Unilateral and bilateral fatiguing contractions similarly alter postural stability but differently modify postural position on bipedal stance

Human Movement Science 32 (2013) 353–362

Contents lists available at SciVerse ScienceDirect

Human Movement Science journal homepage: www.elsevier.com/locate/humov

Unilateral and bilateral fatiguing contractions similarly alter postural stability but differently modify postural position on bipedal stance Thierry Paillard a,⇑, Liliane Borel b a Université de Pau & Pays Adour, Laboratoire Activité Physique, Performance et Santé (EA 4445), Département STAPS, ZA Bastillac Sud, 65000 Tarbes, France b Laboratoire de Neurosciences Intégratives et Adaptatives, UMR 7260, Aix-Marseille Université/CNRS, Centre St Charles, Pôle 3C, Case B, 3 Place Victor Hugo, 13331 Marseille Cedex 03, France

a r t i c l e

i n f o

Article history: Available online 28 April 2013 PsycINFO classification: 2520 Neuropsychology & Neurology Keywords: Unilateral muscle fatigue Bilateral muscle fatigue Postural stability Postural position Sensorimotor alteration

a b s t r a c t The aim of the present study was to compare the effects of unilateral and bilateral muscle fatigue on bipedal postural control and neuromuscular activities. Nineteen subjects completed bilateral fatiguing contractions (BI group), and seventeen subjects completed unilateral fatiguing contractions (UNI group) of the quadriceps femoris. Postural control, maximal voluntary contraction (MVC) and central activation ratio (CAR) were measured before and after the completion of fatiguing tasks for both groups. Postural control was evaluated by using a force platform, which recorded the center of foot pressure (COP). MVC was quantified with an ergometer and CAR was determined with the superimposed electrical stimulation technique. Spatio-temporal COP parameters were used to evaluate postural stability (displacements of COP) and postural position (coordinates of COP) and a frequency analysis of COP excursions (wavelet transform) was performed to estimate the contribution of different neuronal loops. Postural stability, MVC and CAR were similarly affected after unilateral and bilateral fatiguing contractions. Moreover, the impairment of postural position was higher after unilateral fatiguing contractions than after bilateral fatiguing contractions. The study’s results indicated that unilateral and bilateral fatigue equally disturbs postural control as well as central drive. However, unilateral muscle fatigue creates postural asymmetries while bilateral muscle fatigue does not engender any. Ó 2012 Elsevier B.V. All rights reserved.

⇑ Corresponding author. Address: Université de Pau et des Pays de l’Adour, Département STAPS, ZA Bastillac Sud, 65000 Tarbes, France. Tel.: +33 (0)562566100; fax: +33 (0)562566110. E-mail address: [email protected] (T. Paillard). 0167-9457/$ - see front matter Ó 2012 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.humov.2012.12.001

