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Electrical stimulation superimposed onto voluntary muscular contraction reduces deterioration of both postural control and quadriceps femoris muscle strength
Neuroscience 165 (2010) 1471–1475
ELECTRICAL STIMULATION SUPERIMPOSED ONTO VOLUNTARY MUSCULAR CONTRACTION REDUCES DETERIORATION OF BOTH POSTURAL CONTROL AND QUADRICEPS FEMORIS MUSCLE STRENGTH T. PAILLARD,a* E. MARGNES,a J. MAITRE,a V. CHAUBET,a Y. FRANÇOIS,b J. L. JULLY,b G. GONZALEZb AND L. BORELc
tion of the action potential along the muscle membrane, events associated with cross-bridge interaction, and calcium uptake by the sarcoplasmic reticulum (Lee et al., 2000). Central fatigue results from the inability of motoneurons to maintain their firing rates to sustain maximal voluntary contraction; this inability is due to factors acting at spinal and supraspinal sites (Gandevia, 2001). To reduce muscle force and thus generate a fatigue state, sustained submaximal voluntary muscular contractions (VCs) are especially efficient (Yoon et al., 2007). When fatiguing voluntary contractions specifically concern postural tonic muscles (e.g. ankle plantar-flexors and dorsiflexors, ankle invectors and evectors, knee extensors, lumbar erector spinae, or neck muscles), they can induce postural control disturbance (Gribble and Hertel, 2004; Yaggie and McGregor, 2002; Vuillerme et al., 2002; Corbeil et al., 2003; Ledin et al., 2004; Caron, 2003; Johnston et al., 1998; Harkins et al., 2005; Madigan et al., 2006; Gosselin et al., 2004). Thus, localized muscle fatigue produced by the repetition of VCs may alter postural control. Moreover, postural control disturbances differ according to the muscle group. For example, fatigue of knee or hip musculature alters postural control more than fatigue of ankle musculature does (Miller and Bird, 1976; Gribble and Hertel, 2004; Bizid et al., 2009b). It takes longer to recover postural control as muscle strength reduces after fatiguing exercises (Harkins et al., 2005). The physiological impact of neuromuscular electrical stimulation (ES) differs from that of voluntary contraction (Paillard, 2008). Relative to voluntary contraction, neuromuscular ES enhances fatigued muscle soreness and damage (Moreau et al., 1995). Neuromuscular ES acidifies the cytoplasm more than voluntary contraction does (Vanderthommen et al., 2003). This acidity alters proprioceptive sensitivity (Loscher et al., 1996; Rossi et al., 1999; Avela et al., 2001; Zytnicki et al., 1990), a major determinant in postural control mechanisms (Massion, 1994). The question thus arises as to whether the effects of fatigue provoked by neuromuscular ES on postural control differ from those induced by voluntary contraction. The force produced by neuromuscular ES is lower than that generated by voluntary muscular contraction (VC) (Bax et al., 2005). Yet, to compare the effects of muscular fatigue on postural control, the force produced by these two modalities must be equivalent (Vanderthommen et al., 2003; Hamada et al., 2004). To reach an equivalent force production, ES has to be superimposed onto VC (Paillard
a Université de Pau et des Pays de l’Adour, Département STAPS, ZA Bastillac Sud, 65000 Tarbes, France b Centre Medical de la Mutuelle Générale de l’Education Nationale, Domaine L’Arbizon, 65200 Bagnères de Bigorre, France c Laboratoire de Neurosciences Intégratives et Adaptatives UMR 6149, Université de Provence/CNRS, Centre St. Charles, Pôle 3C–Case B, 3, Place Victor Hugo, 13331 Marseille Cedex 03, France
Abstract—Fatiguing exercise of the quadriceps femoris muscle degrades postural control in human subjects. The aim of this work was to compare the effects of the fatigue of the quadriceps femoris induced by voluntary muscular contraction (VC), and by electrical stimulation (ES) superimposed onto voluntary muscular contraction (VCⴙES), on postural control and muscle strength. Fourteen healthy young adults participated in the study. Postural control and muscle strength were evaluated using a stable force platform and an isokinetic dynamometer, respectively, before (PRE condition) and after the completion of each fatiguing exercise (immediately: POST condition; after a 5 min recovery time: POST 5 condition). In POST, both postural control and muscle strength were impaired by both fatiguing exercises. However, the impairment was higher for VC than for VCⴙES. In POST 5, for both fatiguing exercises, postural control recovered its initial level while muscle strength did not. These results suggest that superimposing ES onto voluntary muscular contractions (VCs) impaired muscle strength and postural control less than did VCs alone. However the duration of recovery of these two neurophysiological functions did not differ for the two fatiguing exercises. For both exercises, postural control was restored faster than the ability to produce muscular strength. © 2010 IBRO. Published by Elsevier Ltd. All rights reserved. Key words: muscle fatigue, neuromuscular electrical stimulation, unipedal stance, recovery.
Fatigue can be defined as a progressive increase in the effort required to produce the same level of force, followed by a progressive inability to continuously or repeatedly maintain this force (Enoka and Stuart, 1992). The fatigue originates from peripheral and/or central features. Peripheral fatigue involves the neuromuscular junction, propaga*Corresponding author. Tel: ⫹33(0)562-566-100; fax: ⫹33(0)562-566-110. E-mail address: [email protected] (T. Paillard). Abbreviations: COP, center of foot pressure; ES, electrical stimulation; MVC, measurement of maximal voluntary contraction; VC, voluntary muscular contraction; VCs, voluntary muscular contractions.
