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1Exercise Science Program, Department of Physical Therapy, Marquette University, Milwaukee, Wisconsin; 2Prince of Wales Medical Research Institute, Sydney; and 3Discipline of Physiology, School of Molecular and Biomedical Science, The University of Adelaide, Adelaide, Australia
Submitted 26 January 2006 ; accepted in final form 17 May 2006
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ABSTRACT |
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 TOP ABSTRACT METHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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transcranial magnetic stimulation; central fatigue; voluntary activation; gender; elbow flexor muscles
A failure in voluntary activation during maximal efforts means that the level of neural drive to the muscle is less than optimal (8). The extra force evoked by the superimposed stimulus to the axons indicates either that the motor units were not all recruited voluntarily or that they were discharging at rates that were not high enough to produce full fusion of force (1, 10, 21). This progressive impairment of voluntary activation is known as central fatigue and is due to failure at a site within the central nervous system (8). Stimulation of the motor cortex can also be used to estimate voluntary activation and can further localize the site of failure of voluntary drive to at or above the level of the motor cortical output (9, 31, 34, 35). Supraspinal fatigue is a component of central fatigue and is attributable to suboptimal output from the motor cortex (8). It is seen as an exercise-related fall in voluntary activation measured with cortical stimulation. It is unknown whether the greater central fatigue that develops in men compared with the women (26) is due to failure at sites proximal or distal to the motor cortex, although previous studies have suggested that small-diameter muscle afferents may impair voluntary drive at a supraspinal level (4, 9). Therefore, this study used stimulation of the motor cortex to further define the sites of failure during performance of an intermittent fatiguing contraction in men and women.
The purpose of this study was to compare the supraspinal fatigue measured with transcranial magnetic stimulation (TMS) of the motor cortex during sustained isometric maximal voluntary contractions (MVCs) of the elbow flexor muscles of young men and women. We hypothesized that men would experience greater reductions in maximal force than women and that this would be due to greater deficits in the voluntary supraspinal drive that generates the output from the motor cortex. We also determined whether the changes in voluntary drive during isometric exercise were accompanied by changes in motor cortex "excitability," which we assessed by the short-latency excitatory electromyograph (EMG) response to the motor cortex stimulation and the length of the subsequent EMG silence ("silent period").
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METHODS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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The physical activity level for each subject was assessed with a questionnaire (18) that estimated the relative kilocalorie expenditure of energy per week. The day of the menstrual cycle on which the experimental protocol was performed was recorded for each female participant. The first day of menstruation was considered as day 1 of the cycle.
Recordings
Subjects were seated upright in an adjustable chair with the dominant arm held firmly at the wrist via a secure strap in an isometric myograph that measured elbow flexion torque (Fig. 1A). Subjects were positioned with the dominant shoulder and the elbow flexed at 90° with the forearm vertical and fully supinated. Isometric elbow flexion torque was measured using a linear strain gauge (XTran, Melbourne, Australia; linear to 2 kN). EMG signals were recorded with bipolar surface electrodes (Ag-AgCl, 10-mm diameter) that were placed over the muscle belly and tendon of biceps brachii and triceps brachii. Care was taken to standardize electrode locations. A large self-adhesive ground electrode was fixed on the upper arm. EMG signals were amplified (x100–300) and band-pass filtered (16–1,000 Hz). Force (1,000 samples/s) and EMG (2,000 samples/s) signals were recorded to computer using a 1401 A-D converter and Spike2 software (CED, Cambridge, UK).
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Two forms of stimulation were used during each experiment: stimulation of the brachial plexus and TMS.
Stimulation of the brachial plexus. The brachial plexus was stimulated to produce a maximal compound muscle action potential (Mmax) of the biceps brachii and triceps brachii muscles while the subject was at rest. Single stimuli (100-µs duration) were delivered to the brachial plexus with a cathode in the supraclavicular fossa and an anode on the acromion using a constant-current stimulator (model DS7AH, Digitimer, Welwyn Garden City, Hertfordshire, UK). The stimulation intensity ranged between 60 and 180 mA. The average amplitude of the resting Mmax was 19.5 ± 4.7 mV for the biceps and 12.2 ± 3.9 mV for the triceps.