354

T. Paillard et al. / Human Movement Science 32 (2013) 353–362

1. Introduction Muscle fatigue disturbs postural control in the bipedal stance (Bisson, Chopra, Azzi, Morgan, & Bilodeau, 2010; Chaubet, Maitre, Cormery, & Paillard, 2011; Corbeil, Blouin, Bégin, Nougier, & Teasdale, 2003; Ledin, Fransson, & Magnusson, 2004; Wojcik, Nussbaum, Lin, Shibata, & Madigan, 2011). The number of fatigued muscles influences the magnitude of the postural control disturbance (Boyas et al., 2011; Nelson & Johnson, 1973). The greater the number of fatigued muscles, the greater the postural disturbance. Moreover, exercise applied to few muscles, but very localized such as heel raises, affected postural control less than exercise involving a greater number of muscles interesting the whole body such as squat thrusts or rowing movements (Nelson & Johnson, 1973; Springer & Pincivero, 2009). In the context of localized muscle fatigue, an exercise that involves antagonist ankle muscles such as plantarflexors and dorsiflexors impaired postural control more than an exercise involving either plantarflexors or dorsiflexors (Boyas et al., 2011). In fact, the previous relationship persists with localized muscle fatigue which shows that the greater the number of fatigued muscles, the greater the alteration of motor output and sensory input of the postural system (Boyas et al., 2011). As a consequence, one can expect that for a given muscle chain, the disturbing effects of bilateral fatigue on postural control should be greater than those obtained after unilateral fatigue. Moreover, in the context of localized muscle fatigue, the central nervous system develops compensatory postural strategies to limit the postural disturbance (for a review see Paillard, 2012). Motor drive is adapted to postural muscles to prevent movements and voluntary postural adjustments from being modified (Chabran, Maton, & Fourment, 2002; Kanekar, Santos, & Aruin, 2008). Adaptations occur by rotation of motor units in postural muscles and/or by change of activated muscles during postural regulation. Moreover, reflex amplitude increases in fatigued postural muscles (Herrmann, Madigan, Davidson, & Granata, 2006). Muscle fatigue increases joint stiffness through the coactivation of antagonist muscles to reduce postural sway (De Luca & Mambrito, 1987; Granacher, Gruber, Förderer, Strass, & Gollhofer, 2010). This phenomenon results from an increase in the common drive of motor units of antagonist muscles (De Luca & Mambrito, 1987). In addition, fatigue increases the dynamic stretch reflex to counteract the reduction of intrinsic joint stiffness (Windhorst, 2007; Zhang & Rymer, 2001). Unilateral muscle fatigue facilitates the development of specific compensatory strategies (Berger, Regueme, & Forestier, 2010, 2011; Vuillerme & Boisgontier, 2010; Vuillerme, Sportbert, & Pinsault, 2009) not observed under bilateral muscle fatigue. Under unilateral muscle fatigue, the contribution of each leg to the control of two-legged stance is modified, which results from neural adjustments and compensatory contralateral strategies to optimize bipedal postural control (Berger et al., 2010, 2011; Vuillerme & Boisgontier, 2010; Vuillerme et al., 2009). Compensatory changes take place thanks to supplementary somatosensory inputs provided to the central nervous system by sensors of the nonfatigued leg’s foot (Vuillerme & Boisgontier, 2010; Vuillerme et al., 2009), and the motor activity of specific stabilizer muscles of the non-exercised leg increased (Berger et al., 2010). Thus, unilateral muscle fatigue generates supplementary compensatory strategies compared to bilateral muscle fatigue. On the basis of the above data, unilateral muscle fatigue should minimize the disturbance of postural control compared to bilateral muscle fatigue. To our knowledge, no study has compared the effects of unilateral fatigue versus those of bilateral fatigue on postural control. The aim of this study was to compare the effects of unilateral and bilateral fatiguing contractions of quadriceps femoris performed at the same relative level of force on bipedal postural control and neuromuscular activities whose changes are able to influence the motor output of the postural system.

2. Methods 2.1. Subjects Thirty-six healthy male students in sport sciences, free of any known balance disorder and/or neuro-musculoskeletal impairments in the last 2 years, were volunteered for the experiment. They

T. Paillard, L. Borel / Human Movement Science 32 (2013) 353–362

355

practiced different sports at least 10 hours per week and avoided strenuous activity at least three days before the data collection session. All participants had the right leg as dominant leg (the one used for kicking a ball). They gave their informed consent to participate in the experiment in accordance with the declaration of Helsinki. The subjects were randomized into two groups. Group BI (n = 19) performed a bilateral fatiguing task by voluntary muscular contractions of quadriceps femoris and group UNI (n = 17) performed a unilateral fatiguing task by voluntary muscular contractions of quadriceps femoris. The subjects’ morphological characteristics were similar for the two groups (Table 1). 2.2. Experimental setup and procedure The experiment consisted in examining the neuromuscular and postural responses induced by unilateral or bilateral voluntary muscular contractions of quadriceps femoris. Isometric maximal voluntary contraction (MVC), central activation ratio (CAR) and postural control were measured before (prefatigue or PRE condition) and after (post-fatigue or POST condition) the fatiguing task for the BI and UNI groups. The subjects successively performed a postural test (PRE condition), a 15-min warm-up on a cycle ergometer, MVC and CAR tests, a fatigue protocol, MVC and CAR tests and a postural test (POST condition). 2.3. Postural test The subjects were asked to stand barefoot, as still as possible, for 25 s on the platform, with their arms along the body, on two legs on a force platform (PostureWin, Techno Concept, Cereste, France; 40 Hz frequency, 12 bit A/D conversion) that recorded the displacements of the centre of foot pressure (COP) with three strain gauges. COP signals were smoothed using a second-order Butterworth filter with a 10 Hz low-pass cut off frequency. The subjects were asked to stand feet 30° apart (inter-malleolar distance of 5 cm). Subjects had their eyes closed to prevent vision from contributing to the regulation of postural behaviours. The spatio-temporal parameters of COP displacements analyzed were the COP area (the projection of the COP displacement, mm2), the COPX and COPY velocity (the total COP displacement divided by the total period on the medio-lateral axis or x-axis and the antero-posterior axis or y-axis respectively, mm s1) and the mean xCOP and mean yCOP (the average position of the COP on the x-axis and the yaxis respectively, both in mm). The COP surface and the COPX and COPY velocity were used to specify the postural stability. xCOP and yCOP reflect the topographic features of plantar pressure distribution on the x- and y-axes and define the mean postural position. The frequency parameters of COP displacements were analyzed from the spectral power density of the recorded signal given by the wavelet transform. The spectral analysis was computed for three frequency bands, defined as follows: 0.05–0.5 Hz (low frequencies), 0.5–1.5 Hz (medium frequencies), and 1.5–10 Hz (high frequencies) (Bernard-Demaze, Dumitrescu, Jimeno, Borel, & Lacour, 2009; Tardieu et al., 2009). This analysis characterizes the postural strategy used by the subjects. The low and medium frequencies are in domains mostly related to the visual and vestibular/somatosensory contribution to posture control, respectively, and the higher band rather results from proprioceptive participation (Paillard, Bizid, & Dupui, 2007; Paillard, Lafont, Costes-Salon, & Dupui, 2004). Spectral power density was evaluated in both the x- and the y-axes and expressed in arbitrary units (AU).