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et al., 2005). ES superimposed onto voluntary contraction has been widely employed in therapeutic contexts and has proved highly efficient. In healthy subjects, however, we do not know the effects of ES superimposed onto voluntary contraction on muscular fatigue and postural control immediately after its application and whether these effects differ from those obtained after voluntary contraction. Only Bizid et al. (2009a) have explored the differential effects on postural control of fatigue as provoked by either VC or ES superimposed onto VC. They showed that the triceps surae was equally disturbed by these two exercises. However, postural control subsequent to triceps surae fatigue was less impaired than that subsequent to quadriceps femoris fatigue (Miller and Bird, 1976; Bizid et al., 2009b). The main aim of the present study was to compare the effects of the fatigue of the quadriceps femoris after VCs and after ES superimposed onto VCs on postural control and muscle strength (since this constitutes a fundamental criterion of fatigue state). Another aim was to compare the duration of the recovery of postural control and quadriceps femoris muscle fatigue after these two fatiguing exercises. Therefore, both postural control and quadriceps femoris muscle strength were evaluated before (PRE condition) and after the completion of fatiguing exercises (immediately: POST condition, after a 5 min recovery: POST 5 condition). We hypothesized that the magnitude of the impairment of postural control and muscle strength, and the duration of their recovery, differed after the fatiguing exercises.
EXPERIMENTAL PROCEDURES Fourteen healthy young adult males participated in the study (age: 23.3⫾2.7 years; height: 177.4⫾7.6 cm; body weight: 75.5⫾8.7 kg). Exclusion criteria included a medical condition that might affect postural control and a neurological or musculoskeletal impairment in the past 2 years. Participants signed a consent form as required by the Helsinki Declaration (1964) which was approved by the local Ethics Committee. The equipment and the techniques of measuring quadriceps femoris muscle torque and postural control were similar to those used in a previous study (Bizid et al., 2009a). One fatiguing exercise was performed by VCs of the quadriceps femoris (VC exercise), the other was performed with ES superimposed onto voluntary muscle contractions of the quadriceps femoris (VC⫹ES exercise). The isometric muscle strength and postural control were measured before (pre-fatigue, or PRE condition), and after the completion of the two muscle fatiguing exercises (immediately: post-fatigue, or POST condition; and after a 5 min recovery: POST 5 condition). The completion of each exercise (VC and VC⫹ES) was separated by 10 –12 days for all the subjects. The order of completion of each exercise was randomized; seven subjects began with the VC exercise and the other seven with the VC⫹ES exercise.
Postural control A stable force platform (PostureWin©, Techno Concept, Cereste, France; sampling frequency: 40 Hz; 12 bits A/D conversion) was used to calculate the center of foot pressure (COP) positions. Subjects were required to stand on one leg. The supporting leg was the non-dominant leg, i.e. the one not used when kicking a ball. The foot was placed according to precise landmarks with respect to the platform X and Y axes. The other foot was lifted so
that the subject’s big toe touched the medial malleolus of the supporting leg. The arms were placed across the chest. The subjects were asked to stand on the platform barefooted, as immobile as possible, looking straight ahead with eyes closed. The eyes-closed condition was chosen to prevent vision from contributing to the regulation of postural behavior. Each test lasted 25 s. COP signals were smoothed using a second-order Butterworth filter with a 6 Hz low-pass cut off frequency (Cherng et al., 2003; Eklund and Lofstedt, 1970). Mean COP velocity (mm.s⫺1) was defined as the sum of the displacement scalars (i.e. the cumulated distance over the sampling period) divided by the sampling time. COP velocity was calculated as the mean of the absolute values computed from the recorded position. In addition, COP sways were analyzed in the frequency domain to characterize the subjects’ postural strategy. A fast Fourier transform (FFT) analysis was applied to COP displacements. Hence, the total spectral energy, in Volt2 (V2), was calculated for two frequency bands: a low frequency (0 –2 Hz) and a high frequency (⬎2 Hz) band. Low frequencies account mostly for visuo–vestibular inputs and high frequencies for proprioceptive inputs (e.g., myotatic loop) (Nashner, 1977).
Voluntary contraction Measurement of maximal voluntary contraction (MVC). Before starting the fatiguing exercises, the subjects were required to perform a warm-up period of 15 min on an ergocycler at low intensity (50 and 100 W) to avoid any subsequent muscular or articular trauma during the test of maximal voluntary contraction. The MVC of the knee isometric extension of the supporting leg was measured using an isokinetic dynamometer (BiodexTM, System 3 Pro, Shirley, NY, USA). Subjects were required to sit with a 90° hip flexion and a 90° knee flexion. Stabilization straps were positioned across the subject’s chest and pelvis. The arms were crossed on the chest. Subjects performed three MVCs that lasted 5 s. Thirty seconds separated each contraction. The best performance (peak torque in Nm) was retained. After a 2 min rest period, the subjects began the fatigue protocol. Fatiguing voluntary contraction exercise. The peak torque served as a reference to determine the workload applied during the fatiguing exercise. The fatiguing exercise included five sets of 50 repetitions with a resting period of 10 s between each set (Bizid et al., 2009a). The workload was 50% of the peak torque for the first set, 40% for the second and the third sets, and 30% for the fourth and the fifth sets. For all sets, each isometric knee extension lasted 5 s. Two seconds separated each contraction. The same workload was required for both fatiguing exercises. Visual feedback of the generated force was provided, so the subjects could control each contraction. During the fifth set, the subjects were asked to perform the last three repetitions (48th, 49th, and 50th) to the maximum of their ability in order to calculate their isometric maximal strength at the end of the fatiguing exercise (the best performance was retained). At the end of each fatiguing exercise, the subjects were removed from the dynamometer and began postural control post-testing as quickly as possible.
