MVC torque before eccentric exercise. The area of MEPs evoked by cortical stimulation was analysed. To account for any activity-dependent changes in muscle fibre action potentials (e.g. Cupido et al. 1996), the area of each MEP was normalized to the average area of Mmax elicited during contractions of the same strength. The silent period (SP) was measured in the biceps muscle by cursor and was taken as the interval from the stimulus to the return of ongoing EMG. Throughout the text, results are given as mean ± S.D. Mean ± S.E.M. is depicted in the figures, except where data from a single subject or all data points are presented. Statistical analysis involved one-way repeated-measures analysis of variance (ANOVA). Post hoc discrimination between means was made with the Student–Newman–Keuls procedure. Statistical significance was set at the 5% level.
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Results
The eccentric exercise protocol reduced the force produced by the elbow flexors, changed the relaxed elbow angle and induced muscle soreness. These changes followed different time courses over the 8 days after the exercise. Twitches evoked by motor nerve stimulation and by motor cortical stimulation were used to assess voluntary activation. Voluntary EMG and EMG responses evoked by supramaximal brachial plexus stimulation (Mmax) and by motor cortex stimulation (MEP) were also measured. Examples are given in Fig. 2.
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A, typical traces from one subject of the resting twitch (longer twitch) and superimposed twitch evoked by motor nerve stimulation (overlaid in upper panels) and superimposed twitch evoked by motor cortical stimulation (lower panels) in the control session (left panels) and day 1 after eccentric exercise (right panels). Calibration bars for the superimposed twitches represent 1 Nm and 20 ms (i.e. these traces are amplified two fold). When the maximal voluntary torque decreased to 60% at day 1, impaired voluntary activation from motor nerve stimulation was decreased as indicated by the twitch responses during MVCs and a marked decrease in the resting twitches. B, traces of motor evoked potentials (MEP, upper panels) evoked by motor cortical stimulation and maximal M-wave (Mmax, lower panels) evoked by brachial plexus stimulation during 100% MVC (left panel). Stimulus timing indicated by arrows. There were no changes in the EMG responses to cortical stimulation or brachial plexus stimulation after eccentric exercise.
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Deficit in force production and changes in relaxed elbow angle
Following eccentric exercise, the maximal voluntary isometric torques dropped to 62 ± 3% (mean ± S.D.) of the initial value (from 54.7 ± 15.5 to 34 ± 8.4 Nm as required by the protocol; see Methods) and gradually improved in the subsequent 8 days (Fig. 3A). The angle of the elbow measured with the arm hanging relaxed changed in the direction of flexion immediately after eccentric exercise, and then gradually returned to normal (Fig. 3B). This involuntary flexion at the elbow was not accompanied by EMG. The maximal change in angle was 12.6 ± 8 deg immediately after exercise.
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Maximal voluntary torque and elbow angle were measured under control conditions (C), immediately after (0), 2 h after (2 h), and days 1, 2, 4 and 8 after eccentric exercise for the group of subjects. The time scale from day 1 is linear. In this and subsequent figures, the vertical hatched area shows the period of exercise, the horizontal line indicates a baseline value, and * indicates a statistically significant difference from control values (P < 0.05). Mean ± S.E.M. (n = 8) is plotted in this and subsequent figures. A, maximal isometric voluntary torque decreased to 60% of the control value immediately after eccentric exercise (as required by the protocol), and then improved gradually over the subsequent 8 days. B, relaxed elbow angle became more flexed immediately after exercise and recovered over 8 days.
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Muscle soreness
A sensitive region to palpation of the muscle was identifiable by day 1 in each subject and checked on subsequent days. The force required to elicit pain at this point was low on days 1 and 2 and gradually recovered (Fig. 4A). This change was focal and not evident uniformly over the muscle. When muscle pain was assessed during voluntary contraction at different intensities (50% and 100% of MVC) with a Borg scale, pain scores were not elevated immediately after exercise but were highest 1–4 days after exercise (Fig. 4B).
