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Discipline of Physiology and Research Centre for Human Movement Control, School of Molecular and Biomedical Science, The University of Adelaide, Adelaide, Australia
Submitted 17 December 2007 ; accepted in final form 6 August 2008
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ABSTRACT |
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2x greater) with the greatest effect at low forces. LFF was equivalent immediately after both types of exercise (50–60% reduction in 20:100 Hz force) with a slower recovery following eccentric exercise. A significant association was found between the change in LFF and EMG (r2 values up to 0.52), with the strongest correlations observed at low forces (20% MVC) and at 2 h after exercise. In contrast, there were no significant associations between LFF and force fluctuations during voluntary or electrically evoked contractions, suggesting that other physiological factors located within the muscle are likely to be playing a major role in the impaired motor performance after eccentric exercise. motor performance; eccentric exercise; motor unit; electrical stimulation
Although several mechanisms are possible (see 31), one of the most appealing explanations for an increase in EMG and force fluctuations after eccentric exercise involves an increase in low-frequency fatigue. Low-frequency fatigue is the disproportionate loss of force at low compared with high frequencies of electrical stimulation and is induced following fatiguing exercise (7, 15, 22), with the greatest effect after eccentric exercise (15, 22). Low-frequency fatigue is caused by an impairment of one or more processes of excitation-contraction coupling (7), most likely due to a decrease in calcium release from the sarcoplasmic reticulum (3, 36), with the prolonged recovery after eccentric exercise possibly due to damage and subsequent repair of the contractile machinery within the muscle (38). Several authors have suggested that low-frequency fatigue would lead to increased muscle activation (6, 11, 28), as single motor units discharging at low rates would no longer be producing an equivalent force, necessitating the recruitment of additional motor units and an increase in discharge rate of the already active motor units to compensate for the force loss. Although the deficit in force with low-frequency fatigue can be substantial (50% or more) and long lasting (hours to days), the consequences of this aspect of fatigue have not been established (14).
The purpose of this study was to quantify the association between low-frequency fatigue and the increase in EMG and force fluctuations observed after concentric and eccentric exercise of the elbow flexor muscles. To achieve this goal, we have assessed low-frequency fatigue following electrical stimulation of the biceps brachii muscle and compared it with biceps brachii EMG and elbow flexor force fluctuations obtained before and after concentric and eccentric exercise. On the basis of our previous study (31), we have included an additional measure of EMG and force fluctuations obtained at 2 h after eccentric exercise, as this is likely to coincide with the point of maximum muscle damage while allowing recovery from metabolic fatigue (32, 34). Furthermore, in contrast to previous studies (15, 22), we have examined low-frequency fatigue after concentric and eccentric exercise when the impairment in maximum force is equivalent under both conditions. Using this protocol, we expect to find greater low-frequency fatigue of the biceps brachii after eccentric compared with concentric exercise (15, 22). We also expect that the increase in low-frequency fatigue will be associated with the increase in EMG and force fluctuations following eccentric exercise. These findings would suggest that increased low-frequency fatigue may contribute to the nonlinear EMG-force relation and be detrimental to the performance of submaximal contractions after eccentric exercise.
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METHODS |
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Experimental Arrangement
The experimental arrangement was similar to that which has been described in detail previously (31). Subjects were seated with their forearm positioned vertically and supinated, with the upper arm and forearm at a 90° angle. This allowed isometric force to be measured in the sagittal plane. The forearm was fitted with a heat-moulded plastic cast and secured with two 1-in.-wide nylon straps.
Electrical stimulation was applied to the biceps brachii muscle through 5-cm2 neurostimulation electrodes (PALS, Axelgaard Manufacturing). The cathode was placed over the muscle belly and the anode over the distal tendon. Force evoked from electrical stimulation was recorded using a sensitive transducer (range 0–112 N; model MLP-25, Transducer Techniques) located perpendicular to the forearm at the level of the wrist and mounted on a customized manipulandum. Output from the force transducer was recorded on a digital tape recorder and displayed on an oscilloscope.
