| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
1Institute for Fundamental and Clinical Human Movement Sciences, Vrije Universiteit, Amsterdam, The Netherlands; and 2Insitute for Biophysical and Clinical Research into Human Movement, Manchester Metropolitan University, Cheshire, United Kingdom
Submitted 8 July 2004 ; accepted in final form 8 October 2004
 |
ABSTRACT |
|---|
 TOP ABSTRACT METHODSRESULTSDISCUSSIONREFERENCES |
|---|
muscle activation; endurance; blood flow; muscle length
Another explanation for the reduced endurance at greater muscle length could be a difference in the contribution of oxidative metabolism as a result of differences in muscle perfusion. Muscle perfusion can change with intramuscular pressure (29), which in turn is dependent on internal muscle force. Even though the same external torque is produced at different knee angles, each external torque can correspond to different internal muscle forces because knee moment arm changes with joint angle, as has been shown in the frog (21). In humans, there is no consensus concerning the degree of knee joint angle-dependent changes in moment arm (Refs. 13, 31 vs. Refs. 6, 19). This makes it difficult to investigate the potential effect of internal pressure-related differences in muscle perfusion at different knee angles. However, by occluding the blood supply of the knee extensors, the potential effect of knee angle-dependent differences in muscle perfusion would be excluded as a possible explanation for differences in endurance. Obviously, if blood flow is fully occluded, no differences in muscle perfusion will occur at different knee angles. Hisaeda et al. (14) applied arterial occlusion during sustained (1–2 min) isometric knee extensions, yet still found significantly longer endurance times at shorter muscle lengths. However, it has been suggested by Quaresima and Ferrari (26) that occlusion in the study of Hisaeda et al. (14) may have been incomplete due to insufficient cuff pressure (270 mmHg).
Muscle endurance may further be affected by muscle activation. First, during brief maximal contractions, maximal muscle activation is seldom 100% (3); consequently, the full muscle potential is not used. This should be considered during an endurance task where the exerted torque is a percentage of maximal torque capacity (MTC), particularly because maximal muscle activation is dependent on knee joint angle (33) and equal relative contraction intensities at different knee angles are compared. Second, potential knee angle-dependent differences in voluntary drive, which may occur close to the point of exhaustion, may affect muscle endurance. Hunter and Enoka (15), for example, conclude that muscle activation can limit the duration of submaximal fatiguing contractions of the elbow flexor muscles. However, although a large variation in knee extensor muscle activation at exhaustion between subjects (9, 18) has been found, the variation was unrelated to endurance time at the 90° knee angle (9). Nevertheless, differences in muscle activation could contribute to the knee angle-dependent differences in endurance time and should be taken into consideration.
The main aim of this study, therefore, was to investigate the influence of neural activation on knee extensor endurance at different knee angles. The potential effect of knee angle-dependent differences in muscle perfusion was eliminated by full occlusion of the blood supply during the submaximal isometric contraction. Because endurance time was expected to be longer at 30°, we hypothesized that muscle activation at torque failure would be closer to 100% at the 30° than at the 90° knee angle.
|
METHODS |
|---|
|
TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Force recordings.
Isometric force recordings were made for voluntary and electrically evoked contractions of the knee extensor muscles of the right leg. Subjects were seated in a custom-built ergometer with their hips at 70° (0° = full extension). Shoulders, hips, and lower thigh were strapped to the ergometer. The distal part of the shank was strapped to a force transducer, which was attached to the lever arm of the ergometer. A shinguard ensured that subjects could exert maximal forces without discomfort at the shin. The backrest, force transducer height, and its mediolateral position were adjusted to enable precise alignment of the knee axis with the axis of rotation of the ergometer lever arm. A crank enabled changing of the knee angle of the subject. Despite fixation, some change in knee angle during contraction was unavoidable. Knee angles, therefore, were measured with subjects delivering 
50% of maximal force (0° = full knee extension). Pilot studies had shown that an increase from 50% to maximal force led to a change in knee angle of <2°. The distance from the knee axis to the center of the force transducer was determined for each individual to enable torque calculation. Real-time force applied to the force transducer was displayed online on a computer monitor and digitally stored (1 kHz) on computer disc. The force signals were automatically corrected for gravity at each angle; the average force applied by the weight of the limb to the transducer during the first 50 ms after the start of a recording, with the subject seated in a relaxed manner, was set to zero force by the computer program.