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A, group data for the external force required to elicit local pain in the muscle. Data for one spot () identified as tender on day 1 and studied on subsequent days. Pain was prominent on days 1 and 2. The horizontal continuous line and broken lines indicate the mean and 95% confidence interval for the force required to elicit pain at the reference points on the muscle before exercise. B, subjective pain induced in the muscle by voluntary contractions at 50% MVC () and 100%MVC (). Across contraction intensities from 50% to 100% MVC, muscle pain was most intense 1–4 days after the exercise and recovered after 8 days. A score of 2 is described as ‘mild’.
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Changes in twitch properties
While maximal voluntary isometric torque had dropped by 38% immediately after exercise (Fig. 3A), the resting twitch produced by motor nerve stimulation had decreased by 82% (from 6.1 ± 1.5 to 1.1 ± 0.3 Nm; Figs 2A and 5A). After 8 days, the resting twitch remained depressed by 43% (3.3 ± 0.7 Nm, P < 0.001).
A, group data for twitch torque for biceps measured from motor nerve stimulation under resting conditions (resting twitch, ). Twitch torque from elbow flexor muscles estimated using TMS (; see Methods). Twitch torques produced by nerve stimulation were depressed more than the MVC after eccentric exercise (compare Fig. 3A). S.E.M.s are smaller than the symbol size for some . B, time-to peak value for the resting potentiated twitch of biceps evoked by nerve stimulation () increased slightly at day 2–8 and the half-relaxation time () decreased immediately after exercise.
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Changes in the time course of the twitch following eccentric exercise were small. Immediately after exercise the half-relaxation time declined significantly by 39% (from 68 ± 17.7 to 41.3 ± 22.2 ms) (Fig. 5B) but then recovered. However, the time to peak was slightly, but significantly, longer on day 2 and remained lengthened thereafter.
The size of the ‘resting’ twitch for all elbow flexor muscles was estimated using TMS of the motor cortex (see Methods). This technique provides an estimate of the force-generating capacity of all the elbow flexor muscles (Todd et al. 2003). This decreased by 47% from 12 ± 3 to 6.2 ± 2 Nm immediately after eccentric exercise, and was not completely recovered at day 8 (Fig. 5A). Changes in the estimated resting twitch paralleled changes in the maximal voluntary torque (Fig. 3A).
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Voluntary activation
When assessed the conventional way using motor nerve stimulation, voluntary activation of the elbow flexors decreased by 19% (from 97.3 ± 1.4 to 78.5 ± 6.5%) immediately after exercise, with some recovery at 2 and 24 h (P < 0.001, Fig. 6). However, when assessed with TMS of the motor cortex and using the usual equation (see Methods), there was a trend for voluntary activation to decline immediately after exercise, but this was not statistically significant. Comparison of the two measures of voluntary activation should be made with care (Todd et al. 2003), because the resting twitch to which the superimposed twitches are normalized (see Methods) behaved differently after exercise (Fig. 5A). The resting twitch to nerve stimulation was depressed by eccentric exercise more than maximal voluntary torque (Fig. 3A), and more than the twitch response estimated with motor cortical stimulation during voluntary contractions. Thus, the force generated by a single stimulus is differentially impaired compared to that generated by repetitive activation of the muscle. This may make the resting twitch to motor nerve stimulation inappropriate for normalization. To circumvent this difficulty, the absolute sizes of the responses to motor nerve stimulation and to motor cortical stimulation during MVC are plotted in Fig. 7A. After eccentric exercise, the superimposed responses to motor nerve stimulation did not significantly change, whereas the superimposed responses to motor cortical stimulation showed some depression (P = 0.002 at 2 h and P = 0.006 at day 8). The size of superimposed twitches from motor nerve stimulation did not correlate with the size of superimposed twitches from motor cortical stimulation (r2 = 0.01). Relative to their initial control sizes, responses to cortical stimulation were small compared to those to nerve stimulation (Fig. 7B). Hence, after exercise, superimposed twitches to nerve stimulation clustered to the right of the line of identity (sign test P < 0.01).
