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Stimulated and voluntary fatiguing contractions of quadriceps femoris differently disturb postural control
Neuroscience Letters 477 (2010) 48–51
Contents lists available at ScienceDirect
Neuroscience Letters journal homepage: www.elsevier.com/locate/neulet
Stimulated and voluntary fatiguing contractions of quadriceps femoris differently disturb postural control Thierry Paillard a,∗ , Julien Maitre a , Vincent Chaubet a , Liliane Borel b a
Laboratoire d’Analyse de la Performance Sportive, Université de Pau et des Pays de l’Adour, Département STAPS, ZA Bastillac Sud, 65000 Tarbes, France 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
b
a r t i c l e
i n f o
Article history: Received 29 November 2009 Received in revised form 31 March 2010 Accepted 16 April 2010 Keywords: Muscle fatigue Neuromuscular electrical stimulation Voluntary contraction Unipedal stance
a b s t r a c t Muscle fatigue affects muscle strength and postural control. However, it is not known whether impaired postural control after fatiguing muscular exercise depends on the nature of the muscle contraction. To answer this question, the present study analyzes changes in postural control after two fatiguing exercises of equal duration and intensity but that induced different magnitudes of strength loss. The effects of fatiguing contractions of the femoris quadriceps were compared for voluntary muscular contraction (VOL) and neuromuscular electrical stimulation (ES) on muscle strength and postural control. Seventeen subjects completed these two fatiguing exercises. Maximal voluntary contraction (MVC) and postural control were recorded using an isokinetic dynamometer and a force platform that recorded the center of foot pressure. Recordings were performed before and after the completion of both fatiguing tasks. Results indicate that, after a fatiguing exercise, the ES exercise affected MVC more than the VOL exercise. Inversely, postural control was disturbed more after VOL exercise than after ES exercise. In conclusion, postural control disturbance is influenced by the nature of the muscular contraction (voluntary vs. nonvoluntary) and the type of the motor unit solicited (tonic vs. phasic) rather than by the magnitude of strength loss. © 2010 Elsevier Ireland Ltd. All rights reserved.
Maintenance of posture requires the integration and use of information from sensory and motor systems. When the information is manipulated or impaired, postural control is affected. Manipulation of different sensory receptors (e.g. cutaneous, myo-tendinous, skin thermics, vestibular or visual receptors) affects information integration and deteriorates postural control [17,21,26]. Impaired postural control can originate from the disturbance of the motor pathway by excessive repetitions of submaximal muscular contractions [5,29]. This disturbance emanates from metabolic and/or neurologic changes that induce localized muscle fatigue [23]. Muscle fatigue can be defined as any exercise-induced decrease in maximal voluntary force produced by a muscle or muscle group [2]. The muscle strength decrease constitutes a relevant criterion to determine the fatigue state and can be linked either to central or to peripheral levels. Central fatigue arises proximal to the motor axons and leads to decreases in motor unit activation while peripheral fatigue is localized within the muscle itself, the neuromuscular junction, or the terminal branches of the motor axons. Postural control is especially affected by strength loss in postural tonic muscles such as ankle plantarflexors and dorsiflexors,
∗ Corresponding author. Tel.: +33 5 62566100; fax: +33 5 62566110. E-mail address: [email protected] (T. Paillard). 0304-3940/$ – see front matter © 2010 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.neulet.2010.04.034
ankle invertors and evertors, knee extensors, hip flexor-extensors, hip abductor-adductors, lumbar erector spinae, or neck muscles [5,7,8,10,14,29]. Considering voluntary contractions, for a given muscle group and for a given intensity of submaximal muscular contractions, the duration of fatiguing exercise influences the deterioration of postural control [20]. In addition, those authors showed that, immediately after fatiguing exercise, the magnitude of strength loss influences the level of the disturbance of postural control. However, the influence of the magnitude of strength loss on the postural control disturbance remains to be established when the nature of the contraction differs. To this end, neuromuscular electrical stimulation is of interest since it induces different magnitudes of strength loss for an equal duration and intensity of muscular contractions [27]. Indeed, for an identical force production and contraction duration during fatiguing exercise, the strength loss induced by this technique is greater than that induced by voluntary contractions (e.g. [27]). In the present study, we compared the effects of voluntary muscular contraction with those of neuromuscular electrical stimulation on postural control. Because the neurophysiological (motor drive, motor unit recruitment) and metabolic (metabolic activation, muscle fatigue) effects differ for stimulated and voluntary fatiguing contractions [18], we hypothesized that the relationship between the magnitude of strength loss and the postural
T. Paillard et al. / Neuroscience Letters 477 (2010) 48–51
control disturbance depended on the nature of the fatiguing exercise. Seventeen healthy male subjects participated in the study (age: 22.5 ± 4.1 years; height: 174.3 ± 5.7 cm; body weight: 74.2 ± 16.4 kg). They had not previously been involved in postural tests. Exclusion criteria included a documented postural control disorder or a medical condition that might affect postural control, a neurological or a musculoskeletal impairment in the past 2 years, or current injury making the subjects unable to participate. Participants signed an informed consent form approved by the local Ethics Committee as required by the Helsinki declaration. The experiment consisted in examining the possible neuromuscular and postural modifications induced by two different fatiguing exercises. One fatiguing exercise was performed by voluntary muscular contractions of the quadriceps femoris (VOL exercise); the other was performed by neuromuscular electrical stimulation of the quadriceps femoris (ES exercise). The isometric muscle strength and postural control were measured before (pre-fatigue or PRE condition) and immediately after (post-fatigue or POST condition) the completion of the muscle-fatiguing exercises. The completion of