Surface EMG was recorded with bipolar electrodes (silver-silver chloride, 4-mm diameter) placed 2 cm apart over the upper third of biceps brachii and medial head of triceps brachii. A grounding wrist strap acted as a common reference for all EMG recordings. After the first experimental session, electrodes and stimulation gel pads were removed and their positions marked on the skin for correct placement during the follow-up session performed 24 h later. The EMG signals were amplified (500–1,000x), band-pass filtered (high pass at 13 Hz, low pass at 1,000 Hz), and recorded on a digital tape.
Experimental Procedures
Subjects performed three tasks, two requiring voluntary isometric contraction of the elbow flexor muscles (MVC and a constant-force task) and a third task involving electrical stimulation of the biceps brachii. The three tasks were performed before, immediately after, 2 h after, and 24 h after either eccentric (right arm) or concentric exercise (left arm). The tasks were performed 2 h after exercise as it was expected that this would be the point of maximal muscle damage without fatigue (34), whereas they were performed 24 h after exercise as there is likely to be pain associated with delayed-onset muscle soreness at this time.
MVC force. Subjects performed a 3-s ramp contraction (zero to maximum) in the flexion direction and then maintained the contraction for a further 3 s, receiving strong verbal encouragement. Subjects performed multiple MVCs until two forces were within 5% of each other. This task was then repeated in the extension direction. At least 1 min of recovery was provided between contractions.
Constant-force task. Submaximal isometric contractions were performed at target forces of 5, 10, 20, 40, and 60% MVC expressed relative to the MVC that preceded the submaximal contraction. This was performed to normalize the target force to the maximum force capability of the muscle at that particular time point, with the expectation that EMG should scale linearly with increasing force. A less sensitive force transducer (range 0–670 N; model MLP-150, Transducer Techniques) recorded force for both the MVC and constant-force tasks. Subjects were instructed to match a target elbow-flexor force as closely as possible for 12 s that was represented by a horizontal line located on an oscilloscope. The horizontal target line on the oscilloscope remained in the same location for each target force by adjusting the gain on the vertical axis. Constant-force tasks were randomized with 30 s recovery between tasks.
Electrical stimulation.
To determine the stimulus intensity for the force-frequency measurements, trains of stimuli (1-s train duration, 0.1-ms stimulus duration) were delivered at 100 Hz with a Digitimer (Hertfordshire, UK) DS7A constant-current stimulator that was externally triggered using an appropriate output pulse from a digital-to-analog converter (model 1401) generated using Spike 2 (Cambridge Electronic Design, Cambridge, UK). The amplitude of the stimulus gradually increased until a 10% MVC was achieved. This intensity equated to 25% of the total force-generating capacity of biceps brachii, which was determined from preliminary experiments involving supramaximal stimulation in a previous study using a similar protocol (30). This intensity was selected to reduce discomfort from the electrical stimulation and to avoid unwanted activation of the triceps brachii muscle. Previous studies have shown that the results obtained with submaximal electrical stimulation provide a reliable estimate of the contractile properties of the whole muscle (7, 13). At this intensity, 12 trains of stimuli at various frequencies (1, 5, 10, 20, 30, 40, 50, 60, 70, 80, 90, 100 Hz) were delivered randomly to the biceps brachii muscle with a rest period of 10 s between stimuli. All subjects tolerated the intensity and frequency of stimulation.
Exercise
Eccentric exercise.
Subjects were seated at a bench that consisted of an adjustable height seat and a padded support for the upper arm that was positioned 45 degrees from the torso and their forearm held vertically. A load was placed in the hand by the experimenter, and subjects lowered the weight from an elbow joint angle of 45° (forearm held vertical) to full extension (135° range of motion) by eccentrically contracting the elbow flexor muscles. The load was set to 40% of the subject's isometric MVC obtained at 90° flexion (24, 25). Each eccentric contraction lasted 3 s followed by a 3-s rest and was performed in time with a metronome. During the rest period, the experimenter removed the load, and the subject returned his arm to the starting position. Exercise consisted of 10 repetitions per set, and each set was separated with a 20-s rest interval. Exercise continued until the subject's MVC decreased by at least 30%. This was regularly assessed on a separate testing apparatus by performing brief MVCs after every set of 10 contractions once there were visible signs of tremor and verbal confirmation from the subject that he was having difficulty controlling the load during the contraction. The required force reduction was achieved with 30–170 contractions in all subjects.
Concentric exercise.
