Muscle fatigability is often quantified by the preexercise-to-postexercise reduction in the maximal voluntary contraction (MVC) force or the time to failure of a task performed at a constant power or force level. Several studies reported that, immediately after task failure, the MVC force is higher than the submaximal force that was sustained until failure (8,13,23,29). Consequently, task failure from continuous isometric production of steady low force levels (≤30% MVC) is thought to be largely due to impaired motor drive (“central fatigue”), in contrast to failure from effort at higher intensities when impaired muscle contractility plays an important role (“peripheral fatigue”) (21). Several observations favor this assertion: for instance, during steady low force contractions, the increase in surface EMG signal amplitude remains limited, and at exhaustion, it is still well below that measured during an MVC of the same nonfatigued muscle (7,8,15). Furthermore, compared with the changes in force-generating capacity measured during a sustained contraction performed at 15% MVC with the elbow flexors, the increase in perceived effort was reported to be disproportionately high (31). Finally, Place et al. (23) showed that the MVC force loss consecutive to a prolonged knee extension at 20% MVC was significantly correlated with the reduction in voluntary activation level, as determined with the interpolated twitch technique (19).
Löscher et al. (14) used an elegant approach to determine whether central neural processes were limiting the duration of a sustained isometric plantarflexion performed at 30% MVC. They found that, at task failure, defined as the inability to maintain the initial force level, electrical stimulation enabled to develop the requested force. This finding suggests that a reduction of motor drive was responsible for task failure despite contractile “reserve.” The present study was designed to further investigate the extent to which central mechanisms limit the duration of low-intensity sustained isometric contractions. We chose the knee extensors because a correlation between MVC force loss and impaired voluntary activation level was previously reported (23). The latter finding suggested but did not prove that central fatigue may also limit time to task failure in the knee extensors. Therefore, based on (i) the previously reported correlation between MVC force loss and activation level (23) and (ii) the results obtained by Löscher et al. (14) on plantar flexors, we hypothesized that central fatigue is the main factor limiting the duration of a sustained submaximal isometric contraction (20% MVC) and the force-generating capacity of the knee extensors. We therefore quantified central and peripheral mechanisms responsible for the reduction of muscle force during a sustained contraction of the knee extensors at 20% of MVC in an attempt to verify if the expected central fatigue would affect task failure and MVC force loss to a similar extent.
Fourteen healthy and physically active men (27.8 ± 6.7 yr, 178.6 ± 4.9 cm, 76.5 ± 6.9 kg) volunteered to participate in the study after having been informed of the experimental procedures and possible risks. The study protocol was approved by the Ethics Committee of the University Hospitals of Geneva (protocol 09–284). Before participation, each subject gave written informed consent.
All subjects experienced a familiarization session at least 2 d before the experimental session to get used to controlled voluntary and electrically evoked muscle contractions and to obtain answers to any questions they had regarding the experimental protocol. Each experimental session began with a warming-up period that included between three and six submaximal voluntary isometric knee extensions between 20% and 80% of the estimated MVC force, followed by a 1-min rest before starting the protocol. Two or three MVCs were performed before ET1, and no more than 5% variation between the two last MVCs was tolerated.
The experimental protocol was as follows (Fig. 1):
- Two MVCs (duration of ∼4 s) of the knee flexor muscles separated by 30 s.
- Two or three MVCs of the knee extensor muscles with superimposed doublet and potentiated doublet evoked 3 s after the MVC, separated by 30 s.
- Three single stimuli interspaced by 3 s to evoke M-waves and twitches.
- Fatiguing task, which started after a resting period of 2 min and consisted of:
One MVC of the knee extensors with superimposed and potentiated doublets (called postfatigue MVC).
Three single stimuli interspaced by 3 s.
One MVC of the knee flexor muscles.
- a) Endurance time 1 (ET1): sustained isometric voluntary knee extension at 20% MVC until task failure (defined as the inability to reach the requested force for more than 3 s despite strong verbal encouragement) immediately followed (without any interruption of the contraction) by a MVC with superimposed and potentiated doublets (called post-ET1 MVC).
- b) Myostimulation: 1 min of continuous electrical stimulation of the knee extensors at an initial intensity allowing to reach a force equaling 20% MVC.
