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J Appl Physiol 82: 1654-1661, 1997;
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Journal of Applied Physiology
Vol. 82, No. 5, pp. 1654-1661, May 1997
EXERCISE AND MUSCLE

Effects of fatigue duration and muscle type on voluntary and evoked contractile properties

D. G. Behm and D. M. M. St-Pierre

School of Physical and Occupational Therapy, McGill University, Montreal, Quebec, Canada H3G 1Y5

ABSTRACT
INTRODUCTION
EXPERIMENTAL DESIGN AND METHODOLOGY
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES

ABSTRACT

Behm, D. G., and D. M. M. St-Pierre. Effects of fatigue duration and muscle type on voluntary and evoked contractile properties. J. Appl. Physiol. 82(5): 1654-1661, 1997.---The effects of fatigue duration and muscle type on voluntary and evoked contractile properties were investigated with an isometric, intermittent, submaximal fatigue protocol. Four groups performed contractions of the plantar flexors and quadriceps at various intensities to produce long (LDF; 19 min 30 s)- and short-duration fatigue (SDF; 4 min 17 s). The LDF group had a significantly greater decrease in muscle activation than did the SDF group (12 vs. 5.8%) during recovery, although there was no difference in the impairment of maximum voluntary contraction force beyond 30 s of recovery. The significant decrease in the compound muscle action potential of the LDF group (M-wave amplitude; 14.7%) contrasted with the M-wave potentiation of the SDF group (15.7%), suggesting changes in membrane excitation may affect LDF. The quadriceps group performing contractions at 50% MVC experienced a smaller decrease in agonist electromyograph activity than did other groups, indicating both muscle and fatigue duration specificity. Impairments in excitation-contraction coupling were indicated by changes in quadriceps peak twitch and time to peak twitch while decreases in PF M-wave amplitudes suggested a disruption of membrane potentials. Results suggest that fatigue mechanisms may be duration (activation, half relaxation time) or muscle specific (electromyograph, twitch torque) or a combination of both (M wave, time to peak twitch torque).

recovery; muscle activation; twitch; electromyography; M wave

INTRODUCTION

FATIGUE STUDIES have demonstrated a diversity of mechanisms underlying fatigue-associated decrements in force (for review see Refs. 1, 14, 16, 21). These mechanisms are commonly subdivided in central (alpha -motoneuron pool or above) as well as distal sites (motoneuron end plate and below) and may be task dependent (14). Indeed, changes induced by fatigue may well be influenced by whether the muscle is contracting voluntarily or is being induced to contract (27) and by whether the contraction is static (5-7, 22) or dynamic (11), sustained vs. intermittent (12), maximal (5-7) or submaximal (17, 24), or dependent on the characteristics of the specific muscle.

Muscles with higher percentages of fast-twitch fibers have been shown to fatigue more rapidly than do muscles with a greater percentage of slow-twitch fibers (4, 11, 23). Furthermore, similar fatigue protocols in a variety of muscles have resulted in dissimilar changes in force (10, 25); muscle activation (4), as measured with the interpolated twitch technique (ITT); electromyograph (EMG) activity (24, 27); and M wave (26). This suggests that mechanisms underlying fatigue may differ depending on the muscle (6) or its fiber composition (11, 23). However, because the time to fatigue differs in different muscles, it is difficult to determine whether the differences in underlying fatigue mechanisms are muscle or duration dependent. More specifically, it is not known whether the mechanisms underlying fatigue would be the same in two muscles of different fiber type composition (20) if the time to fatigue were similar. To compare the influence of similar fatigue durations on two different muscles of different fiber type composition [quadriceps and plantar flexors (PF)], different contraction intensities were utilized to alter the duration of an intermittent, submaximal, isometric, fatigue protocol.

EXPERIMENTAL DESIGN AND METHODOLOGY

Subjects. The study had four groups of eight moderately active to active subjects (Table 1). Subjects were recruited from the McGill University staff and student population, were fully informed of the procedures, and signed a consent form before experimentation. The study was approved by McGill University's Ethics Committee.

