REPRODUCIBILITY OF ELECTROMYOGRAPHIC AND MECHANICAL PARAMETERS OF THE TRICEPS SURAE DURING SUBMAXIMAL AND MAXIMAL PLANTAR FLEXIONS NORMAN STUTZIG, PhD, and TOBIAS SIEBERT, PhD Institute of Sport and Movement Science, University of Stuttgart, Allmandring 28, 70569 Stuttgart Germany Accepted 7 July 2015 ABSTRACT: Introduction: Neuromuscular parameters must be reproducible to examine neuromuscular adaptations in interventional and clinical studies. The reproducibility of neuromuscular parameters for the soleus (SOL), lateral gastrocnemius (LG), and medial gastrocnemius (MG) was assessed over a period of 2 weeks. Methods: Thirteen subjects (27.4 years, 69.5 kg) were tested for numerous electromyographic (e.g., voluntary and electrical evoked EMG) and mechanical (e.g., voluntary activation level) parameters in 3 test sessions. Results: The majority of the data (28 of 34) revealed moderate and substantial reproducibility. Hmax20%/Mmax20% and Vsup/Msup were less reproducible in LG than in MG and SOL. Muscle activity and M-waves did not differ between muscles. The ICC for the mechanical data was >0.79. Conclusions: The H-reflex during voluntary contraction of the LG should be considered with caution. Mechanical data on muscle activation level are reproducible. The reproducibility of neuromuscular parameters is sufficient for interventional studies. Muscle Nerve 53: 464–470, 2016
Diagnostic tests of the neuromuscular system are important for clinicians and researchers to assess the neuromuscular function of healthy subjects (e.g., to understand the human neuromuscular system) and patients (e.g., to diagnose neurologic disorders) in both fatigued and non-fatigued muscles.1 Commonly, electrically evoked potentials accompanied by electromyographic and dynamographic methods are used to assess the central and peripheral mechanisms of the human neuromuscular system in vivo. These central and peripheral neuromuscular parameters must be reproducible to detect and justify cross-sectional and longitudinal changes. The triceps surae is a muscle that is frequently examined in neuromuscular research.2–5 This muscle consists of the soleus (SOL), lateral gastrocnemius (LG), and medial gastrocnemius (MG) muscles. Additional Supporting Information may be found in the online version of this article. Abbreviations: ANOVA, analysis of variance; CV, coefficient of variation; EMG, electromyography; LG, lateral gastrocnemius; MG, medial gastrocnemius; Hmax20%, maximal H-reflex (Hoffmann reflex) amplitude during 20% maximal voluntary contraction; ICC, intraclass correlation coefficient; LOA, limits of agreement; Mmax20%, maximal M-wave amplitude during 20% maximal voluntary contraction; Msup, maximal M-wave amplitude during maximal voluntary contraction; MVC, maximal voluntary contraction; RMS, root mean square; SOL, soleus; VAL, voluntary activation level; Vsup, maximal H-reflex amplitude during maximal voluntary contraction Key words: H-reflex, M-wave; neuromuscular parameters; reliability, twitch interpolation technique; V-wave; voluntary muscle activity Correspondence to: N. Stutzig; e-mail: [email protected]. de C 2015 Wiley Periodicals, Inc. V
Published online 14 July 2015 in Wiley Online Library (wileyonlinelibrary.com). DOI 10.1002/mus.24767
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These muscles are innervated by the tibial nerve but differ in their function and composition (for review see Tucker et al.6). Most reproducibility studies have observed SOL but did not examine LG and MG.7–9 Therefore, we examined the reproducibility of the triceps surae and focused on the most relevant parameters in neuromuscular research and clinical studies. The typical electromyographic (EMG) and mechanical parameters used to describe neuromuscular mechanisms are: (1) the M-wave; (2) the Hoffmann reflex (H-reflex) and V-wave; (3) voluntary muscle activity; and (4) the voluntary activation level. The M-wave is the compound muscle action potential obtained in response to a single peripheral electrical stimulus and is used to determine peripheral changes (e.g., decreased propagation of the action potential on the muscle fiber membrane) and normalize EMG parameters (e.g., training studies). The M-wave is usually evoked at rest or during voluntary isometric contraction.8,10 No studies have examined the reproducibility of the M-wave in the MG and LG. The H-reflex measures spinal reflex activity and can be evoked by a single peripheral electrical stimulus of afferent fibers.11,12 Clinicians use the H-reflexes of the SOL, MG, and LG to diagnose neurologic disorders, such as S1 and/or L5 radiculopathy.13 In EMG research, the H-reflex is usually recorded from SOL.12 Zehr12 recommended that Hreflexes be evoked in subjects who are holding a similar level of voluntary contraction. However, studies have not yet tested the reproducibility of H-reflexes evoked during constant voluntary contraction. The H-reflex for the SOL was recently reported to be reproducible when evoked in a resting muscle.7–9,14 The V-wave is a variant of the H-reflex that is determined using a supramaximal electrical stimulus during a maximal voluntary contraction (MVC).15 This parameter measures the efferent neural drive while also reflecting spinal reflex excitability. Under the precondition of averaging 8 MVCs, Solstad et al.10 found that the V-wave is substantially reproducible for SOL and MG. In practice, this process is timeconsuming (or fatiguing) and may be problematic, considering the high number of MVCs required. In particular, if further neuromuscular tests such as twitch interpolation are performed, H-reflexes MUSCLE & NERVE
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FIGURE 1. Experimental design. The left squares (solid frames) show the overall study design, and the right square (dotted frame) shows the neuromuscular tests performed during each session.
