INFLUENCE OF JOINT POSITION ON SYNERGISTIC MUSCLE ACTIVITY AFTER FATIGUE OF A SINGLE MUSCLE HEAD NORMAN STUTZIG, PhD,1,2 and TOBIAS SIEBERT, PhD1 1 Exercise Science, Institute of Sport and Movement Science, University of Stuttgart, Allmandring 28, 70569 Stuttgart, Germany 2 Exercise Science, Institute of Sport Science, Friedrich Schiller University Jena, Seidelstraße 20, 07749 Jena, Germany Accepted 29 May 2014 ABSTRACT: Introduction: We investigated synergistic muscle activity after fatigue of a single muscle in different joint positions. Methods: Two experimental groups (n 5 12 each) performed maximal voluntary contractions (MVCs) before and after fatiguing the gastrocnemius lateralis (GL), using neuromuscular electrical stimulation (NMES). Neuromuscular tests, including muscle activity during MVC, H-reflex, and twitch interpolation, were performed. One group completed the experiment in a knee-extended position with the second group in a knee-flexed position. Results: In the knee-flexed position, the muscle activity increased in non-stimulated synergistic muscles. In contrast, in the knee-extended position, muscle activity of the synergistic muscles remained unaltered. The MVC force remained unaltered in the flexed position and decreased in the extended position. Conclusions: Synergistic muscles compensate for the fatigued muscle in the flexed position but not in the extended position. Compensation mechanisms seem to depend on joint position. Muscle Nerve 51: 259–267, 2015

Functional failure of a single muscle (e.g., due to cooling,1 fatigue,2,3 paralysis,4 or pain5) leads to alterations of the neuromuscular system during voluntary contractions. It has been reported that fatigue of a single muscle leads to increased muscle activity in synergistic muscles during voluntary contractions.6,7 This observation was identified for different muscle groups and is interpreted to be a compensating effect.6,8 It is assumed that the force-compensating effects of synergistic muscles depend on muscle length.4 The contribution of synergistic muscles to isometric force production during maximal voluntary contraction (MVC) is determined mainly by muscle length. It has been shown that fatigue leads to a greater reduction of force in lengthened muscles compared with shortened muscles.9,10 In synergistic muscles, such as the calf muscles, the lengths of gastrocnemius lateralis (GL) and gastrocnemius medialis (GM) change with knee joint position, whereas soleus (SOL) muscle length remains unalAbbreviations: EMG, electromyography; GL, gastrocnemius lateralis; GM, gastrocnemius medialis; Hmax, maximal Hoffmann-reflex amplitude; Mmax, maximal M-wave amplitude; MVC, maximal voluntary contraction; NMES, neuromuscular electrical stimulation; rANOVA, repeated-measures analysis of variance; RMS, root mean square; SOL, soleus; SYN, synergistic muscles; TA, tibialis anterior; VAL, voluntary activation level Key words: compensation; H-reflex; interpolated twitch; neuromuscular electrical stimulation; spinal reflex; triceps surae Correspondence to: N. Stutzig; e-mail: [email protected] C 2014 Wiley Periodicals, Inc. V

Published online 3 June 2014 in Wiley Online Library (wileyonlinelibrary.com). DOI 10.1002/mus.24305

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tered.11 However, the influence of muscle length on synergistic muscle activity after fatigue of a single muscle (e.g., by force compensation) remains unknown. Compensating mechanisms may occur due to alterations of spinal neuronal pathways.12 A common tool to study spinal neuronal pathways is the Hoffmann-reflex (H-reflex). The amplitude of the H-reflex depends on muscle length13 and the history of previously activated Ia afferents.14 Further, it has been reported that the H-reflex increases after muscle fatigue.12 Ia afferents are connected to the a-motoneurons of both homonymous and synergistic muscles15,16 and have an excitatory effect on them. It can be assumed that the H-reflex of synergistic muscles is increased after fatigue of a single muscle and that this mechanism may be length-dependent. A common approach to fatigue a single muscle is to stimulate this muscle using neuromuscular electrical stimulation (NMES).17 NMES activates nerve branches through electrodes placed on the skin above the muscle to produce muscle contraction.18 This type of stimulation leads to decreased force production, or fatigue. Recent studies have reported decreased propagation of electrical potentials on the muscle fiber membrane due to NMES.19,20 In this study, the interaction of synergistic calf muscles after NMES of GL was investigated during maximal voluntary plantarflexion in 2 different joint positions. In 1 position, the knee and ankle angles were 180 (full extension) and 90 , respectively. In this position, both the biarticular gastrocnemii and the mono-articular SOL act in the plateau region of the force-length curve,21,22 and the gastrocnemii contribute greatly to force production. In the second position, both the knee and ankle angles were set at 90 . In this position, the SOL acts in the plateau region of the force-length relation while the gastrocnemii act on the ascending branch of the force-length curve. Thus, the SOL is the main contributor to calf muscle force production.22 The aim of the study was to investigate whether synergistic muscles can compensate for the loss of muscle force induced by fatigue of a single muscle (GL) in a position where the gastrocnemii contribute greatly to torque production (180 knee angle) MUSCLE & NERVE