ES superimposed onto voluntary contraction During the completion of the VC⫹ES exercise, subjects were electrically stimulated by a portable stimulator (Cefar™ Rehab 4 Pro®, Sweden). The protocol for neuromuscular ES was identical to that of voluntary contractions in terms of duration (i.e. 5 s tetanic stimulations followed by pauses of 2 s). Three circular self-adhesive conducting electrodes (Stimrode, diameter 50 mm, Sweden) were placed over the motor point of the vastus medialis, rectus femoris, and vastus lateralis muscles. The quadriceps femoris was stimulated using a biphasic symmetrical rectangular wave (continuous pulse 450 s, 20 mA, frequency 80 Hz).
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Data analysis Results for PRE, POST and POST 5 conditions were expressed as mean⫾standard deviation (SD). Comparisons of muscular (maximal isometric strength) and postural (COP velocity and spectral energy for high and low frequency bands) parameters were performed using a repeated-measures analysis of variance (ANOVA) with two withinsubjects factors: condition (three levels: PRE, POST, and POST 5) and exercise (two levels: VC and VC⫹ES). Newman–Keuls post hoc was used to test differences among means. The F value corresponds to Fisher’s F and the level of significance chosen was P⬍0.05.
RESULTS The MVC revealed a main effect of condition (F⫽12.24; P⬍0.01) and a significant condition⫻exercise interaction (F⫽4.22; P⬍0.05), indicating that quadriceps femoris muscle strength differed for the VC exercise and the VC⫹ES exercise. Immediately after the fatiguing exercises (POST condition), the MVC was significantly decreased for both fatiguing exercises (P⬍0.001). However, the MVC decreased more for the VC exercise than for the VC⫹ES exercise (P⬍0.05). In addition, the MVC was significantly greater in the POST 5 than in the POST condition for both fatiguing exercises (P⬍0.001), showing a progressive recovery of muscular strength. However, after a 5 min recovery (POST 5 condition), the MVC remained significantly lower than in the PRE condition for both VC (P⬍0.05) and VC⫹ES (P⬍0.05) exercises (Fig. 1). The mean COP velocity presented a main effect of condition (F⫽6.08; P⬍0.02) and a significant condition⫻ exercise interaction (F⫽4.86; P⬍0.05), revealing that postural control also differed for the VC exercise and the VC⫹ES exercise. The mean COP velocity was significantly greater in the POST than in the PRE condition for both fatiguing exercises (P⬍0.01). Note that the increase in COP velocity was higher for the VC exercise than for the VC⫹ES exercise (P⬍0.05). In the POST 5 condition, COP velocity regained values similar to those recorded in the PRE condition for both fatiguing exercises (Fig. 2).
Fig. 1. Maximal voluntary contraction after a VC exercise (isometric contractions of quadriceps femoris) and a VC⫹ES exercise (electrical stimulation superimposed on voluntary muscle contractions of quadriceps femoris) in three conditions (PRE, pre-fatigue condition; POST, immediate post-fatigue condition; POST 5, 5 min of recovery postfatigue condition). Vertical bars represent the SD. Horizontal bars represent the comparisons between the different conditions. * indicates a significant condition effect (P⬍0.05); *** indicates a significant condition effect (P⬍0.001).
Fig. 2. Center of foot pressure (COP) velocity for the two exercises (VC, isometric voluntary contractions of quadriceps femoris; VC⫹ES, electrical stimulation superimposed on isometric voluntary contractions of quadriceps femoris) in three conditions (PRE, pre-fatigue condition; POST, immediate post-fatigue condition; POST 5, 5 min of recovery post-fatigue condition). * indicates a significant condition effect (P⬍0.05). ** indicates a significant condition effect (P⬍0.01).
Similar data were observed in the FFT analysis for the high frequency band, since the ANOVA indicated a main effect of condition (F⫽9.6; P⬍0.004) and a condition⫻ exercise interaction (F⫽4.19; P⬍0.05). The spectral energy increased for both fatiguing exercises between the PRE and POST conditions (P⬍0.001). However, the spectral energy increased more for the VC exercise than for the VC⫹ES exercise (P⬍0.05). In the POST 5 condition, the spectral energy did not differ from the PRE condition for both fatiguing exercises. Finally, in the low frequency band, the effect of the fatiguing exercises did not differ significantly, whatever the condition (Fig. 3).
Fig. 3. Low and high frequency bands for both exercises (VC and VC⫹ES) in three conditions (PRE, pre-fatigue condition; POST, immediate post-fatigue condition; POST 5, 5 min of recovery post-fatigue condition). * indicates a significant condition effect (P⬍0.05). *** indicates a significant condition effect (P⬍0.001).