Electrical stimulation. A cathode (self-adhesive stimulation electrode, 5 x 5 cm, Schwa-Medico) was placed over the femoral nerve. The anode (13 x 8 cm) was placed over the gluteal fold. The quadriceps femoris muscle was stimulated transcutaneously with rectangular pulses of 100 µs using a computer-controlled constant current stimulator (Digitimer DS7H, Digitimer, Welwyn Garden City, UK). Stimulation current was increased until torque measured in response to a triplet (three 100-µs pulses applied at 300 Hz) leveled off at a 60° knee angle. The current was then increased by a further 50 mA to ensure supramaximal stimulation. In all subjects, it was verified that supramaximal current at a 60° knee angle was supramaximal at 30 and 90° knee angles as well. The same stimulation current was used during twitch (single pulse) stimulation.
Experimental procedures. A priori, it was considered possible that differences in absolute endurance time itself might contribute to potential differences in voluntary muscle activation during long-lasting isometric contractions performed at different knee angles. Therefore, in the present study, subjects had to perform an additional task during which the relative load was increased in the more extended knee position to decrease the endurance time and to make it similar to the endurance time found with a more flexed knee.
The subjects visited our laboratory on five occasions with at least 2 days in between each session. During the three experimental sessions, MTC (see MVC and MTC) and central activation ratio (CAR; see Fatigue task and postexercise measurements) were determined for each subject before, immediately after, and 10 min after the fatigue task (see Fatigue task and postexercise measurements). The three different fatigue tasks were randomly assigned over the 3 experimental days. The first session was to familiarize the subjects with the setup and the electrical stimulation and to determine the CAR and MTC of the knee extensors with superimposed electrical stimulation. The CAR was calculated using superimposed triplet stimulation during a maximal voluntary contraction (MVC) and calculated by dividing the torque before the delivery of the triplet by the maximum torque produced during the superimposition of the triplet (20). Subjects were excluded from further participation if they were unable to achieve a CAR of >0.9 at 30 and 90° knee angles.
Furthermore, intermittent isometric torque generation was practiced at either 50% MTC at a 30° (3 subjects) or a 90° (3 subjects) knee angle or at 65% MTC at the 30° (2 subjects) knee angle. Pilot studies had indicated that an intensity of 65% MTC at the 30° knee angle resulted in an endurance time comparable to a 50% MTC intensity level at the 90° knee angle. During each following session, the intermittent torque delivery was maintained up to torque failure at one randomly chosen angle and torque level. The second session was not used for analysis to exclude learning effects. To reiterate, each subject performed three fatigue tasks that were included in the analysis: 30° (50%), 90° (50%), and 30° (65%), each on a separate day. Each session lasted 1.5–2 h in total.
MVC and MTC.
In each session, MVC torque and MTC were determined at three knee angles (30, 60, and 90°). Subjects were asked to maximally generate isometric torques for 3–4 s to determine MVC extension and flexion torque [flexion torque was used for normalizing the antagonist EMG from the biceps femoris (BF)]. Two to four attempts were made, separated by 3 min of rest. MVC torque was determined as the peak force from the stable part of the force signal multiplied by the subjects' moment arm. Real-time force was visible on a computer monitor, and subjects were vigorously encouraged to exceed their maximal value, which was also displayed. MVC torque was taken as the highest value, which did not exceed preceding attempts by >5%, allowing a maximum of four attempts. Next, MTC of the quadriceps femoris muscle was determined using electrical stimulation. A superimposed measurement consisting of a triplet applied to a fully relaxed muscle and another triplet superimposed on an MVC was used to determine MTC. The MTC of the muscle was calculated using the following formula:
 | (1) |
If the torque reached just before superimposed stimulation was below 90% of MVC torque, more attempts were made, with a maximum of four attempts. This was done to make the calculation of MTC as accurate as possible. For statistical analysis, in each session, the attempt was used where the highest voluntary torque before the superimposed triplet was reached. In instances where MVC torque exceeded the calculated value of MTC, MVC torque was taken as MTC.
