| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Journal of Physiology (2002), 540.3, pp. 1071-1078
© Copyright 2002 The Physiological Society
DOI: 10.1113/jphysiol.2001.014290
 |
ABSTRACT |
|---|
 TopAbstract IntroductionMethodsResultsDiscussionReferences |
|---|
This study was performed to test two hypotheses: (1) ischaemic preconditioning (development of tolerance to ischaemia) influences muscle fibre conduction velocity (MFCV) during repeated ischaemic isometric exercise and (2) the increase in MFCV to supranormal levels during recovery from ischaemic exercise is caused by activation of Na+-K+-ATPase. For this purpose, MFCV was measured with surface electromyography (sEMG) during repeated ischaemic isometric exercise of the brachioradial muscle (2 min at 30 % of maximal voluntary contraction). The involvement of ischaemic preconditioning was tested by changing the duration of ischaemia and by intra-arterial infusion of adenosine (brachial artery, 50 µg min-1 dl-1). The role of Na+-K+-ATPase was explored using ouabain (0.2 µg min-1 dl-1). During the exercise, MFCV decreased from 4.4 ± 0.2 m s-1 to 3.7 ± 0.2 m s-1 (P < 0.01, n = 13). Similar reductions in MFCV were observed during repeated exercise, irrespective of the reperfusion time (10 min vs. 18 min) or duration of the ischaemia (2 vs. 10 min). However, initial MFCV gradually increased for each subsequent contraction when contractions were repeated at 10 min intervals (4.4 ± 0.2 m s-1 vs. 4.9 ± 0.2 m s-1 for the first and fourth contraction respectively; P < 0.01; n = 13). This increase was not observed when contractions were performed at 18 min intervals, nor when additional ischaemia was applied. Intra-arterial adenosine did not affect MFCV. Intra-arterial ouabain did not affect the reduction in MFCV during exercise but completely prevented the increase in MFCV during recovery: from 4.7 ± 0.2 m s-1 to 5.2 ± 0.2 m s-1 vs. 4.5 ± 0.1 m s-1 to 4.5 ± 0.1 m s-1 in the absence and presence of ouabain respectively (P < 0.05 for ouabain effect; n = 6). In conclusion, ischaemic preconditioning is not involved in changes in MFCV during repeated ischaemic isometric exercise. The increase in MFCV during recovery from repeated ischaemic isometric exercise is caused by rapid activation of Na+-K+-ATPase.
(Received 21 November 2001; accepted after revision 5 February 2002)
Corresponding author G. A. Rongen: Department of Pharmacology-Toxicology (233), University Medical Center, Nijmegen, PO Box 9101, 6500 HB Nijmegen, The Netherlands. Email: g.rongen{at}farm.kun.nl
|
INTRODUCTION |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
Skeletal muscle fibre conduction velocity (MFCV), as measured with surface electromyography (sEMG), is used to study electrophysiological properties of the sarcolemma in humans in vivo (De Luca, 1984). With this technique, a decrease in MFCV has been observed during isometric exercise. This phenomenon has been related to exercise-related ischaemia (Zwarts et al. 1987; Zwarts & Arendt-Nielsen, 1988) and the development of fatigue (Arendt-Nielsen & Zwarts, 1989). The effect of exercise on MFCV has been used successfully to characterize patients with inborn errors of muscle metabolism (Linssen et al. 1990; van der Hoeven et al. 1994; Drost et al. 2001). At a molecular level, the mechanism of this decrease in conduction velocity has not been elucidated. More in particular, the involvement of ion channels or pumps or the accumulation of extracellular ions or metabolites have only partially been characterized (Miller et al. 1995).
When isometric exercise is repeated, a paradoxical increase in baseline MFCV is observed. The mechanism of this 'supranormal' MFCV in intermittent isometric exercise has not been studied in detail. Several hypotheses have been put forward including muscle fibre swelling, an increase in muscle temperature and activation of Na+-K+-ATPase (van der Hoeven et al. 1993; van der Hoeven & Lange, 1994). The significance of the increased conduction velocity in muscle physiology is not known. It may be involved in the 'warm-up' effect: an increase in muscle performance after moderate exercise.
