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1 Centre for Sports Medicine and Human Performance3 School of Health Sciences, Brunel University, Uxbridge, Middlesex, UK 2 Research Institute for Sport and Exercise Sciences, Liverpool John Moores University, UK
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Abstract |
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(Received 29 September 2006;
accepted after revision 9 November 2006; first published online 10 November 2006)
Corresponding author E. Ross: Centre for Sports Medicine and Human Performance, Brunel University, Uxbridge, Middlesex, UB8 3PH, UK. Email: emma.Ross{at}brunel.ac.uk
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Introduction |
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Fatigue, and the neuromuscular mechanisms underlying it, can be investigated by studying mechanical and electromyographic responses to transcranial magnetic stimulation (TMS). Immediately after contraction, the short-latency excitatory response to TMS, termed the motor evoked potential (MEP), is transiently enlarged (termed postexercise facilitation) in the exercised muscle (Brazil-Neto et al. 1993; Samii et al. 1996, 1997). After prolonged fatiguing muscle activation, the MEP is subsequently depressed (Samii et al. 1997), indicating fatigue of motor pathways as a result of changes in cortical excitability. In addition, the period of EMG silence following the MEP elicited by TMS (termed the cortical silent period) is prolonged after fatiguing contractions (McKay et al. 1996; Taylor et al. 1996; Andersen et al. 2003), reflecting a net increase in inhibition to corticospinal cells.
Transcranial magnetic stimulation has also been used to investigate supraspinal fatigue (Todd et al. 2004; Sogaard et al. 2006; Taylor et al. 2006). If cortical stimulation during an isometric maximal voluntary contraction (MVC) produces a twitch-like increment in force from the contracting muscles, voluntary activation (VA) is less than 100%. The presence of a superimposed twitch produced by electrical motor nerve stimulation demonstrates that VA is less than maximal and suggests that the stimulated axons are not all recruited voluntarily, or are discharging at subtetanic rates (Gandevia et al. 1996; Herbert & Gandevia, 1999). Voluntary activation measured with TMS, however, reveals something different. If a superimposed twitch is evoked during an MVC by cortical stimulation then it is implied that output from the motor cortex was not optimal to drive the muscle maximally at the time of stimulation. Therefore, failure of voluntary drive at or above the level of motor cortical output contributes to the manifestations of fatigue. This method has demonstrated submaximal VA of the elbow flexors after maximal (Gandevia et al. 1996; Todd et al. 2003) and submaximal contractions (Sogaard et al. 2006) but has yet to be used to investigate central fatigue in muscles of the lower limb, or after prolonged, whole-body exercise such as running.
The purpose of the present study was twofold: to study the relationship between peripheral and central fatigue after a marathon distance treadmill run and to study the recovery of potential exercise-induced changes at both peripheral and central levels. We hypothesized that after prolonged running, both peripheral and central fatigue would contribute to a decrease in MVC. It is further hypothesized that feedback of the force-generating capacity of the muscle and its biochemical status may impair the drive from the motor cortex, causing a reduction in VA, primarily as a result of suboptimal output from the motor cortex.
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Methods |
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Nine experienced runners (mean ± S.D. age, 32 ± 7 years; height, 179 ± 0.07 cm; weight, 77.8 ± 9 kg; and maximal oxygen uptake, 61.6 ± 3.6 ml kg–1 min–1) volunteered to participate in the study. All but one individual had completed at least one marathon race prior to the study. On the basis of previous marathon finish times and current training status, participants were predicted to complete the experimental marathon within 3–4 h. Subjects gave written informed consent before the experiment, and approval for all experimental procedures was obtained from the institutional ethics committee. The study was conducted according to the Declaration of Helsinki.
Protocol
Baseline values were established for each subject 1 h prior to the exercise protocol. Subjects performed three brief (3 s) control MVCs of the tibialis anterior (TA), from which peak torque and peak surface EMG was measured. Six peripheral stimuli were then delivered to the relaxed muscle. A single peripheral stimulus was also delivered immediately after each of three MVCs, in the relaxed muscle, to elicit a potentiated twitch (Fig. 1A). Potentiated twitch force is suggested to be a more sensitive measure of fatigue than unpotentiated twitch force (Laghi et al. 1998).