TMS. Transcranial magnetic stimuli were delivered via a round coil (13.5-cm outside diameter) over the vertex (Magstim 200, Magstim, Whitland, UK) to evoke motor-evoked potentials (MEPs) in biceps and triceps muscles. The direction of current flow in the coil preferentially activated the motor cortex in the hemisphere, which innervated the dominant arm. A single pulse was delivered over the motor cortex at an intensity (50–90% of maximum stimulator output) that produced a large MEP in the agonist biceps muscle (minimum amplitude of 50–60% of Mmax) during a brief MVC of the elbow flexor muscles but only a small MEP in the antagonist triceps muscle (amplitude <15% of Mmax) (36). TMS was delivered during voluntary contractions only.
Experimental Protocol
Each subject visited the laboratory for one experimental session to assess voluntary activation during brief MVCs and during performance of fatiguing intermittent isometric maximal contractions performed with the elbow flexor muscles over a period of 182 s. The intermittent contractions included 6 22-s maximal contractions with a 10-s interval between each sustained MVC. The motor cortex was stimulated using TMS to elicit MEPs in the biceps brachii and twitches of the elbow flexor muscles to assess voluntary activation at the start and end of each 22-s contraction. TMS was also delivered to the cortex during brief nonfatiguing maximal contractions before and after the fatiguing task.
The protocol comprised:
10 min by performance of a series of brief contraction sets similar to those performed before the fatiguing contractions. Sets of contractions consisted of a brief MVC followed by a contraction at 60 and 80% of the MVC just performed. Ten sets of contractions were performed at the following times after termination of the sustained MVCs: 15 s, 45 s, 1 min 15 s, 2 min 15 s, 3 min 15 s, 4 min 15 s, 5 min 15 s, 6 min 15 s, 8 min 15 s, and 10 min 15 s. Data Analysis
Voluntary activation was quantified by measurement of the torque responses to stimulation of the motor cortex (35, 36). Any increment in elbow flexion torque evoked during a contraction (superimposed twitch) was expressed as a fraction of the torque before the stimulation (9, 31). The superimposed twitch was also expressed as a fraction of the estimated amplitude of the response evoked by the same stimulus at rest (resting twitch). The estimation of the resting twitch was achieved for each subject by linear regression analysis of the amplitude of the superimposed twitch vs. the voluntary torque during the brief maximal and submaximal contractions (60 and 80% MVC). One regression analysis was performed for each set of brief contractions. During the fatigue task, the regression was calculated using the brief 60 and 80% MVCs and the nearest cortical stimulus during a sustained MVC. Thus each superimposed twitch was compared with an estimated resting twitch measured when the muscle was in a similar state of fatigue. For example, the brief submaximal contractions performed during the 10-s interval after the cessation of a 22-s contraction were used as a reference for the superimposed twitches elicited at the end of the previous sustained contraction and at the start of the next sustained contraction. The y-intercept was taken as the estimated amplitude of the resting twitch evoked by motor cortex stimulation (Fig. 2). The amplitude of the estimated resting twitch can be accurately determined from three data points, when the contractions are above 50% MVC (35). The amplitude of the resting twitch was estimated rather than measured directly because motor cortical and spinal cord excitability increase with activity (25). All of the elbow flexor muscles activated by TMS contribute to the amplitude of the estimated resting twitch.
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The contractile properties of the muscle were also assessed. The amplitude of the estimated resting twitch was used as an index of the force-generating capacity of the muscle and the fall of torque after a cortical stimulus was used to determine the peak relaxation rate of muscle fibers (33). The peak relaxation rate of muscle was calculated during each MVC by measurement of the steepest rate of torque decline during the period of EMG silence immediately after motor cortex stimulation. The steepest rate of torque decline was normalized to the total torque (voluntary plus evoked) before the silent period. This measure reflects the peak relaxation rate of elbow flexor muscle fibers.
The amplitude and areas of MEPs and Mmax were measured between sets of cursors set at the start and end of the waveform for the biceps and triceps muscles. Because amplitude and area showed similar changes, only areas are reported. The area of each MEP was normalized to the area of Mmax that was elicited at rest at the start of the experiment. The silent period was measured as the interval from the stimulus to the resumption of continuous EMG.