Recently, ischaemic preconditioning has been demonstrated in skeletal muscle (Pang et al. 1995; Forrest et al. 1997). Ischaemic preconditioning is defined as a delay in ischaemic cell death by previous short periods of ischaemia. Endogenous interstitial adenosine, released during ischaemia, is an important trigger of this phenomenon in skeletal muscle. In animal models, ischaemic preconditioning reduces infarct size in skeletal muscle by approximately 50 %. This protective effect can be mimicked by intra-arterial infusion of adenosine. Pharmacological exploitation of this powerful endogenous protective mechanism is of important clinical relevance in settings of critically reduced muscle blood flow such as, for instance, during surgical procedures involving muscle flap transposition or after acute arterial thrombosis. An in vivo model to study ischaemic preconditioning in humans is lacking. The experimental induction of cell death is, of course, not an option in human in vivo research. Therefore, a validated marker of reversible ischaemic cell injury that detects the development of tolerance against the deleterious consequences of ischaemia is needed to bring the phenomenon of ischaemic preconditioning into the clinical arena. Since MFCV has proven to be a sensitive marker to ischaemic exercises it may fulfil these requirements (Zwarts et al. 1987; Zwarts & Arendt-Nielsen, 1988).
The aims of this study were two-fold: (1) to explore the involvement of ischaemic preconditioning in the course of MFCV during repeated ischaemic isometric exercise and (2) to investigate the role of Na+-K+-ATPase in the increased MFCV after ischaemic isometric exercise.
|
METHODS |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
Subjects
In total, 14 healthy volunteers participated in this study, ranging in age from 19 to 56 years (average: 26 years). Their height and weight were (mean ± S.D.) 179 ± 9 cm and 70.6 ± 7.5 kg respectively. Six of these volunteers were female. All subjects gave written informed consent before participation. The study was approved by the local medical ethics committee.
EMG and force recording
The experiments were performed on the left brachioradial muscle. The subject sat in a chair, with the upper arm in 90 deg abduction, the elbow in 120 deg flexion and the wrist pronated. The arm was supported at the elbow and the wrist. To lower the electrode impedance the skin was scrubbed first, and a small amount of electrode cream was rubbed in. A total of 15 gold-plated electrodes (d = 1.52 mm) were placed 3 mm apart in a rigid holder. This array was placed parallel to the fibre direction on the distal part of the brachioradial muscle. The data were recorded with respect to a reference electrode on the elbow, filtered (3.2-800 Hz), and sampled at 4000 Hz (16 bits, 0.5 µV bit-1) using a 64-channel amplifier (BioSemi, Mark-6). The isometric force of the elbow flexion was measured at the wrist with a specially designed ergometer (Linssen et al. 1990) digitized (100 Hz) and fed to a personal computer. The exerted force was continuously displayed in front of the volunteer on a computer screen.
All analysis were performed off-line. MFCV was calculated for each subsequent period of 0.25 seconds from the delay of each set of two bipolar signals that were 9 mm apart, using the phase difference method (Linssen et al. 1990). Only the bipolar recordings distal to the innervation zone were used. Only correlations > 0.9 were accepted (see Fig. 1). Thus, for each period of 0.25 s a set of conduction velocities was obtained which were averaged to one value. The number of usable bipolar signals varied, depending on the size of the muscle and the location of the innervation zone. At least one set of two bipolar signals was used for each volunteer. Within an experiment the number of sets of two bipolar signals remained constant for the subsequent contractions. In three volunteers, we were not able to obtain a single set of two bipolar signals with a correlation > 0.9. These volunteers were excluded from the study and have not been included in the analysis. In addition, the EMG amplitude was expressed as the root mean square of each bipolar signal and averaged for each period of 0.25 s. Changes in EMG amplitude reflect recruitment or decruitment of motor units that could potentially be responsible for changes in muscle conduction velocity.