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DISCUSSION The aim of this work was to compare the neuromuscular and postural adaptations induced by two types of fatiguing exercises on quadriceps femoris muscle. Muscular fatigue was induced either with VCs (VC exercise) or ES superimposed onto VCs (VC⫹ES exercise). With both exercises, quadriceps femoris muscle fatigue impaired the isometric maximal strength immediately after the fatiguing exercise (POST condition) and also after 5 min of recovery (POST 5 condition). The impairment was greater with the VC exercise than with the VC⫹ES. Moreover, with both exercises, postural control deteriorated immediately after the fatiguing exercises (POST condition) but recovered its initial value after a 5 min recovery (POST 5 condition). In addition, in the POST condition, the VC exercise affected postural control more than the VC⫹ES exercise. Interestingly, the immediate muscle fatigue differed between the exercises. The strength loss induced by the VC⫹ES exercise (40% of MVC) was less than that induced by the VC exercise (53% of MVC) between the PRE and POST conditions. These results are surprising, since acute application of neuromuscular ES is known to induce greater metabolic changes than voluntary contraction for a given level of strength during submaximal muscular contractions (Vanderthommen et al., 2003). Neuromuscular ES also induces greater muscle fatigue than maximal voluntary contraction (Hamada et al., 2004). In that study, the authors progressively adjusted the stimulation intensity, whereas in our study, ES intensity was constant. Moreover, ES activates some motor units directly beneath the stimulation electrodes (MacComas et al., 1971). Large motor units are localized on the quadriceps surface (Lexell et al., 1983). It has been shown that once the muscle fibers localized under the electrodes reach a critical threshold of fatigue, an increase of the ES intensity recruits additional muscle fibers situated further from the electrodes (Hamada et al., 2004). In this work, the intensity was relatively weak (20 mA) and constant, so such progressive recruitment of motor units was not possible. In this context, the muscle fatigue produced by ES during the VC⫹ES exercise was not widespread in the quadriceps muscle. With voluntary muscular action, the order of motor unit recruitment goes from small motor units to large ones, in relation to the intensity of the stimulation (Henneman et al., 1965). Although neuromuscular ES can decrease the quantity of the neural drive to muscle from supraspinal centers (Boerio et al., 2005), for a given submaximal intensity during a long exercise, one can hypothesize that the involuntary activation of large motor units partially limited the effect of central fatigue generated by the fatiguing exercise. Indeed, according to Huffenus and Forestier (2006), voluntary contractions induce greater changes in muscle activation than electrically induced contractions. Hence, the contribution of ES superimposed onto voluntary contraction would limit the changes in muscle activation and then the central fatigue during a fatiguing exercise performed with submaximal contractions. This could explain why the MVC decreased less after the VC⫹ES exercise than after the VC exercise.
Moreover, the muscle group considered may influence the results. Indeed, following the article by Bizid et al. (2009a), we propose that ES induces depolarization of a greater percentage of muscle fibers (proportionally) in triceps surae than in quadriceps femoris. In the case of ES superimposed onto voluntary contraction, for a given level of current intensity, the fatigue (strength loss) is proportionally less pronounced in quadriceps femoris than in triceps surae. After the 5 min recovery, the subjects did not completely recover their initial values of muscle strength for either exercise. This could be due to the relatively long duration of both fatiguing exercises. Previous data have indicated that after long-lasting weak efforts, MVC can still be depressed after 30 to 60 min (Taylor and Gandevia, 2008). These authors proposed that this phenomenon is due to a continued supraspinal influence of small-diameter muscle afferents. They pointed out that an immediate decrease in blood pressure occurs, suggesting that the firing of small-diameter afferents drops quickly during prolonged contractions. This drop may be accompanied by reflex depression and increased motoneuron excitability as long as 15 min to 1 h after 10 –15 min activation, which affects motor activity (Taylor and Gandevia, 2008). Hence, our results corroborate the results of previous studies relative to the slow recovery of strength after longlasting weak contractions. Postural control is differently affected immediately after the two exercises. The COP velocity increased more for the VC exercise than for the VC⫹ES exercise, while muscle strength decreased more. These data indicate that the exercise that impaired muscle strength the most also disturbed postural control the most. Pline et al. (2006) reported that a reduction of 40% of MVC increases the mean COP velocity after a voluntary exercise, whereas a reduction of 27% of MVC does not increase it. Here, the VC exercise, which degraded MVC by 53%, could have affected postural control more than the VC⫹ES exercise, which affected MVC by 40%. As we hypothesized above, the VC⫹ES exercise, compared to the VC exercise, may limit the effect of central fatigue and, subsequently, modify postural control. In addition, spectral analysis of the COP displacement indicated that spectral energy in the high frequency band increased more after the VC exercise than after the VC⫹ES exercise. This suggests that the contribution of proprioceptive information was greater after the VC exercise than after the VC⫹ES exercise. The article by Bizid et al. (2009a) corroborates this result, with an identical protocol on the triceps surae. Those authors, however, did not observe any differences in postural control between the two fatiguing exercises. This may be because triceps surae fatigue disturbs postural control less than quadriceps femoris fatigue (Bizid et al., 2009b). After 5 min of recovery, the subjects recovered their initial abilities to control posture faster than their initial abilities to generate muscular strength. In other words, neuromuscular control is restored before muscle contractility. This may be because muscle fatigue generates compensatory mechanisms (e.g. increased reflex activity in muscle spindles or increased muscle stiffness) to maintain standing balance (Adlerton and Moritz, 1996). This expla-
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nation is supported by the increase in spectral energy in the high frequency band for both exercises.
CONCLUSION In summary, the findings indicate that superimposing ES onto VCs impaired muscle strength and postural control less than VCs did. The duration of the recovery of postural control and quadriceps femoris muscle fatigue did not differ between these two fatiguing exercises. In addition, the ability to control posture was restored faster than the ability to produce muscular strength. In practice, our data suggest that besides its beneficial effects in therapeutic contexts, ES superimposed onto voluntary contraction may limit the deterioration of muscular fatigue and postural control. Acknowledgments—We would like to thank the anonymous reviewers for their valuable comments and suggestions.