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Table 1. Anthropometric data of the participants in both groups. Experimental group 1 (n 5 12)

Experimental group 2 (n 5 12)

Parameter

Mean

SD

K-S test

Mean

SD

K-S test

Student t-test (P-value)

Age (years) Height (cm) Mass (kg) BMI

23.6 178.0 77.4 24.4

3 4.8 7.6 2.3

NS NS NS NS

28.2 174.9 70.7 23.7

5.1 8.6 13.3 2.6

NS NS NS NS

0.01 0.29 0.15 0.17

SD, standard deviation; BMI, body mass index; K-S, Kolmogorov-Smirnov (test for normal distribution).

versus another position where the SOL is the main contributor (90 knee angle). Examination of length-dependent changes in synergistic muscle activity and force compensation may contribute to a deeper understanding of neuromuscular connections of muscle synergists. Neuromuscular and mechanical tests of the plantarflexors were performed before and after NMES of the GL to analyze compensatory mechanisms. We hypothesize that muscle force compensation depends on muscle length. METHODS Study Design and Participants. Two experiments were performed. The participants were divided into 2 groups containing 12 participants each. Each group performed the experiments at different knee angles. In both experiments, the GL was fatigued using NMES. Before and after the NMES phase, maximal isometric plantarflexion and neuromuscular tests were performed. At least 1 week before the experiments participants were accustomed to NMES. Twenty-four subjects (see Table 1 for anthropometric parameters) participated in the study. All participants were informed about the aims and risks of the study and gave written consent before the study started. Exclusion criteria were pregnancy, cardiac disease, and a history of ankle injury within the 4 months before the experiments. The study was approved by the local ethical committee of the University Hospital of Jena (ID 3603-10/12) and was conducted in accordance with the latest Declaration of Helsinki.

In the first experiment, participants were seated on a bench with a knee angle of 90 (180 corresponds to full leg extension) and an ankle angle of 90 . One foot was attached to a foot pedal of an isokinetic system (Isomed 2000; D&R GmbH, Hemau, Germany). In the second experiment, participants lay supine on a bench in the same isokinetic system with knee and ankle angles of 180 and 90 , respectively. In this position, both SOL and gastrocnemii muscles are in the plateau of the force-length curve.11,21 The force signal was recorded at 2000 s21 using an

A/D conversion system (MP 150; Biopac Systems, Goleta, California). Surface Electromyography. Surface electromyographic (EMG) signals were recorded from the SOL, GL, and GM. EMG was measured during MVC to determine alterations of voluntary muscle activity of the plantarflexors. In conjunction with tibial nerve stimulation (see below for details), M-waves and H-reflexes were determined from the EMG signal. The H-reflex was recorded to determine spinal reflex activity before and after fatigue. As recommended in the literature, the H-reflex was evoked during constant voluntary contraction at 20% of maximal torque during MVC (20% MVC).14,23 The M-wave was also evoked at 20% MVC to normalize the H-reflex. Another M-wave was evoked in the resting condition. This M-wave (or rather the M-wave amplitude) was used to: (1) control the process of fatigue; and (2) normalize voluntary muscle activity. The skin above the muscles was shaved, abraded, and cleaned with alcohol pads. The electrodes were placed according to SENIAM recommendations.24 Two Ag-AgCl electrodes (Type H92SG; Kendall Arbo, Tyco Healthcare Deutschland GmbH, Noustadt/Donau, Germany) were fixed on the marked muscle at an interelectrode distance of 20 mm. The ground electrode was placed over the lateral malleolus. EMG signals were recorded at a sampling rate of 2000 s21, preamplified (1000), band-pass filtered (bandwidth 10–500 s21), and stored on a computer. All EMG data were measured in millivolts.