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Voluntary activation calculated from motor nerve stimulation () decreased by 23% immediately after eccentric exercise, and remained significantly decreased for 24 h. The time course of this reduction differed from the time course of muscle pain and tenderness, which peaked at day 1–2 (see Fig. 4). Voluntary activation calculated from motor cortex stimulation () did not change significantly after eccentric exercise.
A, group data for superimposed responses to motor nerve stimulation during MVCs () and for superimposed responses to cortical stimulation during MVCs (). Superimposed twitch torques evoked by nerve stimulation during MVCs did not significantly change after eccentric exercise. Superimposed twitch torques evoked by motor cortex stimulation during MVCs were larger and decreased significantly at 2 h after exercise and at day 8. B, for each subject, the mean of sizes of superimposed twitches evoked by nerve stimulation are plotted against those evoked by motor cortical stimulation in the same measurement sessions. Data for different times are shown using different symbols. Values are expressed relative to control data obtained before exercise. A line of identity is shown.
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EMG responses to brachial plexus and motor cortical stimulation
The area of the maximal compound muscle action potential (Mmax) measured in the relaxed biceps (0.10 ± 0.05 mVs), brachioradialis (0.06 ± 0.03 mVs) and triceps (0.07 ± 0.03 mVs) was unchanged by exercise. The amplitude of Mmax was also unchanged (13.1 ± 13.6 mV for the biceps). The area of the MEPs evoked during 50%, 75% and 100% MVC and expressed relative to Mmax in the biceps and brachioradialis did not change after eccentric exercise. There was no change in the MEP of the antagonist muscle, triceps. The length of the silent periods after cortical stimulation during MVCs was 110 ms in the biceps and brachioradialis. There were no changes in the duration of silent periods in either muscle at any level of contraction after exercise.
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Relationship between EMG and torque
As there were no changes in Mmax, the mean level of EMG was compared for the three contraction levels (50%, 75% and 100%MVC) and is shown in Fig. 8. Prior to eccentric exercise, an EMG level of 54.5 ± 9.3% maximum was required to produce a torque of 50% MVC. Immediately after exercise, this level increased to 88.8 ± 7.2% maximum, and returned to pre-exercise levels after a week.
Mean levels of EMG required to produce 50%, 75% and 100% MVC are shown. Data for different times after exercise are shown using different symbols. As force-generating capacity recovered, there was a gradual reduction in the relative level of EMG required to generate 50% MVC.
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Discussion
Our eccentric exercise produced a target reduction of 40% in MVC of the elbow flexors. Maximal voluntary torque showed little improvement until 48 h after exercise, with slow recovery towards control values over the next week. Such prolonged recovery has been described by others (e.g. Newham et al. 1983; Jones et al. 1986; Howell et al. 1993; Saxton & Donnelly, 1996; Sayers et al. 2003; Weerakkody et al. 2003). The exercised muscles were shortened (i.e. flexed) immediately after exercise (Howell et al. 1993; Weerakkody et al. 2003), and this occurred in the absence of elbow flexor EMG. However, muscle soreness was not present initially, but developed within 24 h, as measured by tenderness in the relaxed muscle (e.g. Schwane et al. 1983; Jones et al. 1986; Ebbeling & Clarkson, 1989; Clarkson et al. 1992; Howell et al. 1993; Weerakkody et al. 2003) and also by pain evoked by voluntary contractions. The pain did not increase with stronger contractions, and was similar for contractions of 50% and 100% MVC. Eccentric exercise produced some profound changes in peripheral force production, and unexpected changes in estimates of voluntary activation of the elbow flexors. These changes will be considered in turn, along with the accompanying EMG changes.
