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Prince of Wales Medical Research Institute and the University of New South Wales, Sydney 2031, Australia
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Responses to transcranial magnetic stimulation in human subjects (n = 9) were studied during series of intermittent isometric maximal voluntary contractions (MVCs) of the elbow. Stimuli were given during MVCs in four fatigue protocols with different duty cycles. As maximal voluntary torque fell during each protocol, the torque increment evoked by cortical stimulation increased from ~1.5 to 7% of ongoing torque. Thus "supraspinal" fatigue developed in each protocol. The motor evoked potential (MEP) and silent period in the elbow flexor muscles also changed. The silent period lengthened by 20-75 ms (lowest to highest duty cycle protocol) and recovered significantly with a 5-s rest. The MEP increased in area by >50% in all protocols and recovered significantly with 10 s, but not 5 s, of rest. These changes are similar to those during sustained MVC. The central fatigue demonstrated by the torque increments evoked by the stimuli did not parallel the changes in the electromyogram responses. This suggests that part of the fatigue developed during intermittent exercise is "upstream" of the motor cortex.
transcranial magnetic stimulation; central fatigue; motor cortex; exercise
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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IN HUMAN EXERCISE, FATIGUE is a decrease in the maximal voluntary force produced by a muscle or muscle group. Although much of fatigue is due to changes in the muscle fibers, some loss of force occurs through inadequate activation of motoneurons. This is known as central fatigue (for review, see Ref. 9). Central fatigue varies between muscles and with different tasks (17, 19). During prolonged isometric maximal voluntary contractions (MVCs) of the elbow flexors lasting 2-3 min, activation of the motor cortex by transcranial magnetic stimulation can evoke extra force from the muscle despite maximal voluntary activation (10). Thus at least some of the inadequate activation of motoneurons can be attributed to suboptimal descending drive from the motor cortex.
At the same time, during a sustained MVC, there are changes in the electromyogram (EMG) responses to transcranial magnetic stimulation. The short-latency excitatory response (motor evoked potential; MEP) grows in size, and the subsequent profound inhibition of ongoing EMG, known as the silent period, is prolonged (18, 21, 25). It is likely that changes in the motor cortex contribute to both phenomena. The latter part of the silent period after cortical stimulation depends on intracortical inhibition of descending drive (13, 22, 24). Thus the prolongation of the silent period with sustained contractions suggests a net increase in inhibition to corticospinal neurons. The size of the MEP depends not only on the excitability of corticospinal neurons but also on the motoneurons and the muscle fiber membrane. Comparison of MEPs and the responses to subcortical stimulation of descending tract axons during a sustained MVC indicates that some of the increase in the size of MEPs is due to an increase in net excitatory output evoked from the cortex (25). Although suboptimal output from the motor cortex (central fatigue) occurs together with the prolongation of the silent period and the growth of the MEP during a 2-min MVC, these changes can be dissociated under some conditions (10). Thus, although changes in the EMG responses to transcranial magnetic stimulation accompany fatigue, they may not be causally related to the loss of voluntary force.
Fatigue induced by periods of submaximal isometric exercise may have a greater central component than fatigue induced by prolonged maximal efforts (16, 17). Throughout a sustained MVC, high intramuscular pressure prevents blood flow to the contracting muscles. This maintained muscle ischemia does not allow recovery of muscle fibers during the contraction and maximizes the fatigue occurring within the muscle. During weak or intermittent exercise, muscle fibers will fatigue more slowly, and this may allow changes within the central nervous system to play a greater role in the overall loss of force production. Hence, this study was designed to examine whether the development of the supraspinal component of central fatigue was similar during exercise protocols with differing levels of activity. Because central fatigue can only be measured during maximal contractions, the level of exercise was varied by changing the duty cycle of the exercise rather than by varying the strength of contractions. The periods of contraction and rest were also chosen to examine the time course of the changes in the EMG responses to transcranial magnetic stimulation that occur during maximal efforts and their relationship to the supraspinal component of central fatigue. From previous studies on sustained MVCs, we expected that central fatigue due to suboptimal output from the motor cortex would not parallel the changes in either of the cortically evoked EMG responses. Results from the study have been published in abstract form (4).