during voluntary contraction and maximal dynamic contractions must also be performed. Voluntary muscle activity is usually assessed using EMG16,17 during voluntary contraction. The reproducibility of muscle activity during the MVC varies between SOL, LG, and MG.14 Differences between interday sessions may be due to differences in electrode positioning and changes in skin resistance.17 The voluntary activation level is a mechanical parameter that can be determined using the twitch interpolation technique, which delivers 1 or more stimuli to the motor axons during voluntary contraction. The increase in torque due to stimulation determines the voluntary activation level (VAL). The reproducibility of VAL for plantar flexion was reported to have an intraclass correlation coefficient (ICC) of 0.60.18 In this study, we aimed to examine the reproducibility of the neuromuscular parameters of SOL, LG, and MG. In particular, we: (1) observe the reproducibility after increased time periods between test sessions (1 and 2 weeks); (2) provide data on the reproducibility of voluntary muscle activity and the H-reflex during voluntary contraction in all muscles of the triceps surae; and (3) provide a comprehensive data set of the reproducibility of neuromuscular parameters. Different statistical methods were used to examine reproducibility: (1) relative reproducibility assumes that individual measurements within a group will maintain their position within the group over repeated measurements; whereas (2) absolute reproducibility indicates the extent to which a score varies for repeated measurements.19 METHODS Subjects.
Thirteen subjects (8 women and 5 men, age 27.4 6 5.1 years, mass 69.5 6 12.6 kg, height 174.1 6 8.2 cm, body mass index 22.8 6 2.7) participated in this study. All subjects reported an average activity level and were free of orthopedic problems. The participants were informed about
Reproducibility of Neuromuscular Parameters
the purpose and risks of the experiments and provided written consent. Approval for the project was obtained from the cantonal ethics committee of Z€ urich, Switzerland (ID: KEK-ZH-Nr. 2011-0247/4). The study was conducted in accordance with the latest Declaration of Helsinki. Test Design. Neuromuscular tests were performed during 3 sessions, which were separated by at least 1 week 6 1 day (Fig. 1). Previous studies showed that the H-reflex may be modulated by variations in posture and time of day.11 Therefore, efforts were made to ensure that the measurements were performed in the same posture and at the same time. In a single test session, a standardized warmup consisting of 15 submaximal voluntary plantar flexions was performed. The subjects then performed 2 MVCs separated by a 1-minute rest. During each MVC, the subjects: (1) were encouraged verbally to push as hard as possible; and (2) received visual feedback from the torque curve.20 When the MVCs differed by >5%, a third MVC was performed. The maximal M-wave and H-reflex were evoked during 20% MVC. Subsequently, the twitch interpolation technique was used to determine the VAL. Therefore, 2 MVCs were performed, separated by a 1-minute rest. Two further MVCs were performed to obtain the V-wave and the corresponding M-wave at 100% MVC. Finally, 4 maximal M-waves were evoked at rest (Fig. 1). Torque Recording. Subjects were seated with 1 foot attached to a plantar flexor device.21 The knee and ankle angles were secured at 1008 and 908, respectively. The torque was recorded using a data acquisition system (MP150; BIOPAC, Inc., Goleta, California) at a sampling rate of 2 kHZ. Electromyographic Recording. EMG measurements were conducted on SOL, LG, and MG. The positions of interest were located as follows: (1) the innervation zones of each muscle were located MUSCLE & NERVE
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using a 16-channel EMG array (OT Bioelettronica, Turin, Italy), as recommended by Rainoldi et al.22; and (2) the position between the innervation zones and the distal part of the muscle was marked. Subjects were asked to refresh the mark between test sessions. In the second and third sessions, the markings were used to position the EMG electrodes. The skin was prepared according to the recommendations of the SENIAM (Surface Electromyography for the Non-Invasive Assessment of Muscles) project, such that the positions of interest were shaved, abraded, and cleaned with alcohol (70%). Two self-adhesive Ag/AgCl electrodes were affixed to the skin overlying each muscle at the marked position at an interelectrode distance of 20 mm. The electrodes were then connected to the BIOPAC system. EMG data were recorded at a sampling rate of 2 kHZ, pre-amplified (31,000), bandpass filtered (bandwidth 10–500 HZ), and stored on a computer.23
To obtain the V-wave, a supramaximal stimulus was delivered to the tibial nerve during MVC.25 The V-wave (Vsup) and the concomitant M-wave (Msup) were assessed, and the Vsup/Msup ratio was calculated.10 Two MVCs were conducted, and the parameters were averaged. Twitch Interpolation. The VAL was determined using the twitch interpolation technique.26 During MVC, 2 supramaximal stimuli (10-ms time interval) were delivered to the tibial nerve. The distance between the torque plateau and peak torque (triggered by the electrical stimulation) was calculated and defined as a superimposed doublet. Three seconds after the MVC, a second paired stimulus was delivered. The distance between the torque baseline and the peak torque of the twitch was defined as a potentiated doublet. VAL was calculated as follows26:
Voluntary activation level5½12ðsuperimposed doublet
Muscle Activity.