Voluntary torque was quantified by calculation of the mean torque over a 100-s period immediately before the stimulus.
Statistical Analysis
Data are reported as means ± SD within the text and are displayed as means ± SE in the figures. Two-way, repeated-measures ANOVAs were used to compare the following variables between men and women across time: voluntary torque, percent decline in MVC torque, voluntary activation measures, MEP area, silent period duration, estimated resting twitch amplitude, and peak rate of relaxation after cortical stimulation. Post hoc analyses (t-tests) were used to test for differences among pairs when appropriate. A significance level of P < 0.05 was used to identify statistical significance.
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RESULTS |
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MVC Torque and Voluntary Activation
Control trials. The men were stronger than the women for the five brief MVCs that were performed before the sustained fatiguing contractions (75.9 ± 9.2 vs. 42.7 ± 8.0 N·m; P < 0.05). The mean voluntary activation measured with cortical stimulation during these contractions was calculated with the estimated resting twitch and was greater for the men (96.5 ± 2.8%) than the women (93.0 ± 5.2%; P = 0.04) when the five control MVCs were pooled. However, voluntary activation was not different between the men and women for the fifth (final) control trial (95.7 ± 3.0 vs. 93.3 ± 3.6%; P > 0.05).
Fatigue. MVC torque declined for men and women during the six contractions sustained for 22 s (P < 0.05). By the end of the last sustained MVC, the men exhibited a greater absolute decline in torque (45.0 ± 6.5 N·m) compared with the women (20.9 ± 6.2 N·m; P < 0.05; Fig. 3A). The relative reduction in torque from mean of the initial control MVCs to the end of the sixth sustained MVC was significantly greater for the men (65 ± 3%) compared with the women (52 ± 9%; P < 0.05; Fig. 3B). Brief MVCs performed in the recovery period increased with time for both men and women (P < 0.05). However, at 10 min recovery, men were significantly less recovered (76.4 ± 9.0% of initial MVC values) compared with the women (88.4 ± 7.8%; P < 0.05; Fig. 3B).
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For the women, there was no association between the day of menstrual cycle on which the experiment was performed and the absolute or relative decline in MVC torque during the fatiguing contraction (P > 0.05).
Voluntary activation and fatigue. The increments in torque (superimposed twitch) generated by motor cortex stimulation during each 22-s maximal effort (Fig. 1C) were expressed relative to the torque before the stimulation. Superimposed twitches increased during the sustained MVCs for men and women from 1.9 ± 1.6% at the start of the contraction to 9.1 ± 5.7% at the termination of the fatiguing task (P < 0.05). Superimposed twitches were similar for men and women throughout the fatiguing task (5.5 ± 4.1 vs. 7.3 ± 4.7%; P > 0.05), as well as at the end of the sustained contraction (7.8 ± 5.9 vs. 10.5 ± 5.5%; P > 0.05; Fig. 4A). During recovery, superimposed twitches decreased to similar levels during the 10 min to 1.9 ± 1.0% for the men and to 2.0 ± 1.3% for the women (Fig. 4A).
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MEPs and Silent Period
Control trials. For the biceps brachii, the largest MEP area (82 ± 18% Mmax in men and 78 ± 14% Mmax in women) occurred during the 60% MVC, and the smallest occurred during the MVC (53 ± 13% Mmax in men and 57 ± 14% Mmax in women). The MEP area was similar for the men and women during each contraction strength of the control trials. There was also no sex difference for the area of the small MEP in triceps brachii (10.7 ± 7.0%).
In biceps, the duration of the silent period following cortical stimulation during a MVC was similar for men (149 ± 97 ms) and women (144 ± 77 ms, P > 0.05) across the five control trials (Fig. 5B).
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The silent period in biceps EMG increased in duration from the start to the end of the fatigue task and during each of the 22-s sustained contractions (P < 0.05; Fig. 5B). The increase in the silent period duration was similar for the men and women (P > 0.05).