Experimental Setup.

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Experimental Procedure. Participants were asked to sit (experiment 1) or lay (experiment 2) in the isokinetic system and perform a standardized warmup consisting of 15 submaximal isometric plantarflexions. The force was increased progressively by the participants from trial to trial. The overall test design and the calculated dependent variables were equal in both experiments and are shown in Figure 1. The main experimental procedure started with 2 MVCs separated by 1 minute of rest. Participants were asked to MUSCLE & NERVE

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FIGURE 1. Diagram of the experimental design. The arrows represent the timeline.

increase the force quickly (but not explosively) and to keep the maximal torque on a plateau for 3 s. During MVC, participants had visual torque feedback and were encouraged verbally by the supervisor.25 If MVC torques differed by >5%, a third MVC was performed. Afterward, the H-reflex and the M-wave were measured at 20% MVC. Then, the voluntary activation level (VAL) was determined using the twitch-interpolation technique.26 After a 2-min rest, 4 maximal M-waves were determined to obtain baseline values for the non-fatigued muscles (for details see below). Subsequently, the GL was stimulated using NMES (SportP; Compex, Ecublens, Switzerland) for 5 s followed by a 20-s rest. Every 5 on:off cycles, a single stimulus was applied to control the progress of fatigue. The GL was stimulated until the M-wave decreased to 80% of baseline. The NMES phase was then stopped, and posttests were conducted. Approximately 10 s after finishing the NMES phase, participants performed 2 MVCs separated by 1 min of rest. A small H-curve was then measured at 20% MVC using a reduced protocol.27 Then, the M-wave at 20% MVC was evoked. Finally, the VAL was determined using the twitch-interpolation technique, which was repeated once after 1-min rest. Electrical Evoked Potentials. To stimulate the tibial nerve, an electrode (cathode) was placed in the Fatigue of a Single Muscle Head

popliteal fossa, and the anode (self-adhesive electrode, size 5 3 10 cm; Compex, Ecublenz, Switzerland) was fixed 2 cm proximal to the patella. The nerve was stimulated with rectangular 1-ms waveforms. Participants were asked to contract the plantarflexors at 20% MVC constantly. During contraction, the electrical potentials were delivered. Starting from the H-threshold, the current was increased by 1 mA every 10 s. When the H-reflex was clearly on the descending limb of the H-curve, the stimulation was stopped. The muscle contraction at 20% MVC did not lead to fatigue. In the posttest, a mini-curve was drawn to measure Hmax20%.27 The current was increased progressively by increments of 1 mA from 26 mA to 16 mA around the intensity of Hmax20% during the pretest. Mmax20% was assessed as follows. The intensity of the M-wave was increased by 10 mA (10-s time interval) until both the twitch torque and the M-wave plateaued. A plateau was defined as 3 consecutive unaltered responses. The current intensity of the third stimulus was increased by 20%. At this intensity level, the tibial nerve was stimulated 4 times (10-s time interval) during 20% MVC, and the mean was defined as Mmax20%. The same stimulation intensity was used to evoke Mmax at rest. MUSCLE & NERVE

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The twitch-interpolation technique was used to determine the VAL. Participants were asked to perform an MVC. During the plateau phase of the MVC, a paired stimulus (10 ms) (superimposed doublet) was delivered at the intensity of Mmax20%. A second paired stimulus (potentiated doublet) was applied 3 s after the MVC. The twitchinterpolation technique was performed twice. Neuromuscular Electrical Stimulation to Fatigue the

Two self-adhesive electrodes (size 5 3 5 cm; Compex) were placed on the GL. The positive NMES electrode was fixed 1 cm proximal to the upper EMG electrode of the GL, and the negative NMES electrode was fixed approximately 1 cm proximal to the positive NMES electrode. Rectangular pulses [pulse width 400 ms; on (stimulation) : off (rest) time 5 s : 20 s; pulse frequency 80 s21] were delivered to the GL.28 After every 5 on:off cycles, a single stimulus was delivered to the resting muscle at the intensity of Mmax to control muscle fatigue. Stimulation intensities were set at the maximal tolerated level and varied between 40 and 60 mA. To reach 80% of the initial GL Mmax, the NMES phase lasted approximately 12 6 5 min (28 6 12 on : off cycles) and 18 6 8 min (40 6 18 on:off cycles) in experiments 1 and 2, respectively. GL.