=potentiated doubledÞ 3100
Electrical stimuli (1-ms pulse width, rectangular waveform) were delivered by a high-voltage stimulator (Model DS7AH; Digitimer, Hertfordshire, UK). A cathode was affixed in the midline of the popliteal fossa to electrically stimulate the tibial nerve. The anode (self-adhesive electrode, size 5 3 10 cm; Compex, Ecublens, Switzerland) was placed approximately 2 cm superior to the patella. The H-reflex curve was determined at 20% MVC. Subjects received visual feedback to maintain constant torque. Starting at the H-reflex threshold, the current was increased by 1 mA every 10 s until the H-reflex was on the descending part of the curve. The maximal peak-to-peak amplitude of the H-reflex was defined as Hmax20%.24 The Mwave was determined during 20% MVC starting at 10 mA. The current was increased by 10 mA every 10 s until the twitch torque and the peak-to-peak amplitude of SOL reached a plateau. A plateau was defined as 3 consecutive consistent values. The current was increased by 20% based on the previous current level (supramaximal stimulus). Subsequently, 4 consecutive electrical stimulations at an interval of 10 s were delivered to the tibial nerve. The average of the 4 M-waves was denoted as Mmax20%.3
Statistical Analysis. The mean and standard deviation (SD) were calculated for all parameters. The Kolmogorov–Smirnov test was used to analyze the normal distribution of the data and revealed that all parameters were normally distributed. A 1-way analysis of variance (ANOVA) with repeated measures (session 1 vs. session 2 vs. session 3) was used to assess differences between test sessions. The Mauchly test of sphericity was used to test variance homogeneity. In case of main effects, post-hoc analyses were performed using the Bonferroni test. The effect size was calculated using partial eta-squared (gP2) for ANOVA and the Cohen d27 for post-hoc tests. The level of significance was set at P < 0.05. The relative and absolute reproducibility are common statistical parameters to assess the reproducibility of repeated measurements. Relative reproducibility assumes that individual measurements within a group will maintain their position within the group over repeated measurements, whereas absolute reproducibility indicates the extent to which a score varies for repeated measurements.19 Both statistical methods should be cited for reproducibility studies.14,28,29 Thus, the relative and absolute reproducibility were calculated. The relative reproducibility is the degree to which individuals maintain the experimental conditions (e.g., their position in a sample with repeated measurements)29,30 and is assessed using a correlation coefficient. The ICC (1,2) (randomeffect model, single-measure reproducibility) was selected for this study. The ICC was calculated for all parameters except for VAL, due to ceiling effects associated with the VAL measurement.14
The muscle activities of SOL, LG, and MG during MVC were assessed using surface EMG. The raw EMG data were rectified and smoothed (obtaining root mean square, RMS) for >250 samples.3 The maximal RMS of each muscle was determined over a time frame of 500 ms around the MVC peak torque. The RMS data of 2 trials were averaged and defined as muscle activation. Evoked Potentials.
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Table 1. Level of significance (P) and effect sizes (gP2, d) for ANOVA and post-hoc tests. Post-hoc tests Main effects (ANOVA) Parameter Mmax20% MG RMS LG RMS LG/Mmax Vsup
P 0.038 0.008 0.026 0.007
Effect size
(gP2)
0.24 0.33 0.26 0.34
Measurement 1–2
Measurement 2–3
Measurement 1–3
P
Effect size (d)
P
Effect size (d)
P
Effect size (d)
1.000 0.678 0.605 0.052
0.11 0.25 0.45 0.57
0.083 0.027 0.104 1.000
0.32 0.64 0.87 0.60
0.187 0.041 0.047 0.059
0.25 0.40 0.47 0.09
ANOVA, analysis of variance; Mmax20% MG, maximal M-wave at 20% maximal voluntary contraction torque of medial gastrocnemius; RMS LG, non-normalized EMG activity of lateral gastrocnemius; RMS GL/Mmax, normalized EMG activity of lateral gastrocnemius; Vsup, V-wave.
The ranges of reproducibility based on the ICC were as follows: (1) 0–0.10, almost no reproducibility; (2) 0.11–0.40, slight reproducibility; (3) 0.41– 0.60, fair reproducibility; (4) 0.61–0.80, moderate reproducibility; and (5) 0.81–1.00, substantial reproducibility.31 The absolute reproducibility measures the degree to which repeated measurements vary and was assessed for all parameters. Therefore, the coefficient of variation (CV) and standard error of the measurement (SEM) were calculated. The CV was determined from the SD of the repeated measures for a single case divided by the mean of the repeated measures for a single case. The SEM was calculated as the mean of the difference for a single case divided by the square root of the number of measurements.28 Furthermore, the limits of agreement (LOA) were calculated for the VAL only. Therefore, Bland–Altman plots were generated for each pair of measurements (session 1 vs. 2, session 2 vs. 3, session 1 vs. 3). Subsequently, the presence of heteroscedasticity was calculated by examining the correlation (R2) between the absolute differences and the mean values of the session pairs. Homoscedasticity was defined as an R2 value between 0 and 0.1, whereas heteroscedasticity was
FIGURE 2. Bland–Altman plots of the differences (session 2 – session 1) versus the mean values for sessions 1 and 2 for voluntary activation level. The solid bold lines at the top and bottom represent the 95% limits of agreement. The solid bold line in the middle represents the mean of the differences. The dotted line represents the regression line. Reproducibility of Neuromuscular Parameters
defined as R2 > 0.1. The LOA ratio was calculated as follows: LOA5½ðSDdiffs =AVGmeans Þ31:963100 where SDdiffs is the standard deviation of all different scores, and AVGmeans is the average of all mean scores.14 Statistical analyses were performed using SPSS (SPSS, Inc., Chicago, Illinois). RESULTS
ANOVA revealed no significant differences for most parameters (30 of 34). Main time effects were found for Mmax20% MG (P 5 0.038; gP2 5 0.24), as well as for RMS LG (P 5 0.008, gP2 5 0.33), RMS/ Mmax LG (P 5 0.026, gP2 5 0.26), and Vsup LG (P 5 0.007, gP2 5 0.34). Post-hoc analysis data are shown in Table 1. Note that significant differences were found in 3 of 4 parameters for the LG. The reproducibility of all parameters is shown in Table S1 (refer to Supplementary Material, available online). Analyses of VAL revealed that the R2 values were 0.1)
0.01
0.91
11.91
No
0.06
22.54
14.31
No
0.02
21.63
14.22
No
0.03
21.09
13.48
No
Measurement 1 vs. 2: analyses of measurements for session 1 vs. 2; R2: correlations between absolute differences and the mean values of the session pairs.
