muscle groups with sustained isometric contractions

Comparison of neuromuscular adjustments associated with sustained isometric contractions of four different muscle groups

Daria Neyroud, Jennifer Rüttimann, Anne F. Mannion, Guillaume Y. Millet, Nicola A. Maffiuletti, Bengt Kayser and Nicolas Place J Appl Physiol 114:1426-1434, 2013. First published 7 March 2013; doi: 10.1152/japplphysiol.01539.2012 You might find this additional info useful... This article cites 78 articles, 31 of which you can access for free at: http://jap.physiology.org/content/114/10/1426.full#ref-list-1

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J Appl Physiol 114: 1426–1434, 2013. First published March 7, 2013; doi:10.1152/japplphysiol.01539.2012.

Comparison of neuromuscular adjustments associated with sustained isometric contractions of four different muscle groups Daria Neyroud,1 Jennifer Rüttimann,1 Anne F. Mannion,2 Guillaume Y. Millet,3 Nicola A. Maffiuletti,4 Bengt Kayser,1 and Nicolas Place1 1

Institute of Movement Sciences and Sports Medicine, University of Geneva, Geneva, Switzerland; 2Spine Center, Schulthess Clinic, Zürich, Switzerland; 3Université de Lyon, Saint-Etienne, France; and 4Neuromuscular Research Laboratory, Schulthess Clinic, Zurich, Switzerland Submitted 21 December 2012; accepted in final form 28 February 2013

endurance time; fatigue; maximal voluntary contraction; contractile properties; surface electromyography

of a sustained submaximal isometric contraction (i.e., endurance time, ET) depends on physiological factors such as relative force level (30, 35), muscle fiber type composition (16, 51, 77), muscular activation strategy (6, 19, 38), muscle size (36), and length (54, 58) but also depends on psychological factors such as motivation, mood, and expectation (24). Whereas the task dependency of ET is well documented (23, 25, 26), little is known about muscle fatigue characteristics induced by a given task sustained until failure in different muscle groups, in the same individuals. Frey-Law and Avin (28) suggested that no single fatigue model applies to all

TIME TO TASK FAILURE

Address for reprint requests and other correspondence: N. Place, Institute of Movement Sciences and Sports Medicine, Faculty of Medicine, Univ. of Geneva, Rue du Conseil Général 10, 1205 Geneva, Switzerland (e-mail: [email protected]). 1426

muscles. Their meta-analysis showed large differences in ET depending on the muscle group considered, especially at low contraction intensities. However, it is unknown whether the extent of maximal voluntary contraction (MVC) force loss immediately after task failure (32) differs between muscle groups for a given subject. The present study was thus designed to compare the extent and the mechanisms underlying the decrease in MVC force between different muscle groups subjected to a similar fatiguing task until failure. Previous work showed that the loss of MVC force after a fatiguing task with a given muscle group remained similar even though performed in different conditions [different feedback types (60), muscle lengths (58), or load types (37, 38)]. These results suggest a mechanism for neuromuscular reserve at task failure (as illustrated by submaximal motor unit recruitment/firing rate at task failure of a sustained submaximal contraction) as proposed by several authors (3, 48, 49, 72). In accordance with this principle, we first hypothesized that, despite different ET, the MVC force decline from a sustained contraction until task failure would be similar for different muscle groups. We further expected that the MVC force decline immediately after task failure would be considerably less than 50% of MVC, even though the sustained contraction was performed at 50% MVC force; in other words, there would still be a reserve in muscle maximal force-generating capacity at the point of task failure. Second, as it has previously been shown that peripheral impairments were more pronounced after high-force-contraction tasks (10, 50), whereas central alterations were found to increase with task duration (7, 50, 78), we hypothesized that, despite a similar decrease in MVC force for the different muscle groups, the relative contribution of central and peripheral mechanisms would be mainly determined by the duration of the sustained contraction. The purpose of the study was to compare endurance time and the associated neuromuscular adjustments when four muscle groups sustained an isometric contraction at 50% MVC force for as long as possible. Two lower [plantar flexors (PF) and knee extensors (KE)] and two upper limb [elbow flexors (EF) and thumb adductor (THU)] muscle groups were evaluated. MATERIALS AND METHODS

Subjects Thirteen healthy and physically active men (25 ⫾ 2 yr, 177 ⫾ 7 cm, 72 ⫾ 3 kg) volunteered to participate in the study after having been informed of the experimental procedures and possible risks. They were all recreationally active but were not involved in any structured training program. The study protocol was approved by the

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Neyroud D, Rüttimann J, Mannion AF, Millet GY, Maffiuletti NA, Kayser B, Place N. Comparison of neuromuscular adjustments associated with sustained isometric contractions of four different muscle groups. J Appl Physiol 114: 1426 –1434, 2013. First published March 7, 2013; doi:10.1152/japplphysiol.01539.2012.—The extent and characteristics of muscle fatigue of different muscle groups when subjected to a similar fatiguing task may differ. Thirteen healthy young men performed sustained contractions at 50% maximal voluntary contraction (MVC) force until task failure, with four different muscle groups, over two sessions. Per session, one upper limb and one lower limb muscle group were tested (knee extensors and thumb adductor, or plantar and elbow flexors). Changes in voluntary activation level and contractile properties were derived from doublet responses evoked during and after MVCs before and after exercise. Time to task failure differed (P ⬍ 0.05) between muscle groups (220 ⫾ 64 s for plantar flexors, 114 ⫾ 27 s for thumb adductor, 77 ⫾ 25 s for knee extensors, and 72 ⫾ 14 s for elbow flexors). MVC force loss immediately after voluntary task failure was similar (⫺30 ⫾ 11% for plantar flexors, ⫺37 ⫾ 13% for thumb adductor, ⫺34 ⫾ 15% for knee extensors, and ⫺40 ⫾ 12% for elbow flexors, P ⬎ 0.05). Voluntary activation was decreased for plantar flexors only (from 95 ⫾ 5% to 82 ⫾ 9%, P ⬍ 0.05). Potentiated evoked doublet amplitude was more depressed for upper limb muscles (⫺59.3 ⫾ 14.7% for elbow flexors and ⫺60.1 ⫾ 24.1% for thumb adductor, P ⬍ 0.05) than for knee extensors (⫺28 ⫾ 15%, P ⬍ 0.05); no reduction was found in plantar flexors (⫺7 ⫾ 12%, P ⬎ 0.05). In conclusion, despite different times to task failure when sustaining an isometric contraction at 50% MVC force for as long as possible, diverse muscle groups present similar loss of MVC force after task failure. Thus the extent of muscle fatigue is not affected by time to task failure, whereas this latter determines the etiology of fatigue.