 |
View larger version [in this window] [in a new window] |
|
|
Figure 1. Example of a subset of the 15 recorded sEMG signals showing four bipolar sEMG leads from proximal (trace 3) to distal (trace 9) part of the brachioradial muscle The distance between each subsequent bipolar trace is constant (6 mm). Note the high similarity between the consecutive signals. These registrations were performed at the start (upper panel) and the end (lower panel) of a 2 min ischaemic isometric exercise at 30 % of maximum voluntary force. Muscle fibre conduction velocity decreased during this bout of exercise, as reflected by the increase in time delay between subsequent bipolar signals. | ||
Procedures
All studies were performed in the morning after at least 24 h of abstinence from caffeine-containing beverages. At least 30 min before the start of the first ischaemic isometric exercise, maximal voluntary contraction (MVC) of the brachioradial muscle was determined three times. The highest value was accepted as 100 % of MVC. In all the protocols, subsequent isometric contractions of the brachioradial muscle were performed at 30 % of MVC for 2 min during occlusion of the forearm circulation using an upper arm cuff that was inflated at 200 mmHg.
The influence of prolonged ischaemia on EMG changes during repeated ischaemic isometric exercise. Ischaemia is an important trigger of ischaemic preconditioning. Therefore, we assumed that, if ischaemic preconditioning is involved in the modulation of MFCV during repeated ischaemic exercise, additional ischaemia should intensify these changes.
First, a group of seven volunteers performed four ischaemic isometric contractions (2 min ischaemia, 10 min reperfusion). At least one month later, five of these volunteers together with two others performed four ischaemic isometric contractions but now, the first three ischaemic isometric contractions were followed by 8 min of ischaemia without exercise and 10 min reperfusion (10 min ischaemia, 10 min reperfusion). Again, at least one month later, six of these volunteers performed four ischaemic isometric contractions but now an 18 min reperfusion period was allowed between each contraction (2 min ischaemia, 18 min reperfusion; time-control experiment).
The effect of intra-arterial adenosine or ouabain on EMG changes during repeated ischaemic isometric contractions. To explore further a possible role of ischaemic preconditioning, the effect of intra-arterial adenosine was studied on the course of MFCV during repeated ischaemic isometric exercise. Adenosine induces ischaemic preconditioning in pig skeletal muscle (Forrest et al. 1997).
Seven volunteers (two of them had participated in the previous studies) performed five ischaemic isometric exercises (2 min ischaemia, 10 min reperfusion) on two separate days, at least one week apart. On one of these days (randomized), the brachial artery was cannulated with a 20 gauge catheter (Angiocath, Deseret Medical, Becton Dickinson Sandy, UT, USA) for intra-arterial drug infusion (automatic syringe infusion pump, type STC-521, Terumo, Tokyo, Japan). Adenosine was infused during the first 8 min of the first four reperfusion periods at a dose of 50 µg min-1 dl-1 forearm volume. Forearm volume was determined using the water displacement method. This adenosine dose was based on work by others in skeletal muscle of the pig, which indicated that this intra-arterial infusion rate should be sufficient to induce ischaemic preconditioning (Forrest et al. 1997; Pang et al. 1997).
Finally, the role of Na+-K+-ATPase in the course of MFCV during repeated ischaemic exercise was studied using intra-arterial infusion of ouabain, an inhibitor of Na+-K+-ATPase. At least one month after completion of the adenosine study, six of the seven volunteers agreed to participate in this additional study. After intra-arterial cannulation and measurement of MVC, the volunteers performed five isometric contractions (2 min ischaemia, 10 min reperfusion), as described for adenosine. Ouabain was infused for 10 min during the first four reperfusion periods at a dose of 0.2 µg min-1 dl-1. The control day of the adenosine study served as a control for this protocol.