Data Analysis. Mechanical Data. Maximal torque was determined from the MVCs at the beginning and after the NMES phase. The individual MVC torque values were averaged during the pretest (Fig. 1A) and posttest (Fig. 1H). The mean data were defined as MVC torque. The VALs during pre- and posttest were calculated from the MVCs in Figure 1D and K, respectively. The superimposed doublet was determined as the difference between MVC plateau and the torque increase due to the doublet. The potentiated doublet was determined as the difference between baseline and maximum torque due to the potentiated doublet. The VAL was calculated with the formula26:

VAL 5½12ðsuperimposed doublet = potentiated doublet Þ3100

The average of the VAL was calculated for the pre- and posttest, respectively. Furthermore, the torque peak of the potentiated doublet and the single twitch at rest were analyzed. Electromyographic Data. The EMG data during MVC of each muscle were rectified separately, and the root mean square (RMS) was calculated over 250 samples. The maximal RMS value of each muscle was determined in a time frame of 500 ms around MVC peak torque and was defined as vol262

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untary muscle activity. The RMS was normalized to the respective Mmax (RMS/Mmax). The mean RMS of the 2 MVCs during pre- and posttest was calculated and used to obtain the mean of RMS/Mmax. The peak-to-peak amplitudes of Hmax20%, Mmax20%, and Mmax at rest were calculated for each muscle. The 4 Mmax20% values at 20% during pretest and posttest as well as the 4 Mmax values at rest were averaged. Furthermore, the Hmax20%/ Mmax20% ratio was determined for each muscle. The non-stimulated GM and SOL were defined as synergistic (SYN) muscles, and each of their EMG parameter values was averaged. To prove if the muscle activity during 20% MVC changed from pre- to posttest due to the fatiguing exercise, RMS of the GL was averaged over 3 s between the first and second stimuli of the H-reflex curve. The averaged RMS at 20% MVC was normalized to Mmax and defined as RMS20%/Mmax. Statistical Analysis. Data are presented as the mean and standard deviation (SD). For further analysis, the data were tested for a normal distribution using the Kolmogorov-Smirnov test. All data were normally distributed. A 2 (POSITION [180 vs. 90 ]) 3 2 (MUSCLE [GL vs. SYN]) 3 2 (FATIGUE [pre- vs. posttest]) repeated-measures analysis of variance (rANOVA) was conducted for the EMG data. The mechanical data were analyzed using a 2 (POSITION [180 vs. 90 ]) 3 2 (FATIGUE [pre- vs. posttest]) rANOVA. The effect size was calculated using the partial eta-squared, (gP2) and set as follows: small effects 0.01; moderate effects 0.06; and large effects 0.14.29 When the rANOVA demonstrated significant main effects or interactions, post hoc analyses were performed using the Tukey honestly significant difference test. The significance level was set at P < 0.05. All analyses were performed using STATISTICA, version 10 (Hamburg, Germany). RESULTS Maximal M-wave Amplitude and Single-Twitch Torque as Markers of Fatigue. Analyses of Mmax yielded significant POSITION 3 MUSCLE 3 FATIGUE interactions (F1,44 5 10.29, P 5 0.002, gP2 5 0.19). The post hoc test revealed significant differences for Mmax amplitude of the GL in the 180 (P < 0.001) and 90 (P < 0.001) positions (Fig. 2). The single twitch torque decreased from pre- to posttest (F1,22 5 39.64, P < 0.001, gP2 5 0.64) (Fig. 3). There was no POSITION 3 FATIGUE interaction (F1,22 5 0.24, P 5 0.632, gP2 5 0.01). Hmax20%/Mmax20% Ratio. The analyses of the Hmax20%/Mmax20% ratio showed significant MUSCLE 3 FATIGUE interactions (F1,44 5 10.21, P 5 0.026, gP2 5 0.19). The post hoc analyses MUSCLE & NERVE

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FIGURE 2. Mean and standard deviation of M-wave amplitudes of the stimulated gastrocnemius lateralis (GL) and the nonstimulated synergistic muscles (SYN) before (black bars) and after (gray bars) neuromuscular electrical stimulation (NMES) of the GL at the 180 (left) and 90 (right) knee angles. Significance: *P < 0.05; **P < 0.01; and ***P < 0.001.

revealed a significant increase of the GL but not of the SYN in response to fatigue of the GL (Fig. 4). RMS was normalized by the corresponding Mmax for each muscle. Significant differences were found for the main factor, FATIGUE (F1,44 5 7.72, P 5 0.008, gP2 5 0.15). The GL increased in the 180 and 90 positions by 17.5% and 17.6%, respectively. Note that SYN increased significantly in the 90 position by 10.7%, but did not change (1.2%) in the 180 position (Table 2). The analyses of RMS20%/Mmax of GL revealed significant differences in the 180 position. RMS20%/Mmax increased from 0.0023 6 0.0016 mV to 0.0040 6 0.0019 mV (P < 0.001). There was no significant difference in RMS20%/Mmax for GL in Muscle Activity during Voluntary Contraction.