Twitch Contractile Properties
Estimated resting twitch amplitude. The amplitude of the estimated resting twitch was greater for men (17.9 ± 7.8 N·m) than women (11.7 ± 3.7 N·; P < 0.05) during the control trials. It declined during the fatiguing task for both men and women (P < 0.05; Figs. 2B and 6A). However, by the end of the sixth sustained MVC, the relative reduction in amplitude was greater for the men (59 ± 12%) than the women (27 ± 19%; P < 0.05). After 10 min of recovery, the men were 42 ± 12% of control twitch amplitude, and the women were at 77 ± 13% (P < 0.05) of control values.
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DISCUSSION |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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Women Were Less Fatigable than Men but Voluntary Activation Was Similar
The men were stronger than the women but the reduction in maximal torque during the fatiguing task was greater for the men. These findings are consistent with other studies that have observed greater fatigue resistance for women compared with men for submaximal and maximal contractions in young adults (2, 3, 5, 12, 15, 26, 28, 38). Furthermore, there was an association such that the stronger subjects experienced greater fatigue (Fig. 3C). Similar relations are observed for sustained isometric contractions (6, 12, 13, 15) but not for intermittent isometric tasks in which the contraction duration is relatively brief (5 s) compared with the rest intervals (7, 14, 26). Consequently, the greater fatigue experienced by the men compared with the women appears related to their greater strength but only for tasks that involve longer duration sustained contractions.
The sex difference in the reduction of MVC torque of the elbow flexor muscles was not related to a sex difference in voluntary activation measured with motor cortex stimulation. This was contrary to our original hypothesis. The size of the superimposed twitch increased in both men and women during the fatiguing task. These results indicate that voluntary descending drive was not sufficient to optimally activate the motoneuron pool, and that the reductions in maximal torque during the fatiguing task were in part due to central fatigue at a site at or above the level of the motor cortical output. However, there was no sex difference in the degree of supraspinal fatigue. Both estimates of voluntary activation (the increments in torque from the cortical stimulation and the voluntary activation calculated using the superimposed twitch torque relative to the estimated twitch torque) were similar for men and women. The level of supraspinal fatigue quantified by the increments in torque relative to the ongoing torque (9.1%) was similar to that observed for maximal sustained and intermittent contractions (range of 5.2–9.8%) (9, 31). Voluntary activation calculated using the estimated resting twitch was also similar at the end of the fatiguing task (76.7%) to another fatiguing protocol (79.6%), which required the force to decline to 60% of the initial MVC (35). The firing of group III and IV muscle afferents, which are sensitive to ischemia and the metabolites of fatigue, may act at a supraspinal level to impair voluntary activation (4, 9), and it has been suggested that the higher intramuscular pressure in stronger muscles may lead to greater discharge of group III and IV muscle afferents in men than women. However, our results do not support a difference in the supraspinal influence of fatigue-sensitive afferents in men and women.
MEP Area and Silent Period Were Similar for Men and Women
Changes in the EMG responses to cortical stimulation with fatigue were similar for the men and women. The area of MEPs elicited during the sustained contractions increased with fatigue as reported in previous studies (30–32). This increase was similar for men and women. The size of the MEP will depend on the balance of all the excitatory and inhibitory influences to the corticospinal neurons, the response of the motoneuron pool to the descending volleys, and the muscle fiber action potentials. We normalized the MEP to Mmax elicited at rest with stimulation of the brachial plexus, and hence we did not account for any activity-dependent changes in the muscle fiber action potential (32). However, this was not likely to be different between men and women. Alterations in the amplitude of the M wave with fatigue did not account for the sex difference in muscle fatigue of the dorsiflexor muscles (26). Furthermore, responses to stimulation of descending tracts at the cervicomedullary level do not increase with fatigue for the elbow flexor muscles (8, 30). Thus the growth in the MEP size likely represented an increase in cortical excitability (30, 32). The MEP recovered relatively quickly compared with the voluntary activation, which remained depressed for both men and women up until 10 min of recovery. The dissociation in recovery between the MEP and voluntary activation has been observed previously (31), and it indicates that for both men and women the increased increments in torque due to the cortical stimulation do not entirely depend on the recruitment of neurons that are represented by the increased MEP.