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the H-reflex. The innervating nerve will be stimulated supramaximally to evoke the V-wave. Solstad et al.10 conducted an interday reproducibility study for SOL and MG. When the V-wave was normalized to the corresponding M-wave, both SOL and MG showed substantial reproducibility in their study. However, the reproducibility of Vsup/Msup was lower for all muscles in our study (Table 1), which may be due to the lower number of trials. Solstad et al.10 performed 8 MVCs and averaged the Vsup/Msup ratio. In our study, only 2 MVCs were performed. Therefore, 2 trials are insufficient to obtain reproducible V-waves, particularly for the SOL and LG. Thus, the V-wave can be examined in long-term studies for SOL and MG, but it must be normalized to the corresponding M-wave. The number of trials should be increased. Reproducibility of Mechanical Data. The level of voluntary activation can be determined using the twitch interpolation technique.20,28,37 For this purpose, paired stimuli (10-ms interval) are transmitted to the nerve during MVC (superimposed stimuli).38,39 After performing MVC, a second pair of stimuli (control stimuli) is evoked as a reference to the superimposed stimuli. Therefore, we tested separately whether paired stimuli and MVCs were reproducible parameters. In accordance with Clark et al.,14 we observed substantial reproducibility for the MVC. However, Clark et al.14 observed moderate reproducibility for paired stimuli (ICC 5 0.7), whereas we observed substantial correlations. Differences may be due to the longer time between test sessions (4 weeks). Based on our results, we can recommend the use of paired stimuli and MVC for the twitch interpolation technique. The determination of VAL was homoscedastic, and the CV values were 4.6%, suggesting good reproducibility. The results are comparable with those of Clark et al.14 and Todd et al.,18 who reported CV values of 3.9% and 0.9%, respectively, for VAL. Therefore, the twitch interpolation technique is a reproducible method to determine VAL for plantar flexors over time periods of several weeks. Some limitations of this study need to be addressed. The experiments were performed in a position with the knee bent (1008). In this position, the bi-articular LG and MG are shortened and thus do not work in the plateau region of the force–length relation.40 Muscle length is known to influence force output,40 H-reflex,41–43 and Mwave.44 Thus, the small changes in muscle length potentially induced by variations in knee angle would impact the force and neuromuscular parameters, particularly for MG and LG. Therefore, we documented the subject’s position to the best of our ability to ensure that the subject was placed in Reproducibility of Neuromuscular Parameters
exactly the same position during each session. In contrast to most studies that examine reproducibility on consecutive days, we examined reproducibility over time. This approach may be important for intervention studies conducted over several weeks (e.g., 2 weeks de-training45,46). However, many intervention studies proceed for >2 weeks (e.g., training studies47,48). These time periods should be examined in future studies. This study has shown substantial and moderate reproducibility for most EMG parameters and mechanical data. Previous studies recommended that H-reflexes be evoked during voluntary contraction to maximize the amplitude. Based on our results, we conclude that this method can be used for study designs that include follow-up measurements. However, the innervation zones for each muscle should be determined before neuromuscular testing to obtain reproducible results. In general, the SOL measurements were more reproducible than the MG and LG measurements. We further conclude that SOL and MG should be selected for longitudinal studies of the adaptations of the triceps surae. The authors gratefully acknowledge Dr. Nicola A. Maffiuletti (Schulthessklinik Clinic Zurich, Zurich, Switzerland) for his cooperation throughout the study, and Dr. Marco A. Minetto (Department of Medical Sciences, University of Turin, Turin, Italy) for methodological mentoring and support. REFERENCES 1. Maffiuletti NA. Physiological and methodological considerations for the use of neuromuscular electrical stimulation. Eur J Appl Physiol 2010;110:223–234. 2. Boerio D, Jubeau M, Zory R, Maffiuletti NA. Central and peripheral fatigue after electrostimulation-induced resistance exercise. Med Sci Sports Exerc 2005;37:973–978. 3. Stutzig N, Siebert T. Influence of joint position on synergistic muscle activity after fatigue of a single muscle head. Muscle Nerve 2015;51: 259–267. 4. 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. 5. Tucker KJ, Turker KS. Muscle spindle feedback differs between the soleus and gastrocnemius in humans. Somatosens Motil Res 2004;21: 189–197. 6. Tucker KJ, Tuncer M, Turker KS. A review of the H-reflex and M-wave in the human triceps surae. Hum Mov Sci 2005;24:667–688. 7. Christie A, Lester S, LaPierre D, Gabriel DA. Reliability of a new measure of H-reflex excitability. Clin Neurophysiol 2004;115:116–123. 8. Palmieri RM, Hoffman MA, Ingersoll CD. Intersession reliability for H-reflex measurements arising from the soleus, peroneal, and tibialis anterior musculature. Int J Neurosci 2002;112:841–850. 9. Hoch MC, Krause BA. Intersession reliability of H:M ratio is greater than the H-reflex at a percentage of M-max. Int J Neurosci 2009;119: 345–352. 10. Solstad GM, Fimland MS, Helgerud J, Iversen VM, Hoff J. Test-retest reliability of v-wave responses in the soleus and gastrocnemius medialis. J Clin Neurophysiol 2011;28:217–221. 11. Brinkworth RS, Tuncer M, Tucker KJ, Jaberzadeh S, Turker KS. Standardization of H-reflex analyses. J Neurosci Methods 2007;162: 1–7. 12. Zehr PE. Considerations for use of the Hoffmann reflex in exercise studies. Eur J Appl Physiol 2002;86:455–468. 13. Young A, Getty J, Jackson A, Kirwan E, Sullivan M, Parry CW. Variations in the pattern of muscle innervation by the L5 and S1 nerve roots. Spine (Phila Pa 1976) 1983;8:616–624. 14. Clark BC, Cook SB, Ploutz-Snyder LL. Reliability of techniques to assess human neuromuscular function in vivo. J Electromyogr Kinesiol 2007;17:90–101.