FIGURE 4. Mean and standard deviation of the Hmax20%/ Mmax20% ratio of the stimulated gastrocnemius lateralis (GL) and the non-stimulated synergistic muscles (SYN) before (black bars) and after (gray bars) neuromuscular electrical stimulation (NMES) of the GL. Significance: *P < 0.05; **P < 0.01; and *** P < 0.001.

the 90 position (P 5 0.223).

between

pre-

and

posttest

Torque during Maximal Voluntary Contraction. Analysis of the MVC torque demonstrated a significant POSITION 3 FATIGUE interaction (F1,22 5 19.51, P 5 0.000, gP2 5 0.47). MVC torque decreased significantly in the 180 position but not in the 90 position (Fig. 5). Hmax20%, Muscle Activity, and Voluntary Activation

Hmax20% did not change for all muscles. There were no main effects and no interaction effects in any position (Table 3). The analyses of VAL demonstrated significant POSITION 3 FATIGUE interactions (F1,22 5 5.51, P 5 0.028, gP2 5 0.20). Further post hoc analyses did not reveal significant differences (180 : P 5 0.518; 90 : P 5 0.245) (Table 3). Level.

DISCUSSION

FIGURE 3. Mean and standard deviation of single twitch torque before (black bars) and after (gray bars) neuromuscular electrical stimulation (NMES) of the gastrocnemius lateralis in the 180 (left) and 90 (right) knee angle positions. Significance: * P < 0.05; **P < 0.01; and ***P < 0.001. Fatigue of a Single Muscle Head

In this study we found that knee joint angle influences synergistic muscle activity after fatigue of a single muscle head. In the knee-flexed position, fatigue of the GL leads to increased EMG activity of the synergistic muscles, increased spinal reflex activity of the fatigued GL, and unaltered spinal reflex activity of the synergistic muscles. Interestingly, despite fatigue of the GL, maximal voluntary isometric force remained unchanged. This is in contrast to results measured in the kneeextended position. The force declined after fatigue of the GL, and EMG activity of the synergistic muscles remained unaltered. Similar to the kneeflexed position, spinal reflex activity of the GL was increased. Stimulated Muscle. Due to NMES of the GL, the Mmax of the fatigued muscle decreased in the MUSCLE & NERVE

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Table 2. Mean (SD) and percentage difference (% difference) of the normalized muscle activity (RMS/Mmax) of the gastrocnemius lateralis (GL) and its synergistic muscles (SYN) after neuromuscular electrical stimulation (NMES) of the GL. Pretest

Posttest

Parameter

Position

Muscle

Mean

SD

Mean

SD

Difference

RMS/Mmax

180

GL (stim) SYN (non-stim) GL (stim) SYN (non-stim)