Table 1 Comparison of the subjects’ morphological characteristics between the 2 groups (one-factor ANOVA).

Age (years) Height (cm) Weight (kg)

BI group (n = 19)

UNI group (n = 17)

21.8 ± 1.6 177.9 ± 6.1 73.0 ± 8.4

21.1 ± 1.7 180.2 ± 5.9 75.2 ± 10.3

None of the inter-group differences were significant (values are means and standard deviations).

356

T. Paillard et al. / Human Movement Science 32 (2013) 353–362

2.4. Measurement of maximal voluntary contraction The MVC of the quadriceps of both legs for the BI group and the MVC of the quadriceps of the non-dominant leg (i.e., the left leg) for the UNI group were measured on an ergometer (Leg extensor, Panatta Sport™, Italia). This device was equipped with two force sensors (Model SSM Series, PM Instrumentation™, France; 200 Hz sampling frequency) attached to the subjects’ ankles. The subjects sat with a 90° knee flexion and a 90° hip flexion. The back of the seat was inclined 20° backwards and the depth of the seat was fitted to the length of the subjects’ thighs. Subjects were stabilized with straps positioned across the chest and pelvis. The arms were crossed on the chest. A period of familiarization was established before this test period (two MVCs for 3 s separated by 10 s, with a 20-s rest before the beginning of the test). During the test, subjects were asked to perform two MVCs for 5 s, with a 30-s rest between each contraction. The subjects received verbal encouragements without having any visual and oral feedback about their performance. The best performance (peak torque in N) was retained. 2.5. Evaluation of central activation ratio To quantify central activation failure during each MVC, an electrical stimulation (ES) was triggered manually after force plateaued (i.e., after 3 s), for 2 s. Central activation ratio was calculated according to the following equation (Kent-Braun & Le Blanc, 1996; Paillard, Noé, Passelergue, & Dupui, 2005):

CAR ¼

MVC MVC þ ES

where MVC + ES = voluntary + stimulated forces. In the case where there was no increase in force during the electrical stimulation, CAR = 1.0 and voluntary activation was considered as complete. Central activation ratio was evaluated on the non-dominant leg for both groups. ES was completed with a portable stimulator (CefarTM Rehab 4 ProÒ, Sweden). Four rectangular self-adhesive conducting electrodes (StimrodeÒ, 50  89 mm, Sweden) were placed over the vastus medialis, vastus lateralis and rectus femoris muscles. Three electrodes were longitudinally placed over the motor point of the vastus medialis, rectus femoris and vastus lateralis muscles and one electrode was placed on the proximal part of quadriceps across the vastus lateralis and rectus femoris. Muscles were stimulated using a biphasic symmetrical rectangular wave (pulse duration 450 ls, 70 mA, frequency 80 Hz). 2.6. Fatiguing exercise Two minutes after the MVC and CAR tests, the subjects began the fatigue protocol. The peak torque served as a reference to determine the workload applied during the fatiguing exercise. The voluntary muscular contractions included 130 repetitions, which were completed with both legs for the BI group and with the non-dominant leg for the UNI group. The workload was 20% of the peak torque during the exercise. Each isometric knee extension lasted 5 s. Two seconds separated each contraction. The subjects received feedback from a computer screen so that they could control each contraction during the fatiguing exercise. At the end of the fatiguing exercise, the subjects were asked to perform the last two repetitions (129th and 130th) to the maximum of their possibility in order to calculate their MVC (the best performance was retained) and their CAR. At the end of the fatiguing exercise, the subjects were removed from the ergometer and began post-testing postural control as quickly as possible. 2.7. Statistical analysis Parameters describing body sway (COP area, mean COPX and COPY velocity, mean XCOP and YCOP, spectral power density in the low, medium and high frequency bands), MVC and CAR were analyzed using a repeated measure analysis of variance (ANOVA) with two within-subjects factors: group (BI vs. UNI) and condition (two levels: PRE and POST). Moreover, only for the BI group, MVC was calculated using a repeated ANOVA measure with two factors: leg (dominant vs. non-dominant) and condition