each exercise (VOL and ES) was separated by a period of 10–12 days for all the subjects. The effects of each fatiguing exercise were assessed in a randomized order. For each exercise, the subjects successively performed a postural test (PRE condition), a warm-up for 15 min on a cycle ergometer, an isometric maximal voluntary contraction test, a fatigue protocol (VOL or ES), an isometric maximal voluntary contraction test, and a postural test (POST condition). A PostureWin force platform with three strain gauges (Techno Concept, Cereste, France) was used to sample the displacements of the center of foot pressure (COP) at 40 Hz. Postural control was analyzed before (pre-fatigue or PRE condition) and immediately after (post-fatigue or POST condition) the fatiguing exercise. The subjects were asked to stand for 25 s on the platform, barefooted and as immobile as possible on one leg, the supporting leg, i.e. the one not used for kicking a ball. The foot was placed according to precise landmarks with respect to the X- and Y-axes of the platform. The other foot was lifted so that the subject’s big toe touched the medial malleolus of the supporting leg. Subjects had their eyes closed to prevent vision from contributing to the regulation of postural behaviors. To characterize the postural control of the subjects, the mean COP velocity in both the X-axis (frontal plane) and the Yaxis (sagittal plane) were independently determined as the mean of the absolute values computed from the recorded position. A Fast Fourier’s Transform was run on the X and Y COP courses, and the areas of the frequency spectrum were distributed into 2 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 myotatic inputs [19]. An isokinetic dynamometer (BiodexTM , System 3 Pro, Shirley, USA) was used to exhaust the knee extensor muscles. The isometric maximal voluntary contraction (MVC) was recorded using the leg evaluated on the force platform and measured on the isokinetic dynamometer. The subjects were seated with a 90◦ hip flexion and a 90◦ knee flexion and performed isometric contractions with the knee extensors. Stabilization straps were positioned across the subjects’ chest and pelvis. The arms were crossed on the chest. The subjects performed three MVCs that lasted 5 s. Thirty seconds separated each contraction. The best performance (peak torque in N m) was retained. After a 2-min rest period, the subjects began the fatigue protocol. Voluntary muscular contraction (VOL). The peak torque served as a reference to determine the workload applied during the fatiguing exercise. This exercise comprised 5 sets of 50 repetitions. Ten seconds separated each set. The workload was 10% of the peak torque during the five sets for both exercises (VOL and ES). Each isometric knee extension lasted 5 s. Two seconds separated each contraction.
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Fig. 1. Magnitude of strength loss under two fatiguing exercises. Maximal isometric strength for voluntary muscle contractions (VOL) or electrical stimulation (ES) of quadriceps femoris in two conditions (PRE: pre-fatigue condition; POST: immediate post-fatigue condition). Vertical bars represent the confidence intervals (95%). *p < 0.05; ***p < 0.0001.
The subjects received feedback from a computer screen so that they could control each contraction during the fatiguing exercise. During the fifth set of the fatiguing exercise, the subjects were asked to perform the last three repetitions (48th, 49th, and 50th) to the maximum of their possibility in order to calculate their isometric maximal strength (the best performance was retained). At the end of the fatiguing exercise, the subjects were removed from the dynamometer and began postural control post-testing as quickly as possible. The force platform was positioned at 3 m from the isokinetic dynamometer. Neuromuscular electrical stimulation (ES). During the completion of the ES exercise, the subjects were electrically stimulated by a portable stimulator (CefarTM Rehab 4 Pro® , Sweden). Four circular self-adhesive conducting electrodes (Stimrode® , diameter 50 mm, Sweden) were placed over each quadriceps. The two proximal electrodes were placed over the proximal part of the vastus medialis and vastus lateralis. The two distal electrodes were placed over the distal part of these muscles. The quadriceps femoris was stimulated using a biphasic symmetrical rectangular wave (continuous pulse 450 s, frequency 80 Hz). The intensity of stimulation was continuously adjusted to reach 10% of MVC (evaluated with the isokinetic dynamometer). The initial mean current intensity was 23 ± 2 mA and the final mean current intensity was 95 ± 24 mA (final minimal value: 59 mA; final maximal value: 120 mA). The configuration of neuromuscular electrical stimulation was identical to that of voluntary contractions in terms of duration (i.e. tetanic stimulations of 5 s followed by pauses of 2 s). As for the VOL exercise, the isometric maximal voluntary strength was measured during the last three repetitions (48th, 49th, and 50th) of the fifth set after the electrical stimulation was stopped. Postural and neuromuscular data were analyzed using a repeated-measures analysis of variance (ANOVA) with two withinsubjects factors: exercise (VOL vs. ES) and condition (PRE and POST). Newman–Keuls post hoc was used to test difference among means. Results were considered significant for p < 0.05. The MVC revealed a main effect of condition (F(1,16) = 38.6; p < 0.0001) and a significant condition × exercise interaction (F(1,16) = 50.6; p < 0.00001), indicating that the quadriceps femoris muscle strength differed for the VOL exercise and the ES exercise. Immediately after the fatiguing exercises (POST condition), the MVC was significantly decreased for both fatiguing exercises. However, the MVC decreased more for the ES exercise than for the VOL exercise. The strength loss for the ES exercise was 41% of MVC whereas that of the VOL exercise was 6% of MVC) (Fig. 1). As regards the COP velocity in the Y-axis, the statistical analysis revealed a main effect of condition (F(1,16) = 9.98; p < 0.01) and a significant exercise × condition interaction (F(1,16) = 5.72;
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T. Paillard et al. / Neuroscience Letters 477 (2010) 48–51
Fig. 2. Changes in COP velocity in the Y-axis for both exercises (VOL: voluntary muscle contractions of quadriceps femoris; ES: electrical stimulation of quadriceps femoris) in two conditions (PRE: pre-fatigue condition; POST: immediate postfatigue condition). Vertical bars represent the confidence intervals (95%). *p < 0.05; **p < 0.01.