0.0549 0.0429 0.0482 0.0336

0.0202 0.0141 0.0190 0.0098

0.0645 0.0434 0.0567 0.0372

0.0334 0.0160 0.0350 0.0101

17.5% 1.2% 17.6% 10.7%

90

extended position as well as in the flexed position. This observation is consistent with previously reported findings.19,20,30 It was postulated that NMES provokes failure of synaptic transmission or failure of action-potential propagation on the muscle fiber membrane, or both.20 The Hmax20%/Mmax20% ratio increased significantly in both positions in response to GL fatigue, which contradicts the results of studies reporting no changes of the Hmax/Mmax ratio due to NMES.19,31,32 We suggest that methodological reasons may be responsible for the differences between the studies. In previous experiments that identified unaltered Hmax/Mmax ratios, the nerve was stimulated at rest. In our study, however, H-reflexes and M-waves were evoked at 20% MVC. During voluntary contraction, central neural drive exists. It is known that increased central neural drive reduces the antidromic stimulus during evoked electrical potentials, and therefore the Hmax/Mmax ratio increases.33 It can be assumed that fatigue of the GL increases the central neural drive to the GL at a given motor output (e.g., 20% MVC) and thus the antidromic stimulus would decrease at a given stimulus intensity. However, if the Hmax/Mmax ratio is obtained without voluntary contraction (i.e., at rest), the antidromic stimulus would be the same. Therefore, the Hmax/Mmax ratio at rest would be unaffected, as observed in the aforementioned studies. We determined RMS20%/Mmax to clarify whether neural drive to the GL is increased during 20% MVC. Indeed, the RMS20%/Mmax of GL increased in the 180 position. However, the RMS20%/Mmax of GL in the 90 position did not change, but the Hmax20%/Mmax20% also increased. Therefore, it can be concluded that the increased central neural drive in the extended knee position had only a minor effect on increase in Hmax20%/Mmax20% in this study. To provide another explanation for the increased Hmax20%/Mmax20% ratio, we analyzed the changes in Hmax20% and Mmax20% separately. One would expect that, due to peripheral fatigue (impairment of action potential propagation on the fiber membrane), Mmax20% and Hmax20% decrease by the same amount. According to this 264

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prediction, the Hmax20%/Mmax20% ratio would not decline. It is noteworthy that Mmax20% decreased due to peripheral fatigue, whereas Hmax20% remained unaltered; consequently, the Hmax20%/ Mmax20% ratio increased (Fig. 4). Therefore, it seems that spinal reflex activity was modified. This can be explained by decreased presynaptic inhibition (PSI) of Ia afferents.23 PSI reduces the release of neurotransmitters from afferent fibers due to their depolarization by primary afferent depolarization interneurons.34,35 It was shown that PSI depends on conditions such as sitting, standing, or lying prone,23 and it also depends on task and muscle fatigue.34 Nordlund et al.12 found that the Hmax20%/Mmax20% ratio increased after repeated maximal voluntary bouts, whereas the Hmax20% did not change (as in our study). They concluded that the increased Hmax20%/Mmax20% is based on decreased PSI. Non-Stimulated Muscles. The Mmax of the synergistic muscles did not change significantly during NMES in both positions. In the 90 position, the RMS/Mmax of the SYN increased by 10.7% from pre- to posttest. This increase was in response to NMES of the GL. Increased muscle activity of synergistic muscles after NMES of 1 muscle has also

FIGURE 5. Mean and standard deviation of the maximal voluntary contraction (MVC) torque before (black bars) and after (gray bars) neuromuscular electrical stimulation of the gastrocnemius lateralis. Significance: *P < 0.05; **P < 0.01; and *** P < 0.001. MUSCLE & NERVE

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Table 3. Mean (SD) and percentage difference of H-reflex amplitude at 20% MVC (Hmax20%) of the gastrocnemius lateralis (GL) and its synergistic muscles (SYN) as well as the voluntary activation level (VAL) after neuromuscular electrical stimulation (NMES) of the GL. Pretest Parameter Hmax20% (mV)

Position

Muscle

Mean

SD

Mean

SD

Difference

180

GL (stim) SYN (non-stim) GL (stim) SYN (non-stim)

1.95 4.27 1.73 3.31 97.2 90.1

1.19 1.89 0.72 1.39 2.84 10.11

1.88 4.62 1.93 3.99 96.0 91.8

1.14 1.96 1.13 1.32 2.66 7.50

23.6% 8.2% 11.6% 20.5% 21.2% 1.9%

90 VAL (%)

Posttest

180 90

been reported.7,8 Akima et al.7 assumed that increased descending central commands are the main source. Alternatively, Stutzig et al.8 suggested that heteronymous Ia spinal facilitation may be the dominant reason for increased synergistic muscle activity. Because Hmax20%/Mmax20% did not increase in the synergistic muscles, it is concluded that spinal reflex activity is not the source of increased RMS/Mmax. Thus, it seems that descending central commands may be responsible for increased synergistic muscle activity. In contrast to the flexed knee position, the RMS/Mmax of the non-stimulated synergistic muscles did not change due to NMES of the GL in the knee-extended position. It seems that the position has an effect on the synergistic muscle activity after NMES of the GL. This interpretation, however, should be interpreted with caution, because there was no POSITION 3 MUSCLE 3 FATIGUE interaction. Twitch torque decreased in the flexed and extended positions to 79.5% and 87.6%, respectively. Furthermore, MVC torque did not change in the flexed position and decreased by 12% in the extended position. There may be several reasons for this: (1) contribution of GL length to joint torque; (2) length-dependent force compensation of a fatigued GL muscle; and (3) joint position-dependent force compensation of the non-fatigued synergistic SOL and GM. First, based on the force-length curve of the GL, the force contribution of GL is greater in the extended position.21,22 Therefore, if the GL is impaired by the same amount, the MVC torque will decline much more in the extended position than it will in the flexed position. The second explanation is based on lengthdependent force production of a fatigued muscle. Fitch et al.36 fatigued the dorsiflexor muscles for 90 s constantly using 20 s21 neuromuscular electrical stimulation at short and optimal muscle length in separate sessions. The twitch torque and the MVC torque both decreased much more when the Mechanical Consequences.