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METHODS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Setup.
Nine normal subjects (25-46 yr old; 4 women) took part in
experiments to examine responses to transcranial magnetic stimulation during fatiguing contractions of the elbow flexors. All procedures were
undertaken with the informed consent of the subject and the approval of
the local ethics committee. Subjects sat with the right arm flexed to
90° in an isometric myograph that measured flexion torque exerted
about the elbow (transducer linear to 2 kN, Xtran, Melbourne,
Australia; see Ref. 1 for details). The arm was positioned with the
forearm vertical and supinated and strapped to the myograph at the
wrist (Fig. 1A). Feedback of
flexion torque was provided to the subject by an LED display. Subjects were encouraged verbally throughout all contractions.
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Protocol. Each subject (n = 9) took part in four sessions, each performed on a different day. In each session, subjects initially performed five brief (1- to 2-s) maximal voluntary isometric elbow flexions separated by rests of at least 1 min. A series of longer fatiguing MVCs followed. The duration of these MVCs and the intervals of rest between them varied between protocols, but each series included a total of at least 3 min of maximal effort (see Fig. 1B). The durations of contractions and rests were chosen to enable examination of the time course of the development and recovery of the changes in EMG responses to cortical stimulation. Previous studies showed that the MEP and silent period had altered after 15 s of continuous MVC and had recovered with 15 s of rest. The patterns used were 5-s MVC and 5-s rest (50% duty cycle) continuing for 7.5 min, 15-s MVC and 10-s rest (12 contractions, 60% duty cycle), 15-s MVC and 5-s rest (12 contractions, 75% duty cycle), and 30-s MVC and 5-s rest (6 contractions, 86% duty cycle). Finally, subjects performed a series of brief MVCs at 15 s, 30 s, and 1, 2, and 3 min after the series of fatiguing contractions. During each brief contraction, a single transcranial magnetic stimulus was given. In the 5-s MVC and 5-s rest series, stimuli were given every 30-s (in the middle of each third 5-s MVC). In the other series, stimuli were given ~2 s after the start and ~2 s before the end of each MVC. Stimulus intensity for each subject was constant in all sessions. When the stimulus was delivered during the contractions, an EMG "silence" followed the MEP, and, as a result, torque dropped. Subjects were instructed repeatedly to regain their maximal torque as fast as possible. EMG was recorded from biceps brachii and brachioradialis through surface electrodes (9-mm diameter Ag/AgCl electrodes fixed over the muscle belly and tendon). EMG signals were amplified (53 Hz to 1 kHz; Digitimer amplifier D150) and sampled with the torque signal at 5 kHz from 50 ms before to 500 ms after each stimulus. Data were recorded on disk for off-line analysis (1401 interface, Cambridge Electronic Design).
Data analysis.
The increment in torque elicited by the magnetic cortical stimulus was
calculated as the difference between the peak torque after the stimulus
and the mean voluntary torque over the 50 ms preceding the stimulus
(see Fig. 2A). To estimate the
relative levels of voluntary drive, the torque increment was expressed as a percentage of the mean prestimulus torque. Because all
contractions were MVCs, prestimulus torque was always an estimate of
the ongoing maximal voluntary torque. Thus an increase in this
percentage represents a decrease in voluntary activation and is termed
central fatigue.
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RESULTS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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During series of intermittent isometric MVCs, maximal voluntary
torque decreased, and the increment in torque evoked by cortical stimulation increased (Figs. 3 and
4). This increase in evoked torque
demonstrates the development of central fatigue. The EMG responses to
transcranial magnetic stimulation were also affected (Fig.
5). The silent period lengthened, and the
MEP increased in size. These findings extend the observation of similar
changes in 2-min sustained fatiguing contractions (10,
25). However, different contraction protocols dissociated
changes in central fatigue and silent period duration and also
dissociated changes in silent period duration and MEP size.