p < 0.03), indicating that the postural control differed for the ES exercise and the VOL exercise. Immediately after the muscle fatigue, the COP velocity increased significantly for the VOL and ES exercises. In addition, the COP velocity increased more for the VOL exercise than for the ES exercise (Fig. 2). The COP velocity in the X-axis showed no difference after the completion of the fatiguing exercises. The frequency analysis on the high-frequency band showed a condition effect for the COP displacement in the X-axis (F(1,16) = 12.62; p < 0.001) and the Y-axis (F(1,16) = 11.93; p < 0.001). The statistical analysis also presented a significant exercise × condition interaction for the COP velocity in the X-axis (F(1,16) = 4.86; p < 0.04) and the Y-axis (F(1,16) = 6.77; p < 0.01). This means that the frequency analysis differed for the ES exercise and the VOL exercise in the X- and Y-axes. Immediately after the muscle fatigue, the contribution of the high frequencies increased for both exercises in the X- and Y-axes. Furthermore, the contribution of the high-frequency band in postural regulation increased more after the VOL exercise than after the ES exercise (Fig. 3). In contrast, the low frequency band did not differ after the fatiguing exercises. The aim of this work was to compare the neuromuscular and postural adaptations induced either by fatiguing voluntary muscular contractions (VOL exercise) or by fatiguing neuromuscular electrical stimulation (ES exercise). First, we verified that the strength loss induced by the ES exercise was greater than that induced by the VOL exercise. This data confirms that of other authors [3] for example, and emphasizes that, for a given intensity and duration of contraction, muscle fatigue is more severe with the ES exercise than with the VOL exercise. The metabolic effects induced by the ES exercise notably differ from those of the VOL exercise. After a low intensity intermittent exercise corresponding to 10% maximal voluntary torque, acute application of neuromuscular electrical stimulation acidifies the cytoplasm more than voluntary muscular contractions [27]. The ES exercise strongly activates anaerobic glycolysis for energy production by phosphocreatine and glycogen degradation with lactate formation and decline of intracellular pH, leading to early fatigue [1]. Hence, the ES exercise brings about a sharper decrease in the intramuscular motor unit spike amplitude than the VOL exercise [9]. Interestingly, the VOL exercise alters postural control more than the ES exercise. Evidence of higher alteration after the VOL exercise is that COP velocity and spectral energy of high-frequency band increased more than after the ES exercise. It appears that despite the greater strength loss with ES exercise, the postural control impairment was lesser. Hence, the present data show that the disturbance of postural control depends on the nature of the muscle contraction
Fig. 3. Changes in distribution of the spectral energy of COP on the X- and Y-axes in high-frequency band (>2 Hz) for both exercises (VOL: voluntary muscle contractions of quadriceps femoris; ES: neuromuscular electrical stimulation of quadriceps femoris) in two conditions (PRE: pre-fatigue condition; POST: immediate postfatigue condition). Vertical bars represent the confidence intervals (95%). *p < 0.05; **p < 0.01; ***p < 0.001.
(voluntary vs. electrically induced) rather than on the magnitude of strength loss. The data from the spectral analysis showed a higher spectral energy in the high-frequency band after both fatiguing exercises. This result suggests that the fatigue induces a greater contribution of the myotatic loops. Admittedly, under a disturbed postural condition, the reflex response augments to increase stiffness joint and reduce postural sway [6]. But under a muscle fatigue condition, the dynamic stretch reflex increases to counteract the reduction of intrinsic joint stiffness and to hold a position [28]. Biro et al. [4] specified that during fatigue the muscle spindle activation is increased from group III and IV afferent excitation of fusimotor neurons with increases in the metabolite concentration, and the gain of the gamma loop is also increased. Obviously, these neuromuscular compensatory mechanisms induced by muscle fatigue are not sufficient to preserve the effectiveness of motor output since postural control is disturbed for both fatiguing exercises. Moreover, the higher spectral energy in the high-frequency band shows that the VOL exercise generates a greater participation of the myotatic loop than the ES exercise. In a muscle fatigue context, Huffenus and Forestier [12] also observed that voluntary contractions induce greater changes in muscle activation than electrically induced contractions for elbow extensor muscles in performing an arm throwing skill. In the present study, the greater participation of the myotatic loop could be linked to the nature of muscular contraction and to the location and the type of the muscle fibers solicited during the two fatiguing exercises. Concerning the nature of muscular contraction, the ES exercise characterizes an artificial muscular activation that is not generated by central drive while the VOL exercise characterizes a voluntary muscular activation that is generated by central drive. After prolonged weak voluntary contractions, the effectiveness