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15. Aagaard P, Simonsen EB, Andersen JL, Magnusson P, Dyhre-Poulsen P. Neural adaptation to resistance training: changes in evoked V-wave and H-reflex responses. J Appl Physiol 2002;92:2309–2318. 16. DeLuca CJ. The use of surface electromyography in biomechanics. J Appl Biomech 1997;13:135–163. 17. Merletti R, Rainoldi A, Farina D. Surface electromyography for noninvasive characterization of muscle. Exerc Sport Sci Rev 2001;29: 20–25. 18. Todd G, Gorman RB, Gandevia SC. Measurement and reproducibility of strength and voluntary activation of lower-limb muscles. Muscle Nerve 2004;29:834–842. 19. Myrer JW, Schulthies SS, Fellingham GW. Relative and absolute reliability of the KT-2000 arthrometer for uninjured knees. Testing at 67, 89, 134, and 178 N and manual maximum forces. Am J Sports Med 1996;24:104–108. 20. Gandevia SC. Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 2001;81:1725–1789. 21. Crivelli G, Borrani F, Capt R, Gremion G, Maffiuletti NA. Actions of beta2-adrenoceptor agonist drug on human soleus muscle contraction. Med Sci Sports Exerc 2013;45:1252–1260. 22. Rainoldi A, Bullock-Saxton JE, Cavarretta F, Hogan N. Repeatability of maximal voluntary force and of surface EMG variables during voluntary isometric contraction of quadriceps muscles in healthy subjects. J Electromyogr Kinesiol 2001;11:425–438. 23. Hermens HJ, Freriks B, Merletti R, Stegeman D, Blok J, Rau G, et al. European recommendations for surface ElectroMyoGraphy—results of the SENIAM project. Enschede, The Netherlands: Roessingh Research and Development; 1999. 24. Pierrot-Deseilligny E, Burke DJ. The circuitry of the human spinal cord: neuroplasticity and corticospinal mechanisms. Cambridge, UK: Cambridge University Press; 2012. 25. Fimland MS, Helgerud J, Gruber M, Leivseth G, Hoff J. Functional maximal strength training induces neural transfer to single-joint tasks. Eur J Appl Physiol 2009;107:21–29. 26. Allen GM, Gandevia SC, McKenzie DK. Reliability of measurements of muscle strength and voluntary activation using twitch interpolation. Muscle Nerve 1995;18:593–600. 27. Cohen J. Statistical power analysis for the behavioral sciences. Hillsdale, NJ: Lawrence Erlbaum Associates; 1988. 28. Place N, Maffiuletti NA, Martin A, Lepers R. Assessment of the reliability of central and peripheral fatigue after sustained maximal voluntary contraction of the quadriceps muscle. Muscle Nerve 2007;35: 486–495. 29. Atkinson G, Nevill AM. Statistical methods for assessing measurement error (reliability) in variables relevant to sports medicine. Sports Med 1998;26:217–238. 30. Baumgarter TA. Norm-referenced measurement: reliability. In: Safrit MJ, Wood TM, editors. Measurement concepts in physical education and exercise science. Champaign, IL: Human Kinetics; 1989. p 45–72. 31. Shrout PE. Measurement reliability and agreement in psychiatry. Stat Methods Med Res 1998;7:301–317.
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32. Saitou K, Masuda T, Michikami D, Kojima R, Okada M. Innervation zones of the upper and lower limb muscles estimated by using multichannel surface EMG. J Hum Ergol (Tokyo) 2000;29:35–52. 33. Enoka RM. Neuromechanics of human movement. Champaign, IL: Human Kinetics; 2008. 34. Rainoldi A, Melchiorri G, Caruso I. A method for positioning electrodes during surface EMG recordings in lower limb muscles. J Neurosci Methods 2004;134:37–43. 35. Alrowayeh HN, Sabbahi MA, Etnyre B. Similarities and differences of the soleus and gastrocnemius H-reflexes during varied body postures, foot positions, and muscle function: multifactor designs for repeated measures. BMC Neurol 2011;11:65. 36. Burke D, Adams RW, Skuse NF. The effects of voluntary contraction on the H reflex of human limb muscles. Brain 1989;112:417–433. 37. Stutzig N, Siebert T. Muscle force compensation among synergistic muscles after fatigue of a single muscle. Hum Mov Sci 2015;42:273– 287. 38. Folland JP, Williams AG. Methodological issues with the interpolated twitch technique. J Electromyogr Kinesiol 2007;17:317–327. 39. Herbert RD, Gandevia SC. Twitch interpolation in human muscles: mechanisms and implications for measurement of voluntary activation. J Neurophysiol 1999;82:2271–2283. 40. 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. 41. Garland SJ, Gerilovsky L, Enoka RM. Association between muscle architecture and quadriceps femoris H-reflex. Muscle Nerve 1994;17: 581–592. 42. Hayashi R, Tako K, Tokuda T, Yanagisawa N. Comparison of amplitude of human soleus H-reflex during sitting and standing. Neurosci Res 1992;13:227–233. 43. Pinniger GJ, Nordlund M, Steele JR, Cresswell AG. H-reflex modulation during passive lengthening and shortening of the human triceps surae. J Physiol 2001;534:913–923. 44. Patikas DA, Kotzamanidis C, Robertson C, Koceja D. The effect of the ankle joint angle in the level of soleus Ia afferent presynaptic inhibition. Electromyogr Clin Neurophysiol 2004;44:503–511. 45. Trappe SW, Trappe TA, Lee GA, Widrick JJ, Costill DL, Fitts RH. Comparison of a space shuttle flight (STS-78) and bed rest on human muscle function. J Appl Physiol 2001;91:57–64. 46. Widrick JJ, Trappe SW, Romatowski JG, Riley DA, Costill DL, Fitts RH. Unilateral lower limb suspension does not mimic bed rest or spaceflight effects on human muscle fiber function. J Appl Physiol 2002;93:354–360. 47. Maffiuletti NA, Dugnani S, Folz M, Di Pierno E, Mauro F. Effect of combined electrostimulation and plyometric training on vertical jump height. Med Sci Sports Exerc 2002;34:1638–1644. 48. Gondin J, Brocca L, Bellinzona E, D’Antona G, Maffiuletti NA, Miotti D, et al. Neuromuscular electrical stimulation training induces atypical adaptations of the human skeletal muscle phenotype: a functional and proteomic analysis. J Appl Physiol 2011;110:433–450.