Fatigue task and postexercise measurements.
Subjects were required to perform a fatigue task at either a 30 or 90° knee angle. Before this fatigue task, blood flow to the right leg was occluded using a sphygmomanometer cuff (400 mmHg) that was placed around the upper thigh as proximal as possible. The fatigue task consisted of the following cycle, which was repeated until torque failure: 4.5 s of rest were followed by an 3-s ramp-up phase to either 50 or 65% MTC, which was held for 15 s (Fig. 1). Exerted and target force were displayed online on a monitor, and subjects were instructed to match exerted force with target force. When the target level could no longer be sustained despite vigorous encouragement, the test was terminated. The exact end of the fatigue task (torque failure) was defined afterward as the point when the exerted torque decreased below 90% of the target level for >2 s. Endurance time was defined as time spent at target torque.
|
Surface electromyography. Electromyographic activity of the vastus lateralis (VL), rectus femoris (RF), and BF muscle was recorded using surface electromyography (EMG) electrodes (Ø = 17 mm; F-454AE, Medeq, Gnosis). After the skin was shaved, roughened, and cleansed with 70% ethanol, electrodes were placed on the muscle belly in a bipolar configuration, parallel to the muscle fiber direction, with an interelectrode distance of 40 mm. Pairs of electrodes were placed on the RF muscle halfway between the anterior spina iliaca superior and the superior border of the patella. Another pair was placed on the VL muscle two-thirds of the distance between the anterior spina iliaca superior and the lateral side of the patella. Electrode placement for the BF muscle was halfway between the ischial tuberosity head of the fibula and the lateral condylus of the tibia. Reference electrodes were placed on the left and right patella and also on the right condylus medialis. The locations of all electrodes were marked with a waterproof felt-tip pen on the first visit to enable precise electrode application in the remaining sessions. Surface EMG signals were amplified (x100), digitized (1 kHz), except superimposed measurements (10 kHz), and stored with the force signal on computer disc. All EMG signals were band-pass filtered (10–400 Hz). Rectified surface EMG amplitude (rsEMG) was calculated for the VL, RF, and BF (VLrsEMG, RFrsEMG, and BFrsEMG) for 500-ms segments during the fatigue task for 5-s segments. Segments including superimposed electrical stimulation were excluded from analysis. Prefatigue MVC extension and flexion maximal rsEMG values were set at 100%.
Peak-to-peak amplitude M-wave in response to twitch stimulation at the end of the fatigue task was normalized with respect to prefatigue values to check for neuromuscular transmission failure.
Statistics. All results are presented as means ± SD. Data were analyzed by means of repeated-measures analysis of variance where appropriate. If significant main effects were observed, Bonferroni tests were performed for post hoc analysis. The level of significance of all statistical analyses was set at P < 0.05.
|
RESULTS |
|---|
|
TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Prefatigue.
MTC and triplet torque recorded at the 60° knee angle were significantly greater than their respective values at the 30 and 90° knee angles (P < 0.05; Table 1). In addition, MTC and triplet torque at the 30° knee angle were not significantly different from their respective values at the 90° knee angle.
|
As expected, endurance time was significantly longer for 30° (50%) compared with 90° (50%) (Fig. 2). Because endurance times for 90° (50%) and 30° (65%) were not significantly different from each other, we succeeded in matching endurance times between the 30 and 90° knee angles. In addition, the endurance time for 30° (50%) was significantly longer than the 30° (65%) endurance time.
|
|
|
Normalized BFrsEMG values were low for all protocols and did not change significantly from the start to the end of the fatigue task; at the 30 and 90° knee angles, their respective values were 7.9 ± 7.8 and 7.5 ± 4.5%. This indicates that coactivation was not an important factor during the course of the fatigue task.