T. Paillard et al. / Neuroscience Letters 477 (2010) 48–51
of corticospinal output can decrease and result from changes in synaptic function [22–25]. This phenomenon is likely to influence the descending drive required to activate motor neurons and affect the control of movement [25]. Decreased effectiveness of corticospinal output has not been observed after submaximal stimulated contractions. Therefore, we hypothesize that the deficiencies of the control of movement, i.e. the postural control after muscle fatigue, could be greater after the VOL exercise than after the ES exercise. Yet, neuromuscular compensatory mechanisms could be more strongly exerted to maintain balance after VOL exercise than after ES exercise since according to Biro et al. [4] the gain of the gamma loop is increased when the descending drive is affected. Concerning the location and the type of the muscle fibers solicited, the two fatiguing exercises exerted some notable differences. During submaximal voluntary muscle actions, the subjects’ motor units were progressively recruited in an orderly fashion from small to large [11], i.e. the depth of the muscle to the surface [15]. Inversely, neuromuscular electrical stimulation activated the motor units located directly beneath the stimulation electrodes [16]. Since the large motor units are mainly located on the surface of the quadriceps femoris [15], they were progressively recruited from the surface of the muscle to the depth, i.e. in an orderly fashion from large to small. Posture is specially controlled by slow-twitch fibers or tonic fibers – small fibers – [13] mainly located in the depth of the muscle. These fibers could be exhausted more after the VOL exercise than after the ES exercise. As the intensity of the VOL exercise was 10% of MVC, this exercise first activated the small motor units and thus could degrade postural control more than the ES exercise. We suggest that the VOL exercise induces a more severe fatigue in the tonic fibers, which are mainly active in postural regulation, whereas the ES exercise generates more severe fatigue in the phasic fibers, which are not especially required in the postural regulation. Moreover, both exercises impaired the subjects’ postural control, particularly in the sagittal plane. This phenomenon would probably be linked to the fact that both exercises fatigued the knee extensors, which assume a more important role in maintaining postural control in the sagittal plane than in the medio-lateral direction [5]. Our work shows that the higher the strength loss, the lesser the postural control impairment, indicating that postural control disturbance depends on the nature of the muscular contraction (voluntary vs. non-voluntary) and the type of motor unit solicited (tonic vs. phasic) rather than on the magnitude of strength loss. Acknowledgments We would like to thank the anonymous reviewers for their valuable comments and suggestions. References [1] M. Bergstrom, E. Hultman, Energy cost and fatigue during intermittent electrical stimulation of human skeletal muscle, J. Appl. Physiol. 65 (1988) 1500–1505. [2] B. Bigland-Ritchie, J.J. Woods, Changes in muscle contractile properties and neural control during human muscular fatigue, Muscle Nerve 7 (1984) 691–699.
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[3] S.A. Binder-Macleod, L. Snyder-Mackler, Muscle fatigue: clinical implications for fatigue assessment and neuromuscular electrical stimulation, Phys. Ther. 73 (1993) 902–910. [4] A. Biro, L. Griffin, E. Cafarelli, Reflex gain of muscle spindle pathways during fatigue, Exp. Brain Res. 177 (2007) 157–166. [5] R. Bizid, E. Margnes, Y. Franc¸ois, G. Gonzalez, J.L. Jully, P. Dupui, T. Paillard, Effects of knee and ankle muscle fatigue on postural control in the unipedal stance, Eur. J. Appl. Physiol. 106 (2009) 375–380. [6] R.C. Fitzpatrick, R.B. Gorman, D. Burke, S.C. Gandevia, Postural proprioceptive reflexes in standing human subjects: bandwidth of response and transmission characteristics, J. Physiol. 458 (1992) 69–83. [7] G. Gosselin, H. Rassoulian, I. Brown, Effects of neck extensor muscles fatigue on balance, Clin. Biomech. 19 (2004) 473–479. [8] P.A. Gribble, J. Hertel, Effect of hip and ankle muscle fatigue on unipodal postural control, J. Electromyogr. Kinesiol. 14 (2004) 641–646. [9] T. Hamada, T. Kimura, T. Moritani, Selective fatigue of fast motor units after electrically elicited muscle contractions, J. Electromyogr. Kinesiol. 14 (2004) 531–538. [10] K.M. Harkins, C.G. Mattacola, T.L. Uhl, T.R. Malone, J.L. McCrory, Effects of 2 ankle fatigue models on the duration of postural stability dysfunction, J. Athl. Train. 40 (2005) 191–196. [11] E. Henneman, G. Somjen, D.O. Carpenter, Functional significance of cell size in spinal motoneurons, J. Neurophysiol. 