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Finally, maximal voluntary hand grip (HG) strength was measured. Subjects were advised to hold the HG dynamometer (T.K.K. Grip A, Takei, Tokyo, Japan) in their dominant hand, exhale, and then squeeze as forcefully as possible. The greatest value of three maximal trials was recorded as the maximal value. This test was used to confirm that the anticipated decrease in postexercise dorsiflexion MVC values was not the result of reduced motivation (Fuller et al. 1996) or general whole-body fatigue (Coast et al. 1999).
After these measurements, subjects performed the exercise protocol. Immediately after (within 20 min), 4 h after and 24 h after the exercise protocol, all baseline measurements were repeated.
Force and EMG recordings
Isometric ankle dorsiflexion force during voluntary and evoked contractions was measured by means of an isokinetic dynamometer (Biodex Corporation, Shirley, NY, USA). Subjects were seated upright on the dynamometer chair with the right hip flexed at 80 deg (full extension = 180 deg) and the right knee flexed at 120 deg (full extension = 180 deg). The right leg was supported under the distal femur with a soft pad. The right foot was securely strapped into the footplate of the dynamometer with the ankle in a neutral (90 deg) position. Straps were also applied across the chest and mid-thigh.
Electromyographic activity was recorded with surface electrodes (Goldy Karaya Gel electrodes, 28 mm diameter, silver–silver chloride, Arbo®, Henley Medical, Stevenage, UK) over the TA muscle. Surface EMG (sEMG) signals were amplified (gain x 1000; 1902, Cambridge Electronic Design, Cambridge, UK), band-pass filtered between 20 Hz and 2 kHz, digitized at a sampling rate of 4 kHz using an analog-to-digital converter (micro1401, Cambridge Electronic Design), and finally acquired and later analysed (Spike2 v4.11, Cambridge Electronic Design).
Stimulation
Two forms of stimulation were used: stimulation of the peroneal nerve [‘peripheral’ magnetic stimulation (PNMS) of the TA] and TMS over the motor cortex. The MEPs were recorded using sEMG and termed MEPP for MEPs evoked via PNMS and MEPC for MEPs evoked via TMS (Fig. 2).
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All peripheral stimulations were performed with the stimulator at 100% of its maximal possible intensity. Supramaximal TA activation (demonstrated by recruitment curves comparing the amplitude of the MEPP obtained using stimulation at 50, 60, 70, 80, 90 and 100% of the maximal power output of the stimulator) was achieved in all subjects.
Transcranial magnetic stimulation was achieved using a Magstim 200 magnetic stimulator and a 70 mm figure-of-eight coil (Magstim Company), with a maximum output of 2 T. Magnetic stimulation was applied over the contralateral (left) motor cortex. Prior to the experimental protocol, a mapping procedure was carried out to establish the optimal cortical site for activation of the TA. In all cases, this was 0–3 cm lateral to the vertex. This position was marked with indelible ink to ensure reproducibility of the stimulation conditions for that individual during the experimental protocol. Also prior to the experimental protocol, MT for the TA was identified by constructing a stimulus–response curve for each individual. Threshold was established by increasing stimulator output from 40% by 5% steps until a TA response was visible, the criterion for this being that the evoked response was present in less than one-half of eight stimuli (Sharshar et al. 2003). Transcranial magnetic stimulation was delivered at both 1.2 x MT and 100% stimulator output throughout the experiment.
Exercise
At least 5 days prior to the experimental protocol, each subject performed a continuous, incremental treadmill test to exhaustion, to determine their individual lactate threshold [defined as the first inflection of blood lactate above resting values (Aunola & Rusko, 1984)] and maximal oxygen uptake.
During the experimental exercise protocol, subjects exercised on a treadmill (HPCosmos, Traunstein, Germany) set at 1% incline gradient, since this has been shown to simulate outdoor running more accurately (Jones & Doust, 1996), at an initial starting speed corresponding to –5% lactate threshold running velocity. If necessary, throughout the running task, subjects were permitted to self direct this running speed within ± 10% range. Subjects ran for 42.2 km (marathon distance). Throughout the exercise, subjects were able to drink water and a self preferenced isotonic sports drink. The mean amount of carbohydrate ingested through the trial was 193 ± 20 g, and the mean volume of ingested fluid was 2.8 ± 0.6 l.