Statistical analysis
Since not all volunteers were able to complete the isometric contraction for 2 min (see Table 1), the duration of each contraction was expressed as a percentage of the total contraction time. For each contraction, MFCV and EMG amplitude were averaged for eight subsequent periods of 12.5 % of the total duration of the contraction. For comparison of the contractions in the presence of adenosine or ouabain with control, the results of contractions 2-5 were normalized to the first contraction on the same day in order to correct for possible differences in position of the electrode array between the two study days. For this purpose, results were expressed as percentage difference from contraction 1 for each subsequent 12.5 % period of each contraction. ANOVA for repeated measures, with contraction order and contraction time as within-subject factors, was used to test differences between contractions. For the studies with intra-arterial drug infusion, treatment (adenosine or ouabain vs. control) was used as an additional within-subject factor. Two-sided P-values < 0.05 were considered statistically significant.
|
RESULTS |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
The influence of prolonged ischaemia on sEMG changes during repeated ischaemic isometric contraction
To describe the effect on sEMG of four periods of 2 min ischaemic exercise, followed by 10 min of reperfusion, the pooled data of 13 experiments (seven from protocol 1 and six from the control day of protocol 2) were analysed (Fig. 2). The initial MFCV values increased gradually from 4.4 ± 0.2 m s-1 for the first contraction to 4.7 ± 0.2, 4.8 ± 0.2 and 4.9 ± 0.2 m s-1 for the subsequent contractions respectively (P < 0.05 for the effect of contraction order; P < 0.01 for first vs. second and second vs. third contraction; P > 0.3 for third vs. fourth contraction). Within each contraction, MFCV was reduced to a similar extent: conduction velocity decreased from 4.4 ± 0.2 to 3.7 ± 0.2 m s-1 and from 4.9 ± 0.2 to 4.2 ± 0.2 m s-1 during the first and fourth contraction respectively (P < 0.001 for effect of contraction time; P > 0.4 for interaction between contraction order and contraction time).
 |
View larger version [in this window] [in a new window] |
|
|
Figure 2. The course of MFCV and EMG amplitude during four subsequent 2 min ischaemic isometric contractions of the brachioradial muscle (30 % of maximal voluntary contraction)
| ||
The EMG amplitude increased from 53.7 ± 1.2 to 62.3 ± 1.6 µV during the first contraction. During the subsequent contractions, sEMG amplitude increased from 57.5 ± 1.3 to 79.7 ± 1.7 µV, from 55.1 ± 1.2 to 89.2 ± 2.4 µV and from 51.7 ± 1.0 to 74.7 ± 1.4 µV respectively (P < 0.05 for contraction time, P > 0.3 for the effect of contraction order and P > 0.2 for the interaction between contraction order and contraction time).
In contrast to the 2 min ischaemia protocol, 2 min ischaemic contractions followed by 8 min of additional ischaemia and 10 min reperfusion did not increase the conduction velocity during subsequent contractions. As in the 2 min ischaemia studies, the EMG amplitude increased towards the end of each contraction but their course did not differ between subsequent contractions (see Fig. 2). Likewise, no carry-over effect of previous ischaemic contractions was observed on MFCV when the reperfusion time was increased to 18 min (see Fig. 2). Thus, prolonged ischaemia did not affect the course of conduction velocity. However, the time between each contraction is critical: a 10 min interval resulted in an increase in MFCV whereas an 18 min interval did not.
The effect of intra-arterial adenosine or ouabain on EMG changes during repeated ischaemic isometric contractions
Intra-arterial infusion of adenosine did not affect the course of MFCV, normalized to the first contraction (P > 0.2 for the effect of adenosine, for the interaction between adenosine and contraction order and for the interaction between adenosine, contraction order and contraction duration; see Fig. 3). Likewise, adenosine did not affect the EMG amplitude.