- c) ET2: resume of the voluntary contraction targeting 20% MVC, again until voluntary exhaustion, immediately followed by a MVC with superimposed and potentiated doublets (called post-ET2 MVC).
A high-voltage (maximal voltage 400 V) constant-current stimulator (model DS7AH; Digitimer, Hertfordshire, UK) was used to deliver single and paired electrical stimuli to the femoral nerve, to evoke twitch (with the associated M-waves) and doublet responses, respectively. Pulse duration was 1 ms, and the interval between paired stimuli was 10 ms. The femoral nerve was stimulated using a circular cathode with a diameter of 5 cm (Dermatrode; American Imex, Irvine, CA) positioned at the femoral triangle level beneath the inguinal ligament. The anode was a 10 × 5-cm rectangular electrode (Compex, Ecublens, Switzerland) fixed on the gluteal fold opposite the cathode. The optimal intensity of stimulation (i.e., that allowing recruitment of all knee extensor motor units) was considered to be reached when an increase in the stimulation intensity did not induce a further increase in the amplitude of the twitch force and vastus lateralis (VL) compound muscle action potential (M-wave). Once the optimal intensity was found, it was further increased by 10%. The relatively small 10% increment to ensure supramaximal stimulation intensity has been used in previous studies (13,20) and was chosen in the present work to limit the discomfort associated with the stimulation. Then this intensity was kept constant throughout the experiment for each subject. There was no significant response of the antagonist biceps femoris muscle from femoral nerve stimulation.
Myostimulation was delivered continuously for 1 min using a Compex-2 unit (Compex). Two large 15 × 9-cm electrodes (Dermatrode; American Imex) were placed in parallel and perpendicularly over the knee extensor muscle bellies. The intensity of stimulation (maximum range = 0–100 mA) was continuously adjusted with the purpose of maintaining the initial 20% MVC target force. Stimulation frequency was set to 40 Hz (pulse width = 350 µs) to obtain a tetanic response (33) and because it was more comfortable for the subjects than higher stimulation frequencies. It should be noted that maximal stimulator output was reached in several subjects before the end of the 1-min period, and in these cases, it was not possible to further maintain the initial 20% MVC force.
Voluntary and evoked force developed by the knee extensors and flexors was recorded using an isometric ergometer consisting of a custom-built chair equipped with a strain gauge (STS 250 kg; sensitivity = 2.0005 mV·V−1 and 0.0017 V·N−1; SWJ, China). The strain gauge was attached to the chair on one end and securely strapped to the ankle with a custom-made mold. Subjects were seated with a knee angle of 90° and a trunk–thigh angle of 100° (180° = full extension). A target line on a computer screen was used as a visual feedback for the target force during the prolonged contractions. Extraneous movement of the upper body was limited by two crossover shoulder harnesses and a belt across the lower abdomen. In all subjects, the right (dominant) leg was investigated. Force signal was recorded at 1 kHz using an AD conversion system (MP150; BIOPAC Systems, Goleta, CA).
The EMG activity of the VL, vastus medialis (VM), rectus femoris (RF), and biceps femoris (BF) muscles were recorded with pairs of silver chloride (Ag/AgCl) circular (recording diameter = 1 cm) surface electrodes (Medi Trace 100; Kendall, Tyco, Canada) positioned lengthwise over the middle of the muscle belly with an interelectrode (center-to-center) distance of 2 cm. The reference electrode was placed over the patella. Low resistance between the two electrodes (<10 kΩ) was obtained by cleaning and lightly abrading the skin. EMG signals were amplified (gain = 1000) with a bandwidth frequency ranging from 10 to 500 Hz, digitized at a sampling frequency of 2 kHz, and recorded by the AD conversion system. Isometric force and EMG data were stored and analyzed offline with commercially available software (AcqKnowledge software; BIOPAC Systems).
As an index of perceived effort, the RPE was assessed on a scale from 0 to 10 according to Borg (6), every 10–15 s during ET1 and ET2. Throughout the two endurance tasks, the subjects were vividly encouraged to keep on contracting at the target level required.