Data analyses
Data were analysed off-line. The EMG signal was analysed in the time domain, as root mean square (r.m.s.) amplitude with a time constant of 25 ms. Computer-aided analysis was performed over a 0.5 s window initiated at the point of peak force during the MVC effort. Peak torque was recorded from each maximal effort, and the highest value was recorded as the maximal value.
A period of EMG ‘silence’ followed the MEPC, delivered during the MVC, at 100% stimulator output. The duration of this cortical silent period (CSP) was measured by cursor and was defined as the interval from the onset of the MEPC to the time when EMG returned to at least 50% of prestimulus EMG values (Andersen et al. 2003). Peak-to-peak amplitude and latency (measured as the time elapsed between stimulus and onset of action potential) were measured in the average waveform of each set of MEPP and MEPC responses in the relaxed TA muscle.
Voluntary activation was quantified in a subset of four subjects by measurement of the torque responses to TMS. Voluntary activation was calculated using a standard twitch interpolation equation: (1 – SIT/POT) x 100, where SIT is the superimposed twitch, i.e. any increment in torque elicited by the stimulation during a maximal dorsiflexion, and POT is the potentiated twitch elicited at rest 1 s after the MVC (Kalmar & Cafarelli, 2004). The amplitude of the ‘resting twitch’ evoked by TMS was estimated rather than measured directly, using methods outlined by Todd et al. (2004). Briefly, for each subject a linear regression of the amplitude of the superimposed twitch evoked by TMS during voluntary contractions of 50, 75 and 100% MVC was performed (Fig. 1C). The y-intercept was taken as the amplitude of the resting twitch evoked by TMS. Interpolated twitches were elicited by stimulation at 100% stimulator output.
Statistical analyses
Repeated measures ANOVA was used to compare TA muscle function across time (before, immediately after, 4 and 24 h after exercise). Following significant main effects, planned pairwise comparisons were made using the Bonferroni method. To increase the power of analysis of variables measured in the subset of four subjects, one-tailed post hoc comparisons were made to test the hypothesis that fatigue caused by MAR would decrease voluntary activation and mechanical twitch force. The level of significance was set at P < 0.05. Results are expressed as means ± S.D. Statistical analyses were performed using SPSS version 13.0 for Windows (SPSS, Chicago, IL, USA).
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Results |
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All subjects completed the 42.2 km treadmill run (average completion time, 208 ± 22 min). Mean heart rate throughout exercise was 86% of maximum heart rate (mean exercising heart rate, 159 ± 11 beats min–1; mean maximum heart rate, 185 ± 9 beats min–1).
Torque
Maximal force generation of the dorsiflexor muscles decreased by 18 ± 7% (P = 0.009) immediately after the marathon distance treadmill run (MAR), and remained significantly decreased 4 h after completion of MAR (P = 0.045; Table 1). Maximal voluntary contraction returned to near baseline levels 24 h after the exercise task.
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Tibialis anterior r.m.s. sEMG during a maximal dorsiflexion increased by 13.7% immediately post-MAR (P = 0.039). After 4 and 24 h of recovery, r.m.s. EMG did not differ significantly from baseline during the MVC manoeuvre.
Responses to TMS
A TA response to TMS delivered at 1.2 x MT and 100% stimulator output was observed in all subjects. Peak-to-peak amplitude of MEPC was depressed by 57 ± 25% (P = 0.04) immediately after MAR (Fig. 3A and B), but not after 4 h and 24 h of recovery (Table 1). The mean latency of the TA MEPC was 31 ± 1 ms at baseline. There was no significant change in the latency of the MEPC response as a consequence of MAR (Table 1).
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Voluntary activation measured with TMS
For each subject, the size of the superimposed twitch evoked by motor cortical stimulation decreased linearly with contraction strength for contractions of 50–100% (average pre-MAR r2 = 0.927 ± 0.011). The resting twitch evoked by TMS was estimated rather than directly measured (Todd et el. 2004). Figure 4 depicts, for one subject, the linear regression of the amplitude of SIT evoked by TMS during voluntary contractions. Voluntary activation was 75.5 ± 16% at baseline, and was reduced to 61.9 ± 18% immediately after MAR (P = 0.015). After 4 and 24 h recovery, voluntary activation did not differ from baseline values (Table 1).
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There was no significant change in the peak-to-peak amplitude of the MEPP response after MAR. However, a 35 ± 2% decrease in the peripherally evoked potentiated twitch torque was observed after MAR (P = 0.037). After 4 and 24 h of recovery, potentiated twitch torques evoked by PNMS were not significantly different from baseline values (Table 1).