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(Accepted 20 November 2009) (Available online 1 December 2009)
ELECTRICAL STIMULATION SUPERIMPOSED ONTO VOLUNTARY MUSCULAR CONTRACTION REDUCES DETERIORATION OF BOTH POSTURAL CONTROL AND QUADRICEPS FEMORIS MUSCLE STRENGTH T. PAILLARD,a* E. MARGNES,a J. MAITRE,a V. CHAUBET,a Y. FRANÇOIS,b J. L. JULLY,b G. GONZALEZb AND L. BORELc
tion of the action potential along the muscle membrane, events associated with cross-bridge interaction, and calcium uptake by the sarcoplasmic reticulum (Lee et al., 2000). Central fatigue results from the inability of motoneurons to maintain their firing rates to sustain maximal voluntary contraction; this inability is due to factors acting at spinal and supraspinal sites (Gandevia, 2001). To reduce muscle force and thus generate a fatigue state, sustained submaximal voluntary muscular contractions (VCs) are especially efficient (Yoon et al., 2007). When fatiguing voluntary contractions specifically concern postural tonic muscles (e.g. ankle plantar-flexors and dorsiflexors, ankle invectors and evectors, knee extensors, lumbar erector spinae, or neck muscles), they can induce postural control disturbance (Gribble and Hertel, 2004; Yaggie and McGregor, 2002; Vuillerme et al., 2002; Corbeil et al., 2003; Ledin et al., 2004; Caron, 2003; Johnston et al., 1998; Harkins et al., 2005; Madigan et al., 2006; Gosselin et al., 2004). Thus, localized muscle fatigue produced by the repetition of VCs may alter postural control. Moreover, postural control disturbances differ according to the muscle group. For example, fatigue of knee or hip musculature alters postural control more than fatigue of ankle musculature does (Miller and Bird, 1976; Gribble and Hertel, 2004; Bizid et al., 2009b). It takes longer to recover postural control as muscle strength reduces after fatiguing exercises (Harkins et al., 2005). The physiological impact of neuromuscular electrical stimulation (ES) differs from that of voluntary contraction (Paillard, 2008). Relative to voluntary contraction, neuromuscular ES enhances fatigued muscle soreness and damage (Moreau et al., 1995). Neuromuscular ES acidifies the cytoplasm more than voluntary contraction does (Vanderthommen et al., 2003). This acidity alters proprioceptive sensitivity (Loscher et al., 1996; Rossi et al., 1999; Avela et al., 2001; Zytnicki et al., 1990), a major determinant in postural control mechanisms (Massion, 1994). The question thus arises as to whether the effects of fatigue provoked by neuromuscular ES on postural control differ from those induced by voluntary contraction. The force produced by neuromuscular ES is lower than that generated by voluntary muscular contraction (VC) (Bax et al., 2005). Yet, to compare the effects of muscular fatigue on postural control, the force produced by these two modalities must be equivalent (Vanderthommen et al., 2003; Hamada et al., 2004). To reach an equivalent force production, ES has to be superimposed onto VC (Paillard
a Université de Pau et des Pays de l’Adour, Département STAPS, ZA Bastillac Sud, 65000 Tarbes, France b Centre Medical de la Mutuelle Générale de l’Education Nationale, Domaine L’Arbizon, 65200 Bagnères de Bigorre, France c Laboratoire de Neurosciences Intégratives et Adaptatives UMR 6149, Université de Provence/CNRS, Centre St. Charles, Pôle 3C–Case B, 3, Place Victor Hugo, 13331 Marseille Cedex 03, France
Abstract—Fatiguing exercise of the quadriceps femoris muscle degrades postural control in human subjects. The aim of this work was to compare the effects of the fatigue of the quadriceps femoris induced by voluntary muscular contraction (VC), and by electrical stimulation (ES) superimposed onto voluntary muscular contraction (VCⴙES), on postural control and muscle strength. Fourteen healthy young adults participated in the study. Postural control and muscle strength were evaluated using a stable force platform and an isokinetic dynamometer, respectively, before (PRE condition) and after the completion of each fatiguing exercise (immediately: POST condition; after a 5 min recovery time: POST 5 condition). In POST, both postural control and muscle strength were impaired by both fatiguing exercises. However, the impairment was higher for VC than for VCⴙES. In POST 5, for both fatiguing exercises, postural control recovered its initial level while muscle strength did not. These results suggest that superimposing ES onto voluntary muscular contractions (VCs) impaired muscle strength and postural control less than did VCs alone. However the duration of recovery of these two neurophysiological functions did not differ for the two fatiguing exercises. For both exercises, postural control was restored faster than the ability to produce muscular strength. © 2010 IBRO. Published by Elsevier Ltd. All rights reserved. Key words: muscle fatigue, neuromuscular electrical stimulation, unipedal stance, recovery.
Fatigue can be defined as a progressive increase in the effort required to produce the same level of force, followed by a progressive inability to continuously or repeatedly maintain this force (Enoka and Stuart, 1992). The fatigue originates from peripheral and/or central features. Peripheral fatigue involves the neuromuscular junction, propaga*Corresponding author. Tel: ⫹33(0)562-566-100; fax: ⫹33(0)562-566-110. E-mail address: [email protected] (T. Paillard). Abbreviations: COP, center of foot pressure; ES, electrical stimulation; MVC, measurement of maximal voluntary contraction; VC, voluntary muscular contraction; VCs, voluntary muscular contractions.