 |
View larger version [in this window] [in a new window] |
|
|
Figure 3. The effect of intra-arterial adenosine on conduction velocity and EMG amplitude
| ||
Ouabain completely neutralized the exercise-induced increase in MFCV (see Fig. 4), but did not affect the EMG amplitude. Without ouabain, MFCV decreased from 4.7 ± 0.2 to 4.0 ± 0.3 m s-1 and from 5.2 ± 0.2 to 4.5 ± 0.3 m s-1 during the first and fifth contraction respectively. In the presence of ouabain, MFCV decreased from 4.5 ± 0.1 to 4.0 ± 0.3 m s-1 and from 4.5 ± 0.1 to 4.0 ± 0.1 m s-1 during the first and fifth contraction respectively (P = 0.05 for effect of ouabain on baseline; P > 0.2 for effect of ouabain on reduction during exercise; n = 6).
 |
View larger version [in this window] [in a new window] |
|
|
Figure 4. The effect of intra-arterial ouabain on conduction velocity and EMG amplitude
| ||
|
DISCUSSION |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
This study confirms that MFCV decreases during isometric exercise and is subsequently increased after recovery to values above baseline. The main new finding of this study is that the initial increase of MFCV following repeated contraction is prevented by ouabain, indicating that it is caused by activation of Na+-K+-ATPase. In addition, the increased MFCV lasted for at least 10 min but returned to baseline within 18 min. Additional ischaemia did not prevent recovery of MFCV to baseline, indicating that ischaemia is not the stimulus for the increase in Na+-K+-ATPase activity. Therefore, ischaemic preconditioning is not likely to mediate the increased Na+-K+-ATPase activity. This notion is further supported by the lack of an effect of intra-arterial adenosine on the course of MFCV.
In contrast to the supranormal MFCV during recovery, the reduction in MFCV during exercise was not affected by the duration of the recovery period or the infusion of ouabain. Therefore, these two phenomena are probably mediated by two independent underlying mechanisms.
The observed time course of increased MFCV contrasts with a previous report in which an increased MFCV is described in the biceps for up to 1 h (van der Hoeven et al. 1993). However, in this study, conduction velocity was repeatedly measured at intervals of 1-5 min. Since measurement of MFCV requires muscle contraction, the prolonged increase in MFCV in this study could be caused by repeated exercise-related stimulation of Na+-K+-ATPase. This problem was circumvented in the present study by using separate protocols with different recovery periods.
Cell swelling has been suggested to cause the increase in MFCV during recovery from isometric exercise. Indeed, van der Hoeven et al. observed an increase in circumference of the upper arm during the first 10-15 min after isometric exercise of the biceps (van der Hoeven & Lange, 1994). However, muscle blood flow is increased after exercise and an increase in upper arm circumference does not discriminate between muscle cell swelling and increased blood volume within the muscle.
We used a pharmacological approach to study the underlying mechanisms of changes in EMG during and after ischaemic exercise. For this purpose, we infused drugs into the brachial artery. Using this technique, the local concentration of drugs in the forearm mainly depends on local blood flow and infusion rate. The systemic concentration of the infused drug depends on its volume of distribution, which is large for ouabain (700 l for a person of 70 kg), local extraction or metabolism in the forearm (which is high for adenosine) and elimination half-life, which is very short for adenosine (a few seconds). Therefore, intra-arterial infusion of low doses of ouabain or adenosine allowed us to reach effective local concentrations without inducing systemic actions. This concept has been confirmed previously for both adenosine and ouabain using bilateral forearm blood flow, blood pressure and heart rate as the dependent variables (Rongen et al. 1995; Tack et al. 1996; Rongen et al. 1998). In the present study, we measured MFCV in the brachioradial muscle. This muscle was chosen because of its parallel orientation of muscle fibres and its superficial location, which makes it an ideal candidate for measurement of conduction velocity by surface EMG. Furthermore, its relation to the brachial artery allowed us to study the effect of local pharmacological interventions on muscle conduction. The proof for this concept is given by the