Neuromuscular Adjustments in Different Muscle Groups

120s

2s

2s 2s 60s

60s

Antag MVC

Antag MVC

The dominant side, as determined by the revised Waterloo questionnaire (22), was evaluated except for the THU, in which the right thumb was always used (dominant for 11 out of 13 subjects) due to technical constraints. Evoked contractions. A high-voltage (400 V maximum) constantcurrent stimulator (DS7AH; Digitimer, Hertfordshire, UK) was used to deliver single and paired electrical stimuli. For KE, the cathode (5-cm diameter, Dermatrode; American Imex, Irvine, CA) and the anode (5 ⫻ 10 cm; Compex, Ecublens, Switzerland) were placed over the femoral nerve at the femoral triangle level beneath the inguinal ligament and on the lower part of the gluteal fold opposite to the cathode, respectively (53). For the PF, the cathode (1-cm diameter, Meditrace 100 Kendall; Tyco, Markham, Ontario, Canada) was placed in the popliteal fossa (over the tibial nerve), and the anode (5 ⫻ 10 cm, Compex) was located on the anterior surface of the knee (57). For the EF, the cathode (1-cm diameter, Kendall Meditrace 100) was positioned over the brachial plexus in the supraclavicular fossa and the anode (5 ⫻ 10 cm, Compex) on the acromion (68). Because stimulation of the brachial plexus led to contraction of both the agonist and antagonist muscles, we also stimulated the muscle belly of the biceps via a cathode located midway between the anterior edge of the deltoid and the proximal elbow crease and an anode placed over the bicipital tendon (68); both the anode and the cathode measured 5 ⫻ 5 cm (Compex). For the THU, the cathode and the anode (4-mm plug barhandle stimulator; SPES Medica, Genova, Italy) were located over the ulnar nerve anteriorly and just proximal to the wrist (33). Supramaximal stimulation intensity level was determined by increasing the applied current until maximal twitch and corresponding M-wave amplitudes were obtained. This intensity was then increased by 10% and kept constant throughout the experiment. Such supramaximal stimulation intensity, as used in previous studies (46, 53, 56), limits the discomfort associated with the stimulation compared with higher supramaximal levels. Pulse width was set at 0.1 ms for the upper limbs (68) and at 1 ms for the lower limbs (53, 57). Force recordings. During all fatiguing tasks, isometric force feedback was displayed as a line on a computer screen. All force signals were recorded at 1 kHz using an AD conversion system (MP150; BIOPAC, Goleta, CA). KE. Voluntary and evoked force developed by the KE and knee flexors was recorded using an isometric ergometer consisting of a custom-built chair equipped with a strain gauge (STS 2500 N, sensi-

PS10

Fatiguing contraction: 50% MVC

60s

MVC

MVC

PS100

Data Collection

Single stimulations

Fig. 1. Experimental design scheme. Antag, antagonist muscles; MVC, maximal voluntary contraction; PS100, 100-Hz paired stimuli; PS10, 10-Hz paired stimuli.

J Appl Physiol • doi:10.1152/japplphysiol.01539.2012 • www.jappl.org


All subjects were familiarized with the different ergometers as well as voluntary and electrically evoked muscle contractions at least 24 h before the first experimental session. This was done as Button and Behm (18) reported that nonhabituated subjects produced a smaller MVC force when they were told that electrical stimulation might be sent compared with when subjects knew that no stimulation would be evoked. Full voluntary activation before the fatiguing task was not obtained in our subjects for KE but was obtained in two subjects for PF, three subjects for EF, and four subjects for THU, indicating that stimulus anticipation could be avoided even after a single familiarization session. Furthermore, questions regarding the experimental protocol were answered during this session. The experimental procedure consisted of the subjects reporting to the laboratory on two separate occasions (for a given subject performed at the same time during the day) separated by at least 48 h. One upper and one lower limb muscle group were tested within a single session. Subjects either performed the PF and EF or the KE and THU tasks. A 50-min resting period was given to the subject between the tasks to limit the potential influence of the first fatiguing task on the second one, performed with a different muscle group. This 50-min recovery period was longer than those reported in previous studies with comparable protocols [10 min of recovery in Smolander et al. (69), 20 min in Avin et al. (6), and 30 – 60 min in Williams (76)]. The order of the two sessions was randomized, and the order between tasks within a session was counterbalanced between subjects. Each session began with a warm-up of 8 to 10 submaximal voluntary isometric contractions (4 –5 s) between 20 and 80% of the estimated MVC force, followed by a 1-min rest before starting the protocol. The experimental protocol was as follows (Fig. 1). Prefatigue tests. This test was comprised of the following: two MVCs (duration of ⬃4 s) of the antagonist muscles separated by 1 min of rest; two or three MVCs of the agonist muscles with superimposed supramaximal paired stimuli (doublet) at 100 Hz and followed (2 s intervals) by paired stimuli at 100 Hz and 10 Hz (hereafter referred to as PS100 and PS10, respectively), delivered in a relaxed state. MVCs were separated by 1-min rest, and no more than 5% variation between the two highest MVCs was tolerated (typically 2 to 4 MVCs were done). Then we conducted three single supramaximal stimulations at rest, interspaced by 2 s, to evoke M waves and twitches (3 more single stimulations were delivered to obtain the M wave in the EF). This was followed by 2 min of rest. Fatiguing task. We conducted sustained submaximal voluntary isometric contraction of the agonist muscles at 50% MVC force until task failure (i.e., inability of the subject to maintain the target force for more than 3 consecutive seconds despite strong verbal encouragements).