T. Paillard, L. Borel / Human Movement Science 32 (2013) 353–362

357

(two levels: PRE and POST). Newman–Keuls post hoc was used to test difference among means. Results were considered significant for p < .05. 3. Results 3.1. Maximal voluntary contraction Before the fatiguing task was performed, the MVC of the non-dominant-leg did not significantly differ for the BI and the UNI groups. At the end of the fatiguing tasks, MVC significantly decreased in both groups, F(1, 34) = 284.69, p < .001, and the ANOVA did not reveal a significant Group  Condition interaction (Fig. 1), suggesting that MVC did not differ for unilateral and bilateral fatigue. Moreover, we checked that MVC did not differ between the two legs for the BI group in the PRE and POST conditions. In fact, for the BI group, MVC significantly decreased in the two legs (non-dominant leg: PRE condition 511 ± 84 N versus POST condition 407 ± 81 N and dominant leg: PRE condition 522 ± 89 N versus POST condition 423 ± 84 N, F(1, 36) = 293.03, p < .001). However, the ANOVA analysis did not reveal a significant Leg  Condition interaction. 3.2. Central activation ratio In the POST condition, CAR significantly decreased in both groups, F(1, 34) = 21.92, p < .001. Nevertheless, the Group  Condition interaction was not significant, suggesting that the central activation did not differ for the two groups (Fig. 2). 3.3. Postural responses Parameters describing body sway are reported on Table 2. The COP area indicated a significant condition effect, F(1, 34) = 26.54, p < .001, without a significant Group  Condition interaction. Similarly, 700

MVC+ES MVC

600

Force (N)

500 400 300 200 100 0 PRE

POST

PRE

BI group

POST UNI group

Fig. 1. Means and standard deviations for isometric maximal voluntary contraction (MVC) of knee extensors of non-dominantleg and the corresponding values for muscle activated MVC together with surimposed electrical stimulation (ES), i.e., MVC + ES, for the two groups (BI and UNI) in two conditions (PRE: pre-fatigue and POST: post-fatigue condition).

Central activation ratio

PRE POST

1.00

0.96

0.92 BI group

UNI group

Fig. 2. Means and standard deviations for central activation ratio (CAR) for the two groups (BI and UNI) in two conditions (PRE: pre-fatigue condition and POST: post-fatigue condition).

358

T. Paillard et al. / Human Movement Science 32 (2013) 353–362

Table 2 Comparison of the postural parameters for the two groups in the two conditions (PRE: pre-fatigue condition; POST: post-fatigue condition). Postural parameters

BI group

COP surface (mm2) COPX velocity (mm s1) COPY velocity (mm s1) XCOP mean (mm) YCOP mean (mm)