At the beginning and at the end of the 1-min myostimulation period, the subjects were asked to place a vertical mark on a horizontal visual analog scale (100 mm) to rate the intensity of discomfort. As anchors, we used “no discomfort” (0 mm) and “worst possible discomfort” (100 mm).
Isometric MVC force of the knee extensors and knee flexors was considered as the maximum force attained during the contraction. Voluntary activation level during MVCs was estimated with the superimposed and potentiated doublets according to the following formula (1):
Peak twitch force (i.e., the amplitude of the mechanical response from a single electrical stimulation of a relaxed muscle) was averaged from the three single stimuli; potentiated peak doublet force was also measured.
The EMG signals of the VL, VM, RF, and BF muscles during knee extension and knee flexion MVCs were quantified as the root mean square (RMS) amplitudes for a 500-ms interval around maximum force (250-ms periods either side of the maximum force). EMG RMS of the four muscles was also quantified during ET1 and ET2 every 10% of endurance time. BF EMG RMS calculated during knee extension was normalized to that calculated when this muscle acted as an agonist, that is, during knee flexion MVC, to assess coactivation levels. VL, VM, and RF M-wave peak-to-peak amplitude and duration were calculated and averaged from the three electrical stimuli.
RPE was analyzed at 0%, 25%, 50%, 75%, and 100% of the endurance time for both ET1 and ET2.
Separate one-way ANOVAs were used to compare the different variables (knee extensor MVC force, voluntary activation level, potentiated doublet) at the four different times (prefatigue, post-ET1, post-ET2, and postfatigue), as well as to compare BF EMG RMS (within an ET and between the two ETs) and to compare RPE at 0%, 25%, 50%, 75%, and 100% during the fatiguing task. One-way ANOVAs were used to compare knee flexor MVC force and knee flexor EMG RMS values between prefatigue and postfatigue. Separate two-way ANOVAs [time (0%, 10%, …, 100%) × sustained contraction (ET1 vs ET2)] were used to compare variables (force, knee extensor EMG RMS) during the fatiguing task (every 10% of the endurance time) as well as knee extensor EMG RMS between prefatigue, post-ET1, post-ET2, and postfatigue. Post hoc analyses (Student-Newman-Keuls) were used to test for differences among pairs of means when appropriate. Friedman ANOVA was used in a few cases where conditions to use parametric statistics were not respected. Depending on the outcome of the normality test, paired t-test, or Wilcoxon signed rank test were used to compare prefatigue with postfatigue M-wave data. Pearson correlation coefficients were calculated between selected pairs of variables. The α level for statistical significance was set to P < 0.05. SigmaPlot software for Windows (version 11; Systat, Chicago, IL) was used for the statistical analyses. Data are reported as mean ± SD in text and tables and mean ± SE in figures.
Force and endurance time.
ET1 (246 ± 87 s) was about 3.5 times longer than ET2 (73 ± 27 s; P < 0.001); total endurance time (ET1 + ET2) was 319 ± 80 s. Force remained constant throughout the two sustained submaximal voluntary contractions (P > 0.05; Fig. 2A). A significant decrease in force was observed during the 1-min myostimulation period (P < 0.001; Fig. 2A), despite the increase of stimulation intensity from 71 ± 17 to 97 ± 11 mA and in several subjects to the maximal stimulator output (100 mA; P < 0.001). The level of discomfort significantly increased during the 1-min myostimulation period but remained submaximal, from 35 ± 20 to 51 ± 26 mm, P < 0.05.
We observed an increase in EMG RMS activity for the three knee extensor muscles; this increase being significant from 80% ET1 (P < 0.001; Fig. 2B). The EMG RMS activity of the knee extensor muscles attained 44% ± 12%, 39% ± 17%, and 35% ± 13% of MVC RMS for VL, VM, and RF muscles, respectively, during the final 10% of ET1. We also observed an increase in EMG RMS activity of the antagonist muscle; this increase being significant from 70% ET1 (P < 0.05; Fig. 2B).
Knee extensor EMG RMS activity increased from 60% ET2 (P < 0.001; Fig. 2B), whereas knee flexor EMG RMS activity increased from 20% ET2 (P < 0.05; Fig. 2B).
ET1 versus ET2.
We further observed that, from 20% ET2, EMG RMS activity of the knee extensors and knee flexors was higher during ET2 in comparison to the same time point expressed as a percentage of ET1 (P < 0.05; Fig. 2B).