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Postfatigue tests (no interruption of the contraction between the fatiguing task and the agonist MVC). We conducted one MVC of the agonist muscles with superimposed supramaximal PS100 followed (2-s intervals) by PS100 and PS10 at rest; three single supramaximal stimulations at rest, interspaced by 2 s, to evoke M waves and twitches (3 more single stimulations were delivered to obtain the M wave in the EF); and one MVC of the antagonist muscles (Fig. 1).

Antag MVC

Experimental Protocol

Neyroud D et al.

MVC

Ethics Committee of the University Hospitals of Geneva (protocol 10-238) and conformed to the declaration of Helsinki. Before participation, each subject gave written informed consent.

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Data Analysis Force data. Isometric MVC force was considered as the peak force attained during the MVC. Maximal voluntary activation level (VAL) during MVCs was quantified as follows: VAL ⫽ [1 ⫺ (superimposed PS100 amplitude/resting PS100 amplitude)] ⫻ 100 (2). A correction was consistently applied to this equation when the superimposed doublet was elicited slightly before or after the actual peak force during a MVC (71). In accordance with Behm et al. (8), prefatigue VAL was maximal (i.e., 100%) in several subjects for PF, EF, and THU, whereas none of our subjects maximally activated their KE. Pre- and postfatigue doublet and twitch amplitudes were measured. Resting PS100 and PS10 amplitudes were analyzed for the trials, yielding the highest MVC in the prefatigue. The PS10/PS100 ratio was calculated both pre- and postfatigue as an index of low-frequency fatigue (74). Mean force was quantified for every 10% period of endurance time. EMG data. EMG signals recorded during the MVCs with the greatest force (EMGmax) were quantified as root mean square (RMS) amplitudes for a 500-ms interval around maximum force (250-ms periods either side of peak force during MVC) for both agonist and antagonist muscles. M-wave properties (peak-to-peak amplitude and duration) were measured from the EMG response following the greatest MVC obtained by single stimulation of the motor nerve. For EF motor nerve stimulation, M-wave properties were averaged from the three single stimuli (following the greatest MVC) to ensure data accuracy, as the twitch and M-wave responses were produced via two different stimulation methods. The RMS/M ratio (EMGmax divided by M-wave amplitude) was calculated as an index of muscle activation (65). The EMG RMS was quantified for every 10% period of endurance time. Antagonist coactivation was calculated according to the following equation: Coactivation(%) ⫽ (RMS of the antagonist during agonist contraction/RMS of the antagonist when acting as an agonist during MVC) ⫻ 100. RPE. RPE was analyzed at 25, 50, 75, and 100% of the endurance time (53), and the rate of increase was calculated using the linear mixed effect model. Statistical Analysis Depending on the outcome of the normality test, paired t-tests or Wilcoxon signed rank tests were used to compare prefatigue to postfatigue changes in MVC force, VAL, and M-wave characteristics for the four muscle groups. As absolute force values cannot be compared between the different muscle groups, one-way repeatedmeasures ANOVA was used to compare the relative changes of dependent variables between the four muscle groups. One-way ANOVA was also used to test for differences between pre- and postfatigue RMS/M ratio. As conditions for parametric statistics were not met, one-way Friedman ANOVA was used to compare the ET for the different muscle groups as well as pre- and postfatigue RMS/M ratio for adductor pollicis, vastus medialis, and brachioradialis muscles. One-way Friedman ANOVA was also used for the force time course throughout the fatiguing exercise. Post hoc analyses (StudentNewman-Keuls) were used to test for differences among pairs of means when appropriate. Linear mixed-effect model was used to analyze EMG, force, and RPE data collected during the fatiguing contractions. Pearson’s correlation coefficients were calculated between selected pairs of variables. The ␣-level for statistical significance was set to P ⬍ 0.05. Sigmaplot software for Windows (version 11; Systat, Chicago, IL) and R software for the linear mixed effect model (version 2.13.1, R Foundation for Statistical Computing, Vienna, Austria; www.R-project.org) were used for the statistical analyses. Data are reported as means ⫾ SD in text and the tables and means ⫾ SE in figures.