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Diagnostic tests of the neuromuscular system are important for clinicians and researchers to assess the neuromuscular function of healthy subjects (e.g., to understand the human neuromuscular system) and patients (e.g., to diagnose neurologic disorders) in both fatigued and non-fatigued muscles.1 Commonly, electrically evoked potentials accompanied by electromyographic and dynamographic methods are used to assess the central and peripheral mechanisms of the human neuromuscular system in vivo. These central and peripheral neuromuscular parameters must be reproducible to detect and justify cross-sectional and longitudinal changes. The triceps surae is a muscle that is frequently examined in neuromuscular research.2–5 This muscle consists of the soleus (SOL), lateral gastrocnemius (LG), and medial gastrocnemius (MG) muscles. Additional Supporting Information may be found in the online version of this article. Abbreviations: ANOVA, analysis of variance; CV, coefficient of variation; EMG, electromyography; LG, lateral gastrocnemius; MG, medial gastrocnemius; Hmax20%, maximal H-reflex (Hoffmann reflex) amplitude during 20% maximal voluntary contraction; ICC, intraclass correlation coefficient; LOA, limits of agreement; Mmax20%, maximal M-wave amplitude during 20% maximal voluntary contraction; Msup, maximal M-wave amplitude during maximal voluntary contraction; MVC, maximal voluntary contraction; RMS, root mean square; SOL, soleus; VAL, voluntary activation level; Vsup, maximal H-reflex amplitude during maximal voluntary contraction Key words: H-reflex, M-wave; neuromuscular parameters; reliability, twitch interpolation technique; V-wave; voluntary muscle activity Correspondence to: N. Stutzig; e-mail: [email protected]. de C 2015 Wiley Periodicals, Inc. V
Published online 14 July 2015 in Wiley Online Library (wileyonlinelibrary.com). DOI 10.1002/mus.24767
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These muscles are innervated by the tibial nerve but differ in their function and composition (for review see Tucker et al.6). Most reproducibility studies have observed SOL but did not examine LG and MG.7–9 Therefore, we examined the reproducibility of the triceps surae and focused on the most relevant parameters in neuromuscular research and clinical studies. The typical electromyographic (EMG) and mechanical parameters used to describe neuromuscular mechanisms are: (1) the M-wave; (2) the Hoffmann reflex (H-reflex) and V-wave; (3) voluntary muscle activity; and (4) the voluntary activation level. The M-wave is the compound muscle action potential obtained in response to a single peripheral electrical stimulus and is used to determine peripheral changes (e.g., decreased propagation of the action potential on the muscle fiber membrane) and normalize EMG parameters (e.g., training studies). The M-wave is usually evoked at rest or during voluntary isometric contraction.8,10 No studies have examined the reproducibility of the M-wave in the MG and LG. The H-reflex measures spinal reflex activity and can be evoked by a single peripheral electrical stimulus of afferent fibers.11,12 Clinicians use the H-reflexes of the SOL, MG, and LG to diagnose neurologic disorders, such as S1 and/or L5 radiculopathy.13 In EMG research, the H-reflex is usually recorded from SOL.12 Zehr12 recommended that Hreflexes be evoked in subjects who are holding a similar level of voluntary contraction. However, studies have not yet tested the reproducibility of H-reflexes evoked during constant voluntary contraction. The H-reflex for the SOL was recently reported to be reproducible when evoked in a resting muscle.7–9,14 The V-wave is a variant of the H-reflex that is determined using a supramaximal electrical stimulus during a maximal voluntary contraction (MVC).15 This parameter measures the efferent neural drive while also reflecting spinal reflex excitability. Under the precondition of averaging 8 MVCs, Solstad et al.10 found that the V-wave is substantially reproducible for SOL and MG. In practice, this process is timeconsuming (or fatiguing) and may be problematic, considering the high number of MVCs required. In particular, if further neuromuscular tests such as twitch interpolation are performed, H-reflexes MUSCLE & NERVE
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FIGURE 1. Experimental design. The left squares (solid frames) show the overall study design, and the right square (dotted frame) shows the neuromuscular tests performed during each session.