Hand grip strength
No significant change was observed in maximal hand grip force as a consequence of MAR (Table 1).
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Discussion |
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Decrease in dorsiflexor MVC
Studies of fatigue following prolonged (> 2 h) running have tended to evaluate maximal isometric torque of the knee extensors (vastus lateralis), which decreases by 
20% (Millet et al. 2002; Millet et al. 2003). Changes in isometric force generation of the tibialis anterior following prolonged running are not well documented, but our findings of a 16.7% decrease in MVC force is somewhat similar to those decreases found in the vastus lateralis. This impairment of muscle function is indicative of fatigue following the marathon run, which may originate from central and/or peripheral sites.
Central fatigue
Post-MAR depression of corticomotor output.
A depression in postexercise MEPC amplitude of an involved muscle has previously been observed after fatiguing whole-body exercise (Hollge et al. 1997; Verin et al. 2004). However, the decrease in MEPC amplitude in these studies was 35%, whereas in the present study MEPC amplitude was depressed by 67% immediately post-MAR. This difference in the depression of MEPC amplitude postexercise may be due to the nature of the exercise, which previously has involved a short-duration incremental running test to exhaustion (e.g. Verin et al. 2004; mean exercise time, 18 ± 4 min), whereas the present study involved a marathon run. This may reflect the complex activity-dependent changes in corticospinal excitability that relate to differential exercise intensity and duration of whole-body exercise.
The immediate post-MAR decrease in MEPC amplitude suggests that corticomotor output to the tested muscle was depressed as a consequence of the exercise protocol. Although the MEPC amplitude was still depressed by 43% after 4 h of recovery, this result did not reach significance, and after 24 h of recovery MEPC amplitude was restored to baseline values. This ‘profile’ of MEPC amplitude response is similar to that observed after shorter bouts of running (Verin et al. 2004) where immediately after task cessation, quadriceps MEPC amplitude shows the greatest decrease from baseline (35%). The observed depression slowly recovers, so that after 40 min recovery there is a significant MEPC amplitude depression of 26%, and after 60 min, a non-significant depression of 12%. Whilst the depressed MEPC amplitude is evidence of central fatigue, it does not allow discrimination between spinal, cortical or supraspinal sites of fatigue, since it is influenced not only by the excitability of the cortcospinal cells, but also by the excitability of the spinal motoneurones onto which they project (Morita et al. 2000).
Following TMS during tonic contraction of a target muscle, the MEPC response is followed by an interruption of the EMG signal. This cortical silent period (CSP) results from the stimulation of cortical inhibitory pathways, and the resumption of EMG activity depends on the recovery of motor cortical excitability from GABAergic inhibition following the TMS stimulus (Orth & Rothwell, 2004). The notable increase in TA CSP duration immediately and 4 h post-MAR may implicate increased cortical inhibition as a contributing factor to the fatigue-related decrease in dorsiflexor MVC.
Evidence of supraspinal fatigue. Using twitch interpolation, in response to motor cortical stimulation, supraspinal fatigue has been shown to develop in the elbow flexors after sustained maximal isometric contractions (Todd et al. 2003), intermittent contractions (Taylor et al. 2000) and prolonged low-intensity contractions (Sogaard et al. 2006). However, no studies have used this technique after several hours of stretch shortening exercise, which characterizes marathon running. Taylor et al. (2006) observed that this technique has previously been successfully employed in elbow flexors because they have stronger excitatory connections from the motor cortex than the elbow extensors. The ankle flexors are similar, in that stronger TA corticomotoneuronal connections have been observed when compared with those onto soleus motoneurones (Bawa et al. 2002). Since the majority of TA motoneurones are excited monsynaptically (Morita et al. 2000), yet only a very small percentage of soleus motoneurones receive excitatory connections (Brouwer & Qiao, 1995), a near-maximal excitatory response in the ankle flexors can be achieved with only a small response in the ankle extensors, even with the decreased precision in stimulating one muscle or muscle groups from the motor cortex (Taylor et al. 2006).