tivity 2.0005 mV/V and 0.0017 V/N; SWJ, Shenzhen, China). The strain gauge was attached to the chair on one end and securely strapped to the ankle with a custom-made mold. Subjects were seated with a knee angle of 90° and a trunk-thigh angle of 100° (180° ⫽ full extension). Extraneous movements of the upper body were limited by two crossover shoulder harnesses and a belt across the lower abdomen. PF. Voluntary and evoked force developed by the PF and dorsiflexors was recorded using an isometric ergometer consisting of a custom-built chair equipped with a strain gauge (S2 1000 N, sensitivity 2 mV/V and 0.0043 V/N; HBM, Darmstadt, Germany) fixed on a pedal. The foot was strapped to the pedal at the ankle as well as at the metatarsi level. Ankle and knee joints were fixed at 90°, and the trunk-thigh angle was 100°. To limit the contribution of muscle groups other than PF and dorsiflexors and to optimize force recordings, the upper leg was clamped down to the chair just proximal to the knee. As for the KE, harnesses limited upper body movements. EF. Voluntary and evoked force developed by the EF and elbow extensors were recorded using a custom-built ergometer equipped with a strain gauge (SAS 2000 N, sensitivity 1.998 mV/V and 0.0014 V/N; SWJ) and custom-made molds to support both parts of the arm. Subjects were seated with the arm flexed at 90° and the forearm vertical and supinated (for elbow flexion) or pronated (for elbow extension) with the subject’s hand holding an adjustable handle connected to the strain gauge. The shoulder-trunk angle was 90° in the sagittal axis. THU. An isometric ergometer consisting of a mold for the front arm and equipped with a strain gauge (Z8 500 N, sensitivity 2 mV/V and 0.0083 V/N; HBM) attached to a thumb support was used to record voluntary and evoked force of THU. Straps were used to minimize hand and arm contribution to force production. The forearm was at 45° from full supination toward full pronation. The thumb’s proximal phalanx rested on a support connected to the strain gauge. Elbow and shoulder were positioned at 90° in the sagittal axis, and the thumb’s adduction angle was determined as the angle allowing optimal force production for each subject during the familiarization session. Electromyographic recordings. Electromyographic (EMG) activity from the agonist KE (vastus lateralis, vastus medialis, and rectus femoris), PF (soleus, gastrocnemius lateralis, and gastrocnemius medialis), EF (biceps brachii and brachioradialis), as well as the respective antagonist muscles (biceps femoris, tibialis anterior, and triceps brachii) was recorded. Only EMG activity from the agonist adductor pollicis was recorded for the exercise involving thumb adduction. For all muscles, EMG activity was recorded with pairs of silver chloride (Ag/AgCl) circular (recording diameter of 1 cm) surface electrodes (Kendall Meditrace 100) positioned lengthwise over the middle of the muscle belly [according to SENIAM recommendations, (34)] with an interelectrode (center-to-center) distance of 2 cm. The reference electrodes were placed over nearby bony protuberances. Low resistance between the two electrodes (⬍ 10 k⍀) was consistently obtained by cleaning and lightly abrading the skin. EMG signals were amplified with a gain of 1,000, filtered with a bandwidth frequency between 10 Hz and 500 Hz, digitized at a sampling frequency of 2 kHz and recorded by the AD conversion system. Isometric force and EMG data were stored and analyzed offline with commercially available software (AcqKnowledge, BIOPAC Systems). Rate of perceived exertion. As an index of perceived effort, the rate of perceived exertion (RPE) was asked regularly every ⬃15 s during each of the fatiguing tasks using a scale from 0 to 10 (15). It should be noted that strong verbal encouragement was given to the subjects throughout the experiment.

•

Neuromuscular Adjustments in Different Muscle Groups RESULTS

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end of the task. The rate of increase was lower for PF compared with the other muscle groups (P ⬍ 0.01).

Endurance Time ET differed significantly (P ⬍ 0.05) between the different muscle groups, except between KE and EF (Table 1). ET from the different muscle groups did not correlate, e.g., individuals with shorter ETs for the KE did not necessarily have shorter ETs for the PF (Table 1). Neuromuscular Adaptations During the Fatiguing Task

MVC force. At task failure, there was a significant reduction in MVC force for all muscle groups (P ⬍ 0.001) (KE: from 430.2 ⫾ 83.2 to 276.2 ⫾ 53.7 N; PF: from 951.6 ⫾ 161.4 to 661.8 ⫾ 143.2 N; EF: from 219.2 ⫾ 35.8 to 132.7 ⫾ 36.2 N; THU: from 142.1 ⫾ 19.5 to 88.5 ⫾ 14.8 N). The relative decrease in MVC force was similar between the different muscle groups (P ⬎ 0.05; Table 1). MVC force of EF antagonists (i.e., elbow extensors) also decreased after the fatiguing task (from 161.9 ⫾ 37.3 to 146.9 ⫾ 40.0 N, P ⬍ 0.01). No antagonist MVC force alteration was found for KE and PF (P ⬎ 0.05). Additionally, comparing fresh to fatigued states, elbow extensor coactivation increased from 15.4 ⫾ 3.8% to 32.9 ⫾ 43.8% (P ⬍ 0.05). No changes in coactivation were observed for the other muscle groups (P ⬎ 0.05). Voluntary activation level. At task failure, PF VAL decreased from 95 ⫾ 5% to 82 ⫾ 9% (⫺13 ⫾ 6%, P ⬍ 0.001, Table 1). No alteration was found in KE, EF, and THU (from 89 ⫾ 12% to 92 ⫾ 8%, from 96 ⫾ 3% to 91 ⫾ 13%, and from 95 ⫾ 6% to 92 ⫾ 8%, for prefatigue to postfatigue, respectively, P ⬎ 0.05). Furthermore, maximal RMS/M ratio was found to be reduced only for the gastrocnemius medialis muscle (⫺17.8 ⫾ 38.2%, P ⬍ 0.05) but not for the other muscles (see Table 2, P ⬎ 0.05). Peripheral fatigue. A greater decrease in electrically evoked force (single twitch, PS10 and PS100 amplitudes) was observed in EF and THU compared with KE (P ⬍ 0.05), whereas the only contractile alteration in PF was a slight decrease in PS10 amplitude (P ⬍ 0.01, Table 3). The PS10/PS100 ratio decreased for KE (⫺20.7 ⫾ 13.0%, P ⬍ 0.001), PF (⫺5.8 ⫾ 6.4%, P ⬍ 0.01), and EF (⫺42.4 ⫾ 14.8%, P ⬍ 0.01) but not for THU (⫺7.9 ⫾ 38%, P ⬎ 0.05). The decrease was greater for EF compared with PF and KE (P ⬍ 0.05, Table 3). M-wave properties remained relatively well preserved at task failure, except for increased soleus and decreased gastrocnemius medialis amplitudes and increased rectus femoris and soleus durations (see Table 2). DISCUSSION