observation that ouabain, a specific inhibitor of Na+-K+-ATPase, prevented the increase in MFCV. Ouabain infusion did not affect EMG amplitude. Therefore, recruitment of different motor units does not explain the impressive effect of ouabain on MFCV. Thus, activation of Na+-K+-ATPase is critically involved in the observed supranormal MFCV during recovery from isometric exercise. Na+-K+-ATPase exchanges three sodium ions against two potassium ions. Therefore, activation of this ion pump results in hyperpolarization of the sarcolemmal membrane, which in turn facilitates propagation of action potentials (Knochel et al. 1985). Several human studies have shown an increased expression of Na+-K+-ATPase in response to exercise (Green et al. 1993; McKenna et al. 1993). However, our observation that MFCV did not increase when 18 min of recovery were allowed between the contractions does not support an increased protein expression as the explanation for this short-lived activation of Na+-K+-ATPase activity. More likely, these short bouts of exercise temporarily induced post-translational changes in Na+-K+-ATPase activity (Beguin et al. 1996; Ragolia et al. 1997). This concept is further supported by observations in isolated animal muscle preparations where muscle contraction is associated with a rapid increase in Na+-K+-ATPase activity (Clausen, 1996). The physiological importance of activation of sarcolemmal Na+-K+-ATPase in response to exercise is not exactly known. Two hypotheses have been put forward in the literature. The first hypothesis concentrates on the consequences of Na+-K+-ATPase activity for the function of the muscle itself. Exercise is associated with considerable ion fluxes across the sarcolemmal membrane: the muscle fibre looses potassium and gains sodium. As a consequence potassium concentration rises in the interstitium and, due to its small volume, especially in the T-tubules, high concentrations of potassium may occur during exercise, which may reduce contractile performance. Increased Na+-K+-ATPase activity may prevent these changes in ion gradients and preserve contractile performance (Nielsen & Overgaard, 1996). The second hypothesis focuses on the deleterious cardiac effects of muscle potassium loss during intensive exercise. Activation of Na+-K+-ATPase may reduce the spill of muscular potassium into the systemic circulation and may prevent cardiac toxicity (Knochel et al. 1985).
Based on evidence that the reduction in MFCV during isometric exercise relates to ischaemia (Zwarts et al. 1987; Zwarts & Arendt-Nielsen, 1988) and the possible involvement of Na+-K+-ATPase activation in ischaemic preconditioning (Haruna et al. 1998), we explored the possibility that ischaemic preconditioning may be involved in changes in MFCV during repeated ischaemic isometric exercise. Three observations in this study argue against such an involvement. The reduction in MFCV during ischaemic exercise was not reduced by previous bouts of exercise. Furthermore, neither prolonged ischaemia nor adenosine, the supposed triggers for ischaemic preconditioning, affect the course of MFCV.
Insufficient power may have prevented us from detecting a possible effect of adenosine on MFCV. Unfortunately, we did not have data available to perform a power calculation prior to the study. Nevertheless, it is possible to use the data that were obtained in this study to estimate the power of the EMG technique used in this cross-over design, assuming that intra-arterial adenosine did not affect MFCV. With these assumptions, the detectable difference between the two days in conduction velocity for the fifth contraction (expressed as a percentage change from MFCV during the first contraction) is 15 % (n = 7, 
= 0.05 and a power of 0.8; paired t-test for first 12.5 % of contraction duration). Since the increase in MFCV during subsequent contractions was 15 %, the power of our study was sufficient to detect a complete inhibition or a doubling of the contraction-induced increase in MFCV in response to intra-arterial adenosine. Smaller changes may have been missed due to a type II error. Apart from a type II error, the adenosine dose may not have been sufficient to trigger ischaemic preconditioning. Although the used dose has been applied successfully in pigs to induce ischaemic preconditioning (Forrest et al. 1997; Pang et al. 1997), we cannot exclude the possibility that humans require a larger dose to trigger this phenomenon.