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et al., 2005). ES superimposed onto voluntary contraction has been widely employed in therapeutic contexts and has proved highly efficient. In healthy subjects, however, we do not know the effects of ES superimposed onto voluntary contraction on muscular fatigue and postural control immediately after its application and whether these effects differ from those obtained after voluntary contraction. Only Bizid et al. (2009a) have explored the differential effects on postural control of fatigue as provoked by either VC or ES superimposed onto VC. They showed that the triceps surae was equally disturbed by these two exercises. However, postural control subsequent to triceps surae fatigue was less impaired than that subsequent to quadriceps femoris fatigue (Miller and Bird, 1976; Bizid et al., 2009b). The main aim of the present study was to compare the effects of the fatigue of the quadriceps femoris after VCs and after ES superimposed onto VCs on postural control and muscle strength (since this constitutes a fundamental criterion of fatigue state). Another aim was to compare the duration of the recovery of postural control and quadriceps femoris muscle fatigue after these two fatiguing exercises. Therefore, both postural control and quadriceps femoris muscle strength were evaluated before (PRE condition) and after the completion of fatiguing exercises (immediately: POST condition, after a 5 min recovery: POST 5 condition). We hypothesized that the magnitude of the impairment of postural control and muscle strength, and the duration of their recovery, differed after the fatiguing exercises.
EXPERIMENTAL PROCEDURES Fourteen healthy young adult males participated in the study (age: 23.3⫾2.7 years; height: 177.4⫾7.6 cm; body weight: 75.5⫾8.7 kg). Exclusion criteria included a medical condition that might affect postural control and a neurological or musculoskeletal impairment in the past 2 years. Participants signed a consent form as required by the Helsinki Declaration (1964) which was approved by the local Ethics Committee. The equipment and the techniques of measuring quadriceps femoris muscle torque and postural control were similar to those used in a previous study (Bizid et al., 2009a). One fatiguing exercise was performed by VCs of the quadriceps femoris (VC exercise), the other was performed with ES superimposed onto voluntary muscle contractions of the quadriceps femoris (VC⫹ES exercise). The isometric muscle strength and postural control were measured before (pre-fatigue, or PRE condition), and after the completion of the two muscle fatiguing exercises (immediately: post-fatigue, or POST condition; and after a 5 min recovery: POST 5 condition). The completion of each exercise (VC and VC⫹ES) was separated by 10 –12 days for all the subjects. The order of completion of each exercise was randomized; seven subjects began with the VC exercise and the other seven with the VC⫹ES exercise.
Postural control A stable force platform (PostureWin©, Techno Concept, Cereste, France; sampling frequency: 40 Hz; 12 bits A/D conversion) was used to calculate the center of foot pressure (COP) positions. Subjects were required to stand on one leg. The supporting leg was the non-dominant leg, i.e. the one not used when kicking a ball. The foot was placed according to precise landmarks with respect to the platform X and Y axes. The other foot was lifted so
that the subject’s big toe touched the medial malleolus of the supporting leg. The arms were placed across the chest. The subjects were asked to stand on the platform barefooted, as immobile as possible, looking straight ahead with eyes closed. The eyes-closed condition was chosen to prevent vision from contributing to the regulation of postural behavior. Each test lasted 25 s. COP signals were smoothed using a second-order Butterworth filter with a 6 Hz low-pass cut off frequency (Cherng et al., 2003; Eklund and Lofstedt, 1970). Mean COP velocity (mm.s⫺1) was defined as the sum of the displacement scalars (i.e. the cumulated distance over the sampling period) divided by the sampling time. COP velocity was calculated as the mean of the absolute values computed from the recorded position. In addition, COP sways were analyzed in the frequency domain to characterize the subjects’ postural strategy. A fast Fourier transform (FFT) analysis was applied to COP displacements. Hence, the total spectral energy, in Volt2 (V2), was calculated for two frequency bands: a low frequency (0 –2 Hz) and a high frequency (⬎2 Hz) band. Low frequencies account mostly for visuo–vestibular inputs and high frequencies for proprioceptive inputs (e.g., myotatic loop) (Nashner, 1977).
Voluntary contraction Measurement of maximal voluntary contraction (MVC). Before starting the fatiguing exercises, the subjects were required to perform a warm-up period of 15 min on an ergocycler at low intensity (50 and 100 W) to avoid any subsequent muscular or articular trauma during the test of maximal voluntary contraction. The MVC of the knee isometric extension of the supporting leg was measured using an isokinetic dynamometer (BiodexTM, System 3 Pro, Shirley, NY, USA). Subjects were required to sit with a 90° hip flexion and a 90° knee flexion. Stabilization straps were positioned across the subject’s chest and pelvis. The arms were crossed on the chest. Subjects performed three MVCs that lasted 5 s. Thirty seconds separated each contraction. The best performance (peak torque in Nm) was retained. After a 2 min rest period, the subjects began the fatigue protocol. Fatiguing voluntary contraction exercise. The peak torque served as a reference to determine the workload applied during the fatiguing exercise. The fatiguing exercise included five sets of 50 repetitions with a resting period of 10 s between each set (Bizid et al., 2009a). The workload was 50% of the peak torque for the first set, 40% for the second and the third sets, and 30% for the fourth and the fifth sets. For all sets, each isometric knee extension lasted 5 s. Two seconds separated each contraction. The same workload was required for both fatiguing exercises. Visual feedback of the generated force was provided, so the subjects could control each contraction. During the fifth set, the subjects were asked to perform the last three repetitions (48th, 49th, and 50th) to the maximum of their ability in order to calculate their isometric maximal strength at the end of the fatiguing exercise (the best performance was retained). At the end of each fatiguing exercise, the subjects were removed from the dynamometer and began postural control post-testing as quickly as possible.