Table 1. Subject characteristics

Group Height, cm Weight, kg Age, yr Gender
M F
75% PF 163.4 ± 7.1  71.7 ± 13.0  25.3 ± 3.4  5 3
50% PF 160.9 ± 10.2  70.1 ± 12.1  21.7 ± 9.6  4 4
25% quadriceps 166.8 ± 6.9  76.8 ± 17.4  24.6 ± 5.2  5 3
50% quadriceps 162.8 ± 8.9  69.4 ± 21.6  22.4 ± 7.4  4 4
Values are means ± SD for 8 subjects in each group. PF, plantar flexors; M, male; F, female.

Experimental setup. Subjects were seated in a straight-back chair with hips and knees at 90°. PF subjects had their legs secured in a modified boot apparatus with their ankles at 90° (2). Quadriceps subjects were seated in a Cybex chair (Lumex, NY) with their feet in a padded strap attached to a strain gauge, perpendicular to the lower limb. All voluntary and evoked torques were detected by a force transducer (PF: custom design; quadriceps: BLH Electronics 3SB), amplified (model NL107, recording amplifier and model NL106 analog-to-digital converter differential amplifiers, Neurolog Systems), and monitored on an oscilloscope (model 2220, Tektronix). All data were stored on computer (Seanix ASI 9000, 486 DX) at a sampling rate of 2,000 Hz after being directed through an analog-to-digital board (Lab Master). Data were recorded and analyzed with a commercially designed software program (Actran, Distributions Physiomonitor, Montreal, PQ).

Bipolar surface-stimulating electrodes were secured to the superior and distal aspects of the triceps surae or quadriceps muscle group. Stimulating electrodes were constructed in the laboratory from tin foil coated with a conduction gel, wrapped in cheesecloth and paper, and immersed in a saline solution. The electrode length was sufficient to wrap the width of the muscle belly with an electrode width of ~4-5 cm. The electrodes were placed in approximately the same positions for each subject. Surface EMG-recording electrodes were placed 3-5 cm apart over the distal segment of the tibialis anterior and soleus (PF group) or vastus lateralis and biceps femoris (quadriceps group). A ground electrode was secured superficially to the head of the tibia. Thorough skin preparation for all electrodes included sanding of the skin around the designated areas followed by cleansing with an isopropyl alcohol swab. Agonist and antagonist EMG activities were analyzed during maximal voluntary contractions (MVCs). EMG activity was amplified (Isolation Head Stage 830 amplifier, Biomedical 830 amplifier CWA, Ardmore PA), filtered (10-1,000 Hz), monitored on oscilloscope, and stored on computer. The computer software program rectified and integrated the EMG signal (iEMG) over a 500-ms period during a MVC. iEMG activity was normalized to prefatigue values for analysis. M-wave amplitudes elicited by the twitch were measured under the same conditions before MVCs, both pre- and postfatigue.

Pre- and postfatigue measurements. Peak twitch torques were evoked with electrodes connected to a high-voltage stimulator (model DS7H+, Digitimer Stimulator). The amperage (10 mA to 1 A) and duration (50-100 µs) of a 400-V rectangular pulse were progressively increased until a maximum twitch torque was achieved in the PF. Dependent on the mass of an individual's quadriceps, voltage was increased until either a plateau in the twitch torque was obtained or the stimulator reached maximum output. Nine of 16 quadriceps subjects achieved maximal twitch torque. Prefatigue, the average of three trials was used to measure twitch amplitude, time to peak twitch torque (TPT), and half relaxation time (RT1/2).