RPE significantly increased during both ET1 and ET2 (P < 0.01; Fig. 2C) and was higher at the start of ET2 compared with the start of ET1 (3.6 ± 2.2 vs 1.5 ± 1.0, P < 0.001; Fig. 2C).
The decrease in MVC force was 51% ± 11% at post-ET1 and 57% ± 12% at post-ET2 MVC (P < 0.05; Fig. 3A). We observed a significant MVC force recovery between post-ET2 and postfatigue MVC (P < 0.05; Fig. 3A), whereas only ∼7 s separated these two MVCs; MVC force reduction measured during postfatigue MVC was 44% ± 9% (P < 0.05). Decreases in the knee extensor’s averaged maximal EMG RMS of ∼16% and ∼12% were also observed (P < 0.05; Fig. 3B) during post-ET1 and post-ET2 MVC, respectively. Knee flexor MVC remained unchanged after the fatiguing protocol (from 176 ± 32 to 172 ± 29 N, P > 0.05), and BF maximal EMG RMS was also unaltered (P > 0.05).
A slight but significant reduction in voluntary activation level was observed at post-ET1 MVC from 93% ± 7% to 87% ± 10% (P < 0.01; Fig. 4A). No further decrease was detected at post-ET2 MVC, and complete recovery was attained at postfatigue.
We observed a decrease in potentiated peak doublet force after ET1 (−36.7% ± 14.7%, P < 0.001; Fig. 4B); the drop in peak doublet force was even greater after ET2 (−48.3% ± 17.2%, P < 0.001; Fig. 4B), with no recovery at postfatigue. Peak twitch force decreased (P < 0.001) from 98.6 ± 15.5 to 47.5 ± 22.7 N after the whole fatiguing protocol, i.e., a reduction of 50.8% ± 23.9%, whereas M-wave properties remained unchanged for VL, VM, and RF muscles (P > 0.05; Table 1).
To gain insight into the mechanisms underlying muscle fatigue and muscle fatigability, we correlated (i) MVC force loss with potentiated doublet force reduction and (ii) the duration of the initial sustained contraction (ET1) with the average voluntary EMG RMS attained at the end of ET1, respectively. We observed a linear correlation (r = 0.77, P < 0.01; Fig. 5A) between the decrease in post-ET2 MVC force and the reduction in potentiated doublet after ET2, as well as a trend (P = 0.06) for a relationship between MVC loss and potentiated doublet reduction after ET1. The latter correlation was also found postfatigue (r = 0.70, P < 0.01; data not shown).
A linear correlation between the knee extensor averaged EMG RMS (average of VL, VM, and RF muscles’ EMG RMS) during the last 10% of ET1 and ET1 was also found (r = 0.62, P < 0.05; Fig. 5B). However, we did not find any relationship between the MVC reductions consecutive to ET1 and ET1, neither between the MVC reductions consecutive to ET2 and ET2.
In the present study, we used a combination of voluntary and electrically evoked contractions to induce fatigue and assessed the mechanisms of muscle fatigability distinguishing between central and peripheral adjustments. Our results show that 1) at task failure from a maximally sustained 20% MVC contraction (ET1), the knee extensors were still able to develop the target force (20% MVC) when electrically stimulated; 2) peripheral contractile impairment (as evidenced by the reduction in potentiated peak doublet force) was far greater than activation failure; 3) all subjects were able to resume the submaximal voluntary contraction for more than 1 min on average after the completion of the continuous electrical stimulation period.
This study presents some limitations. First, although increasing the intensity of myostimulation up to the maximal stimulator output allowed to reach and maintain the 20% MVC target, it was not possible to sustain this force level for 1 min in most subjects. Our results are similar to those of Löscher et al. (14): force level during myostimulation was not reported in their study but their Figure 1A indicates that the force evoked by myostimulation was quite unstable compared with voluntary force. Second, myostimulation certainly did not recruit motor units in the same way (both spatially and temporally) as did voluntary contraction (22), and it can be speculated that some motor units, perhaps those located the furthest from the stimulation electrodes, were given a break and could partially recover over the myostimulation period. Nevertheless, small diameter afferents, whose role in muscle fatigue has been debated recently (2), were most probably solicited during myostimulation (14). The present results show that all subjects were able to resume the voluntary contraction at 20% MVC after the myostimulation period with lower EMG RMS activities and lower RPE than at the end of ET1, suggesting that muscle afferents were most certainly not the only limitations to exercise performance (14,30). Similarly, our findings indicate that task failure does not seem to be associated to a peripheral fatigue threshold because the reduction in potentiated peak doublet force was greater after ET2 than after ET1.