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After eccentric exercise, the resting twitch produced by stimulation of the biceps motor nerve was reduced by more than 75%. This reduction showed little change over the first two hours of recovery, and even after a week, the twitches were less than half their pre-exercise values. The magnitude of this prolonged reduction in twitch force is greater than previously observed (see Table 3 in Sayers et al. 2003). When cortical stimulation was used to estimate the size of the resting twitch of the combined elbow flexor muscles (Todd et al. 2003, 2004), again there was a reduction, but this was of smaller magnitude than when biceps motor nerve stimulation was used. Hence, the changes in the estimated resting twitch more closely matched the changes in maximal voluntary force than the changes in the twitch evoked by nerve stimulation. Altered excitation of the sarcolemma is unlikely to have caused the reduction in twitch amplitude, because the maximal M-wave showed no significant change after exercise (cf. Sayers et al. 2003). A likely explanation for these changes is a rapid and prolonged impairment in excitation–contraction coupling. This is consistent with animal studies. Eccentric exercise disrupts the T-tubule network immediately after downhill running in rats (e.g. Takekura et al. 2001). The increase in intracellular Ca2+ concentration during tetanic stimulation is decreased immediately after eccentric damage (Balnave & Allen, 1995). Furthermore, the maximal Ca2+-activated force is reduced less than the force produced by tetanic stimulation, particularly when the eccentric exercise protocol is severe (Warren et al. 1994; Balnave & Allen, 1995). That is, contraction can occur when Ca2+ is provided, but the link between excitation of the sarcolemma and release of Ca2+ is disrupted.
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A second contribution to the changes in contractile force after exercise may involve changes in the length–tension relation of the elbow flexors. There is an acute shift immediately after eccentric exercise, towards longer lengths for the peak of this relation for a twitch contraction (Saxton & Donnelly, 1996; Jones et al. 1997). This reflects focal lengthening and disruption of occasional sarcomeres (Proske & Morgan, 2001), so that overall muscle length must be increased beyond the original optimum to produce the same myofilament overlap in undamaged sarcomeres. Some studies in animals (Lynn & Morgan, 1994) and humans (Brockett et al. 2001) suggest that incorporation of new sarcomeres in series produces a sustained shift to longer lengths in the length–tension relationship. Presumably changes in both excitation–contraction coupling and the length–tension relation underlie the prolonged reduction in the twitch after eccentric damage in the present study. The relative contribution of the two effects is difficult to determine because we assessed forces only at 90 deg of elbow flexion, an angle close to the usual optimum for maximal voluntary forces. However, a recent study suggests that for voluntary forces the shift in the length–tension relation after eccentric damage of human elbow flexors may explain only a modest part of our observed changes (Philippou et al. 2004).
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Changes in force-generating capacity after eccentric exercise altered neural drive to the elbow flexor muscles during submaximal contractions. The near-linear relation between force and EMG became flatter immediately after eccentric exercise, so that almost 90% of maximal voluntary EMG was needed to generate a 50% MVC. This distortion recovered progressively over the following week. One explanation is that the motor units used to lower the load during the eccentric exercise were damaged so that they generated much less force although their sarcolemmal activation was preserved (i.e. there was EMG but little force). Changes in the length–tension relation for motor units firing at physiological frequencies will also affect this force–EMG relation, as may changes in motor unit synchronization (e.g. Yao et al. 2000). A surprising finding is that MEPs recorded during 50% MVCs did not change in size. In undamaged biceps, MEP size increases with the increasing strength of voluntary contractions up to 50% MVC, and then decreases with stronger contractions (Todd et al. 2003). This decrease probably reflects increased motoneurone firing rates. Thus, after eccentric exercise, the lack of decrease in the MEP suggests that mechanisms other than firing rates may be important in increasing background EMG.