UNI group

PRE

POST

PRE

POST

121.4 ± 60.0 6.5 ± 1.8 7.6 ± 1.9 0.11 ± 9.4 3.1 ± 13.4

225.3 ± 105.9 9.7 ± 3.6 10.5 ± 3.2 1.1 ± 8.2 2.5 ± 14.9

127.4 ± 60.9 5.7 ± 2.0 6.8 ± 1.7 2.5 ± 9.3 1.8 ± 12.4

195.7 ± 104.3 8.8 ± 3.6 9.3 ± 2.9 9.0 ± 8.7 2.6 ± 12.2

COPx and COPy velocity revealed a main effect of condition, F(1, 34) = 58.72, p < .001, and F(1, 34) = 69.25, p < .001, respectively. Nevertheless, the Group  Condition interactions were not significant for the COPx and COPy velocity, indicating that these postural parameters differed before and after the fatiguing tasks for the two groups. The mean xCOP showed a significant condition effect, F(1, 34) = 4.46, p < .05, and a significant Group  Condition interaction, F(1, 34) = 9.6, p < .01. Immediately after the fatiguing tasks (POST condition), there was a shift of the mean xCOP towards the side of the fatigued leg for the UNI group (p < .001) without significant changes for the BI group. The mean yCOP did not reveal any significant difference neither after unilateral nor after bilateral fatigue. The spectral analysis with the application of the wavelet transform evaluated in the y-axis and xaxis showed a condition effect for the low, F(1, 34) = 13.81, p < .001, and F(1, 34) = 22.82, p < .001, respectively, medium, F(1, 34) = 34.34, p < .001, and F(1, 34) = 28.38, p < .001, respectively, and high, F(1, 34) = 35.48, p < .001, and F(1, 34) = 26.13, p < .001, frequency bands. In the POST condition, spectral

80 70 60 50 BI group

UNI group

Spectral power density (AU)

60

PRE POST

90

Spectral power density (AU)

Spectral power density (AU)

80

(b)

Axis Y (0,05-0,5 Hz)

80

Spectral power density (AU)

Spectral power density (AU)

90

Spectral power density (AU)

(a)

60

Axis X (0,05-0,5 Hz) PRE POST

80 70 60 50 BI group

Axis Y (0,5-1,5 Hz)

Axis X (0,5-1,5 Hz)

PRE POST

70 60 50 40 BI group

UNI group

PRE POST

70 60 50 40 BI group

UNI group

Axis X (1,5-10 Hz)

Axis Y (1,5-10 Hz) PRE POST

50

40 30 BI group

UNI group

UNI group

PRE POST

50

40 30 BI group

UNI group

Fig. 3. Changes of the low, medium and high frequency bands for the two groups (BI and UNI) in two conditions (PRE: prefatigue condition and POST: post-fatigue condition), in (a) the y-axis and (b) the x-axis (arbitrary units or AU). Vertical bars represent the standard deviation.

T. Paillard, L. Borel / Human Movement Science 32 (2013) 353–362

359

power density increased in the three frequency bands for both groups. Nevertheless, the Group  Condition interactions were not significant (Fig. 3). 4. Discussion The findings of this study showed that the isometric maximal voluntary contraction (MVC), central activation ratio (CAR) and postural stability were similarly degraded immediately after completion of bilateral and unilateral fatiguing tasks of the quadriceps femoris. However, the unilateral fatiguing task altered the mean postural position more than the bilateral fatiguing task. 4.1. Similar disturbance of the postural stability The fact that the spatiotemporal and frequency parameters of displacement of the center of foot pressure were similarly altered for both groups showed that the efficiency of the postural system was equally affected for the unilateral and bilateral fatiguing tasks. Previous studies already emphasized that localized muscle fatigue deteriorates postural stability in the bipedal stance after unilateral (Berger et al., 2010, 2011; Vuillerme & Boisgontier, 2010; Vuillerme et al., 2009) and bilateral (Bisson et al., 2010; Chaubet et al., 2011; Corbeil et al., 2003; Ledin et al., 2004; Wojcik et al., 2011) fatiguing tasks. The present study is the first to describe the fact that unilateral and bilateral fatiguing tasks similarly disturb postural stability. The reduction of the MVC after unilateral and bilateral fatiguing tasks constitutes a disturbing factor on the bipedal postural control as previously reported for the bilateral muscle fatigue (Chaubet et al., 2011). In fact, the larger the magnitude of strength loss, the greater the disturbance of postural control after voluntary contractions (Pline, Madigan, & Nussbaum, 2006). In addition, after a fatigue protocol, the variation of the force generated is increased for a given motor task (Duchateau, Semmler, & Enoka, 2006; Hunter, Critchlow, & Enoka, 2004), which induces an increase in the net muscular force variation during a postural task (Caron, 2003) and then a disturbance of the postural stability. Moreover, postural alteration did not differ for the unilateral and bilateral fatiguing tasks. Two opposite factors could explain such a similarity. On the one hand, unilateral fatigue could minimize postural disturbance thanks to a weaker strength loss due to a smaller number of fatigued muscles compared to bilateral fatigue. On the other hand, unilateral fatigue could amplify postural disturbance compared to bilateral fatigue because of a neuromuscular functional asymmetry induced between the left and right legs, which would create an imbalance in the motor output of the two legs. A third factor could contribute to attenuate the difference in postural disturbance after both fatiguing tasks since the bipedal stance could be particularly prone to facilitate compensatory postural strategies under muscle fatigue condition (Chaubet et al., 2011). A change from ankle strategy to hip strategy would occur when proprioception and motor output of the lower limb are disturbed (Bizid, Margnes, et al., 2009; Paillard, 2012). A redistribution of the contribution of active muscles and a reorganization of multi-joint coordination could also take place (Yiou, Heugas, Mezaour, & Le Bosec, 2009), especially a reduction of movements of distal joints associated with an increase in movements of proximal joints (Bonnard, Sirin, Oddsson, & Thorstensson, 1994). Hence, in the bipedal stance, adaptation capabilities of the postural system may limit the disturbance induced by both fatiguing tasks. The data from the spectral analysis showed a higher spectral energy in the three frequency bands after both the unilateral and bilateral fatiguing tasks. This suggests that the contribution of the different neuronal loops is increased under both muscle fatigue conditions to compensate sensory disturbances and thus limit postural sway (Bizid, Jully, et al., 2009; Chaubet et al., 2011; Paillard, Margnes, et al., 2010; Paillard, Maitre, Chaubet, Borel, 2010; Paillard, Chaubet, Maitre, Dumitrescu, Borel, 2010). These compensatory mechanisms are not sufficient to preserve the efficiency of the postural system since postural stability is affected, but they are sufficient to prevent the occurrence of differences in the postural disturbance between bilateral fatigue and unilateral fatigue. The alteration of the CAR for both fatiguing tasks reveals central disturbances that can result from changes related to intrinsic cortical processes and/or descending drive and/or excitability of spinal motoneurons (Taylor & Gandevia, 2008; Taylor, Todd, & Gandevia, 2006). These disturbances could