We compared the extent and characteristics of muscle fatigue induced by a similar fatiguing task in four different

Table 1. ET and correlation coefficients for the various pairwise comparisons of the tested muscles, MVC force, and VAL loss ET, s Pairwise comparison Pairwise comparison Pairwise comparison Pairwise comparison MVC force loss, % VAL loss, %

with with with with

KE ET, r PF ET, r EF ET, r THU ET, r

KE

PF

EF

THU

76.5 ⫾ 24.6 — ⫺0.26 0.11 0.47 ⫺34.0 ⫾ 15.4† ⫺5.0 ⫾ 10.0

220.4 ⫾ 63.7* ⫺0.26 — 0.025 ⫺0.21 ⫺30.2 ⫾ 11.0† ⫺13.3 ⫾ 6.2†

71.9 ⫾ 14.4 0.11 0.025 — 0.079 ⫺39.8 ⫾ 11.7† ⫺5.7 ⫾ 13.1

113.8 ⫾ 26.5* 0.47 ⫺0.21 0.079 — ⫺36.8 ⫾ 12.8† ⫺2.1 ⫾ 11.1

Values are means ⫾ SD. *Significant differences with the other muscle group endurance times (ETs) (P ⬍ 0.01). †Significant decrease (P ⬍ 0.001). None of the pairwise comparisons was significant (P ⬎ 0.05). MVC, maximal voluntary contraction; VAL, voluntary activation level; r, Pearson correlation coefficient; PF, plantar flexors; KE, knee extensors; EF, elbow flexors; THU, thumb adductor. J Appl Physiol • doi:10.1152/japplphysiol.01539.2012 • www.jappl.org


Force. For all muscle groups, the target force remained constant (⬃50% MVC) until 90% ET (P ⬎ 0.05). A slight drop (P ⬍ 0.05) was observed in the last 10% of ET for all muscles, leading to comparable force values of 44.9 ⫾ 2.1% prefatigue MVC for KE, 45.7 ⫾ 3.5% MVC for PF, 43.3 ⫾ 3.6% MVC for EF, and 45.9 ⫾ 2.1% MVC for THU. EMG activity. For the KE, vastus lateralis and vastus medialis RMS increased similarly (P ⬎ 0.05) from 41.1 ⫾ 8.2 and 39.9 ⫾ 8.1% EMGmax up to 56.6 ⫾ 14.2 and 55.8 ⫾ 11.9% EMGmax, respectively (P ⬍ 0.001, Fig. 2). Conversely, rectus femoris RMS remained constant throughout the fatiguing task (P ⬎ 0.05). At task failure, rectus femoris RMS was lower than vastus lateralis activity (P ⬍ 0.01). For the PF, gastrocnemius lateralis and gastrocnemius medialis RMS increased similarly (P ⬎ 0.05) from 24.4 ⫾ 12.3 and 26.5 ⫾ 14.4% EMGmax up to 58.0 ⫾ 22.5% and 55.7 ⫾ 16.2% EMGmax, respectively (P ⬍ 0.001, Fig. 2). The soleus RMS remained unchanged throughout the task (P ⬎ 0.05). As a consequence, soleus RMS started higher and ended lower than gastrocnemius lateralis and gastrocnemius medialis RMS (P ⬍ 0.001). For the EF, biceps brachii and brachioradialis EMG activity increased from 36.1 ⫾ 13.4 and 59.1 ⫾ 12.2% EMGmax up to 63.8 ⫾ 24.3 and 76.7 ⫾ 24.6% EMGmax, respectively (P ⬍ 0.001, Fig. 2). Biceps brachii started at a lower value (P ⬍ 0.001) but ended at the same level as brachioradialis (P ⬎ 0.05). Adductor pollicis. RMS increased from 49.7 ⫾ 19.4 to 72.6 ⫾ 31.2% EMGmax (P ⬍ 0.05, Fig. 2). The coactivation level increased during the fatiguing task in the three muscle groups considered (from 3.9 ⫾ 2.6% to 4.6 ⫾ 2.5% for biceps femoris, from 5.0 ⫾ 5.4% to 7.6 ⫾ 7.0% for tibialis anterior, and from 5.8 ⫾ 1.5% to 15.2 ⫾ 12.9% for triceps brachii, P ⬍ 0.05) (Fig. 2). RPE. RPE increased for all muscle groups (0.071/%ET for PF, 0.093/%ET for EF, 0.092/%ET for THU and 0.080/%ET for KE, P ⬍ 0.001), and RPE reached maximal levels at the

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•

Knee extensors 70

†††

50 40

*** (VL,VM)

30

*** (GL,GM)

60

VL VM RF BF

20 10

†††

50 40

§§ 30 20

*

10

0

Sol GL GM TA

0 0

10 20 30 40 50 60 70 80 90 100

0

10 20 30 40 50 60 70 80 90 100

ET (%)

ET (%)

Elbow flexors

Thumb adductor

*

100

***

80

††† 60

BB BRA TRI

40

20

RMS (%MVC)

RMS (% MVC)

80 70

60

50

*

0

0 0

10 20 30 40 50 60 70 80 90 100

0

10 20 30 40 50 60 70 80 90 100

ET (%)

muscle groups. Our results show that, whereas ET differed widely between muscle groups, the relative strength loss immediately after task failure was similar, a finding confirming our first hypothesis. Additionally, in agreement with our sec-

ET (%)

ond hypothesis, VAL reduction was only observed in the muscle group presenting the longest ET (PF), whereas the other three muscle groups (EF, THU, and KE), with shorter ET, only showed impaired excitation-contraction coupling.