28 (1965) 560–580. [12] A.F. Huffenus, N. Forestier, Effects of fatigue of elbow extensor muscles voluntarily induced and induced by electromyostimulation on multi-joint movement organization, Neurosci. Lett. 403 (2006) 109–113. [13] J. Ijkema-Paassen, A. Gramsbergen, Development of postural muscles and their innervation, Neural. Plast. 12 (2005) 141–151. [14] R. Johnston, M.E. Howard, P. Cawley, G. Losse, Effect of lower extremities muscle fatigue on motor control performance, Med. Sci. Sports Excerc. 30 (1998) 1703–1707. [15] J. Lexell, K. Henriksson-Larsen, M. Sjostrom, Distribution of different fibre types in human skeletal muscles. 2. A study of cross-sections of whole m. vastus lateralis, Acta Physiol. Scand. 117 (1983) 115–122. [16] A.J. McComas, P.R. Fawcett, M.J. Campbell, R.E. Sica, Electrophysiological estimation of the number of motor units within a human muscle, J. Neurol. Neurosurg. Psychiatry 34 (1971) 121–131. [17] T. Paillard, R. Bizid, P. Dupui, Do sensorial manipulations affect subjects differently depending on their postural abilities? Br. J. Sports Med. 41 (2007) 435–438. [18] T. Paillard, Combined applications of neuromuscular electrical stimulation and voluntary muscular contractions, Sports Med. 38 (2008) 161–177. [19] T. Paillard, F. Noé, T. Rivière, V. Marion, R. Montoya, P. Dupui, Postural performance and strategy in the unipedal stance of soccer players at different levels of competition, J. Athl. Train. 41 (2006) 172–176. [20] K.M. Pline, M.L. Madigan, M.A. Nussbaum, Influence of fatigue time and level on increases in postural sway, Ergonomics 49 (2006) 1639–1648. [21] K.E. Popov, G.V. Kozhina, B.N. Smetanin, V.Y. Shlikov, Postural responses to combined vestibular and hip proprioceptive stimulation in man, Eur. J. Neurosci. 11 (1999) 3307–3311. [22] K. Sogaard, S.C. Gandevia, G. Todd, N.T. Petersen, J.L. Taylor, The effect of sustained low-intensity contractions on supraspinal fatigue in human elbow flexor muscles, J. Physiol. 573.2 (2006) 511–523. [23] J.L. Taylor, S.C. Gandevia, A comparison of central aspects of fatigue in submaximal and maximal voluntary contractions, J. Appl. Physiol. 104 (2008) 542–550. [24] J.L. Taylor, G. Todd, S.C. Gandevia, Evidence for a supraspinal contribution to human muscle fatigue, Clin. Exp. Pharmacol. Physiol. 33 (2006) 400–405. [25] J.L. Taylor, N.T. Petersen, J.E. Butler, S.C. Gandevia, Corticospinal transmission after voluntary contractions, Adv. Exp. Med. Biol. 508 (2002) 435–441. [26] S. Uimonen, M. Sorri, K. Laitakari, T. Jämsä, A comparison of three vibrators in static posturography: the effect of vibration amplitude on body sway, Med. Eng. Phys. 18 (1996) 405–409. [27] M. Vanderthommen, S. Duteil, C. Wary, J.S. Raynaud, A. Leroy-Willig, J.M. Crielaard, P.G. Carlier, A comparison of voluntary and electrically induced contractions by interleaved 1 H and 31 P-NMRS in humans, J. Appl. Physiol. 94 (2003) 1012–1024. [28] U. Windhorst, Muscle proprioceptive feedback and spinal networks, Brain Res. Bull. 73 (2007) 155–202. [29] J.A. Yaggie, S.J. McGregor, Effects of isokinetic ankle fatigue on the maintenance of balance and postural limits, Arch. Phys. Med. Rehabil. 83 (2002) 224–228.
Contents lists available at ScienceDirect
Neuroscience Letters journal homepage: www.elsevier.com/locate/neulet
Stimulated and voluntary fatiguing contractions of quadriceps femoris differently disturb postural control Thierry Paillard a,∗ , Julien Maitre a , Vincent Chaubet a , Liliane Borel b a
Laboratoire d’Analyse de la Performance Sportive, Université de Pau et des Pays de l’Adour, Département STAPS, ZA Bastillac Sud, 65000 Tarbes, France 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
b
a r t i c l e
i n f o
Article history: Received 29 November 2009 Received in revised form 31 March 2010 Accepted 16 April 2010 Keywords: Muscle fatigue Neuromuscular electrical stimulation Voluntary contraction Unipedal stance
a b s t r a c t Muscle fatigue affects muscle strength and postural control. However, it is not known whether impaired postural control after fatiguing muscular exercise depends on the nature of the muscle contraction. To answer this question, the present study analyzes changes in postural control after two fatiguing exercises of equal duration and intensity but that induced different magnitudes of strength loss. The effects of fatiguing contractions of the femoris quadriceps were compared for voluntary muscular contraction (VOL) and neuromuscular electrical stimulation (ES) on muscle strength and postural control. Seventeen subjects completed these two fatiguing exercises. Maximal voluntary contraction (MVC) and postural control were recorded using an isokinetic dynamometer and a force platform that recorded the center of foot pressure. Recordings were performed before and after the completion of both fatiguing tasks. Results indicate that, after a fatiguing exercise, the ES exercise affected MVC more than the VOL exercise. Inversely, postural control was disturbed more after VOL exercise than after ES exercise. In conclusion, postural control disturbance is influenced by the nature of the muscular contraction (voluntary vs. nonvoluntary) and the type of the motor unit solicited (tonic vs. phasic) rather than by the magnitude of strength loss. © 2010 Elsevier Ireland Ltd. All rights reserved.