The duration of the silent period increased with fatigue similarly for the men and women. Whereas the initial part of the silent period (the first 50–100 ms) is likely influenced by spinal mechanisms, including recurrent inhibition and afterhyperpolization, the latter part represents intracortical inhibition (16). Thus the increase in the duration of the silent period with fatigue may reflect increased intracortical inhibition. Because the silent period lengthened similarly for the men and women, this change is unlikely to contribute to the sex difference in muscle fatigue that we observed. Our findings of similar changes in the EMG responses to TMS, as well as similar supraspinal fatigue in men and women, suggest that the cortical effects of muscle fatigue are not different between the sexes.
Peripheral Fatigue Was Greater for the Men than the Women
The mechanisms for the sex differences in muscle fatigue must be located at levels distal to the output of the motor cortex, potentially at sites in the spinal cord or the muscle. Accordingly, we found evidence that the elbow flexor muscles of women were less fatigable. The amplitude of the estimated resting twitch decreased with fatigue and this reduction was greater for the men than the women. Thus the men experienced greater peripheral fatigue of the muscle compared with the women by the end of the fatigue task. Furthermore, twitch amplitude was not fully recovered for either sex after 10 min but was more depressed for the men than the women. The changes in the amplitude of the estimated resting twitch were similar to those observed in the MVC for the men and women. The parallel changes in the estimated resting twitch and MVC suggests that the sex difference in muscle fatigue may be largely explained by processes within the muscle. The peak relaxation rates of the muscle were consistent with a different distribution of fiber types in the elbow flexors of men and women with more fast twitch fibers in the men. The men had faster relaxation rates prior to fatigue and slowed more during the fatigue task. A recent study by Russ et al. (27) showed higher rates of glycolytic metabolism in men than women during isometric MVCs (27). This is also consistent with differences in the fiber-type composition and area of muscle in men and women although some studies show this sex difference is equivocal (17, 22–24, 29, 37).
Although our study does not provide direct evidence on motoneuron behavior, the firing of group III and IV muscle afferents does not appear to reduce motoneuron excitability for the elbow flexor muscles (4), so that sites at the spinal level may have a limited contribution to the sex difference in muscle fatigue for these muscles. However, for other muscles, central mechanisms may be more important in explaining the sex difference in muscle fatigue. For the ankle dorsiflexor muscle, men had greater decrements in voluntary activation measured with stimulation at the motor nerve during maximal contractions (26), indicating that the sex differences for this muscle were central in origin. Indeed, there maybe differences between muscle groups in the actions of group III and IV afferents on the motoneuron pool. Although group III and IV afferents do not inhibit motoneuron activity of the elbow flexor muscles (4), stimulation of the descending tracts shows that the motoneuron pool of the elbow extensors muscles is depressed by maintained firing of group III and IV muscle afferents after a fatiguing contraction (19). Consequently, it is conceivable that the site for the sex difference in muscle fatigue varies not only with the task performed but also with the muscle being assessed.
In conclusion, men had greater reductions in MVC torque than women during repeated sustained maximal fatiguing contractions. Supraspinal fatigue was similar for men and women. This was shown by the similar increases in the superimposed twitch torques and similar reductions in voluntary activation. Changes in the EMG responses to cortical stimulation were also similar for men and women. In contrast, peripheral fatigue, which was assessed by the size of the estimated resting twitch, was greater for men than women, and comparison of muscle relaxation rates suggested that this may be due to a different distribution of muscle fiber types. Thus the greater fatigue exhibited by men compared with women during a maximal fatiguing contraction of the elbow flexor muscles is not explained by a sex difference in supraspinal fatigue but is largely due to sex differences in limitations within the elbow flexor muscles.
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GRANTS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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ACKNOWLEDGMENTS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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FOOTNOTES |
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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. Section 1734 solely to indicate this fact.
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REFERENCES |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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0.9 between the voluntary torque and superimposed twitch torque are plotted. Data for the end of the 3rd and start and end of the 4th 22-s MVC are not shown because regressions were nonlinear for several subjects in this period. There were no sex differences during the fatiguing contractions or recovery (P > 0.05).