Finally, it should also be kept in mind that the experiment has been done in laboratory conditions, and the endurance time might also depend on motivational factors; to limit the lack of motivation that might occur during the exercise, subjects were vigorously encouraged and a small money prize was awarded for the longest total endurance time (ET1 + ET2).
Endurance Time and MVC Force Reduction
We found an ET1 of 246 ± 87 s, which is in agreement with the duration of 291 ± 84 s found in a previous study conducted on the knee extensors at the same intensity and at a comparable knee angle (29). Similarly, Matkowski et al. (17) obtained an endurance time of 295 ± 85 s for the same target force (20% MVC) at a knee angle of 80°.
The 50% force loss we observed during post-ET1 MVC is greater than that reported in earlier studies (42% in Rochette et al. , 37% in Matkowski et al. , and 28% in Place et al. ) and underlines the importance of assessing MVC force as closely as possible to the voluntary exhaustion point; in the studies cited above, subjects were allowed to relax for a few seconds before measuring MVC after exercise, which certainly led to an underestimation of the MVC force loss at task failure. This is confirmed by the significant recovery we observed in MVC force between post-ET2 and postfatigue MVC, where the time between task failure and the postfatigue MVC was 7.3 ± 1.6 s.
Task failure from central origin.
In the present study, several findings suggest that the task duration was limited by central mechanisms:
- Although at ET1, the 20% MVC force goal could not be sustained any more and the subjects stopped their effort, they were able to produce a greater force (∼50% of the initial MVC) during a brief MVC performed immediately after ET1, despite not having had time to recover. We believe that this surprising result may be explained, at least in part, by the central role of the brain in determining the end of the exercise (11). Our results support the hypothesis that exhaustion from a voluntary knee extensor muscle contraction effort may occur well before recruitment is complete, despite maximum levels of perceived exertion (see point 4 below). On the other hand, although our cooperative and willing subjects were strongly encouraged and knew that a money prize would be awarded for the longest endurance time, we cannot fully exclude that lack of motivation led to early disengagement from the task (16).
- Immediately after the point of voluntary exhaustion (task failure), all subjects were capable of developing the target force (20% MVC) under electrical stimulation, as previously observed by Löscher et al. (14) on the plantar flexor muscles. This intriguing finding suggests that processes within the knee extensor muscles themselves were not directly limiting the task. It is important to mention that the time between the end of ET1 and the myostimulation task was only 5.1 ± 1.5 s, which possibly prevented any recovery process; this duration was significantly (P < 0.01) shorter than the transition between post-ET2 and postfatigue MVCs. We also observed that, in most subjects, the maximal output (100 mA) of our stimulator was reached well before the end of the 1-min period; as a result, force decreased significantly throughout the myostimulation period because of important local fatigue (see below). Despite that, peripheral stimulation was maintained during this period. As a consequence, RPE was greater at the beginning of ET2 than at the beginning of ET1, which indicates that a greater effort was required to maintain the target force level after myostimulation. Accordingly, we also found greater EMG RMS activity throughout ET2 than throughout ET1. These results corroborate previous findings of Søgaard et al. (31), who evidenced central (supraspinal) fatigue during MVCs performed regularly during a sustained submaximal elbow flexion (15% MVC), whereas the perceived effort increased disproportionally during the low-intensity task. In the present study, the decrease in voluntary activation level was much less (−7% at ET1) than that observed by Søgaard et al. (−30%) (31). This would suggest that activation failure depends on the muscle, the intensity, and the duration of the sustained contraction (elbow flexors, 15% MVC, 43 min in Søgaard et al. (31); vs knee extensors, 20% MVC, 4 min for ET1 in the present study). Søgaard et al. (31) concluded that “central fatigue may have contributed to the disproportionate increase in perceived effort reported during the prolonged low-force contraction”; similarly, in our study, there was clear evidence that peripheral fatigue was not limiting the duration of the sustained contraction. Collectively, these results indicate that the assessment of voluntary activation during MVCs may be inappropriate for determining whether or not task failure of a submaximal exercise is due to central factors.