The ITT was administered with a series of 3-s-duration MVCs (3 trials). Three doublets (2 twitches with a 10-ms interval) interspersed at 900-ms intervals were evoked and superimposed on the voluntary contractions to obtain an average response (Fig. 1). Superimposed doublets were utilized in an attempt to ensure a large signal-to-noise ratio. Two potentiated doublets were also recorded at 1-s intervals after the voluntary contractions. Torque signals were sent through both low- and high-gain amplifiers. The resident software program offset the gained superimposed signal, 100 ms before each stimulation, for improved resolution. A ratio was calculated that compared the amplitudes of the superimposed doublets with the potentiated doublet, representing muscle fibers that were not voluntarily activated. The percentage of muscle fibers activated was estimated by subtracting the ratio from a value of 1 and multiplying by 100 to represent an index of muscle activation during a voluntary contraction.
Fig. 1. Top: prefatigue (left) and postfatigue (right) of long-duration fatigue (LDF) protocol [25% maximum voluntary force contraction (MVC) of quadriceps]. Bottom: prefatigue (left) and postfatigue (right) of short-duration fatigue (SDF) protocol (50% MVC of quadriceps). Increase in interpolated twitch ratio postfatigue was greater in subject after LDF protocol than after SDF protocol. Also illustrated is greater drop in MVC immediately after fatigue observed in LDF protocol. Twitch preceding interpolated twitch technique postfatigue was compared with unpotentiated evoked resting twitch (twitches generated at rest before any voluntary muscle contractions; data not shown). y-Axes are in volts. Pre- and postfatigue gains are the same.
[View Larger Version of this Image (26K GIF file)]

Fatigue. After voluntary and evoked testing, the subjects proceeded with the fatigue test. Each of the four groups were subjected to a different contraction intensity. The two quadriceps groups performed voluntary contractions at 50 or 25% MVC while the PF groups performed voluntary contractions at 50 or 75% MVC. Preliminary work indicated that quadriceps contractions performed at 25% of MVC led to a similar number of contractions as when work was performed with the PF at 50% MVC. In addition, the time to fatigue for the quadriceps at 50% MVC was similar to the fatigue duration of the PF at 75% MVC. However, the number of contractions to fatigue was less in the latter (50% quadriceps, 75% PF) than in the former (25% quadriceps, 50% PF), leading to what will be referred to as short- (SDF) and long-duration fatigue (LDF) protocols. In all protocols, the subject's contraction intensity was gradually increased for 3 s until the desired force was attained. This intensity was maintained for 10 s, followed by a 3-s gradual decrease to a resting state. The sequence was resumed after a 4-s rest period. Contraction cycles (work-to-rest ratio of 16 min 4 s) continued until the effects of fatigue disrupted the subject's ability to maintain the desired force for the 10-s period. Voluntary and evoked properties were monitored immediately postfatigue and after 30 s and 1, 2, 5, and 10 min of recovery.

Statistical analyses. The effect of fatigue duration and muscle type on voluntary and evoked twitch properties were analyzed by using a three-way analysis of variance with repeated measures on the third factor. The three factors (2 × 2 × 7) included muscle type (quadriceps and PF), fatigue duration (long and short), and testing period (prefatigue, postfatigue, and recovery periods of 30 s and 1, 2, 5, and 10 min). F-ratios were considered significant at P < 0.05. If significant interactions were present, a Tukey post hoc test was conducted. Descriptive statistics include means ± SD. Figures 1-7 include means ± SE.

RESULTS

Fatigue. When contracting at the same intensity (50% MVC), the quadriceps (4 min 4 s ± 1 min 2 s) fatigued more rapidly than did the PF (19 min 33 s ± 8 min 0 s). However, there were no significant differences in the time to fatigue between the 50% PF (19 min 33 s) and 25% quadriceps (19 min 27 s ± 3 min 8 s) groups (LDF) or between the 75% PF (4 min 30 s ± 1 min 44 s) and 50% quadriceps (4 min 4 s) groups (SDF). The LDF group (50% PF and 25% quadriceps) had a significantly (P < 0.0001) greater number of contractions to fatigue than did the SDF group (75% PF and 50% quadriceps). Immediately after the fatigue protocol, the LDF group had a significantly (P = 0.03) greater drop in MVC force than did the SDF group (40% LDF vs. 30.9% SDF). MVC recovered to the same extent in the subsequent 10 min of recovery in both the LDF and SDF groups, although significant differences from prefatigue were still observed (Fig. 2).
Fig. 2. Mean percent drop in MVC after fatigue in LDF (black-square) and SDF (triangle ) groups. Pre, prefatigue; Post, postfatigue. Vertical bars, SE. Vertical arrow, significant difference between groups (P < 0.05); horizontal arrow, significant difference from prefatigue values for both groups (P < 0.05).
[View Larger Version of this Image (13K GIF file)]