Table 2. M-wave amplitudes and durations and RMS/M changes for the different muscles Amplitude, mV

KE VL VM RF PF Sol GL GM EF BB BRA THU ADD

Duration, ms

Pre

Post

Variation, %

Pre

Post

Variation, %

RMS/M Variation, %

12.6 ⫾ 4.3 14.2 ⫾ 4.9 7.2 ⫾ 2.1

12.7 ⫾ 4.3 12.8 ⫾ 4.6 6.9 ⫾ 2.1

0.8 ⫾ 8.7 ⫺8.6 ⫾ 17.0 ⫺3.1 ⫾ 13.3

8.5 ⫾ 2.3 7.0 ⫾ 1.3 9.8 ⫾ 2.5

8.9 ⫾ 2.7 7.2 ⫾ 1.6 11.0 ⫾ 2.7†

4.8 ⫾ 8.9 2.8 ⫾ 11.3 12.3 ⫾ 10.5

8.1 ⫾ 29.6 22.0 ⫾ 37.5 ⫺4.5 ⫾ 36.8

12.4 ⫾ 3.7 12.2 ⫾ 8.4 9.8 ⫾ 6.0

8.8 ⫾ 3.4† 11.8 ⫾ 8.4 11.8 ⫾ 5.6†

⫺27.3 ⫾ 21.2 ⫺4.9 ⫾ 15.6 33.7 ⫾ 34.5

2.6 ⫾ 1.0 3.2 ⫾ 1.8 3.2 ⫾ 1.0

3.0 ⫾ 1.1* 3.2 ⫾ 2.0 3.1 ⫾ 1.1

13.0 ⫾ 17.2 3.7 ⫾ 25.3 ⫺2.3 ⫾ 18.1

⫺1.6 ⫾ 41.3 12.6 ⫾ 27.2 ⫺17.8 ⫾ 38.2*

13.1 ⫾ 7.3 7.4 ⫾ 4.6

12.5 ⫾ 6.4 6.7 ⫾ 3.3

⫺1.6 ⫾ 25.9 ⫺3.2 ⫾ 20.6

8.1 ⫾ 2.5 7.8 ⫾ 2.5

8.3 ⫾ 2.5 8.5 ⫾ 2.6

3.8 ⫾ 11.8 10.0 ⫾ 15.8

9.5 ⫾ 46.9 12.5 ⫾ 20.0

1.5 ⫾ 1.9

1.2 ⫾ 1.4

⫺2.5 ⫾ 78.7

4.4 ⫾ 1.7

5.0 ⫾ 1.7

13.1 ⫾ 30.9

6.9 ⫾ 63.0

Values are means ⫾ SD. Significant changes (*P ⬍ 0.05 and †P ⬍ 0.001, respectively). RMS, root mean square; VL, vastus lateralis; VM, vastus medialis; RF, rectus femoris; Sol, soleus; GL, gastrocnemius lateralis; GM, gastrocnemius medialis; BB, biceps brachii; BRA, brachioradialis; ADD, adductor pollicis. J Appl Physiol • doi:10.1152/japplphysiol.01539.2012 • www.jappl.org


*

RMS (%MVC)

RMS (%MVC)

70

§§

60

Fig. 2. Relative root mean square (RMS) (% MVC preexercise) throughout the fatiguing exercise. *P ⬍ 0.05 and ***P ⬍ 0.001 indicate a significant increase in relative RMS throughout the fatiguing task. †††P ⬍ 0.001 indicates a higher starting point compared with the other agonists, and §§P ⬍ 0.01 shows significantly different ending points. VL, vastus lateralis; VM, vastus medialis; RF, rectus femoris; BF, biceps femoris; GL, gastrocnemius lateralis; GM, gastrocnemius medialis; Sol, soleus; TA, tibialis anterior; BB, biceps brachii; BRA, brachioradialis; TRI, triceps brachii. ET, endurance time; Values are mean ⫾ SE.

Plantar flexors


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Table 3. Single-twitch amplitude, PS10 and PS100, before (Pre) and after (Post) fatiguing contraction Peak twitch, N

KE PF EF THU

PS10, N

PS100, N

Pre

Post

Pre

Post

Pre

Post

109.7 ⫾ 16.8 167.3 ⫾ 32.2 21.7 ⫾ 4.6 11.9 ⫾ 3.8

69.8 ⫾ 23.1† 164.0 ⫾ 30.4 6.0 ⫾ 2.3† 4.4 ⫾ 3.2†

148.3 ⫾ 27.5 251.2 ⫾ 45.6 29.4 ⫾ 7.2 20.1 ⫾ 6.4

86.4 ⫾ 31.6† 220.1 ⫾ 50.0* 7.0 ⫾ 3.6† 6.8 ⫾ 4.7†

150.8 ⫾ 27.1 270.6 ⫾ 51.2 35.1 ⫾ 7.8 25.6 ⫾ 6.2

109.6 ⫾ 34.2† 251.2 ⫾ 52.0 14.1 ⫾ 4.9† 9.9 ⫾ 5.9†

Values are means ⫾ SD. Significant decreases compared with Pre (*P ⬍ 0.01 and †P ⬍ 0.001). PS10, 10-Hz doublet amplitude; PS100, 100-Hz doublet amplitude.