ES superimposed onto voluntary contraction During the completion of the VC⫹ES exercise, subjects were electrically stimulated by a portable stimulator (Cefar™ Rehab 4 Pro®, Sweden). The protocol for neuromuscular ES was identical to that of voluntary contractions in terms of duration (i.e. 5 s tetanic stimulations followed by pauses of 2 s). Three circular self-adhesive conducting electrodes (Stimrode, diameter 50 mm, Sweden) were placed over the motor point of the vastus medialis, rectus femoris, and vastus lateralis muscles. The quadriceps femoris was stimulated using a biphasic symmetrical rectangular wave (continuous pulse 450 s, 20 mA, frequency 80 Hz).
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Data analysis Results for PRE, POST and POST 5 conditions were expressed as mean⫾standard deviation (SD). Comparisons of muscular (maximal isometric strength) and postural (COP velocity and spectral energy for high and low frequency bands) parameters were performed using a repeated-measures analysis of variance (ANOVA) with two withinsubjects factors: condition (three levels: PRE, POST, and POST 5) and exercise (two levels: VC and VC⫹ES). Newman–Keuls post hoc was used to test differences among means. The F value corresponds to Fisher’s F and the level of significance chosen was P⬍0.05.
RESULTS The MVC revealed a main effect of condition (F⫽12.24; P⬍0.01) and a significant condition⫻exercise interaction (F⫽4.22; P⬍0.05), indicating that quadriceps femoris muscle strength differed for the VC exercise and the VC⫹ES exercise. Immediately after the fatiguing exercises (POST condition), the MVC was significantly decreased for both fatiguing exercises (P⬍0.001). However, the MVC decreased more for the VC exercise than for the VC⫹ES exercise (P⬍0.05). In addition, the MVC was significantly greater in the POST 5 than in the POST condition for both fatiguing exercises (P⬍0.001), showing a progressive recovery of muscular strength. However, after a 5 min recovery (POST 5 condition), the MVC remained significantly lower than in the PRE condition for both VC (P⬍0.05) and VC⫹ES (P⬍0.05) exercises (Fig. 1). The mean COP velocity presented a main effect of condition (F⫽6.08; P⬍0.02) and a significant condition⫻ exercise interaction (F⫽4.86; P⬍0.05), revealing that postural control also differed for the VC exercise and the VC⫹ES exercise. The mean COP velocity was significantly greater in the POST than in the PRE condition for both fatiguing exercises (P⬍0.01). Note that the increase in COP velocity was higher for the VC exercise than for the VC⫹ES exercise (P⬍0.05). In the POST 5 condition, COP velocity regained values similar to those recorded in the PRE condition for both fatiguing exercises (Fig. 2).
Fig. 1. Maximal voluntary contraction after a VC exercise (isometric contractions of quadriceps femoris) and a VC⫹ES exercise (electrical stimulation superimposed on voluntary muscle contractions of quadriceps femoris) in three conditions (PRE, pre-fatigue condition; POST, immediate post-fatigue condition; POST 5, 5 min of recovery postfatigue condition). Vertical bars represent the SD. Horizontal bars represent the comparisons between the different conditions. * indicates a significant condition effect (P⬍0.05); *** indicates a significant condition effect (P⬍0.001).
Fig. 2. Center of foot pressure (COP) velocity for the two exercises (VC, isometric voluntary contractions of quadriceps femoris; VC⫹ES, electrical stimulation superimposed on isometric voluntary contractions of quadriceps femoris) in three conditions (PRE, pre-fatigue condition; POST, immediate post-fatigue condition; POST 5, 5 min of recovery post-fatigue condition). * indicates a significant condition effect (P⬍0.05). ** indicates a significant condition effect (P⬍0.01).
Similar data were observed in the FFT analysis for the high frequency band, since the ANOVA indicated a main effect of condition (F⫽9.6; P⬍0.004) and a condition⫻ exercise interaction (F⫽4.19; P⬍0.05). The spectral energy increased for both fatiguing exercises between the PRE and POST conditions (P⬍0.001). However, the spectral energy increased more for the VC exercise than for the VC⫹ES exercise (P⬍0.05). In the POST 5 condition, the spectral energy did not differ from the PRE condition for both fatiguing exercises. Finally, in the low frequency band, the effect of the fatiguing exercises did not differ significantly, whatever the condition (Fig. 3).
Fig. 3. Low and high frequency bands for both exercises (VC and VC⫹ES) in three conditions (PRE, pre-fatigue condition; POST, immediate post-fatigue condition; POST 5, 5 min of recovery post-fatigue condition). * indicates a significant condition effect (P⬍0.05). *** indicates a significant condition effect (P⬍0.001).