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Torque. With duty cycles of 50, 60, 75, and 86%, all the tasks were fatiguing. By the end of the total of 3 min of contraction, maximal voluntary torque dropped to 60 ± 11.5% of its initial value in the 5-s MVC and 5-s rest (50% duty cycle) task and to ~40% in the other three protocols. Figure 4 shows that ~80% of the drop in torque occurred over the first half of each task. Over the last half of the protocols, torque showed some recovery over each period of rest so that torque measured near the beginning of each contraction was greater than that measured near the end of the previous contraction. More recovery occurred with 10-s rest between contractions [9.1 ± 8.9% (mean ± SD) of initial MVC; Fig. 4B] than with 5-s rest (Fig. 4, C and D; 6.0 ± 7.4% and 4.9 ± 10.9%; P < 0.05, one-way ANOVA and post hoc Student-Newman-Keuls). Over each final contraction, torque went from 59 ± 14.4% to 42 ± 15.5% of initial MVC during the 15-s MVC and 10-s rest task, but from 53 ± 6.4% to 42 ± 5.3% with 15-s MVC and 5-s rest and from 51 ± 6.2% to 40 ± 10.4% with 30-s MVC and 5-s rest. With 3 min of rest after the end of the fatiguing protocols, maximal voluntary torque recovered to 70 ± 10.7% (5-s MVC and 5-s rest), 72 ± 12.2% (15-s MVC and 10-s rest), 73 ± 9.6% (15-s MVC and 5-s rest), and 81 ± 8.7% (30-s MVC and 5-s rest) of its initial value.
When data for all subjects were pooled, voluntary activation decreased in all protocols. Figure 3 shows examples of torque increments evoked by cortical stimulation during the 60% duty cycle task in one subject. On average, during the brief control MVCs, the cortical stimulus evoked an increment of 1.4 ± 1.0% of the prestimulus torque. Although there was variability between subjects, this increment in prestimulus torque increased throughout each protocol (Fig. 4,
). On average,
torque increments evoked over the last third of each task were larger
than those evoked in the first third (t-tests;
P < 0.05, 5-s MVC and 5-s rest; P < 0.005, 15-s MVC and 10-s rest; P < 0.001, 15-s MVC and
5-s rest; P < 0.005, 30-s MVC and 5-s rest). The mean
increments observed in the last third of each protocol were 6.0 ± 4.3% of prestimulus torque in the 5-s MVC and 5-s rest protocol,
6.4 ± 6.4% in the 15-s MVC and 10-s rest protocol, 7.7 ± 6.8% in the 15-s MVC and 5-s rest protocol, and 8.5 ± 6.5% in
the 30-s MVC and 5-s rest protocol. Voluntary activation was not more
affected by any one of the contraction protocols. During the fatigue
protocols, voluntary activation was lower than 80% in 2-3% of
observations in each protocol. Cortical stimulation evoked some
increments of more than 25% of ongoing torque in some subjects.
After the end of each fatiguing protocol, recovery of voluntary
activation occurred over the first minute. Grouped data from all
protocols showed that the increments in ongoing torque evoked by
cortical stimulation remained significantly greater than in control
trials after 15 and 30 s of the recovery period but had returned
to control levels by 1 min. Consistent with this relatively slow
recovery, voluntary activation was similar near the beginnings and ends
of the intermittent contractions during each of the protocols (t-tests for each protocol, P > 0.05). Even
rest intervals of 10 s did not allow significant recovery of
activation (Figs. 3 and Fig. 4B).
Silent period.
In control trials, the duration of the silent period did not vary
significantly between different sessions. For biceps brachii, the mean
duration for all subjects was 192 ± 26 ms and for brachioradialis 193 ± 29 ms. With all four fatiguing protocols, the duration of the silent period increased, although the extent and time course of the
prolongation differed between protocols (Fig.