In a separate session, subjects lifted the load from full elbow extension to a fully flexed position (135° range of motion) over 3 s, with 3 s rest between contractions. The experimenter removed the load following the concentric contraction, and the subject returned the arm to a fully extended position. The load during concentric exercise was set to 30% MVC (35). Ten repetitions were performed followed by 20 s rest between sets. Exercise continued until subject's MVC decreased by 30%, which required from 50 to 165 contractions for all subjects.
Muscle damage. In addition to the reduction in maximal force, muscle damage was assessed using two other indirect indicators. Relaxed elbow angle was measured using three landmarks of the arm: the midpoint of the acromion and coracoid process, the lateral epicondyle of the humerus, and the midpoint of the ulnar and radius styloid processes. These three points were marked with a permanent ink pen to facilitate comparisons between days. With the subject's arm hanging relaxed by his side, a goniometer was lined up to the three points and the elbow angle was recorded. Subjects were asked to rate their pain within the muscle using a visual analog scale (0 = no pain, 10 = extremely painful) during forced extension of the elbow joint, which was performed with the experimenter slowly moving the forearm to 180° (full extension). Relaxed elbow angle and pain were measured before exercise and at the conclusion of each testing session (immediately after, 2 h after, and 24 h after exercise).
Data Analysis
All recorded signals were downloaded onto a computer hard drive using a 16-bit analog-to-digital converter (model 1401, CED) and sampled at either 200 Hz (MVC and submaximal force) or 2,000 Hz (EMG and electrical stimulation force). All data were analyzed offline using customized scripts within the Spike2 data analysis software. The EMG from the MVC was full-wave rectified, and the average EMG was measured during a 1-s period at the point of maximum force production. During the constant-force task, a 10-s sample of force during the middle of the trial was used to calculate the mean and coefficient of variation (CV) of force, which is used to quantify force fluctuations. EMG from biceps brachii and triceps brachii was rectified and averaged over a user-defined 1-s period corresponding to a stable portion of the EMG and force record. EMG obtained during the constant-force task was normalized to the maximum EMG obtained during the most recent MVC to facilitate comparisons between subjects and across time periods. To calculate force variability during the electrical stimulation task, the mean force was calculated from the middle 0.5 s of the contraction. The SD and CV of force were quantified over the same time epoch after removing any slow drift in force with a detrending procedure using a digital high-pass filter at 0.5 Hz.
Statistical Analysis
For MVC, maximum elbow flexor force was analyzed with a two-way ANOVA with a repeated-measures design, with one between-subject factor of exercise (eccentric, concentric) and one within-subject factor of time (before, immediately after, 2 h after, and 24 h after). For the constant-force tasks, a three-way repeated-measures ANOVA for exercise, time, and force level (5, 10, 20, 40, and 60% MVC) was used to compare CV of force and average EMG. A two-way repeated-measures ANOVA for exercise and time was used to compare 20:100 Hz force, which was used as an indicator of low-frequency fatigue (7, 22). Correlations between changes in CV and EMG with low-frequency fatigue were performed using simple linear regression analysis. A two-way repeated-measures ANOVA for exercise and time was used to compare both relaxed elbow angle and pain. Significant main effects in the ANOVA were analyzed using a Fisher's post hoc test that performed all possible comparisons. Statistical significance was designated at P < 0.05 for all comparisons, and all values are reported as means ± SE.
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RESULTS |
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35% (312 ± 14 N before exercise to 207 ± 14 N immediately after exercise, P < 0.001), which was achieved with a mean load of 12.6 ± 0.6 kg and required an average of 63 ± 12 contractions. MVC remained significantly depressed 2 h (30%) and 24 h after eccentric exercise (22%) despite some recovery (P < 0.05; Fig. 1A). Concentric exercise also resulted in a reduction in MVC of 35% (281 ± 17 N before to 190 ± 12 N immediately after, P < 0.001), which required an average of 99 ± 12 contractions with a mean load of 8.0 ± 0.4 kg. MVC had recovered 2 h after (254 ± 17 N) concentric exercise (Fig. 1A). Maximum EMG was not different between concentric and eccentric exercise (exercise effect, P = 0.14). Furthermore, the maximum EMG at the different recording times was consistent between the two exercise conditions (exercise x time interaction, P = 0.99). No significant differences were observed for maximum triceps EMG between exercise conditions or at the different recording times.