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DISCUSSION The aim of this work was to compare the neuromuscular and postural adaptations induced by two types of fatiguing exercises on quadriceps femoris muscle. Muscular fatigue was induced either with VCs (VC exercise) or ES superimposed onto VCs (VC⫹ES exercise). With both exercises, quadriceps femoris muscle fatigue impaired the isometric maximal strength immediately after the fatiguing exercise (POST condition) and also after 5 min of recovery (POST 5 condition). The impairment was greater with the VC exercise than with the VC⫹ES. Moreover, with both exercises, postural control deteriorated immediately after the fatiguing exercises (POST condition) but recovered its initial value after a 5 min recovery (POST 5 condition). In addition, in the POST condition, the VC exercise affected postural control more than the VC⫹ES exercise. Interestingly, the immediate muscle fatigue differed between the exercises. The strength loss induced by the VC⫹ES exercise (40% of MVC) was less than that induced by the VC exercise (53% of MVC) between the PRE and POST conditions. These results are surprising, since acute application of neuromuscular ES is known to induce greater metabolic changes than voluntary contraction for a given level of strength during submaximal muscular contractions (Vanderthommen et al., 2003). Neuromuscular ES also induces greater muscle fatigue than maximal voluntary contraction (Hamada et al., 2004). In that study, the authors progressively adjusted the stimulation intensity, whereas in our study, ES intensity was constant. Moreover, ES activates some motor units directly beneath the stimulation electrodes (MacComas et al., 1971). Large motor units are localized on the quadriceps surface (Lexell et al., 1983). It has been shown that once the muscle fibers localized under the electrodes reach a critical threshold of fatigue, an increase of the ES intensity recruits additional muscle fibers situated further from the electrodes (Hamada et al., 2004). In this work, the intensity was relatively weak (20 mA) and constant, so such progressive recruitment of motor units was not possible. In this context, the muscle fatigue produced by ES during the VC⫹ES exercise was not widespread in the quadriceps muscle. With voluntary muscular action, the order of motor unit recruitment goes from small motor units to large ones, in relation to the intensity of the stimulation (Henneman et al., 1965). Although neuromuscular ES can decrease the quantity of the neural drive to muscle from supraspinal centers (Boerio et al., 2005), for a given submaximal intensity during a long exercise, one can hypothesize that the involuntary activation of large motor units partially limited the effect of central fatigue generated by the fatiguing exercise. Indeed, according to Huffenus and Forestier (2006), voluntary contractions induce greater changes in muscle activation than electrically induced contractions. Hence, the contribution of ES superimposed onto voluntary contraction would limit the changes in muscle activation and then the central fatigue during a fatiguing exercise performed with submaximal contractions. This could explain why the MVC decreased less after the VC⫹ES exercise than after the VC exercise.
Moreover, the muscle group considered may influence the results. Indeed, following the article by Bizid et al. (2009a), we propose that ES induces depolarization of a greater percentage of muscle fibers (proportionally) in triceps surae than in quadriceps femoris. In the case of ES superimposed onto voluntary contraction, for a given level of current intensity, the fatigue (strength loss) is proportionally less pronounced in quadriceps femoris than in triceps surae. After the 5 min recovery, the subjects did not completely recover their initial values of muscle strength for either exercise. This could be due to the relatively long duration of both fatiguing exercises. Previous data have indicated that after long-lasting weak efforts, MVC can still be depressed after 30 to 60 min (Taylor and Gandevia, 2008). These authors proposed that this phenomenon is due to a continued supraspinal influence of small-diameter muscle afferents. They pointed out that an immediate decrease in blood pressure occurs, suggesting that the firing of small-diameter afferents drops quickly during prolonged contractions. This drop may be accompanied by reflex depression and increased motoneuron excitability as long as 15 min to 1 h after 10 –15 min activation, which affects motor activity (Taylor and Gandevia, 2008). Hence, our results corroborate the results of previous studies relative to the slow recovery of strength after longlasting weak contractions. Postural control is differently affected immediately after the two exercises. The COP velocity increased more for the VC exercise than for the VC⫹ES exercise, while muscle strength decreased more. These data indicate that the exercise that impaired muscle strength the most also disturbed postural control the most. Pline et al. (2006) reported that a reduction of 40% of MVC increases the mean COP velocity after a voluntary exercise, whereas a reduction of 27% of MVC does not increase it. Here, the VC exercise, which degraded MVC by 53%, could have affected postural control more than the VC⫹ES exercise, which affected MVC by 40%. As we hypothesized above, the VC⫹ES exercise, compared to the VC exercise, may limit the effect of central fatigue and, subsequently, modify postural control. In addition, spectral analysis of the COP displacement indicated that spectral energy in the high frequency band increased more after the VC exercise than after the VC⫹ES exercise. This suggests that the contribution of proprioceptive information was greater after the VC exercise than after the VC⫹ES exercise. The article by Bizid et al. (2009a) corroborates this result, with an identical protocol on the triceps surae. Those authors, however, did not observe any differences in postural control between the two fatiguing exercises. This may be because triceps surae fatigue disturbs postural control less than quadriceps femoris fatigue (Bizid et al., 2009b). After 5 min of recovery, the subjects recovered their initial abilities to control posture faster than their initial abilities to generate muscular strength. In other words, neuromuscular control is restored before muscle contractility. This may be because muscle fatigue generates compensatory mechanisms (e.g. increased reflex activity in muscle spindles or increased muscle stiffness) to maintain standing balance (Adlerton and Moritz, 1996). This expla-
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nation is supported by the increase in spectral energy in the high frequency band for both exercises.
CONCLUSION In summary, the findings indicate that superimposing ES onto VCs impaired muscle strength and postural control less than VCs did. The duration of the recovery of postural control and quadriceps femoris muscle fatigue did not differ between these two fatiguing exercises. In addition, the ability to control posture was restored faster than the ability to produce muscular strength. In practice, our data suggest that besides its beneficial effects in therapeutic contexts, ES superimposed onto voluntary contraction may limit the deterioration of muscular fatigue and postural control. Acknowledgments—We would like to thank the anonymous reviewers for their valuable comments and suggestions.
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(Accepted 20 November 2009) (Available online 1 December 2009)