After MAR, the superimposed twitch evoked by motor cortical stimulation during brief maximal efforts increased. Using the methods of Todd et al. (2004) this superimposed twitch was used to calculate a 14% decrease in voluntary activation immediately after MAR, which demonstrates central fatigue. Central fatigue has also been observed in the knee extensor muscles after a 30 km run, measured by a superimposed electrically evoked twitch delivered at the motor nerve (Millet et al. 2003), demonstrating an 8% decrease in voluntary activation. However, this method cannot define whether the central fatigue originates at a spinal or supraspinal site. In the present study, stimulation of the motor cortex elicited extra output from the cortex, and this extra output recruited additional motoneurones, which resulted in an increment in force production. It is suggested, therefore, that suboptimal output from the motor cortex contributed to this failure of voluntary activation. During the MVC, immediately post-MAR, the motoneurones were not unresponsive to extra input, but it seemed that that the descending drive was not maximal, and the descending drive was insufficient to activate the motoneurone pool optimally (Taylor et al. 2000). This provides evidence that a contribution to fatigue occurs at a supraspinal level.
Whilst we may attribute the observed fatigue to a central locus, and in particular implicate suboptimal output from the motor cortex as a contributing factor to this central fatigue, the mechanisms that underlie the apparent increasing failure to use all cortical output are not fully understood. Taylor et al. (2006) do, however, suggest two possible mechanisms. First, they suggest that changes in the properties of corticospinal neurones or input to corticospinal neurones may reduce descending output from the motor cortex, or second, that the efficacy of output from the motor cortex to produce force is reduced, by less responsive motoneurones or changes in muscle contractile properties.
The observed maintenance of grip strength post-MAR provides evidence that supraspinal fatigue after prolonged running is selective and specific to involved muscles, rather than a global phenomenon. Grip strength has also been observed to be unaltered after a 30 km run (Millet et al. 2003). Nybo (2003) reported that exercise-induced hypoglycaemia attenuates CNS activation during voluntary contraction, but if euglycaemia is maintained throughout exercise, this attenuation is not observed. The subjects in the present study consumed similar amounts of carbohydrate (193 ± 20 g) throughout the marathon run to those studied by Nybo (2003) during 3 h of cycling (200 ± 10 g), who were shown to maintain euglycaemia compared with those subjects who ingested a placebo during exercise. This, along with the maintenance of grip strength after MAR, suggests that hypoglycaemia, which would presumably exert effects globally, did not contribute significantly to the observed central fatigue.
Peripheral fatigue
Peripheral MEP amplitude remained unchanged post-MAR; however, the level of force developed by the TA in response to tibial nerve stimulation was diminished by the exercise protocol. This may suggest that disturbance to the actual structure of the muscle fibre and the excitation–contraction coupling mechanism is the cause of this peripheral fatigue, rather than any reduction in action potential transmission (since MEPP amplitude remained unchanged). An electrically evoked M-wave, commonly used as an index of neuromuscular transmission and action potential propagation in muscle fibres, has also been shown to be unaltered after prolonged endurance exercise (Lepers et al. 2000, 2002; Millet et al. 2002), and it has been suggested that sarcolemmal excitability does not play a fundamental role in fatigue for such exercise (Avela et al. 1999).
It is well reported that long-distance running leads to damage of muscle fibres, especially since running involves a component of eccentric work (Overgaard et al. 2002, 2004). Total muscle Ca2+ and plasma creatine kinase increase after prolonged running of up to 100 km distance (Overgaard et al. 2002), and it has been suggested that Ca2+ accumulation in the muscle may contribute to postexercise muscle damage. The reduction in the peripherally evoked twitch force post-MAR in the present study may result from such disruptions in the muscle contractile machinery.
The results of the present study suggest that there are probably multiple fatigue sites, both peripheral and central, although the most prominent changes post-MAR seem to originate at sites within the CNS. It has previously been hypothesized that the relationship between neural and peripheral fatigue is a safety mechanism, whereby motor unit firing rate is reduced by the CNS to avoid excessive damage to the muscle fibres (Gabriel et al. 2001; St Clair Gibson et al. 2001; Abbiss & Laursen, 2005; Noakes et al. 2005) or to maintain whole-body homeostasis (Noakes et al. 2005). Whilst the mechanisms attributable to this central and peripheral fatigue cannot be definitively assigned, there is evidence within the present study that there is disruption to the contractile muscle machinery after marathon running which is present in conjunction with fatigue at a spinal and supraspinal level.
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