In conclusion, this study shows that intra-arterial drug infusions can be applied successfully to study exercise-induced changes in MFCV. Ouabain prevented the increase in MFCV during recovery from exercise, indicating the involvement of Na+-K+-ATPase in this response. Our observations do not support a role for ischaemic preconditioning in the exercise-induced changes in MFCV.
|
REFERENCES |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
| ARENDT-NIELSEN, L. & ZWARTS, M. (1989). Measurement of muscle fibre conduction velocity in humans: techniques and applications. Journal of Clinical Neurophysiology 6, 173-190 | [Medline] |
| BEGUIN, P., BEGGAH, A., COTECCHIA, S. & GEERING, K. (1996). Adrenergic, dopaminergic, and muscarinic receptor stimulation leads to PKA phosphorylation of Na-K-ATPase. American Journal of Physiology 270, C131-137 | [Medline] |
| CLAUSEN, T. (1996). The Na+, K+ pump in skeletal muscle: quantification, regulation and functional significance. Acta Physiologica Scandinavica 156, 227-235 | [Medline] |
| DE LUCA, C. J. (1984). Myoelectrical manifestations of localized muscular fatigue in humans. Critical Reviews of Biomedical Engineering 11, 251-279 | |
| DROST, G., BLOK, J. H., STEGEMAN, D. F., VAN DIJK, J. P., VAN ENGELEN, B. G. & ZWARTS, M. J. (2001). Propagation disturbance of motor unit action potentials during transient paresis in generalized myotonia: a high-density surface EMG study. Brain 124, 352-360 | [Abstract/Full Text] |
| FORREST, C. R., NELIGAN, P., ZHONG, A., HE, W., YANG, R. Z. & PANG, C. Y. (1997). Acute adenosine treatment is effective in augmentation of ischemic tolerance in muscle flaps in the pig. Plastic and Reconstructive Surgery 99, 172-182 | [Medline] |
| GREEN, H. J., CHIN, E. R., BALL-BURNETT, M. & RANNEY, D. (1993). Increases in human skeletal muscle Na+-K+-ATPase concentration with short-term training. American Journal of Physiology 264, C1538-1541 | [Medline] |
| HARUNA, T., HORIE, M., KOUCHI, I., NAWADA, R., TSUCHIYA, K., AKAO, M., OTANI, H., MURAKAMI, T. & SASAYAMA, S. (1998). Coordinate interaction between ATP-sensitive K+ channel and Na+, K+-ATPase modulates ischemic preconditioning. Circulation 98, 2905-2910 | [Abstract/Full Text] |
| KNOCHEL, J. P., BLACHLEY, J. D., JOHNSON, J. H. & CARTER, N. W. (1985). Muscle cell electrical hyperpolarization and reduced exercise hyperkalemia in physically conditioned dogs. Journal of Clinical Investigation 75, 740-745 | [Medline] |
| LINSSEN, W. H. J. P., JACOBS, M., STEGEMAN, D. F., JOOSTEN, E. M. G. & MOLEMAN, J. (1990). Muscle fatigue in McArdle's disease. Muscle fibre conduction velocity and surface EMG frequency spectrum during ischemic exercise. Brain 113, 1779-1793 | [Abstract] |
| MCKENNA, M. J., SCHMIDT, T. A., HARGREAVES, M., CAMERON, L., SKINNER, S. L. & KJELDSEN, K. (1993). Sprint training increases human skeletal muscle Na+-K+-ATPase concentration and improves K+ regulation. Journal of Applied Physiology 75, 173-180 | [Medline] |
| MILLER, R. G., KENT-BRAUN, J. A., SHARMA, K. R. & WEINER, M. W. (1995). Mechanisms of human muscle fatigue. Quantitating the contribution of metabolic factors and activation impairment. Advances in Experimental and Medical Biology 384, 195-210 | |
| NIELSEN, O. B. & OVERGAARD, K. (1996). Ion gradients and contractility in skeletal muscle: the role of active Na+, K+ transport. Acta Physiologica Scandinavica 156, 247-256 | [Medline] |