Muscle activation. Before the fatigue test, full muscle activation was achieved in 11 of 16 PF subjects and 5 of 16 quadriceps subjects. Changes in activation with fatigue were influenced by the duration of the fatigue protocol and not by muscle type (Fig. 1). When averaged over the entire recovery period, the index of muscle activation decreased significantly (P = 0.02) more in the LDF (12 ± 7.5%) than in the SDF protocol (5.8 ± 4.5%; Fig. 3).
Fig. 3. Mean percent drop in index of muscle activation over prefatigue, postfatigue, and recovery testing periods in LDF (black-square) and SDF (triangle ) groups. Bars, SE. Vertical arrows, significant differences between groups (P < 0.05); horizontal arrow, significant difference from prefatigue values for both groups (P < 0.05).
[View Larger Version of this Image (16K GIF file)]

In contrast, changes in M wave after fatigue were influenced by both fatigue duration (Fig. 4; P = 0.003) and muscle type (P = 0.002). LDF protocols diminished M-wave amplitudes by 14.7 ± 15.5%, contrasting with the 15.7 ± 25.6 potentiation with SDF (Fig. 5). Muscle type differences were demonstrated by the average 16.7 ± 15.5% potentiation of the quadriceps M waves, contrasting with the 15.7 ± 25.5% reduction in PF M waves throughout the recovery period (Fig. 6).
Fig. 4. Quadriceps M wave of 2 subjects pre- and postfatigue. Decrease in M wave after LDF protocol (25% MVC) contrasted with increase observed after SDF protocol (50% MVC). See Fig. 1 legend for more details.
[View Larger Version of this Image (19K GIF file)]

Fig. 5. Mean percent change in time to peak twitch torque (TPT; top), half-relaxation time (RT1/2; middle), and M-wave amplitude (bottom) after fatigue in LDF (black-square) and SDF (triangle ) groups. Vertical bars, SE. Vertical arrows, significant differences between groups, (P < 0.05); horizontal arrow, significant difference from prefatigue values for both groups (P < 0.05).
[View Larger Version of this Image (11K GIF file)]

Fig. 6. Mean percent change in peak twitch (top), TPT (middle), and M-wave amplitude (bottom) after fatigue in quadriceps (hexagons) and plantar flexors (stars). Vertical bars, SE. Vertical arrows, significant differences between muscles (P < 0.05); horizontal arrows, significant differences from prefatigue values for both muscles (P < 0.05).
[View Larger Version of this Image (11K GIF file)]

The most important factor underlying the changes in maximum iEMG after fatigue was not as clear cut. Irrespective of fatigue duration, all PF iEMG activity significantly decreased after fatigue to a similar extent (50% PF: 19.3 ± 25.2%; 75% PF: 26.3 ± 8.7%). Although the LDF quadriceps group (25% MVC: 30.4 ± 17%) experienced a corresponding iEMG decrease, the SDF quadriceps group (50% MVC: 3.7 ± 1.9%) exhibited no significant change in iEMG after fatigue.

To ensure that changes in soleus iEMG represented the activity of the triceps surae, gastrocnemius iEMG activity was calculated after a 50% MVC fatiguing protocol of the PF in five subjects. Medial and lateral gastrocnemius iEMG activity had an average decrease over the entire recovery period of 22.9 ± 8.1 and 20.7 ± 11.6%, respectively.

Evoked twitch contractile properties. Changes in peak twitch torque with fatigue were dependent on muscle type and not fatigue duration (Fig. 7). Quadriceps twitch torque had an insignificant (P = 0.34) average decrease of 14.1 ± 2.3%, contrasting with the 16.1 ± 2.6% potentiation of the PF (P = 0.004) during the recovery period (Fig. 6). TPT was affected by both muscle type and fatigue duration. The lack of change in PF TPT contrasted with the significant prolongation (P = 0.02) of the quadriceps TPT (15.3 ± 3.2%) over the entire recovery period (Fig. 6). Fatigue-duration effects were exhibited by the subjects in the SDF protocol, who experienced significantly (P = 0.008) longer TPT postfatigue and at 30 s of recovery than did subjects in the LDF protocol (Fig. 5).
Fig. 7. Top: plantar flexors twitches before (left) and after (right) fatigue in 1 subject. Bottom: potentiation of plantar flexors twitches contrasted with marked depression in quadriceps twitches. See Fig. 1 legend for more details.
[View Larger Version of this Image (17K GIF file)]

In contrast, fatigue duration was the only significant (P = 0.0007) factor affecting RT1/2. The RT1/2 of the LDF group was shortened 16.8 ± 12.2 compared with the 9.7 ± 2.5% increase in the RT1/2 of the SDF group during the recovery period (Fig. 5).