Previous studies reported similar MVC force reductions after different types of fatiguing tasks but performed with the same muscle group (37, 38, 58, 59). We now show that, at failure of a similar task, despite different ETs, the loss of MVC force was similar for four different muscle groups. Taken together, these observations support the neuromuscular reserve/threshold hypothesis proposed by different authors (3, 48, 49, 72). Accordingly, all our subjects were able to develop a force level superior to the 50% MVC target force during the short MVC executed immediately after task failure, reaching about 60 –70% MVC. A lack of motivation is obviously a potential mechanism for task failure but was considered unlikely in our setup. Our subjects were young, motivated, healthy, and physically active subjects who were strongly encouraged during the experiments by their peers and the investigators. We contend that our subjects were truly unable to voluntarily sustain the requested force level any longer when reaching task failure. This contention is corroborated by the slight force decline below 50% MVC, observed just before task failure, and the maximal RPE when task failure was reached. These results are in agreement with our previous study in which the subjects’ muscles were still capable of developing briefly a force equal to about 50% of prefatigue MVC force, despite being unable to voluntarily sustain anymore the mere 20% MVC force level requested in that study (53). Burnley et al. (17) reported that, after repeated sustained submaximal contractions below a “critical torque” threshold (corresponding to the intensity below which the contraction could theoretically be sustained indefinitely), a greater force than that requested could still be produced immediately after the exercise. The 50% MVC we used was well above this critical threshold, which has been estimated to be ⬃15% MVC for sustained contractions (52). Nonetheless, it appears from our results that the subjects we tested were able to produce a force level higher than the target force at task failure of a sustained contraction at 50% MVC, an intensity at which blood flow into the muscle is impeded (21, 27, 42, 64). Although results from Burnley et al. (17) and from the present investigation cannot be directly compared (intermittent vs. continuous contractions), we can suppose that the metabolic consequences of a reduction in muscle oxygen availability contributed to the advent of task failure in the present study. The ability to produce a force during the short MVC greater than that sustained during the last seconds of the fatiguing task may be under the influence of the subject’s awareness that he will be done with the effort for the specific session right after the last MVC. According to Tucker et al. (73), when approaching the finish of a closed-end exercise task (e.g., a time trial,

covering a given distance in the shortest time possible), the uncertainty regarding the remaining duration of the task progressively decreases, releasing the threat to homeostasis because metabolic and motor unit reserves will not be needed anymore; often this leads to end spurts with higher effort intensities as observed during the time trial. For open-ended exercise tests (e.g., time to exhaustion at a fixed work rate, incremental exercise testing, or contraction until task failure as in our experiment), the termination of the effort is mainly the result of the sense of effort, as well as other unpleasant sensations such as muscle pain becoming more intense than tolerable (14, 41, 44, 70). Our present finding of the capacity to produce a force, for a brief period of time, greater than the requested one at task failure, further reinforces the concept of neuromuscular reserve. Contrary to previous work for dynamic exercise (3, 5), our data do not support the existence of a single generic peripheral threshold, as large differences in contractile impairment were observed between the four muscle groups just after task failure. We found no significant alteration in potentiated peak twitch [the index of peripheral fatigue used in Amann and coworkers’ articles (3, 5)] in the PFs at task failure. Thus the reserve in maximal force-generating capacity at task failure of a sustained contraction cannot be solely explained by a peripheral fatigue threshold. Origin of MVC Force Loss The origin of force loss differed between the four muscle groups. PFs were the only muscle group exhibiting activation failure. We observed a VAL loss of 13%, indicating a reduced capacity to voluntarily activate this muscle group. Accordingly, gastrocnemius medialis RMS/M ratio was diminished after the sustained contraction, also indicating reduced muscle activation. Taken together, these alterations indicate that task failure was most likely the result of greater central impairment for this muscle group compared with the other ones, in which only peripheral impediment was found. Changes in contractile properties immediately after task failure suggest a role for peripheral fatigue in the termination of exercise for EF, KE, and THU, whereas only a slight peripheral impairment (⬃10% for PS10 amplitude) was found in PF. This substantial muscular fatigue could be attributed to the limited blood flow in the working muscles (see above), leading to metabolite accumulation, which would activate group III/IV afferents and therefore reduce neural drive, causing task failure (4). In the present study, we observed a reduction in peak twitch, PS10, and PS100 amplitudes in the KE by ⬃30 – 40% compared with the nonfatigued state, in agreement with the literature (29, 75). In a repeated-contrac-



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Adjustments During the Fatiguing Task Increases in EMG activity have been widely reported during sustained submaximal isometric contractions (30, 47, 63, 75), suggesting an increase in motor unit firing frequencies and/or additional motor unit recruitment to compensate for decreased force development in fatiguing motor units. We found that, whereas soleus EMG activity and RMS/M ratio remained constant throughout fatigue, gastrocnemius lateralis and gastrocnemius medialis EMG activities showed a twofold increase by the end of the task. Therefore, one could conclude that soleus was not the limiting factor to the task continuation, even though soleus has been reported to be the main contributor to PF force production at 90° knee flexion (20, 43, 65). Both our study and that of Ochs et al. (55), which shows a greater decrease in gastrocnemii EMG activity during repeated MVC, suggest that gastrocnemii are more fatigable than soleus and therefore might be the limiting factor for enduring the contraction. This is in agreement with the respective fiber type compositions of these muscles, mainly slow for the soleus vs. predominantly fast for the gastrocnemii (39). In the KE, vastus lateralis and vastus medialis EMG activity increased by about 1.5 times (Fig. 2), whereas rectus femoris activity remained constant throughout the contraction. In line with our results, Rochette et al. (63) found a smaller rate of EMG increase in rectus femoris compared with vastus lateralis and vastus medialis muscles during a sustained contraction at 20% MVC. Moreover, Place et al. (61) found a lower rectus femoris EMG activity compared with vastus lateralis and vastus medialis