- All subjects were able to resume the voluntary contraction and to sustain the required target force for another 73 s after myostimulation. This corroborates the results obtained by Löscher et al. (14) on the triceps surae, where subjects were able to maintain the target force for another 85 s after myostimulation. This, again, points to activation failure as a reason for task failure, whereas the hypothesis of relative recovery of the central nervous system during myostimulation (14) could explain the relatively long duration of ET2 in our study. Furthermore, our finding of a considerable decrease in RPE between the end of ET1 and the start of ET2 favors the hypothesis of a central limitation of the task.
- The level of EMG RMS activity measured at the end of ET1 remained considerably below the EMG RMS activity measured during the prefatigue MVC, as reported for instance by Löscher et al. (14,15) and Fuglevand et al. (8). Indeed, during the last 10% of ET1, the averaged RMS was only 40% of the prefatigue MVC RMS, and it was slightly higher (47%) when normalized by post-ET1 MVC. EMG amplitude cancellation may partly explain the inability to approach maximal EMG RMS values (7), although the use of EMG RMS values normalized to the MVC EMG RMS values certainly minimized this phenomenon (12). Again, this shows that central neural mechanisms limited the ability to recruit more motor units to continue the exercise. This hypothesis is illustrated by the correlation presented in Figure 5B, which suggests that exercise duration is limited by the inability of the subjects to increase motor unit recruitment, as previously discussed in point 1. The fact that EMG RMS activity was higher during ET2 than ET1 seems to confirm this hypothesis. It has been shown that the EMG RMS activity recorded at the end of a sustained fatiguing contraction performed at 50% MVC with the ankle dorsiflexors almost equals (∼93%) the postfatigue MVC EMG RMS (13), indicating a lower degree of central fatigue than presently found. This lets us believe that activation failure would be more important at low contraction intensities (such as the 20% MVC in the present study) than at higher ones (21).
However, our results do not favor central neural mechanisms as the principal cause of MVC force reduction, in contrast to what we observed in a previous study performed at the same relative intensity (23). These contradictory findings might be explained by differences between the two studies in muscle length (knee angle of 90° vs 35° or 75°), recovery time between the end of the endurance time (no recovery vs ∼15 s) and peripheral fatigue index (potentiated vs nonpotentiated doublet). Indeed, we only observed a slight decrease in voluntary activation level, in accordance with the results of Matkowski et al. (17). Voluntary activation level is supposed to reflect central adaptations, and one would have expected a large drop in this parameter if the mechanisms underlying MVC force reduction and time to task failure were similar. It should be remembered that no consensus has been reached in the scientific community regarding central fatigue and the validity of the twitch interpolation technique (3,10,26). Despite this lack of consensus, if a large drop in voluntary activation occurred during the MVC, the twitch interpolation technique would have been able to detect it.
MVC force loss is related to peripheral fatigue.
We observed an increased EMG RMS activity during ET1 and ET2 as widely reported for sustained submaximal contractions of the knee extensors (21,29,32) and other muscle groups (8,9,14,18,31). This is thought to reflect additional recruitment of motor units and/or to increased firing frequency to maintain the same force level in view of the loss of force from other motor units, thus providing indirect evidence of an increased central drive necessary to compensate for peripheral fatigue development.
We also noted a decrease in potentiated peak doublet and peak twitch forces. The absence of alteration in M-wave properties indicates that action potential propagation or transmission was not impaired (4), and the reduced evoked force can thus be attributed to alterations located beyond the sarcolemma (i.e., contractile failure), presumably involving Ca2+ handling (27). Similar results have been observed after sustained knee extensor (21,24,25,28,32) and elbow flexor (5,31) contractions. M-wave properties are usually impaired after myostimulation of the quadriceps muscle (34); the absence of alteration in M-wave parameters after the entire protocol may be attributed to the delay (and thus, to the relative recovery) between the end of the stimulation period and the evoked twitches (although ET2 was performed in this time frame) and to the stimulation parameters used in our study in comparison to Zory et al. (34): 40 versus 75 Hz, continuous versus intermittent stimulation, which resulted in 20% versus ∼40% MVC force evoked at the start of the exercise. The current findings suggest that the exercise-induced reduction in maximal force-generating capacity may largely be explained by an impairment in any of the final steps of the excitation–contraction coupling process, involving Ca2+ release, myofibrillar sensitivity to Ca2+ and/or the force produced by each active cross-bridge.