during voluntary contraction and maximal dynamic contractions must also be performed. Voluntary muscle activity is usually assessed using EMG16,17 during voluntary contraction. The reproducibility of muscle activity during the MVC varies between SOL, LG, and MG.14 Differences between interday sessions may be due to differences in electrode positioning and changes in skin resistance.17 The voluntary activation level is a mechanical parameter that can be determined using the twitch interpolation technique, which delivers 1 or more stimuli to the motor axons during voluntary contraction. The increase in torque due to stimulation determines the voluntary activation level (VAL). The reproducibility of VAL for plantar flexion was reported to have an intraclass correlation coefficient (ICC) of 0.60.18 In this study, we aimed to examine the reproducibility of the neuromuscular parameters of SOL, LG, and MG. In particular, we: (1) observe the reproducibility after increased time periods between test sessions (1 and 2 weeks); (2) provide data on the reproducibility of voluntary muscle activity and the H-reflex during voluntary contraction in all muscles of the triceps surae; and (3) provide a comprehensive data set of the reproducibility of neuromuscular parameters. Different statistical methods were used to examine reproducibility: (1) relative reproducibility assumes that individual measurements within a group will maintain their position within the group over repeated measurements; whereas (2) absolute reproducibility indicates the extent to which a score varies for repeated measurements.19 METHODS Subjects.
Thirteen subjects (8 women and 5 men, age 27.4 6 5.1 years, mass 69.5 6 12.6 kg, height 174.1 6 8.2 cm, body mass index 22.8 6 2.7) participated in this study. All subjects reported an average activity level and were free of orthopedic problems. The participants were informed about
Reproducibility of Neuromuscular Parameters
the purpose and risks of the experiments and provided written consent. Approval for the project was obtained from the cantonal ethics committee of Z€ urich, Switzerland (ID: KEK-ZH-Nr. 2011-0247/4). The study was conducted in accordance with the latest Declaration of Helsinki. Test Design. Neuromuscular tests were performed during 3 sessions, which were separated by at least 1 week 6 1 day (Fig. 1). Previous studies showed that the H-reflex may be modulated by variations in posture and time of day.11 Therefore, efforts were made to ensure that the measurements were performed in the same posture and at the same time. In a single test session, a standardized warmup consisting of 15 submaximal voluntary plantar flexions was performed. The subjects then performed 2 MVCs separated by a 1-minute rest. During each MVC, the subjects: (1) were encouraged verbally to push as hard as possible; and (2) received visual feedback from the torque curve.20 When the MVCs differed by >5%, a third MVC was performed. The maximal M-wave and H-reflex were evoked during 20% MVC. Subsequently, the twitch interpolation technique was used to determine the VAL. Therefore, 2 MVCs were performed, separated by a 1-minute rest. Two further MVCs were performed to obtain the V-wave and the corresponding M-wave at 100% MVC. Finally, 4 maximal M-waves were evoked at rest (Fig. 1). Torque Recording. Subjects were seated with 1 foot attached to a plantar flexor device.21 The knee and ankle angles were secured at 1008 and 908, respectively. The torque was recorded using a data acquisition system (MP150; BIOPAC, Inc., Goleta, California) at a sampling rate of 2 kHZ. Electromyographic Recording. EMG measurements were conducted on SOL, LG, and MG. The positions of interest were located as follows: (1) the innervation zones of each muscle were located MUSCLE & NERVE
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using a 16-channel EMG array (OT Bioelettronica, Turin, Italy), as recommended by Rainoldi et al.22; and (2) the position between the innervation zones and the distal part of the muscle was marked. Subjects were asked to refresh the mark between test sessions. In the second and third sessions, the markings were used to position the EMG electrodes. The skin was prepared according to the recommendations of the SENIAM (Surface Electromyography for the Non-Invasive Assessment of Muscles) project, such that the positions of interest were shaved, abraded, and cleaned with alcohol (70%). Two self-adhesive Ag/AgCl electrodes were affixed to the skin overlying each muscle at the marked position at an interelectrode distance of 20 mm. The electrodes were then connected to the BIOPAC system. EMG data were recorded at a sampling rate of 2 kHZ, pre-amplified (31,000), bandpass filtered (bandwidth 10–500 HZ), and stored on a computer.23
To obtain the V-wave, a supramaximal stimulus was delivered to the tibial nerve during MVC.25 The V-wave (Vsup) and the concomitant M-wave (Msup) were assessed, and the Vsup/Msup ratio was calculated.10 Two MVCs were conducted, and the parameters were averaged. Twitch Interpolation. The VAL was determined using the twitch interpolation technique.26 During MVC, 2 supramaximal stimuli (10-ms time interval) were delivered to the tibial nerve. The distance between the torque plateau and peak torque (triggered by the electrical stimulation) was calculated and defined as a superimposed doublet. Three seconds after the MVC, a second paired stimulus was delivered. The distance between the torque baseline and the peak torque of the twitch was defined as a potentiated doublet. VAL was calculated as follows26:
Voluntary activation level5½12ðsuperimposed doublet
Muscle Activity.