Maintenance of posture requires the integration and use of information from sensory and motor systems. When the information is manipulated or impaired, postural control is affected. Manipulation of different sensory receptors (e.g. cutaneous, myo-tendinous, skin thermics, vestibular or visual receptors) affects information integration and deteriorates postural control [17,21,26]. Impaired postural control can originate from the disturbance of the motor pathway by excessive repetitions of submaximal muscular contractions [5,29]. This disturbance emanates from metabolic and/or neurologic changes that induce localized muscle fatigue [23]. Muscle fatigue can be defined as any exercise-induced decrease in maximal voluntary force produced by a muscle or muscle group [2]. The muscle strength decrease constitutes a relevant criterion to determine the fatigue state and can be linked either to central or to peripheral levels. Central fatigue arises proximal to the motor axons and leads to decreases in motor unit activation while peripheral fatigue is localized within the muscle itself, the neuromuscular junction, or the terminal branches of the motor axons. Postural control is especially affected by strength loss in postural tonic muscles such as ankle plantarflexors and dorsiflexors,
∗ Corresponding author. Tel.: +33 5 62566100; fax: +33 5 62566110. E-mail address: [email protected] (T. Paillard). 0304-3940/$ – see front matter © 2010 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.neulet.2010.04.034
ankle invertors and evertors, knee extensors, hip flexor-extensors, hip abductor-adductors, lumbar erector spinae, or neck muscles [5,7,8,10,14,29]. Considering voluntary contractions, for a given muscle group and for a given intensity of submaximal muscular contractions, the duration of fatiguing exercise influences the deterioration of postural control [20]. In addition, those authors showed that, immediately after fatiguing exercise, the magnitude of strength loss influences the level of the disturbance of postural control. However, the influence of the magnitude of strength loss on the postural control disturbance remains to be established when the nature of the contraction differs. To this end, neuromuscular electrical stimulation is of interest since it induces different magnitudes of strength loss for an equal duration and intensity of muscular contractions [27]. Indeed, for an identical force production and contraction duration during fatiguing exercise, the strength loss induced by this technique is greater than that induced by voluntary contractions (e.g. [27]). In the present study, we compared the effects of voluntary muscular contraction with those of neuromuscular electrical stimulation on postural control. Because the neurophysiological (motor drive, motor unit recruitment) and metabolic (metabolic activation, muscle fatigue) effects differ for stimulated and voluntary fatiguing contractions [18], we hypothesized that the relationship between the magnitude of strength loss and the postural
T. Paillard et al. / Neuroscience Letters 477 (2010) 48–51
control disturbance depended on the nature of the fatiguing exercise. Seventeen healthy male subjects participated in the study (age: 22.5 ± 4.1 years; height: 174.3 ± 5.7 cm; body weight: 74.2 ± 16.4 kg). They had not previously been involved in postural tests. Exclusion criteria included a documented postural control disorder or a medical condition that might affect postural control, a neurological or a musculoskeletal impairment in the past 2 years, or current injury making the subjects unable to participate. Participants signed an informed consent form approved by the local Ethics Committee as required by the Helsinki declaration. The experiment consisted in examining the possible neuromuscular and postural modifications induced by two different fatiguing exercises. One fatiguing exercise was performed by voluntary muscular contractions of the quadriceps femoris (VOL exercise); the other was performed by neuromuscular electrical stimulation of the quadriceps femoris (ES exercise). The isometric muscle strength and postural control were measured before (pre-fatigue or PRE condition) and immediately after (post-fatigue or POST condition) the completion of the muscle-fatiguing exercises. The completion of each exercise (VOL and ES) was separated by a period of 10–12 days for all the subjects. The effects of each fatiguing exercise were assessed in a randomized order. For each exercise, the subjects successively performed a postural test (PRE condition), a warm-up for 15 min on a cycle ergometer, an isometric maximal voluntary contraction test, a fatigue protocol (VOL or ES), an isometric maximal voluntary contraction test, and a postural test (POST condition). A PostureWin force platform with three strain gauges (Techno Concept, Cereste, France) was used to sample the displacements of the center of foot pressure (COP) at 40 Hz. Postural control was analyzed before (pre-fatigue or PRE condition) and immediately after (post-fatigue or POST condition) the fatiguing exercise. The subjects were asked to stand for 25 s on the platform, barefooted and as immobile as possible on one leg, the supporting leg, i.e. the one not used for kicking a ball. The foot was placed according to precise landmarks with respect to the X- and Y-axes of the platform. The other foot was lifted so that the subject’s big toe touched the medial malleolus of the supporting leg. Subjects had their eyes closed to prevent vision from contributing to the regulation of postural behaviors. To characterize the postural control of the subjects, the mean COP velocity in both the X-axis (frontal plane) and the Yaxis (sagittal plane) were independently determined as the mean of the absolute values computed from the recorded position. A Fast Fourier’s Transform was run on the X and Y COP courses, and the areas of the frequency spectrum were distributed into 2 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 myotatic inputs [19]. An isokinetic dynamometer (BiodexTM , System 3 Pro, Shirley, USA) was used to exhaust the knee extensor muscles. The isometric maximal voluntary contraction (MVC) was recorded using the leg evaluated on the force platform and measured on the isokinetic dynamometer. The subjects were seated with a 90◦ hip flexion and a 90◦ knee flexion and performed isometric contractions with the knee extensors. Stabilization straps were positioned across the subjects’ chest and pelvis. The arms were crossed on the chest. The subjects performed three MVCs that lasted 5 s. Thirty seconds separated each contraction. The best performance (peak torque in N m) was retained. After a 2-min rest period, the subjects began the fatigue protocol. Voluntary muscular contraction (VOL). The peak torque served as a reference to determine the workload applied during the fatiguing exercise. This exercise comprised 5 sets of 50 repetitions. Ten seconds separated each set. The workload was 10% of the peak torque during the five sets for both exercises (VOL and ES). Each isometric knee extension lasted 5 s. Two seconds separated each contraction.