Reliability. Intraclass correlation coefficients were used to determine the test-retest reliability of the variables. Very high correlation coefficients (>0.9) were established for the index of muscle activation, MVC, potentiated doublet, TPT, and RT1/2. Moderate to high correlation coefficients were found with PF twitch torque (0.74) and quadriceps twitch torque (0.54).

DISCUSSION

One of the most important findings of this study was that fatigue-related changes of specific voluntary and evoked contractile properties were influenced by different factors. Fatigue duration exerted its greatest effect on muscle activation and RT1/2. However, the effect of fatigue on twitch torque was primarily determined by muscle type. Fatigue-related changes in M-wave amplitude and TPT were affected by both duration and muscle type (Table 2).

Table 2. Factors (muscle type or fatigue duration) affecting selected voluntary and evoked contractile properties

Muscle Type Fatigue Duration
iEMG Yes Yes (?)
Twitch torque Yes No
TPT Yes Yes
M-wave amplitude Yes Yes
RT1/2 No Yes
Muscle activation No Yes
iEMG, integrated EMG activity; TPT, time to peak twitch torque; M wave, compound muscle action potential; RT1/2, half relaxation time.

Muscle activation. Increased time to fatigue resulted in greater decreases in muscle activation. The 12% decrease in the index of muscle activation after fatigue in the LDF group was significantly greater than the 5.8% decrease in the SDF group. The soleus has been reported to be more susceptible to central (neural) fatigue than the quadriceps (4). This could suggest that fatigue-induced muscle inactivation was related to the specific muscle. It was shown in this study, however, that the muscle type was incidental to the amount of muscle inactivation. Alterations in contraction intensity allowed the 25% quadriceps and 50% PF groups to contract longer than the 50% quadriceps and 75% PF groups, resulting in greater inactivation in the LDF groups independent of the muscle utilized.

M-wave amplitudes in this study decreased with LDF but increased with SDF. Bigland-Ritchie et al. (7), who used a 60-s MVC fatigue protocol of the adductor pollicis, did not find any change in M-wave amplitude, suggesting muscle membrane transmission failure was not a component of high-intensity, short-term fatigue. Other studies using short-duration voluntary (4, 22) or evoked (18) fatigue protocols have not shown decreases in M-wave amplitude. Decline in M-wave amplitude has been reported in the abductor pollicis, after 90-100 s of fatiguing MVCs (3). Fuglevand et al. (17) illustrated greater declines in M-wave amplitude with lower intensity (i.e., longer duration) contractions and concluded that when force is sustained at a submaximal value, impairment in muscle membrane propagation may occur. Decline in M-wave amplitude with LDF was evident in our study as well, indicating an impairment of the muscle membrane excitability or neuromuscular propagation. The 14.7% depression of M-wave amplitude of the LDF group contrasted with the 15.7% potentiation of the SDF group.

The fact that the M wave potentiated during SDF would suggest that muscle membrane propagation failure is not the primary determinant of muscle fatigue with SDF. Potentiation of the M wave during the first 30 s of tetanic fatiguing contractions has also been observed, suggesting an increased excitability of the muscle fibers (15). M-wave potentiation may signify that presynaptic and/or end-plate potentials are facilitated possibly by a reduction in the dispersion of fiber action potentials (12). The increase in M-wave amplitude could support Buchthal and Madsen's (9) report of increased synchronization with fatiguing contractions.