6). Data from brachioradialis are not
shown but resembled those from biceps brachii. At the end of the
fatiguing protocol after a total 3 min of contraction, the prolongation
of the silent period varied between ~20 ms with the 50% duty cycle
(5-s MVC and 5-s rest; biceps brachii, 21 ± 14 ms;
brachioradialis, 18 ± 16 ms) and >75 ms with the 30-s MVC and
5-s rest protocol (biceps brachii, 75 ± 43 ms; brachioradialis,
83 ± 40 ms). Figure 6A shows the change in the silent
period in the 5-s MVC and 5-s rest protocol. A single stimulus was
delivered during each contraction, and there was a small, gradual
increase in duration of the silent period over the 6 min of the
protocol. In the other protocols, which involved 15-s or 30-s MVCs, two
stimuli were delivered during each contraction so that a silent period
near the beginning and end of each MVC could be observed.
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MEP.
The MEP increased in area in all contraction protocols (Fig.
7; see also Fig. 5). The growth of the
MEP did not differ significantly between the different protocols, with
a maximal mean growth in biceps of 56 ± 36% with 5-s MVC and 5-s
rest, 76 ± 46% with 15-s MVC and 10-s rest, 72 ± 68% with
15-s MVC and 5-s rest, and 78 ± 45% with 30-s MVC and 5-s rest.
Similar growth was seen in brachioradialis (56 ± 28%, 63 ± 56%, 76 ± 46%, and 65 ± 39%, respectively). Like its
area, the amplitude of the MEP also increased in all protocols. However, the extent of this increase was about half that of the increase in area and was less consistent.
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Failure of voluntary activation and development of central fatigue. As maximal voluntary torque fell in each contraction protocol, increments in elbow flexor torque were elicited by transcranial magnetic stimulation. Subjects became unable to activate the elbow flexor muscles fully with continuing maximal voluntary efforts. The increments in torque were larger than during brief control contractions and increased relative to ongoing maximal torque with the total time of contraction. This progressive failure of voluntary activation demonstrated central fatigue during each of the contraction protocols. Furthermore, suboptimal output from the motor cortex contributed to the failure of voluntary activation. To evoke extra force from the muscle, stimulation of the motor cortex elicited extra output from the cortex, and this extra output recruited additional motoneurons. This implies that maximal voluntary effort did not generate maximal descending drive and that the descending drive that it did generate was insufficient to activate the motoneuron pool optimally. Thus the central fatigue demonstrated here did not occur because the motoneurons were impossible to activate but occurred at a supraspinal level.
Central fatigue, as tested by cortical stimulation, was similar in all the exercise protocols (50-86% duty cycle), even though overall fatigue, shown by the drop in maximal voluntary torque, was less with the lowest duty cycle. A similar progressive failure of motor cortical output to optimally drive motoneurons also occurs during sustained MVCs (10). The increment in torque at the end of a sustained 2-min MVC of the elbow flexors was 9.8 ± 8.3%. This is not different from the mean increments between 5.2 ± 6.0% and 7.9 ± 3.8% seen at the end of the first 2 min of contraction in the intermittent protocols. Although we failed to demonstrate differences in supraspinal fatigue with the protocols in the present study, such differences might become apparent in exercise of longer duration or with submaximal contractions. However, no differences in central fatigue were found in exercise that consisted of intermittent maximal contractions at low-to-medium duty cycles (5-50%; 20). Although increments in torque elicited by magnetic cortical stimulation during a maximal effort reflect failure of voluntary activation, it is not possible to compare these quantitatively with the measurements of voluntary activation [derived by comparing the twitch resulting from supramaximal stimulation of a muscle nerve during a maximal effort with that evoked in the relaxed muscle ("twitch interpolation"; e.g., Refs. 1, 2, 3)]. There are a number of problems associated with cortical stimulation used to measure central fatigue. 1) The twitch in the relaxed muscle cannot be used as a control. Cortical stimuli do not evoke maximal twitches in the relaxed muscle, and the changes in cortical and spinal motoneuron excitability during a voluntary contraction mean that, for any submaximal stimulus, more motor units are recruited during contraction than during relaxation (12, 26, 29). The evoked increment in torque can be normalized to the ongoing maximal voluntary torque to account for fatigue in the muscle fiber, but this is not ideal (see Ref. 10). 