360

T. Paillard et al. / Human Movement Science 32 (2013) 353–362

affect the voluntary motor command which would be compensated by an increased contribution of cognitive processes in postural control under fatigue condition to limit/counteract its disturbing effects (Paillard, 2012). Since the alteration of the CAR was equally impaired after both fatiguing tasks, one can expect similar central disturbances under unilateral and bilateral muscle fatigue. These results are not in accordance with those of Matkowski, Place, Martin, and Lepers (2011), which show that the voluntary activation level is more affected for unilateral than for bilateral muscle fatigue. However, the fatigue protocol of the study by Matkowski et al. (2011) differed from the present ones by the nature of muscle contractions (continuous vs intermittent, respectively) and the strength loss value (37% vs 22%, respectively). Finally, a central integration of erroneous sensory information related to disturbance of the proprioception (myotatic, tendineous and articular information) (Paillard, 2012) as well as an alteration of the body scheme (Kanekar et al., 2008; Schieppati, Nardone, & Schmid, 2003) could constitute other causes of postural instability under fatigue condition. However, other complementary tests would be necessary to specify the part of these different perturbations in the two fatiguing tasks. This study suggests that unilateral muscle fatigue is enough to disturb motor output and sensory input of the postural system as well as central drive, but it disturbs them as bilateral muscle fatigue since the possible disturbances in the postural system above evoked cannot be differentiated between the two types of muscle fatigue. 4.2. Different changes of the mean postural position xCOP shifted towards the side of the fatigued leg after the unilateral fatiguing task, whereas it did not shift after the bilateral fatiguing task. The postural bias induced by unilateral muscle fatigue could result from an increased contribution of the non-fatigued leg in the regulation of posture. Previous studies reinforce this hypothesis since they showed that spatio-temporal parameters of COP were more altered under the non-fatigued leg than under the fatigued leg, due to compensatory contralateral strategies, which are of a sensory and motor nature (Berger et al., 2010, 2011; Vuillerme & Boisgontier, 2010; Vuillerme et al., 2009). These authors reported an increased contribution of the foot sensors of the non-fatigued leg as well as an increased electromyographic activity of the tibialis anterior of the non-fatigued leg to preserve bipedal postural control. Moreover, Berger et al. (2011) also suggested that the shift towards the side of the fatigued leg would enable to limit the sensation of fatigue and/or to attenuate the painful sensations. In conclusion, unilateral and bilateral fatiguing tasks of quadriceps femoris similarly affect the postural stability while only the unilateral fatiguing task alters the mean lateral postural position. Hence, patients or healthy subjects, who completed a repetitive or long-lasting unilateral motor task that generates muscle fatigue, would risk modifying their postural position more than those who performed the same task on the two sides. In the long run, unilateral tasks are likely to engender disorders of postural statics more than bilateral tasks, particularly in people who work in the bipedal stance in the professional context. Acknowledgment The authors thank all the subjects for their helpful cooperation and Vincent Chaubet for his help in the data acquisition. References Bernard-Demaze, L., Dumitrescu, M., Jimeno, P., Borel, L., & Lacour, M. (2009). Age-related changes in posture control are differentially affected by postural and cognitive task complexity. Current Aging Science, 2, 139–149. Berger, L. L., Regueme, S. C., & Forestier, N. (2010). Unilateral lower limb muscle fatigue induces bilateral effects on undisturbed stance and muscle EMG activities. Journal of Electromyography and Kinesiology, 20, 947–952. Berger, L., Regueme, S. C., & Forestier, N. (2011). Effects of unilateral fatigue of triceps surae on undisturbed stance. Clinical Neurophysiology, 41, 61–65. Bisson, J. E., Chopra, S., Azzi, E., Morgan, M., & Bilodeau, M. (2010). Acute effects of fatigue of the plantarflexor muscles on different postural tasks. Gait and Posture, 32, 482–486. Bizid, R., Jully, J. L., Gonzalez, G., François, Y., Dupui, P., & Paillard, T. (2009). Effets of fatigue induced by neuromuscular electrical stimulation on postural control. Journal of Science and Medicine in Sport, 12, 60–66.