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Constant-Force Task
Figure 2 shows original data for a single subject during an electrical stimulation task and a 10% MVC constant-force task before and after eccentric exercise. The MVC for this subject was 347 N before, 247 N 2 h after, and 290 N 24 h after eccentric exercise. After eccentric exercise there was a reduction in both the 20-Hz and 100-Hz force, with a greater relative decline in force at 20 Hz. The 20:100 Hz ratio declined by 50% 2 h after (0.48 before to 0.23) eccentric exercise, indicating an increase in low-frequency fatigue (7, 22). The 20:100 Hz force was not fully recovered 24 h after the exercise (0.38). The constant-force trial for the same subject (Fig. 2, bottom) shows biceps brachii and triceps brachii EMG as well as force during a 10% MVC task. At each time point the target force was normalized to the subject's maximum strength at that time point, to ensure that the subject was contracting at the same relative force. Despite this, biceps brachii EMG was 3% of maximum EMG before exercise, 27% of maximum (8x larger) 2 h after, and 8% of maximum 24 h later. Similarly, the CV of force during this trial was 2.7% before exercise, 4.1% 2 h after exercise, and 2.8% 24 h later.
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0.02). Electrical Stimulation
Peak force following electrical stimulation of the biceps brachii was measured across a range of frequencies and expressed relative to the peak force obtained at 100 Hz (Fig. 4). The effect of both forms of exercise was to shift the force-frequency curve to the right (Fig. 4, A and B), indicating that a lower force was produced at any given frequency of stimulation after exercise. This effect was most pronounced at low frequencies of stimulation when measured immediately after both concentric and eccentric exercise. To quantify this shift in the force-frequency curve, the ratio of 20:100 Hz peak force was obtained as an indicator of the extent of low-frequency fatigue (Fig. 4C), although this procedure may underestimate the extent of low-frequency fatigue if a force plateau has not been reached with high-frequency stimulation (see Fig. 4, A and B). This analysis reveals that there was a significant decline (50–60% reduction) in 20:100 Hz force immediately after both concentric and eccentric exercise. For eccentric exercise, the 20:100 Hz force was 0.53 ± 0.04 before exercise and 0.21 ± 0.02 immediately after exercise (P < 0.001), whereas for concentric exercise it was 0.55 ± 0.03 before and 0.26 ± 0.02 immediately after exercise (P < 0.001). No significant difference was observed in 20:100 Hz force between concentric and eccentric exercise when examined immediately after exercise. However, there was a much faster recovery of 20:100 Hz force after concentric compared with eccentric exercise. At 2 h after eccentric exercise, the 20:100 Hz force was significantly lower (55% reduction) compared with 2 h after concentric exercise (24% reduction, P < 0.001). The 20:100 Hz force remained significantly depressed (40% reduction) 24 h after eccentric exercise but had recovered 24 h after concentric exercise. Furthermore, the fluctuations in force at 20-Hz stimulation were larger in eccentric compared with concentric exercise (exercise effect, P = 0.02). Despite no difference before exercise, the force fluctuations were 3x larger immediately after and 2x larger 2 h after eccentric compared with concentric exercise (exercise x time effect, P = 0.004; Fig. 4D). No difference between exercise conditions was observed at any time point with 100-Hz stimulation (all CV values ranged from 0.40 to 0.53%).
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To assess the association between low-frequency fatigue and the increase in EMG and force fluctuations during voluntary contractions, a linear correlation was performed for the change (after – before) in 20:100 Hz force compared with the change (before – after) in EMG and force fluctuations (CV of force) induced by concentric and eccentric exercise. A significant positive correlation indicated that an increase in low-frequency fatigue (decrease in 20:100 Hz force) was associated with an increase in EMG and force fluctuations in individual subjects. The data obtained immediately after exercise were excluded from analysis, as there is likely to be a complex interaction between several physiological factors in addition to low-frequency fatigue that can influence the EMG and force fluctuations. For example, greater extents of fatigue are associated with a slowing of muscle fiber conduction velocity (1) and contractile speed (2), which are likely to influence EMG amplitude and force during voluntary contractions. Furthermore, alterations in muscle temperature with fatigue can also affect muscle fiber action potentials and motor unit twitch force (9). Therefore, the relative contribution of the mechanisms responsible for the increase in EMG and force fluctuations are likely to be most consistent when obtained 2 h and 24 h after exercise. Furthermore, the data for concentric and eccentric exercise were analyzed separately, because the type of exercise performed had divergent effects on low-frequency fatigue and neuromuscular performance, particularly at 24 h after exercise.