No differences in triplet torque at torque failure, normalized to maximal triplet torque, were found between 30° (50%) and 90° (50%) (47.4 ± 14.6 and 34.5 ± 17.7%, respectively). The triplet torque at 30° (65%) (56.4 ± 17.4%) was significantly higher than 90° (50%) only. These findings indicate that, at torque failure, fatigue of the knee extensor muscles was rather similar among the protocols.
Postexercise with occluded blood flow.
As expected from the different exercise intensities during the task, postexercise MVC levels were significantly higher for the 30° (65%) protocol (69.8 ± 11.7%) compared with the 30° (50%) and 90° (50%) protocols (54.7 ± 9.5 and 47.0 ± 8.1%, respectively).
During MVC, the postexercise CAR [0.97 ± 0.05, 0.99 ± 0.03, and 0.97 ± 0.02 for 30° (50%), 90° (50%), and 30° (65%) protocols, respectively] was similar (P > 0.05) compared with the prefatigue CAR [0.94 ± 0.05, 0.98 ± 0.02, and 0.94 ± 0.07 for 30° (50%), 90° (50%), and 30° (65%) protocols, respectively].
VLrsEMG values during MVC postexercise were not significantly different from preexercise (Fig. 5). RFrsEMG values, however, were significantly lower compared with prefatigue values. There were no significant differences among protocols. Note that postexercise rsEMG values were significantly higher than rsEMG values at torque failure for both VL and RF muscles (Figs. 4 and 5). Thus, despite the ongoing occlusion, maximal rsEMG increased within several seconds after exercise, but this did not result in an increase of maximal torque.
|
Recovery.
Ten minutes after deflation of the cuff, triplet torque was not significantly different from preexercise values. They had respectively recovered to 94.1 ± 4.5, 101.8 ± 7.4, and 99.6 ± 5.9% for the 30° (50%), 90° (50%), and 30° (65%) tasks. MTC was marginally, but significantly, lower after 10 min of recovery compared with the preexercise values: 96.8 ± 4.7, 95.5 ± 2.7, and 97.9 ± 2.9% for 30° (50%), 90° (50%), and 30° (65%) protocols, respectively. There were no significant differences among protocols.
|
DISCUSSION |
|---|
|
TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Neural activation.
The prolonged endurance times for the 30° compared with the 90° knee angle found in the present study correspond well to other studies (14, 22). This difference in endurance time between knee angles does not appear to originate from any differences in intensity at the start of the fatigue task. For both knee angles, at the start of the fatigue task, the equal relative intensity and similar torque levels were reflected by similar CAR and VLrsEMG levels (Figs. 3 and 4A). At the 90° knee angle, EMG activity of the VL and RF muscle at 50% MTC corresponds well to other literature (2, 25, 27). (Note that these studies did not use external occlusion. However, because root mean square values remained unaffected by the use of a cuff at different knee angles and contraction intensities in pilot studies, we felt it reasonable to compare our results with these studies.) The RFrsEMG levels were lower at the 30° compared with the 90° knee angle at the start of the fatigue task. This could indicate that exercise for the RF was less demanding at the 30° compared with the 90° knee angle. However, because the RF represents only 10% of the total knee extensor volume (34), its influence on knee extensor external torque and endurance time will probably be rather small.
A potential limitation of our study was that we did not measure the EMG activity of the vastus medialis muscle, nor is it possible to record surface EMG of the vastus intermedius muscle. Consequently, we cannot exclude preferential activation among the different heads of the quadriceps at different joint angles. However, because the degrees of freedom of the knee joint impose a restriction to extension and flexion, the task was straightforward in nature (isometric knee extension). Thus it is doubtful that, at relatively high force levels, the monoarticular head of the VL would differ from the vastus medialis. In addition, Weir et al. (35) found no difference in surface EMG of the VL and vastus medialis muscle across different joint angles (15, 45, and 75°). Moreover, at torque failure, CAR values were very high (mean > 0.95), indicating that the force measured of the entire quadriceps was near maximal, thereby excluding a large variation in activation of the separate muscle heads.