T. Paillard, L. Borel / Human Movement Science 32 (2013) 353–362

361

Bizid, R., Margnes, E., François, Y., Gonzalez, G., Jully, J. L., Dupui, P., et al (2009). Effects of knee and ankle muscle fatigue on postural control in the unipedal stance. European Journal of Applied Physiology, 106, 375–380. Bonnard, M., Sirin, A. V., Oddsson, L., & Thorstensson, A. (1994). Different strategies to compensate for the effects of fatigue revealed by neuromuscular adaptation processes in human. Neuroscience Letters, 166, 101–105. Boyas, S., Remaud, A., Bisson, E. J., Cadieux, S., Morel, B., & Bilodeau, M. (2011). Impairment in postural control is greater when ankle plantarflexors and dorsiflexors are fatigued simultaneously than when fatigued separately. Gait and Posture, 34, 254–259. Caron, O. (2003). Effects of local fatigue of the lower limbs on postural control and postural stability in standing posture. Neuroscience Letters, 340, 83–86. Chabran, E., Maton, B., & Fourment, A. (2002). Effects of postural muscle fatigue on the relation between segmental posture and movement. Journal of Electromyography and Kinesiology, 12, 67–79. Chaubet, V., Maitre, J., Cormery, B., & Paillard, T. (2011). Stimulated and voluntary fatiguing contractions of quadriceps femoris similarly disturb postural control in the bipedal stance. European Journal of Applied Physiology. http://dx.doi.org/10.1007/ s00421-011-2168-9. Corbeil, P., Blouin, J. S., Bégin, F., Nougier, V., & Teasdale, N. P. (2003). Perturbation of the postural control system induced by muscular fatigue. Gait and Posture, 18, 92–100. De Luca, C. J., & Mambrito, B. (1987). Voluntary control of motor units in human antagonist muscles: Coactivation and reciprocal activation. Journal of Neurophysiology, 58, 525–542. Duchateau, J., Semmler, J. G., & Enoka, R. M. (2006). Training adaptations in the behavior of human motor units. Journal of Applied Physiology, 101, 1766–1775. Granacher, U., Gruber, M., Förderer, D., Strass, D., & Gollhofer, A. (2010). Effects of ankle fatigue on functional reflex activity during gait perturbations in young and elderly men. Gait and Posture, 32, 107–112. Herrmann, C. M., Madigan, M. L., Davidson, B. S., & Granata, K. P. (2006). Effect of lumbar extensor fatigue on paraspinal muscle reflexes. Journal of Electromyography and Kinesiology, 16, 637–641. Hunter, S. K., Critchlow, A., & Enoka, R. M. (2004). Influence of aging on sex differences in muscle fatigability. Journal of Applied Physiology, 97, 1723–1732. Kanekar, N., Santos, M. J., & Aruin, A. S. (2008). Anticipatory postural control following fatigue of postural and focal muscles. Clinical Neurophysiology, 119, 2304–2313. Kent-Braun, J. A., & Le Blanc, R. (1996). Quantitation of central activation failure during maximal voluntary contractions in humans. Muscle and Nerve, 19, 861–869. Ledin, T., Fransson, P. A., & Magnusson, M. (2004). Effects of postural disturbances with fatigued triceps surae muscles or with 20% additional body weight. Gait and Posture, 19, 184–193. Matkowski, B., Place, N., Martin, A., & Lepers, R. (2011). Neuromuscular fatigue differs following unilateral vs bilateral sustained submaximal contractions. Scandinavian Journal of Medicine and Science in Sports, 21, 268–276. Nelson, J. K., & Johnson, B. L. (1973). Effects of local and general fatigue on static balance. Perceptual and Motor Skills, 37, 615–618. Paillard, T. (2012). Effects of general and local fatigue on postural control: A review. Neuroscience Biobehavioral Review, 36, 162–176. Paillard, T., Bizid, R., & Dupui, P. (2007). Do