The association between the change in low-frequency fatigue to the change in EMG and force fluctuations after eccentric exercise is shown in Table 1. Following exercise, there were significant associations between the change in 20:100 Hz force and the change in EMG when assessed 2 h and 24 h after exercise. The strongest associations were observed 2 h after eccentric exercise at moderate forces (r2 range from 0.33 to 0.52 at 10–40% MVC), with the highest correlation at 24 h (r2 = 0.44) obtained at the 20% target force. In contrast, there were no significant associations between the change in 20:100 Hz force and the change in force fluctuations at any target force after eccentric exercise. For concentric exercise (data not shown), the associations between the change in 20:100 Hz force and the change in EMG (2 h, mean r2 = 0.14; 24 h, mean r2 = 0.25) and force fluctuations (2 h, mean r2 = 0.17; 24 h, mean r2 = 0.11) were weak and largely nonsignificant. Furthermore, we examined the association between the change in low-frequency fatigue and force fluctuations during the 20-Hz electrical stimulation. There was no significant association between the change in 20:100 Hz force and the change in CV of 20 Hz force at 2 or 24 h after exercise.
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DISCUSSION |
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Increased EMG and Force Fluctuations with Muscle Damage
In a previous study, we showed that eccentric exercise resulted in an increase in elbow flexor EMG and force fluctuations, with the greatest impact of the exercise apparent at low forces (31). However, this effect was observed only in the presence of putative muscle fatigue that occurred immediately after the exercise and not 24 h later. In the present study, we found that EMG and force fluctuations were largest 2 h after eccentric exercise, when there is likely to be no metabolic fatigue (32, 34). Furthermore, in contrast to our previous study (31), the increased EMG and force fluctuations were still elevated 24 h later, possibly because of the inclusion of additional target forces biased toward low contraction levels. These findings after eccentric exercise therefore indicate that the series of physiological and mechanical events that lead to muscle damage alter the neural drive and impair motor performance during submaximal isometric contractions in elbow flexor muscles for up to 24 h after exercise.
Prolonged Recovery of Low-Frequency Fatigue After Muscle Damage
Low-frequency fatigue, originally described by Edwards et al. (7), is characterized by a disproportionate loss of force at low frequencies of stimulation, with a slow recovery process (hours to days), and occurs in the absence of any metabolic disturbance within the muscle (14). The mechanism of low-frequency fatigue is likely to involve an impairment of one or more of the processes associated with excitation-contraction coupling, most likely from a diminished availability of calcium (18), resulting in reduced calcium released per action potential (3, 4). The sigmoidal relationship between force and intracellular calcium concentration means that a small reduction in calcium concentration will have the largest effect on force in the steep portion of the curve (38), which is most likely to occur when motor units are discharging action potentials between 10 and 30 Hz (see Fig. 4). Accordingly, we have quantified low-frequency fatigue in the present study by comparing the force responses with 20-Hz stimulation to that of 100-Hz stimulation (15), with any decrease in the ratio after exercise representing an increase in low-frequency fatigue (17).