2) Even during a strong voluntary contraction, the cortical stimulus may not recruit all motor units and thus may underestimate failure of voluntary activation. 3) The cortical stimulus does not recruit only the corticospinal neurons and motoneurons that activate the muscles of interest. The stimulus can evoke twitches in many muscles, including antagonists to the action being investigated (11). Thus, at some joints, the twitch of the antagonists can "counteract" that of the agonists, especially after the agonists are fatigued. Again, central fatigue will be underestimated. Hence, an increment in torque evoked by magnetic cortical stimulation during a maximal effort reveals suboptimal voluntary activation, but lack of an increment in torque is not a reliable indicator of complete activation. Magnetic cortical stimulation most reliably shows suboptimal activation when the target muscle group is stronger and more easily activated than its antagonists. At the elbow, the flexors are nearly twice as strong as the extensors (6) and have a stronger short-latency facilitatory response to magnetic stimulation (23).Fatigue and changes in EMG responses to transcranial magnetic stimulation. Changes in the EMG responses to transcranial magnetic stimulation occur with fatiguing intermittent contractions as previously shown for sustained voluntary contractions. The silent period is prolonged, and the MEP grows in size. However, the different exercise protocols demonstrate that the development and the recovery of the changes in the inhibitory and excitatory responses have different time courses. The increase in size of the MEP occurs more quickly and recovers more slowly than the prolongation of the silent period. As a consequence, the changes in silent period duration were quite different in the different contraction protocols, whereas the MEP grew similarly in each protocol.
The silent period is a period of EMG silence that immediately follows the excitatory response to magnetic cortical stimulation. Initially, there is a decrease in excitability of spinal motoneurons (shown by a decreased H-reflex), but this recovers after ~100 ms (8, 28). The continued inhibition of voluntary EMG after recovery of motoneurons is attributed to inhibition of corticospinal neurons within the cortex (13, 22, 24). Long-lasting inhibitory postsynaptic potentials (IPSPs) can be evoked in pyramidal neurons by electrical stimulation of the cortex (14, 15), and this is likely to involve GABAergic interneurons (22). The duration of the silent period increases with the intensity of the magnetic stimulus and decreases with the voluntary effort that the subject exerts to regain torque output after the stimulus (5, 30). The duration of the silent period may reflect a balance between excitatory and inhibitory inputs to the output neurons of the motor cortex. With fatiguing contractions, the silent period lengthens when the subject's effort becomes near maximal. Either the magnetic stimulus becomes more effective at generating IPSPs, or the subject's voluntary drive to the motor cortex decreases. The behavior of the silent period in the different protocols in this study demonstrates an effect that builds up over 30-45 s of continuous maximal effort, that starts to recover quickly, and that approaches complete recovery after a 10-s rest. The very slow lengthening of the silent period with repeated 5-s MVCs separated by 5-s rest periods indicates that whatever change underlies the prolongation of the silent period starts to occur within a 5-s MVC, even though the silent period itself is not yet detectably prolonged. Furthermore, in each protocol, the effect is cumulative if additional exercise is undertaken before complete recovery. The change in the silent period was not inevitably associated with central fatigue. In the 50% duty cycle task, the increments in torque elicited by the cortical stimuli increased although the prolongation of the silent period was small, and, after the end of each fatiguing protocol, when silent-period duration recovered in 15 s, subjects continued to be unable to activate the motor cortex optimally. These instances of dissociation of the ability to drive the motor cortex and the lengthening of the silent period confirm that the suboptimal drive to the motoneurons from the motor cortex is not due to the motor cortical changes represented by the prolongation of the silent period. Furthermore, the observation that the silent period is not necessarily increased in duration when the motor cortex is activated suboptimally suggests that the fatigue-induced prolongation of the silent period is not due to inadequate drive to the motor cortex. The size of the short-latency excitatory response to transcranial magnetic stimulation (i.e., MEP) depends on the descending volleys evoked from the cortex, on the response of the motoneuron pool to the volleys, and on the individual muscle