sensorial manipulations affect subjects differently depending on their postural abilities? British Journal of Sports Medicine, 41, 435–438. Paillard, T., Chaubet, V., Maitre, J., Dumitrescu, M., & Borel, L. (2010). Disturbance of contralateral unipedal postural control after stimulated and voluntary contractions of the ipsilateral limb. Neuroscience Research, 68, 301–306. Paillard, T., Lafont, C., Costes-Salon, M. C., & Dupui, P. (2004). Effects of brisk walking on static and dynamic balance, locomotion, body composition, and aerobic capacity in ageing healthy active men. International Journal of Sports Medicine, 25, 539–546. Paillard, T., Maitre, J., Chaubet, V., & Borel, L. (2010). Stimulated and voluntary fatiguing contractions of quadriceps femoris differently disturb postural control. Neuroscience Letters, 477, 48–51. Paillard, T., Margnes, E., Maitre, J., Chaubet, V., François, Y., Jully, J. L., et al (2010). Electrical stimulation superimposed onto voluntary muscular contraction reduces deterioration of both postural control and quadriceps femoris muscle strength. Neuroscience, 165, 1471–1475. Paillard, T., Noé, F., Passelergue, P., & Dupui, P. (2005). Electrical stimulation superimposed onto voluntary muscular contraction. Sports Medicine, 35, 951–966. Pline, K. M., Madigan, M. L., & Nussbaum, M. A. (2006). Influence of fatigue time and level on increases in postural sway. Ergonomics, 49, 1639–1648. Schieppati, M., Nardone, A., & Schmid, M. (2003). Neck muscle fatigue affects postural control in man. Neuroscience, 121, 277–285. Springer, B. K., & Pincivero, D. M. (2009). The effects of localized muscle and whole-body fatigue on single-leg balance between healthy men and women. Gait and Posture, 30, 50–54. Tardieu, C., Dumitrescu, M., Giraudeau, A., Blanc, J. L., Cheynet, F., & Borel, L. (2009). Dental occlusion and postural control in adults. Neuroscience Letters, 450, 221–224. Taylor, J. L., Todd, G., & Gandevia, S. C. (2006). Evidence for a supraspinal contribution to human muscle fatigue. Clinical and Experimental Pharmacology and Physiology, 33, 400–405. Taylor, J. L., & Gandevia, S. C. (2008). A comparison of central aspects of fatigue in submaximal and maximal voluntary contractions. Journal of Applied Physiology, 104, 542–550. Vuillerme, N., & Boisgontier, M. (2010). Changes in the relative contribution of each leg to the control of quiet two-legged stance following unilateral plantar-flexor muscles fatigue. European Journal of Applied Physiology, 110, 207–213. Vuillerme, N., Sportbert, C., & Pinsault, N. (2009). Postural adaptation to unilateral hip muscle fatigue during human bipedal standing. Gait and Posture, 30, 122–125. Windhorst, U. (2007). Muscle proprioceptive feedback and spinal networks. Brain Research Bulletin, 73, 155–202. Wojcik, L. A., Nussbaum, M. A., Lin, D., Shibata, P. A., & Madigan, M. L. (2011). Age and gender moderate the effects of localized muscle fatigue on lower extremity joint torques used during quiet stance. Human Movement Science, 30, 574–583.

362

T. Paillard et al. / Human Movement Science 32 (2013) 353–362

Yiou, E., Heugas, A. M., Mezaour, M., & Le Bosec, S. (2009). Effect of lower limb muscle fatigue induced by high-level isometric contractions on postural maintenance and postural adjustments associated with bilateral forward-reach task. Gait and Posture, 29, 97–101. Zhang, L. Q., & Rymer, W. Z. (2001). Reflex and intrinsic changes induced by fatigue of human elbow extensor muscles. Journal of Neurophysiology, 86, 1086–1094.