It is a commonly held view that low-frequency fatigue is greater after eccentric compared with concentric or isometric exercise (15, 22). However, in these often-cited studies, the extent of metabolic fatigue (decline in maximal strength) induced by the exercise was not equivalent under all exercise conditions. For example, following isometric, concentric, and eccentric exercise of the elbow flexor muscles, Jones et al. (15) showed that eccentric exercise resulted in a 50% reduction in MVC and 20:100 Hz force that recovered slowly over the next 7 days. In contrast, there were minimal changes in MVC and 20:100 Hz force following isometric or concentric exercise. In the present study, we have shown that when the decline in maximal strength induced by concentric and eccentric exercise is equivalent, the extent of low-frequency fatigue (20:100 Hz force) is similar between the two conditions when assessed soon (within minutes) after the exercise. Despite this, the recovery of low-frequency fatigue following eccentric exercise was significantly prolonged, with a maximum difference between exercise conditions obtained 2 h after exercise. The prolonged recovery of eccentric exercise is likely to be attributed to muscle damage induced by the stretching of active muscle, where the eccentric exercise leads to sarcomere disruption and the opening of stretch-activated cation channels, producing inward movement of sodium and calcium into the sarcoplasm (40). The increase of sarcoplasmic calcium then triggers proteolysis that is associated with muscle fiber breakdown and repair (26). Therefore, the delay in the recovery of low-frequency fatigue with eccentric exercise is likely to reflect a process of repair and regeneration with a time course related to protein turnover, rather than metabolite synthesis (14).
Low-Frequency fatigue and Neuromuscular Performance
Although an increase in low-frequency fatigue is a common phenomenon after many types of exercise, it is not immediately clear how this might influence motor performance during voluntary contractions. On a theoretical basis, however, low-frequency fatigue would be expected to alter neural drive to the muscle during submaximal contractions, as the loss of force from motor units discharging at low rates would require the additional recruitment and increased discharge rate of active motor units to compensate for the force loss (see 11, 28). In support of this, de Ruiter et al. (6) showed that the presence of low-frequency fatigue induced by a 50% submaximal isometric fatiguing contraction of the quadriceps muscle was accompanied by an increase in vastus lateralis motor unit discharge rates of 4 Hz during postexercise contractions at 50% MVC. When correlating the change in low-frequency fatigue with the change in EMG after eccentric exercise, we found that the amount of variability in EMG explained by low-frequency fatigue ranged from 12 to 52%, with the strongest correlations observed 2 h after exercise (Table 1). Furthermore, the strongest correlations were observed at low to moderate forces (5–40% MVC, Table 1), which are the target forces that are likely to have a relatively large proportion of the active motor units discharging on the steep portion of the force-frequency curve.
The mechanisms responsible for a change in the relation between surface EMG and force has been a topic of extensive investigation over a number of decades. From these studies under normal physiological conditions, it is generally accepted that the EMG-force relation in different human muscles is either linear, or there is a more than proportional increase in EMG at high force levels (see 20). However, when the muscle is damaged with eccentric exercise, there is an unusual EMG-force relation where there is a more than proportional increase in EMG at low forces. This type of EMG-force relation has been observed previously in computer models of motor unit activation and has been attributed to a narrowing of the force range over which motor units are recruited (12). We provide evidence that the increase in EMG at low forces is associated with increased low-frequency fatigue after eccentric exercise, and is a possible contributor to the abnormal EMG-force relation when the muscle is damaged with eccentric exercise. Although a compression of the recruitment range is a likely consequence of low-frequency fatigue, the effect of eccentric exercise on motor unit recruitment remains to be determined.
The findings from the present study suggest that the occurrence of low-frequency fatigue may contribute to the increased EMG that resulted in a nonlinear EMG-force relation, but only when the muscle is damaged by eccentric exercise. There are at least two reasons why there is increased EMG after eccentric but not concentric exercise. First, the change in low-frequency fatigue at 2 h after concentric exercise was less than half of what it was after eccentric exercise, which may not be of sufficient magnitude to influence EMG under these experimental circumstances. Second, the greater low-frequency fatigue after eccentric exercise is likely to be accompanied by other neuromuscular adjustments due to muscle damage that may accentuate the change in EMG after eccentric contractions. For example, the damage to the muscle fiber membrane could alter the amplitude or frequency of the sarcolemmal action potential (23), which may influence the summation and cancellation of the muscle fiber action potentials when detected with surface electrodes (16). Furthermore, we have recently shown that motor unit synchronization is increased after eccentric exercise (5), which can influence EMG amplitude under some circumstances (39).