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Maximal voluntary activation assessed using conventional twitch interpolation with motor nerve stimulation was diminished immediately after exercise and had largely, but not completely, recovered after 24 h. This time course did not parallel estimates of muscle pain which peaked 1–2 days after exercise. Maximal voluntary activation assessed with motor cortical stimulation showed little impairment, and did not correlate with measurements of muscle pain. Previous comparative measurements of voluntary activation using motor nerve and cortical stimulation have shown that voluntary activation measured with nerve stimulation was similar to, or higher than, when measured with cortical stimulation (Todd et al. 2003). Furthermore, during fatiguing isometric exercise, progressively impaired voluntary activation (or central fatigue) was demonstrated by both nerve and cortical stimulation (e.g. Gandevia et al. 1996). The findings of Todd et al. (2003) suggest that output from neither the motor cortex nor from the motoneurones is fully engaged during maximal efforts of non-fatigued muscle. That is, some contribution to the failure to drive the muscle fully comes from a failure to drive the motor cortex to generate output. Similarly, during fatiguing isometric exercise some central fatigue is due to impairment ‘upstream’ of motor cortical output. This was not the case after eccentric exercise. We considered whether the disparity in the measurements of voluntary activation with nerve and cortical stimulation might simply reflect differences in the resting twitch contractions used to calculate voluntary activation: the twitch force evoked by nerve stimulation was depressed more than that estimated by cortical stimulation. However, this difference is not the full explanation because superimposed twitches to cortical stimulation declined after eccentric exercise, whereas those to nerve stimulation showed no significant change but tended to increase. Compared to the superimposed twitches during MVCs with fresh muscles, the relative size of superimposed twitches to cortical stimulation was 70% of control after eccentric exercise, whereas that to nerve stimulation increased to 200% of control (Fig. 7B). A possible explanation for this behaviour is that although some motoneurones were not recruited or not firing fast enough to produce maximal muscle force and the axons of these motoneurones could be activated by nerve stimulation, motor cortical stimulation failed to activate them synaptically. One possibility is that TMS did not evoke extra output from the cortex. Another is that any such output failed to activate the motoneurones. This would imply that despite maximal voluntary effort, some inhibition or disfacilitation occurred at the level of motor cortex or motoneurones. Furthermore, in contrast to what happens during muscle fatigue, failure to drive the motor cortex to use all available output did not contribute to poor voluntary activation after eccentric exercise.
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The current study cannot determine the specific mechanism of reduced voluntary activation after eccentric exercise, it can only localize a change in the motor pathway to somewhere between the sites of stimulation at the motor cortex and motor axons. Changes either in afferent discharge or in generation of descending drive could underlie the effects on the motor pathway. We postulated that the muscle soreness that develops after eccentric exercise might impair voluntary activation. As acute muscle pain can reduce the size of MEPs in the resting muscle, pain may inhibit the motor cortex (Le Pera et al. 2001). The firing of group III and IV muscle afferents has also been linked to poor voluntary activation (Gandevia et al. 1996). However, the different time course of muscle soreness after eccentric exercise and changes in voluntary activation make it unlikely that muscle pain directly causes the changes in voluntary drive.
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In summary, eccentric exercise of human elbow flexors produces a marked and long-lasting reduction in voluntary torque. The prolonged decrease in the size of the resting twitch from motor nerve stimulation confirms that much of the loss of force occurs through muscle damage. The lack of change in the maximal M-wave points to major defects in excitation–contraction coupling, although a contribution from altered length–tension characteristics cannot be excluded. When measured with motor nerve stimulation, voluntary activation is impaired and must contribute to the early loss of maximal voluntary torque. However, we failed to show an association between the later muscle soreness and impaired voluntary drive. When measured with motor cortical stimulation, voluntary activation was not impaired. The disparate results of motor nerve and motor cortical stimulation suggest that inhibition at the motor cortex and/or the motoneurones limits voluntary drive to the muscle in the first 24 h after eccentric exercise.
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