It has been suggested that muscle endurance could be limited by the neural activation of muscle (15). In the present study, the high and similar CAR values (mean > 0.95) among knee angles at torque failure indicate that, at both knee angles, the central nervous system seemed capable of maximally activating the motoneurons supplying the muscle. Evidently, differences in endurance between knee angles are not attributable to differences in central activation. In addition, at torque failure, triplets applied to the relaxed muscle were similar, indicating comparable levels of fatigue at the level of the contractile elements, independent of voluntary drive, at both knee angles.
A priori, it was considered possible that a difference in endurance time between long-lasting isometric contractions at the 30 and 90° knee angles could contribute to potential differences in muscle activation between the knee angles. In retrospect, this seems no longer relevant since, at torque failure, CARs for the 30° (50%) and 90° (50%) protocols were similar. Nevertheless, it is remarkable that at the 30° knee angle relative torque production had to be increased to 65% MTC (70% is probably an even more accurate percentage) for isometric endurance time to become similar to that obtained at 50% MTC at the 90° knee angle.
A potential error may have occurred in determining the MTC because we assumed a linear relationship to exist between voluntary and superimposed torque. However, because subjects were only allowed to participate if their CAR values exceeded 0.9, any error made in determining the muscles' maximal potential will be minimal. Moreover, it is highly doubtful that the minor error in determining MTC would be knee angle dependent and could therefore account for the large difference in isometric endurance time between the 30° (50%) and 90° (50%) protocols.
VLrsEMG levels were not different between knee angles at torque failure (Fig. 4A). The fact that normalized VLrsEMG values failed to reach prefatigue maximal values (58.5% mean of all protocols) could not be ascribed to neuromuscular transmission failure, because the postexercise M-wave peak-to-peak value remained high (mean > 92% of prefatigue value). The failure of EMG to reach 100% of the prefatigue maximal values during submaximal isometric contractions has been reported previously (9, 12, 27) and has, in part, been attributed to the cancellation of the interference EMG from overlapping positive and negative phases of action potentials (7).
At torque failure, RF surface EMG activity was significantly higher at the 90° compared with the 30° knee angle. This could indicate that neural activation of the fatigued RF muscle at the 90° knee angle was higher, which may reflect a neurophysiological mechanism partly compensating for a mechanical disadvantage (e.g., moment arm, relative position on the muscle length-tension relation) of the RF compared with the VL muscle. However, this remains highly speculative. We applied superimposed electrical nerve stimulation to obtain activation levels of the entire muscle group, but it is not possible to check for potential differences in activation among the different heads of the quadriceps muscle with this technique.
Postexercise rsEMG values of the VL and RF muscle, recorded during MVC <5 s after torque failure but with the blood flow to the muscle still occluded, were significantly higher compared with the values at torque failure for all protocols (Figs. 4 and 5). In our study, this recovery of EMG occurred without any recovery of torque. Torque recovery was not expected since blood flow was occluded and voluntary activation at torque failure was close to maximal. How can this clear decoupling of EMG and torque be explained? During exercise, considerable ion fluxes occur across the sarcolemmal membrane, which may result in high concentrations of potassium in the interfiber spaces (30). Fitch and McComas (11) have suggested that, as a result of ionic imbalance across the T-tubular membrane, a breakdown in the excitation-contraction coupling could occur, causing failure of inwardly propagated action potentials. Sacco et al. (28) have proposed that a brief respite from contraction, which occurred in our study, could restore a previously defective process of activation. However, in the latter study, and in contrast to the present study, this coincided with force recovery (28). Moreover, and also in contrast to the study of Sacco et al. (28), who electrically stimulated the muscle, neuromuscular transmission failure did not occur in the present study since postexercise M-wave peak-to-peak values remained high (mean > 92% of prefatigue value). Several decades ago, it was suggested that the output of the central nervous system is optimized to the slowing of the muscle contractile speed during fatigue. This so-called "muscle-wisdom" implies that motor unit firing rate can decrease during a sustained MVC without contributing to the decline in force output. The present observation of an increase in maximal surface EMG a few seconds after torque failure, during blood flow occlusion, without a concomitant increase of torque therefore may indicate that, at torque failure, activation was optimized to the slowed contractile properties of the muscle. Indeed, superimposed electrical stimulation indicated that muscle activation was close to maximal at that time. Therefore, it is possible that the higher electrical activity (EMG) of the muscle fibers a few seconds after torque failure did not lead to an increase of isometric torque, thereby accounting for the dissociation of the EMG activity and contractile capability of the muscle.