Due to the nature of the experimental techniques used to assess low-frequency fatigue in humans, it is not possible to directly compare the effects of muscle damage on the same motor units that are activated with electrical stimulation and voluntary contractions. The low-force voluntary contractions performed in the present study recruit motor units according to the size principle and are therefore likely to involve a high proportion of slow-twitch motor units. In contrast, the classical view is that peripheral electrical stimulation reverses the activation order in electrically evoked contractions and is likely to include a higher proportion of fast-twitch motor units. This comparison is also complicated by the finding that fast-twitch motor units are preferentially damaged (10, 21) and display the greatest low-frequency fatigue (27) after eccentric exercise, although slow-twitch motor units are also affected (33). We have attempted to account for these discrepancies by performing voluntary contractions over a range of contraction intensities (5–60% MVC) that presumably involve an increasing contribution from higher-threshold motor units. We have compared this with low-frequency fatigue using a procedure that has been shown to provide a reliable indicator of whole muscle contractile properties (13). This comparison produced the strongest associations between the change in low-frequency fatigue and the change in EMG after eccentric exercise at low to moderate forces (Table 1). Because low-frequency fatigue is largely manifested in motor units discharging at low rates, it seems reasonable to suggest that the strongest associations obtained at low to moderate forces are due to physiological factors, rather than any methodological factors that may bias the sampling to separate populations of motor units. The weakest associations were observed at high forces, suggesting that factors other than low-frequency fatigue may make a greater relative contribution to the increased EMG under these circumstances (see 31).
Several studies have attempted to examine the contribution of low-frequency fatigue on motor performance with limited success. In one such study, Smith and Newham (32) found that there was no decrement in visuomotor-tracking performance of the elbow joint with the development of low-frequency fatigue after concentric or eccentric exercise and concluded that low-frequency fatigue does not influence skilled motor performance. As eccentric exercise leads to increased force fluctuations and low-frequency fatigue, we have compared the change in these dependent variables during voluntary and electrically induced contractions in individual subjects to examine any association between them. During voluntary contractions, it was anticipated that low-frequency fatigue would lead to the recruitment of larger motor units that is necessary to maintain the required target force due to the loss of force experienced in motor units discharging at low rates. It is the size of the last recruited motor unit that has the greatest effect on force fluctuations, because it has the largest twitch force (according to the size principle) and is most likely discharging at the lowest, subtetanic rates (see 8). However, we found no association between the change in low-frequency fatigue and the change in force fluctuations during voluntary contractions after eccentric exercise, indicating that the alteration in neural drive and motor unit activity with low-frequency fatigue is not manifested in the increased force fluctuations under the experimental conditions described in the present study. Furthermore, during electrical stimulation of the muscle at 20 Hz, we found a substantial increase in force fluctuations after eccentric exercise, but this was not associated with the increase in low-frequency fatigue in individual subjects. These findings from electrical stimulation suggest that the increased force fluctuations after eccentric exercise are largely attributed to peripheral factors that disrupt the force-producing elements of the muscle but are not related to a change in low-frequency fatigue.
In conclusion, we have used concentric and eccentric exercise to induce low-frequency fatigue and used a regression analysis to examine if a change in low-frequency fatigue is a potential mechanism responsible for the altered neuromuscular performance after eccentric exercise. Despite similar reductions in maximal strength, we found a delayed recovery of low-frequency fatigue after eccentric exercise, which was associated with an increase in EMG during submaximal contractions. We found that the change in low-frequency fatigue after eccentric exercise could explain up to 52% of the variability in EMG, with the largest effects observed at low forces. We regard this as an important association, considering that there are several methodological factors that may act to weaken this relation, and more direct tests are not feasible in human subjects. We therefore suggest that eccentric contractions that induce prolonged recovery of force at low frequencies may contribute to increased neural drive and an abnormal EMG-force relation during submaximal isometric contractions. In contrast, there was no association between low-frequency fatigue and increased force fluctuations during voluntary or electrically evoked contractions, suggesting that other physiological factors related to the force-producing elements of the muscle are likely to be playing a major role in the impaired motor performance after eccentric exercise.
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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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  T. J. Dartnall, N. C. Rogasch, M. A. Nordstrom, and J. G. Semmler Eccentric Muscle Damage Has Variable Effects on Motor Unit Recruitment Thresholds and Discharge Patterns in Elbow Flexor Muscles J Neurophysiol, July 1, 2009; 102(1): 413 - 423. [Abstract] [Full Text] [PDF]
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P < 0.05 compared with after and 2 h after eccentric exercise.