Neyroud D et al.

muscles during a sustained isometric contraction performed at a constant quadriceps global EMG activity. Therefore, it seems that the ability to increase rectus femoris EMG activity is more limited than the ability to increase the activity of vastus lateralis and vastus medialis. When looking at PF and KE results together, we can observe a different EMG activity behavior in the two muscles that differ anatomically from their other synergists. Accordingly, soleus is the only monoarticular muscle in the PF, and rectus femoris is the only biarticular muscle in the KE. Bolhuis et al. (12) also reported that monoand biarticular muscles present different EMG activity patterns during voluntary contractions. Whereas monoarticular muscle EMG activity is influenced both by force and movement direction, EMG activity of biarticular muscles only depends on force direction (12). Thus it can be conjectured that the differences in EMG activity alterations observed in this study could be related to anatomical function of the different muscle groups. In agreement with Booghs et al. (13), EF also presented an increased EMG activity of about 1.5 times at task failure (Fig. 2). Again, differences in the rate of increase in EMG activity were observed between the two agonists. Contrary to Gamet and Maton (31), we found a greater EMG increase in biceps brachii compared with brachioradialis. This incongruence between the two studies can be explained by the different contraction intensities [25% MVC in Gamet and Maton (31) vs. 50% in the present study] and possibly by different joint positions (pronation-supination was not reported in their study), as it has been reported that biceps brachii contribution to the elbow flexion is favored by supination (66). Lastly and in line with the other muscle groups, adductor pollicis EMG activity also increased by about 1.5 times at the end of the fatiguing contraction (Fig. 2). Final agonist EMG values were similar between muscle groups when the average activities for each muscle group was considered, except for THU that showed a higher final EMG activity compared with PF (P ⬍ 0.01). This result might be explained by different dependence on rate coding vs. recruitment strategy between small and large muscles (45, 67). In conclusion, the present study is the first to show that lower and upper limb muscles subjected to the same fatigue task present the same MVC force decline immediately after task failure, despite widely different ET. The sustained contraction was limited by impaired activation level in the PF, which presented the longest ET. On the other hand, muscle fatigue was mainly attributed to contractile alterations in the other muscle groups. Thus the extent of muscle fatigue is not affected by endurance time, whereas this latter determines the etiology of fatigue. ACKNOWLEDGMENTS The authors thank all the subjects who volunteered to participate, Antoine Poncet (CRC & Division of Clinical Epidemiology, Department of Health and Community Medicine, University of Geneva & University Hospitals of Geneva) for help with the statistical analysis and Marc Buclin for the design and conception of the ergometers. GRANTS This study was supported by the De Reuter Foundation and the Geneva Academic Society. DISCLOSURES No conflicts of interest, financial or otherwise, are declared by the authors.



tions setup at 50% MVC (6 s contraction: 4 s rest), BiglandRitchie et al. (10) also observed greater contractile alterations in KE compared with PF, which confirms the greater susceptibility of KE toward peripheral fatigue. Regarding the upper limb muscles, THU and EF showed a decline of ⬃60 –70% in peak twitch, PS10, and PS100 amplitudes. Upper limb muscle contractile response was thus more affected compared with lower limb muscles. We speculate that this difference may be linked to the respective muscle’s function and structure; upper limb nonpostural muscle groups, not continuously counteracting gravity, could be expected to experience greater contractile impairments than postural muscle groups that regularly counteract gravity, as is the case in the present study. Our results suggest that EF are the most fatigable muscle group of the four tested, with a short ET and sizeable contractile alterations. Additionally, at task failure, MVC force was also impaired for the antagonistic elbow extensor muscles, suggesting a higher susceptibility to fatigue for muscles around the elbow joint compared with the others tested in the present work. Low-frequency fatigue (assessed by the PS10/PS100 ratio) was more pronounced in EF (⫺42 ⫾ 15%) but was also present in KE and to a minor extent in PF. Such contractile failure points to alterations beyond the neuromuscular junction (40). Strikingly, no low-frequency fatigue was found in the THU (⫺8 ⫾ 38%, P ⬎ 0.05). As M-wave changes were quite small compared with the extent of peak twitch and doublet reductions, we argue that the force decline was likely caused by alterations occurring beyond the sarcolemma (11). The decrease in peak twitch, PS100, and PS10 amplitudes may therefore be related to altered Ca2⫹ handling (1, 9, 62).

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Neuromuscular Adjustments in Different Muscle Groups AUTHOR CONTRIBUTIONS Author contributions: D.N., J.R., A.F.M., G.Y.M., N.A.M., B.K., and N.P. conception and design of research; D.N., J.R., and N.P. performed experiments; D.N., J.R., and N.P. analyzed data; D.N., J.R., A.F.M., G.Y.M., N.A.M., B.K., and N.P. interpreted results of experiments; D.N. and N.P. prepared figures; D.N., J.R., and N.P. drafted manuscript; D.N., A.F.M., G.Y.M., N.A.M., B.K., and N.P. edited and revised manuscript; D.N., J.R., A.F.M., G.Y.M., N.A.M., B.K., and N.P. approved final version of manuscript. REFERENCES

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