These results are in contrast with our findings suggesting that central mechanisms limited the duration of the sustained submaximal contraction. Loss seems to be more related to the extent of contractile failure (as evidenced by the strong correlation between MVC force loss and the decline in peak doublet force; Fig. 5A).
This study was supported by the De Reuter Foundation, the Geneva Academic Society, and the Ernest Boninchi Foundation.
The authors thank Marc Buclin for the design and conception of the ergometer, the Cefar-Compex company (Ecublens, Switzerland) for providing the stimulator and all the subjects who volunteered to participate.
The authors have no conflict of interests.
The results of the present study do not constitute endorsement by the American College of Sports Medicine.
1. Allen GM, Gandevia SC, McKenzie DK. Reliability of measurements of muscle strength and voluntary activation using twitch
interpolation. Muscle Nerve. 1995; 18 (6): 593–600.
2. Amann M, Secher NH. Point: Afferent feedback from fatigued locomotor muscles is an important determinant of endurance exercise performance. J Appl Physiol. 2010; 108 (2): 452–4; discussion 457; author reply 470.
3. Babault N. The interpolated twitch
to determine voluntary activation in various conditions. J Appl Physiol. 2009; 107 (1): 360; discussion 367–8.
4. Bigland-Ritchie B, Kukulka CG, Lippold OC, Woods JJ. The absence of neuromuscular transmission failure in sustained maximal voluntary contractions. J Physiol. 1982; 330: 265–78.
5. Bilodeau M, Henderson TK, Nolta BE, Pursley PJ, Sandfort GL. Effect of aging on fatigue characteristics of elbow flexor muscles during sustained submaximal contraction. J Appl Physiol. 2001; 91 (6): 2654–64.
6. Borg GA. Psychophysical bases of perceived exertion. Med Sci Sports Exerc. 1982; 14 (5): 377–81.
7. Dideriksen JL, Enoka RM, Farina D. Neuromuscular adjustments that constrain submaximal EMG amplitude at task failure of sustained isometric contractions. J Appl Physiol. 2011; 111 (2): 485–94.
8. Fuglevand AJ, Zackowski KM, Huey KA, Enoka RM. Impairment of neuromuscular propagation during human fatiguing contractions at submaximal forces. J Physiol. 1993; 460: 549–72.
9. Gamet D, Maton B. The fatigability of two agonistic muscles in human isometric voluntary submaximal contraction: an EMG study. I. Assessment of muscular fatigue by means of surface EMG. Eur J Appl Physiol Occup Physiol. 1989; 58 (4): 361–8.
10. Herzog W. Twitch
interpolation represents muscle activation in a qualitative manner only. J Appl Physiol. 2009; 107 (1): 360–1; discussion 367–8.
11. Kayser B. Exercise starts and ends in the brain. Eur J Appl Physiol. 2003; 90 (3–4): 411–9.
12. Keenan KG, Farina D, Maluf KS, Merletti R, Enoka RM. Influence of amplitude cancellation on the simulated surface electromyogram. J Appl Physiol. 2005; 98 (1): 120–31.
13. Lévenez M, Kotzamanidis C, Carpentier A, Duchateau J. Spinal reflexes and coactivation of ankle muscles during a submaximal fatiguing contraction. J Appl Physiol. 2005; 99 (3): 1182–8.
14. Löscher WN, Cresswell AG, Thorstensson A. Central fatigue during a long-lasting submaximal contraction of the triceps surae. Exp Brain Res. 1996; 108 (2): 305–14.
15. Löscher WN, Cresswell AG, Thorstensson A. Excitatory drive to the alpha-motoneuron pool during a fatiguing submaximal contraction in man. J Physiol. 1996; 491 (Pt 1): 271–80.