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Fig. 1. Magnitude of strength loss under two fatiguing exercises. Maximal isometric strength for voluntary muscle contractions (VOL) or electrical stimulation (ES) of quadriceps femoris in two conditions (PRE: pre-fatigue condition; POST: immediate post-fatigue condition). Vertical bars represent the confidence intervals (95%). *p < 0.05; ***p < 0.0001.
The subjects received feedback from a computer screen so that they could control each contraction during the fatiguing exercise. During the fifth set of the fatiguing exercise, the subjects were asked to perform the last three repetitions (48th, 49th, and 50th) to the maximum of their possibility in order to calculate their isometric maximal strength (the best performance was retained). At the end of the fatiguing exercise, the subjects were removed from the dynamometer and began postural control post-testing as quickly as possible. The force platform was positioned at 3 m from the isokinetic dynamometer. Neuromuscular electrical stimulation (ES). During the completion of the ES exercise, the subjects were electrically stimulated by a portable stimulator (CefarTM Rehab 4 Pro® , Sweden). Four circular self-adhesive conducting electrodes (Stimrode® , diameter 50 mm, Sweden) were placed over each quadriceps. The two proximal electrodes were placed over the proximal part of the vastus medialis and vastus lateralis. The two distal electrodes were placed over the distal part of these muscles. The quadriceps femoris was stimulated using a biphasic symmetrical rectangular wave (continuous pulse 450 s, frequency 80 Hz). The intensity of stimulation was continuously adjusted to reach 10% of MVC (evaluated with the isokinetic dynamometer). The initial mean current intensity was 23 ± 2 mA and the final mean current intensity was 95 ± 24 mA (final minimal value: 59 mA; final maximal value: 120 mA). The configuration of neuromuscular electrical stimulation was identical to that of voluntary contractions in terms of duration (i.e. tetanic stimulations of 5 s followed by pauses of 2 s). As for the VOL exercise, the isometric maximal voluntary strength was measured during the last three repetitions (48th, 49th, and 50th) of the fifth set after the electrical stimulation was stopped. Postural and neuromuscular data were analyzed using a repeated-measures analysis of variance (ANOVA) with two withinsubjects factors: exercise (VOL vs. ES) and condition (PRE and POST). Newman–Keuls post hoc was used to test difference among means. Results were considered significant for p < 0.05. The MVC revealed a main effect of condition (F(1,16) = 38.6; p < 0.0001) and a significant condition × exercise interaction (F(1,16) = 50.6; p < 0.00001), indicating that the quadriceps femoris muscle strength differed for the VOL exercise and the ES exercise. Immediately after the fatiguing exercises (POST condition), the MVC was significantly decreased for both fatiguing exercises. However, the MVC decreased more for the ES exercise than for the VOL exercise. The strength loss for the ES exercise was 41% of MVC whereas that of the VOL exercise was 6% of MVC) (Fig. 1). As regards the COP velocity in the Y-axis, the statistical analysis revealed a main effect of condition (F(1,16) = 9.98; p < 0.01) and a significant exercise × condition interaction (F(1,16) = 5.72;
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Fig. 2. Changes in COP velocity in the Y-axis for both exercises (VOL: voluntary muscle contractions of quadriceps femoris; ES: electrical stimulation of quadriceps femoris) in two conditions (PRE: pre-fatigue condition; POST: immediate postfatigue condition). Vertical bars represent the confidence intervals (95%). *p < 0.05; **p < 0.01.
p < 0.03), indicating that the postural control differed for the ES exercise and the VOL exercise. Immediately after the muscle fatigue, the COP velocity increased significantly for the VOL and ES exercises. In addition, the COP velocity increased more for the VOL exercise than for the ES exercise (Fig. 2). The COP velocity in the X-axis showed no difference after the completion of the fatiguing exercises. The frequency analysis on the high-frequency band showed a condition effect for the COP displacement in the X-axis (F(1,16) = 12.62; p < 0.001) and the Y-axis (F(1,16) = 11.93; p < 0.001). The statistical analysis also presented a significant exercise × condition interaction for the COP velocity in the X-axis (F(1,16) = 4.86; p < 0.04) and the Y-axis (F(1,16) = 6.77; p < 0.01). This means that the frequency analysis differed for the ES exercise and the VOL exercise in the X- and Y-axes. Immediately after the muscle fatigue, the contribution of the high frequencies increased for both exercises in the X- and Y-axes. Furthermore, the contribution of the high-frequency band in postural regulation increased more after the VOL exercise than after the ES exercise (Fig. 3). In contrast, the low frequency band did not differ after the fatiguing exercises. The aim of this work was to compare the neuromuscular and postural adaptations induced either by fatiguing voluntary muscular contractions (VOL exercise) or by fatiguing neuromuscular electrical stimulation (ES exercise). First, we verified that the strength loss induced by the ES exercise was greater than that induced by the VOL exercise. This data confirms that of other authors [3] for example, and emphasizes that, for a given intensity and duration of contraction, muscle fatigue is more severe with the ES exercise than with the VOL exercise. The metabolic effects induced by the ES exercise notably differ from those of the VOL exercise. After a low intensity intermittent exercise corresponding to 10% maximal voluntary torque, acute application of neuromuscular electrical stimulation acidifies the cytoplasm more than voluntary muscular contractions [27]. The ES exercise strongly activates anaerobic glycolysis for energy production by phosphocreatine and glycogen degradation with lactate formation and decline of intracellular pH, leading to early fatigue [1]. Hence, the ES exercise brings about a sharper decrease in the intramuscular motor unit spike amplitude than the VOL exercise [9]. Interestingly, the VOL exercise alters postural control more than the ES exercise. Evidence of higher alteration after the VOL exercise is that COP velocity and spectral energy of high-frequency band increased more than after the ES exercise. It appears that despite the greater strength loss with ES exercise, the postural control impairment was lesser. Hence, the present data show that the disturbance of postural control depends on the nature of the muscle contraction
Fig. 3. Changes in distribution of the spectral energy of COP on the X- and Y-axes in high-frequency band (>2 Hz) for both exercises (VOL: voluntary muscle contractions of quadriceps femoris; ES: neuromuscular electrical stimulation of quadriceps femoris) in two conditions (PRE: pre-fatigue condition; POST: immediate postfatigue condition). Vertical bars represent the confidence intervals (95%). *p < 0.05; **p < 0.01; ***p < 0.001.