Alterations in M-wave amplitude were dependent not only on fatigue duration but also on muscle type. Overall, quadriceps M waves were potentiated 16.7% while PF M waves were depressed 15.7%. Milner-Brown and Miller (26) concluded that the impairment of membrane propagation depends both on the duration and degree of fatigue and on the intrinsic properties of the individual muscle. Pagala et al. (28) reported greater decreases in the action potentials of the extensor digitorum longus and diaphragm than with the soleus while Moritani et al. (27) found similar results when comparing the gastrocnemius and soleus.

The unchanged iEMG activity of the 50% quadriceps group (3.7%) contrasted with significant decreases for both PF and 25% quadriceps groups. Because the extent of muscle activation and compound muscle action potential (M wave) both contribute to the EMG signal, the differing response of the 50% quadriceps group might suggest that the EMG is also affected by both duration and muscle type.

Evoked twitch contractile properties. Changes in twitch torque were muscle dependent. Quadriceps twitch torque had an insignificant 14.1% decrease, in contrast to the 16.1% potentiation of PF. Conversely, alterations in TPT were both muscle and fatigue duration dependent. Quadriceps TPT was prolonged 15.3%, whereas PF TPT was not significantly changed. The prolongation of quadriceps TPT may help to explain why the decreased quadriceps twitch torque did not achieve significance. Muscle dependence was also reported by Hatcher and Luff (19), who found contrasting results when comparing the heterogenous flexor digitorum longus (FDL) and slow-twitch soleus muscles of the cat. In contrast to the significant changes in the FDL, the soleus had smaller decreases in tetanic tension and no change in maximum shortening velocity. The decline in quadriceps twitch torque and prolongation of TPT in the present study may imply an impairment in excitation-contraction (E-C) coupling (13, 30). The quadriceps M-wave potentiation would argue against failure in membrane propagation, suggesting the impairment was related more to the sarcoplasmic reticulum's release of Ca2+ and/or cross-bridge kinetics. Potentiation of PF twitch torque and a lack of change in PF TPT in conjunction with decreases in M-wave amplitude would reinforce the hypothesis that impairments in PF-evoked properties can be mainly attributed to impairments of membrane potentials.

Fatigue duration was the major factor affecting RT1/2, with subjects in the LDF group experiencing a 16.8% decrease, in contrast with a 9.7% increase in RT1/2 of subjects in the SDF group. Alterations in twitch torque or TPT did not correspond to changes in RT1/2. The divergence of TPT and RT1/2 has also been reported by Viitasalo and Komi (30), who found differing recovery profiles. Bigland-Ritchie et al. (9) demonstrated a prolongation in RT1/2 contrasted with a lack of change in TPT. Impairment in E-C coupling affecting Ca2+ release (TPT) may not automatically coincide with a hindrance of Ca2+ sequestering (RT1/2). The sequestration of Ca2+ is an active process involving ATP (8) and thus would be affected by alterations in the muscle metabolic milieu. Resynthesis of ATP in glycolysis has been suggested to be inhibited by low intramuscular pH (29) and thus may affect RT1/2 more with the higher intensity contractions of the SDF. The release of Ca2+, however, is not an active process (8). The differing effects of metabolism may explain the lack of correlation between changes in RT1/2 and the other evoked contractile properties of twitch torque and TPT.

Summary. In summary, this study found duration-induced impairments in muscle activation and RT1/2, muscle-dependent decreases in peak twitch torque and iEMG, and effects by both factors in M-wave amplitude and TPT. The decrease in LDF muscle activation and M-wave amplitude indicated that impairment in muscle activation and membrane action potentials contributed to fatigue with long-duration contractions. The potentiation of SDF M waves decreased the possibility of muscle membrane impairments. Potentiation of PF twitch torque and a lack of change in PF TPT in conjunction with decreases in M-wave amplitude would suggest impairments of PF membrane potentials. Fatigue-related decreases in quadriceps twitch torque and prolongation of TPT may be associated with disruptions in E-C coupling. Impairments in RT1/2 were directly affected by fatigue duration and thus possibly related to muscle metabolic changes.

ACKNOWLEDGEMENTS

Present address and address for reprint requests: D. G. Behm, School of Physical Education and Athletics, Memorial Univ. of Newfoundland, St. John's, Newfoundland, Canada A1C 5S7.

FOOTNOTES

Received 20 October 1995; accepted in final form 6 January 1997.

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