16. Marcora SM, Staiano W, Manning V. Mental fatigue impairs physical performance in humans. J Appl Physiol. 2009; 106 (3): 857–64.
17. Matkowski B, Place N, Martin A, Lepers R. Neuromuscular fatigue differs following unilateral vs bilateral sustained submaximal contractions. Scand J Med Sci Sports. 2011; 21 (2): 268–76.
18. Maton B, Gamet D. The fatigability of two agonistic muscles in human isometric voluntary submaximal contraction: an EMG study. II. Motor unit firing rate and recruitment. Eur J Appl Physiol Occup Physiol. 1989; 58 (4): 369–74.
19. Merton PA. Voluntary strength and fatigue. J Physiol. 1954; 123 (3): 553–64.
20. Papaiordanidou M, Guiraud D, Varray A. Does central fatigue exist under low-frequency stimulation of a low fatigue-resistant muscle? Eur J Appl Physiol. 2010; 110 (4): 815–23.
21. Place N, Bruton JD, Westerblad H. Mechanisms of fatigue induced by isometric contractions in exercising humans and in mouse isolated single muscle fibres. Clin Exp Pharmacol Physiol. 2009; 36 (3): 334–9.
22. Place N, Casartelli N, Glatthorn JF, Maffiuletti NA. Comparison of quadriceps inactivation between nerve and muscle stimulation. Muscle Nerve. 2010; 42 (6): 894–900.
23. Place N, Maffiuletti NA, Ballay Y, Lepers R. Twitch
potentiation is greater after a fatiguing submaximal isometric contraction performed at short vs. long quadriceps muscle length. J Appl Physiol. 2005; 98 (2): 429–36.
24. Place N, Martin A, Ballay Y, Lepers R. Neuromuscular fatigue differs with biofeedback type when performing a submaximal contraction. J Electromyogr Kinesiol. 2007; 17 (3): 253–63.
25. Place N, Matkowski B, Martin A, Lepers R. Synergists activation pattern of the quadriceps muscle differs when performing sustained isometric contractions with different EMG biofeedback. Exp Brain Res. 2006; 174 (4): 595–603.
26. Place N, Yamada T, Bruton JD, Westerblad H. Interpolated twitches in fatiguing single mouse muscle fibres: implications for the assessment of central fatigue. J Physiol. 2008; 586 (Pt 11): 2799–805.
27. Place N, Yamada T, Bruton JD, Westerblad H. Muscle fatigue: from observations in humans to underlying mechanisms studied in intact single muscle fibres. Eur J Appl Physiol. 2010; 110 (1): 1–15.
28. Plaskett CJ, Cafarelli E. Caffeine increases endurance and attenuates force sensation during submaximal isometric contractions. J Appl Physiol. 2001; 91 (4): 1535–44.
29. Rochette L, Hunter SK, Place N, Lepers R. Activation varies among the knee extensor muscles during a submaximal fatiguing contraction in the seated and supine postures. J Appl Physiol. 2003; 95 (4): 1515–22.
30. Smirmaul Bde P, Fontes EB, Noakes TD. Afferent feedback from fatigued locomotor muscles is important, but not limiting, for endurance exercise performance. J Appl Physiol. 2010; 108 (2): 458.
31. Søgaard K, Gandevia SC, Todd G, Petersen NT, Taylor JL. The effect of sustained low-intensity contractions on supraspinal fatigue in human elbow flexor muscles. J Physiol. 2006; 573 (Pt 2): 511–23.
32. West W, Hicks A, McKelvie R, O’Brien J. The relationship between plasma potassium, muscle membrane excitability and force following quadriceps fatigue. Pflugers Arch. 1996; 432 (1): 43–9.
33. Wüst RC, Morse CI, de Haan A, Jones DA, Degens H. Sex differences in contractile properties and fatigue resistance of human skeletal muscle. Exp Physiol. 2008; 93 (7): 843–50.
34. Zory R, Boerio D, Jubeau M, Maffiuletti NA. Central and peripheral fatigue of the knee extensor muscles induced by electromyostimulation. Int J Sports Med. 2005; 26 (10): 847–53.