Fatigue of a Single Muscle Head

muscle length was optimal than when it was short, which is consistent with our observations. They concluded that muscle fatigue correlates with the number of actin-myosin crossbridge interactions.36 One could assume that, at short muscle lengths, fewer actin-myosin crossbridge interactions are available compared with optimal muscle length, and therefore the metabolic costs during fatigue would be reduced accordingly. In contrast, Baker et al.37 observed that the metabolic costs during fatigue were independent of muscle length. Hence, it is concluded that other mechanisms may contribute to muscle length-dependent force decrease during fatigue. The third mechanism may be based on increased synergistic muscle activity.7,8 In addition to the differences in GL activity as a function of muscle length, we also observed increased RMS/ Mmax of the non-fatigued synergistic muscles in the flexed position, whereas the synergistic muscle activity remained unaltered in the extended position. Thus, force compensation of synergistic muscles may depend on their muscle lengths. However, the length of both gastrocnemius muscle heads increases with knee extension, whereas the mono-articular SOL length does not change between the flexed and extended knee positions. Therefore, it seems that force compensation by synergistic muscles, particularly SOL, may be a reasonable mechanism.38,39 A force-compensating mechanism after NMES was also reported in other studies.6–8 Sacco et al.3 conducted a study very similar to ours. They also fatigued the GL using NMES until the M-wave amplitude of the GL reached 65% of the baseline. Their twitch torque declined to 88% of the baseline after NMES of the GL, which is comparable to the result of our study. Similar to our study, Sacco et al.3 performed MVCs in a sitting position with knee and ankle angles of 90 . In contrast to our study, Sacco et al.3 inflated a cuff around the thigh during NMES of the GL and performed MVC under ischemic conditions. In their study, MVC torque declined (by 29.7%), as one MUSCLE & NERVE

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would expect after fatiguing 1 muscle. However, in our study, the MVC torque did not change in the flexed position, which supports our assumption that fatigue of the GL was compensated by synergistic muscles. This mismatch may depend on different conditions, such as ischemia and position. The assumption of force compensation should be considered with caution because we did not measure the force produced by the individual muscles. Furthermore, it has been reported that central fatigue occurs due to NMES and repeated maximal voluntary contractions.12,19 However, the VAL did not change in our study in either position. This result is consistent with findings by Zory et al.20 Therefore, it is concluded that the VAL has no effect on the torque differences between the extended and flexed positions. It is a limitation of the study that different subgroups performed the experiments instead of a single population performing both experiments. Considering this fact, we have been careful that both subgroups were similar with respect to body mass index and physical activity of the participants. Another limitation of our study is that the experiments were performed in different body positions. In the knee-extended position participants lay supine, whereas in the knee-flexed position they were seated upright. In 1 study it was reported that body position may have an effect on force production during fatigue.40 In that study, Caffier et al. reported no difference in MVC force production in sitting and laying positions. For sustained voluntary contraction they found that the force decline was higher when participants were laying down compared with sitting. However, we used NMES to fatigue the GL. The muscle contraction is quite different between NMES and voluntary contraction with regard to motor unit recruitment and fatigue.17,41 A further limitation is that we did not measure the EMG activity of the antagonistic tibialis anterior (TA). Alteration of the antagonistic cocontraction could influence the results. For example, an increase of TA co-contraction would decrease the force output during MVC. Also, muscle excitability of the agonistic SYN would be reduced by antagonistic activity of the TA.42 However, as SYN muscle activity did not decrease (Table 2), co-contraction of the TA may be excluded. In conclusion, we have demonstrated that fatigue of a single muscle head induces different effects during MVC depending on joint position. The MVC decreased in the knee-extended position, and the muscle activity of the synergistic muscles remained unaltered. In contrast, in the knee-flexed position, the MVC did not change, and the muscle activity of the synergistic muscles increased. These findings suggest that GL fatigue 266