fiber action potentials. Hence, change in the excitability of the motor cortex or of the motoneuron pool or any change in the muscle fiber action potential can alter the size of the MEP. In a sustained MVC of the elbow flexors, the MEP grows in size. This results, in part, from an increase in size of the muscle fiber action potentials due to hyperpolarization of the muscle fiber membrane by increased activation of the electrogenic Na+/K+ pump (7). Other factors, including changes in pH and temperature, might also act in the muscle to change the size of the muscle action potential, but their overall effect is difficult to predict. However, on the basis of studies using supramaximal stimulation of the brachial plexus, some of the increase in size of the MEP cannot be accounted for by changes in the periphery and is probably due to increased net excitatory output evoked from the motor cortex by the magnetic stimulus (27). In the present study, the MEP grew similarly during all intermittent MVC protocols. Overall, it increased more quickly than the duration of the silent period and recovered more slowly. However, recovery of the MEP occurred more quickly than recovery of voluntary activation. The MEP recovered partially in 10 s and fully in 15 s, whereas voluntary activation did not recover with 10-s rest and took ~1 min to recover. Thus the increased increment in torque elicited by cortical stimulation near the end of the fatiguing protocols does not depend solely on the greater recruitment of motor units that might be represented by the larger MEP. A failure of voluntary activation remained despite reduction of the MEP to its control size. The seemingly parallel changes in the size of the MEP and duration of the silent period during sustained MVCs has led to the suggestion that a common source may facilitate both excitatory and inhibitory elements within the cortex (18). In the present study, different time courses for the development of the growth of the MEP and prolongation of the silent period were clear in the lowest duty cycle task. Furthermore, the silent period recovered fully with 10-s rest, but the MEP did not. These differences argue against a common source for the changes.Change in evoked EMG responses and central fatigue. Recovery of voluntary activation occurred more slowly than recovery of the silent period or the MEP but faster than recovery from muscle fatigue. Whereas the EMG responses to cortical stimulation recovered in 15-s or less, the elicited increments in torque returned to control levels over 1 min, and maximal voluntary torque recovered to only 70-80% of control levels with 3-min rest. The temporal disparity between recovery of the EMG changes and recovery from central fatigue is consistent with our previous study of sustained MVCs. In that study, descending drive from the motor cortex remained suboptimal if the fatigued muscle was held ischemic at the end of the contraction (10). During this maintained ischemia, the silent period and MEP recovered fully. This suggests that neural signals related to the fatigued state of the muscle contributed to central fatigue but that this fatigue was somehow "upstream" of the motor cortex.
In summary, the current study demonstrates a supraspinal component to the central fatigue produced by a series of intermittent MVCs. The loss of voluntary torque represented by this central fatigue is on average ~7% but can be substantial (>25% of ongoing maximal voluntary torque) in individual trials in individual subjects. Changes in the EMG responses to transcranial magnetic stimulation resemble those seen during sustained MVCs and demonstrate net changes in the motor pathway from the motor cortex to the muscle fiber. However, the changes demonstrated by these altered EMG responses cannot fully account for the failure of voluntary activation.| |
ACKNOWLEDGEMENTS |
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We thank Dr. Brenda Bigland-Ritchie for reading the manuscript.
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FOOTNOTES |
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This work was supported by the National Health and Medical Research Council of Australia.
Address for reprint requests and other correspondence: J. L. Taylor, Prince of Wales Medical Research Institute, High St., Randwick, N.S.W. 2031, Australia (E-mail: jl.taylor{at}unsw.edu.au).
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact.
Received 7 November 1999; accepted in final form 11 February 2000.
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REFERENCES |
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TOP
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METHODS
RESULTS
DISCUSSION
REFERENCES
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,
Left axis: fall in ongoing maximal voluntary torque, with data from the
start and end of each 15-s MVC joined by a line.