Energy metabolism.
The greater endurance at the 30° compared with the 90° knee angle could arise as the result of differences in 1) availability of oxygen for aerobic metabolism or 2) energy requirement. The extent of muscle perfusion (i.e., oxygenation), which has been shown to cause differences in endurance (23), is an important parameter to take into account. Muscle perfusion can change with intramuscular pressure (29), which in turn may depend on internal muscle force or muscle morphology (16), both of which are knee angle dependent. In the present study, by occluding the blood supply to the knee extensors during the contractions, possible differences in muscle perfusion at different knee angles were eliminated and consequently cannot have influenced endurance time.
It has also been proposed that muscle endurance is related to the number of force-producing cross bridges and its corresponding energy consumption (11). Hence, muscle endurance would depend on actin-myosin filament overlap, and fatigue would be greatest at optimum length. Support for this view has been found in frog muscle, in which a reduced energy cost of contraction has been shown at short compared with optimum length (1, 4, 17). In isolated mammalian muscle, however, energy consumption did not change from short to optimum length (24, 32). In contrast, de Haan et al. (8) showed lower energy-rich phosphate consumption at high and low muscle lengths compared with optimum lengths. Baker et al. (5) and Sacco et al. (28), using nuclear magnetic resonance spectroscopy, reported similar rates of ATP use at short and optimum length of the tibialis anterior muscle in humans during contraction. This suggests that the lower fatigability at shorter muscle lengths, such as found in the present study, cannot be explained by differences in energy consumption. However, in the present study, voluntary activation at torque failure was close to maximal, and there was no indication of neuromuscular transmission failure. Moreover, postexercise triplet torque was similar among knee angles, which suggests similar levels of fatigue of the contractile elements at both knee angles. Yet, endurance was higher at the 30° compared with the 90° knee angle despite full occlusion of the blood supply to the knee extensors. It therefore seems that isometric exercise is less strenuous at shorter compared with longer muscle lengths. This is supported further by the increase of torque intensity from 50 to 65% MTC that was required to match the endurance time at the 30° to the 90° knee angle in the present study. Moreover, during a long-lasting MVC, torque declined less steeply at the 30° than the 90° knee angle (unpublished observations). Together, these findings do suggest that isometric exercise is energetically less demanding at the 30° compared with the 90° knee angle.
In conclusion, the present findings show that muscle oxygenation and neural activation can be excluded as causes of knee angle-dependent differences in muscle endurance. It remains to be shown whether (sub)maximal isometric exercise is energetically less demanding at extended knee angles.
|
FOOTNOTES |
|---|
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.
|
REFERENCES |
|---|
|
TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
This article has been cited by other articles:
|
|
 |
|
  J P Weir, T W Beck, J T Cramer, T J Housh, T D Noakes, A St Clair Gibson, and E V Lambert Is fatigue all in your head? A critical review of the central governor model * Commentary. Br. J. Sports Med., July 1, 2006; 40(7): 573 - 586. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 O. Prasartwuth, T. J. Allen, J. E. Butler, S. C. Gandevia, and J. L. Taylor Length-dependent changes in voluntary activation, maximum voluntary torque and twitch responses after eccentric damage in humans J. Physiol., February 15, 2006; 571(1): 243 - 252. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. J. de Ruiter, M. D. de Boer, M. Spanjaard, and A. de Haan Knee angle-dependent oxygen consumption during isometric contractions of the knee extensors determined with near-infrared spectroscopy J Appl Physiol, August 1, 2005; 99(2): 579 - 586. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| Visit Other APS Journals Online |
Significantly lower than 90 (50%) and 30° (65%) at the start of the fatigue task. 
Significantly lower than 90 (50%) at the end of the fatigue task.