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may be compensated by increased synergistic muscle activity in the knee-flexed position. It seems that descending central commands may be responsible for the observed increase in synergistic muscle activity. Spinal pathways of the synergistic muscles and the voluntary activation level are not affected by NMES of the GL. These results deepen our understanding of the neuromuscular connections of synergistic muscles as well as the force compensation mechanisms of these muscles. Insight into synergistic muscle interaction may have an impact on construction and control of neuroprostheses43 for patients with paralysis of single muscles or synergistic muscle groups. Furthermore, with increasing use of artificial mono- and bi-articular muscles in robotics,44 the relevance of synergistic muscle interconnection may increase further. REFERENCES 1. Kinugasa R, Yoshida K, Horii A. The effects of ice application over the vastus medialis on the activity of quadriceps femoris assessed by muscle function magnetic resonance imaging. J Sports Med Phys Fitness 2005;45:360–364. 2. Hellsing G, Lindstrom L. Rotation of synergistic activity during isometric jaw closing muscle contraction in man. Acta Physiol Scand 1983;118:203–207. 3. Sacco P, Newberry R, McFadden L, Brown T, McComas AJ. Depression of human electromyographic activity by fatigue of a synergistic muscle. Muscle Nerve 1997;20:710–717. 4. Maas H, Gregor RJ, Hodson-Tole EF, Farrell BJ, English AW, Prilutsky BI. Locomotor changes in length and EMG activity of feline medial gastrocnemius muscle following paralysis of two synergists. Exp Brain Res 2010;203:681–692. 5. Ciubotariu A, Arendt-Nielsen L, Graven-Nielsen T. The influence of muscle pain and fatigue on the activity of synergistic muscles of the leg. Eur J Appl Physiol 2004;91:604–614. 6. de Ruiter CJ, Hoddenbach JG, Huurnink A, de Haan A. Relative torque contribution of vastus medialis muscle at different knee angles. Acta Physiol (Oxf) 2008;194:223–237. 7. Akima H, Foley JM, Prior BM, Dudley GA, Meyer RA. Vastus lateralis fatigue alters recruitment of musculus quadriceps femoris in humans. J Appl Physiol 2002;92:679–684. 8. Stutzig N, Siebert T, Granacher U, Blickhan R. Alteration of synergistic muscle activity following neuromuscular electrical stimulation of one muscle. Brain Behav 2012;2:640–646. 9. Gandevia SC, McKenzie DK. Activation of human muscles at short muscle lengths during maximal static efforts. J Physiol 1988;407:599– 613. 10. McKenzie DK, Gandevia SC. Influence of muscle length on human inspiratory and limb muscle endurance. Respir Physiol 1987;67:171– 182. 11. Mueller R, Siebert T, Blickhan R. Muscle preactivation control: simulation of ankle joint adjustments at touchdown during running on uneven ground. J Appl Biomech 2012;28:718–725. 12. Nordlund MM, Thorstensson A, Cresswell AG. Central and peripheral contributions to fatigue in relation to level of activation during repeated maximal voluntary isometric plantar flexions. J Appl Physiol 2004;96:218–225. 13. Hwang IS. Assessment of soleus motoneuronal excitability using the joint angle dependent H reflex in humans. J Electromyogr Kinesiol 2002;12:361–366. 14. Knikou M. The H-reflex as a probe: pathways and pitfalls. J Neurosci Methods 2008;171:1–12. 15. Eccles JC, Eccles RM, Lundberg A. The convergence of monosynaptic excitatory afferents on to many different species of alpha motoneurones. J Physiol 1957;137:22–50. 16. Nichols TR. The organization of heterogenic reflexes among muscles crossing the ankle joint in the decerebrate cat. J Physiol 1989;410: 463–477. 17. Gregory CM, Bickel CS. Recruitment patterns in human skeletal muscle during electrical stimulation. Phys Ther 2005;85:358–364. 18. Kuhn A, Keller T, Lawrence M, Morari M. A model for transcutaneous current stimulation: simulations and experiments. Med Biol Eng Comput 2009;47:279–289.

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Influence of joint position on synergistic muscle activity after fatigue of a single muscle head.

We investigated synergistic muscle activity after fatigue of a single muscle in different joint positions...
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