| PANG, C. Y., NELIGAN, P., ZHONG, A., HE, W., XU, H. & FORREST, C. R. (1997). Effector mechanism of adenosine in acute ischemic preconditioning of skeletal muscle against infarction. American Journal of Physiology 273, R887-895 | [Medline] |
| PANG, C. Y., YANG, R. Z., ZHONG, A., XU, N., BOYD, B. & FORREST, C. R. (1995). Acute ischaemic preconditioning protects against skeletal muscle infarction in the pig. Cardiovascular Research 29, 782-788 | [Medline] |
| RAGOLIA, L., CHERPALIS, B., SRINIVASAN, M. & BEGUM, N. (1997). Role of serine/threonine protein phosphatases in insulin regulation of Na+/K+-ATPase activity in cultured rat skeletal muscle cells. Journal of Biological Chemistry 272, 23 653-23 658 | [Abstract/Full Text] |
| RONGEN, G. A., BROOKS, S. C., ANDO, S., ABRAMSON, B. L. & FLORAS, J. S. (1998). Angiotensin AT 1 Author: style OK?receptor blockade abolishes the reflex sympatho-excitatory response to adenosine. Journal of Clinical Investigation 101, 769-776 | [Abstract/Full Text] |
| RONGEN, G. A., SMITS, P., VER DONCK, K., WILLEMSEN, J. J., DE ABREU, R. A., VAN BELLE, H. & THIEN, T. (1995). Hemodynamic and neurohumoral effects of various grades of selective adenosine transport inhibition in humans. Implications for its future role in cardioprotection. Journal of Clinical Investigation 95, 658-668 | [Medline] |
| TACK, C. J. J., LUTTERMAN, J. A., VERVOORT, G., THIEN, T. & SMITS, P. (1996). Activation of the sodium-potassium pump contributes to insulin-induced vasodilation in humans. Hypertension 28, 426-432 | [Abstract/Full Text] |
| VAN DER HOEVEN, J. H. & LANGE, F. (1994). Supernormal muscle fibre conduction velocity during intermittent isometric exercise in human muscle. Journal of Applied Physiology 77, 802-806 | [Medline] |
| VAN DER HOEVEN, J. H., LINKS, T. P., ZWARTS, M. J. & VAN WEERDEN, T. W. (1994). Muscle fibre conduction velocity in the diagnosis of familial hypokalemic periodic paralysis - invasive versus surface determination. Muscle Nerve 17, 898-905 | [Medline] |
| VAN DER HOEVEN, J. H., VAN WEERDEN, T. W. & ZWARTS, M. J. (1993). Long-lasting supernormal conduction velocity after sustained maximal isometric contraction in human muscle. Muscle Nerve 16, 312-320 | [Medline] |
| ZWARTS, M. J. & ARENDT-NIELSEN, L. (1988). The influence of force and circulation on average muscle fibre conduction velocity during local muscle fatigue. European Journal of Applied Physiology 58, 278-283 | |
| ZWARTS, M. J., VAN WEERDEN, T. W. & HAENEN, H. T. (1987). Relationship between average muscle fibre conduction velocity and EMG power spectra during isometric contraction, recovery and applied ischemia. European Journal of Applied Physiology and Occupational Physiology 56, 212-216 | [Medline] |
Acknowledgements
The research of Dr G. A. Rongen has been made possible by a fellowship of the Royal Netherlands Academy of Arts and Sciences.
This article has been cited by other articles:
|
|
 |
|
  D. Farina, M. Gazzoni, and F. Camelia Conduction velocity of low-threshold motor units during ischemic contractions performed with surface EMG feedback J Appl Physiol, April 1, 2005; 98(4): 1487 - 1494. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 T. CLAUSEN Na+-K+ Pump Regulation and Skeletal Muscle Contractility Physiol Rev, October 1, 2003; 83(4): 1269 - 1324. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
, first contraction; 
, second contraction; 
, third contraction; 
, fourth contraction. P-values indicate level of significance for the effect of contraction duration; *P < 0.05 vs. first contraction. The effect of contraction duration never differed significantly between subsequent contractions.