(voluntary vs. electrically induced) rather than on the magnitude of strength loss. The data from the spectral analysis showed a higher spectral energy in the high-frequency band after both fatiguing exercises. This result suggests that the fatigue induces a greater contribution of the myotatic loops. Admittedly, under a disturbed postural condition, the reflex response augments to increase stiffness joint and reduce postural sway [6]. But under a muscle fatigue condition, the dynamic stretch reflex increases to counteract the reduction of intrinsic joint stiffness and to hold a position [28]. Biro et al. [4] specified that during fatigue the muscle spindle activation is increased from group III and IV afferent excitation of fusimotor neurons with increases in the metabolite concentration, and the gain of the gamma loop is also increased. Obviously, these neuromuscular compensatory mechanisms induced by muscle fatigue are not sufficient to preserve the effectiveness of motor output since postural control is disturbed for both fatiguing exercises. Moreover, the higher spectral energy in the high-frequency band shows that the VOL exercise generates a greater participation of the myotatic loop than the ES exercise. In a muscle fatigue context, Huffenus and Forestier [12] also observed that voluntary contractions induce greater changes in muscle activation than electrically induced contractions for elbow extensor muscles in performing an arm throwing skill. In the present study, the greater participation of the myotatic loop could be linked to the nature of muscular contraction and to the location and the type of the muscle fibers solicited during the two fatiguing exercises. Concerning the nature of muscular contraction, the ES exercise characterizes an artificial muscular activation that is not generated by central drive while the VOL exercise characterizes a voluntary muscular activation that is generated by central drive. After prolonged weak voluntary contractions, the effectiveness
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of corticospinal output can decrease and result from changes in synaptic function [22–25]. This phenomenon is likely to influence the descending drive required to activate motor neurons and affect the control of movement [25]. Decreased effectiveness of corticospinal output has not been observed after submaximal stimulated contractions. Therefore, we hypothesize that the deficiencies of the control of movement, i.e. the postural control after muscle fatigue, could be greater after the VOL exercise than after the ES exercise. Yet, neuromuscular compensatory mechanisms could be more strongly exerted to maintain balance after VOL exercise than after ES exercise since according to Biro et al. [4] the gain of the gamma loop is increased when the descending drive is affected. Concerning the location and the type of the muscle fibers solicited, the two fatiguing exercises exerted some notable differences. During submaximal voluntary muscle actions, the subjects’ motor units were progressively recruited in an orderly fashion from small to large [11], i.e. the depth of the muscle to the surface [15]. Inversely, neuromuscular electrical stimulation activated the motor units located directly beneath the stimulation electrodes [16]. Since the large motor units are mainly located on the surface of the quadriceps femoris [15], they were progressively recruited from the surface of the muscle to the depth, i.e. in an orderly fashion from large to small. Posture is specially controlled by slow-twitch fibers or tonic fibers – small fibers – [13] mainly located in the depth of the muscle. These fibers could be exhausted more after the VOL exercise than after the ES exercise. As the intensity of the VOL exercise was 10% of MVC, this exercise first activated the small motor units and thus could degrade postural control more than the ES exercise. We suggest that the VOL exercise induces a more severe fatigue in the tonic fibers, which are mainly active in postural regulation, whereas the ES exercise generates more severe fatigue in the phasic fibers, which are not especially required in the postural regulation. Moreover, both exercises impaired the subjects’ postural control, particularly in the sagittal plane. This phenomenon would probably be linked to the fact that both exercises fatigued the knee extensors, which assume a more important role in maintaining postural control in the sagittal plane than in the medio-lateral direction [5]. Our work shows that the higher the strength loss, the lesser the postural control impairment, indicating that postural control disturbance depends on the nature of the muscular contraction (voluntary vs. non-voluntary) and the type of motor unit solicited (tonic vs. phasic) rather than on the magnitude of strength loss. Acknowledgments We would like to thank the anonymous reviewers for their valuable comments and suggestions. References [1] M. Bergstrom, E. Hultman, Energy cost and fatigue during intermittent electrical stimulation of human skeletal muscle, J. Appl. Physiol. 65 (1988) 1500–1505. [2] B. Bigland-Ritchie, J.J. Woods, Changes in muscle contractile properties and neural control during human muscular fatigue, Muscle Nerve 7 (1984) 691–699.
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