=potentiated doubledÞ 3100
Electrical stimuli (1-ms pulse width, rectangular waveform) were delivered by a high-voltage stimulator (Model DS7AH; Digitimer, Hertfordshire, UK). A cathode was affixed in the midline of the popliteal fossa to electrically stimulate the tibial nerve. The anode (self-adhesive electrode, size 5 3 10 cm; Compex, Ecublens, Switzerland) was placed approximately 2 cm superior to the patella. The H-reflex curve was determined at 20% MVC. Subjects received visual feedback to maintain constant torque. Starting at the H-reflex threshold, the current was increased by 1 mA every 10 s until the H-reflex was on the descending part of the curve. The maximal peak-to-peak amplitude of the H-reflex was defined as Hmax20%.24 The Mwave was determined during 20% MVC starting at 10 mA. The current was increased by 10 mA every 10 s until the twitch torque and the peak-to-peak amplitude of SOL reached a plateau. A plateau was defined as 3 consecutive consistent values. The current was increased by 20% based on the previous current level (supramaximal stimulus). Subsequently, 4 consecutive electrical stimulations at an interval of 10 s were delivered to the tibial nerve. The average of the 4 M-waves was denoted as Mmax20%.3
Statistical Analysis. The mean and standard deviation (SD) were calculated for all parameters. The Kolmogorov–Smirnov test was used to analyze the normal distribution of the data and revealed that all parameters were normally distributed. A 1-way analysis of variance (ANOVA) with repeated measures (session 1 vs. session 2 vs. session 3) was used to assess differences between test sessions. The Mauchly test of sphericity was used to test variance homogeneity. In case of main effects, post-hoc analyses were performed using the Bonferroni test. The effect size was calculated using partial eta-squared (gP2) for ANOVA and the Cohen d27 for post-hoc tests. The level of significance was set at P < 0.05. The relative and absolute reproducibility are common statistical parameters to assess the reproducibility of repeated measurements. Relative reproducibility assumes that individual measurements within a group will maintain their position within the group over repeated measurements, whereas absolute reproducibility indicates the extent to which a score varies for repeated measurements.19 Both statistical methods should be cited for reproducibility studies.14,28,29 Thus, the relative and absolute reproducibility were calculated. The relative reproducibility is the degree to which individuals maintain the experimental conditions (e.g., their position in a sample with repeated measurements)29,30 and is assessed using a correlation coefficient. The ICC (1,2) (randomeffect model, single-measure reproducibility) was selected for this study. The ICC was calculated for all parameters except for VAL, due to ceiling effects associated with the VAL measurement.14
The muscle activities of SOL, LG, and MG during MVC were assessed using surface EMG. The raw EMG data were rectified and smoothed (obtaining root mean square, RMS) for >250 samples.3 The maximal RMS of each muscle was determined over a time frame of 500 ms around the MVC peak torque. The RMS data of 2 trials were averaged and defined as muscle activation. Evoked Potentials.
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Table 1. Level of significance (P) and effect sizes (gP2, d) for ANOVA and post-hoc tests. Post-hoc tests Main effects (ANOVA) Parameter Mmax20% MG RMS LG RMS LG/Mmax Vsup
P 0.038 0.008 0.026 0.007
Effect size
(gP2)
0.24 0.33 0.26 0.34
Measurement 1–2
Measurement 2–3
Measurement 1–3
P
Effect size (d)
P
Effect size (d)
P
Effect size (d)
1.000 0.678 0.605 0.052
0.11 0.25 0.45 0.57
0.083 0.027 0.104 1.000
0.32 0.64 0.87 0.60
0.187 0.041 0.047 0.059
0.25 0.40 0.47 0.09
ANOVA, analysis of variance; Mmax20% MG, maximal M-wave at 20% maximal voluntary contraction torque of medial gastrocnemius; RMS LG, non-normalized EMG activity of lateral gastrocnemius; RMS GL/Mmax, normalized EMG activity of lateral gastrocnemius; Vsup, V-wave.
The ranges of reproducibility based on the ICC were as follows: (1) 0–0.10, almost no reproducibility; (2) 0.11–0.40, slight reproducibility; (3) 0.41– 0.60, fair reproducibility; (4) 0.61–0.80, moderate reproducibility; and (5) 0.81–1.00, substantial reproducibility.31 The absolute reproducibility measures the degree to which repeated measurements vary and was assessed for all parameters. Therefore, the coefficient of variation (CV) and standard error of the measurement (SEM) were calculated. The CV was determined from the SD of the repeated measures for a single case divided by the mean of the repeated measures for a single case. The SEM was calculated as the mean of the difference for a single case divided by the square root of the number of measurements.28 Furthermore, the limits of agreement (LOA) were calculated for the VAL only. Therefore, Bland–Altman plots were generated for each pair of measurements (session 1 vs. 2, session 2 vs. 3, session 1 vs. 3). Subsequently, the presence of heteroscedasticity was calculated by examining the correlation (R2) between the absolute differences and the mean values of the session pairs. Homoscedasticity was defined as an R2 value between 0 and 0.1, whereas heteroscedasticity was
FIGURE 2. Bland–Altman plots of the differences (session 2 – session 1) versus the mean values for sessions 1 and 2 for voluntary activation level. The solid bold lines at the top and bottom represent the 95% limits of agreement. The solid bold line in the middle represents the mean of the differences. The dotted line represents the regression line. Reproducibility of Neuromuscular Parameters
defined as R2 > 0.1. The LOA ratio was calculated as follows: LOA5½ðSDdiffs =AVGmeans Þ31:963100 where SDdiffs is the standard deviation of all different scores, and AVGmeans is the average of all mean scores.14 Statistical analyses were performed using SPSS (SPSS, Inc., Chicago, Illinois). RESULTS
ANOVA revealed no significant differences for most parameters (30 of 34). Main time effects were found for Mmax20% MG (P 5 0.038; gP2 5 0.24), as well as for RMS LG (P 5 0.008, gP2 5 0.33), RMS/ Mmax LG (P 5 0.026, gP2 5 0.26), and Vsup LG (P 5 0.007, gP2 5 0.34). Post-hoc analysis data are shown in Table 1. Note that significant differences were found in 3 of 4 parameters for the LG. The reproducibility of all parameters is shown in Table S1 (refer to Supplementary Material, available online). Analyses of VAL revealed that the R2 values were 0.1)
0.01
0.91
11.91
No
0.06
22.54
14.31
No
0.02
21.63
14.22
No
0.03
21.09
13.48
No
Measurement 1 vs. 2: analyses of measurements for session 1 vs. 2; R2: correlations between absolute differences and the mean values of the session pairs.
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the H-reflex. The innervating nerve will be stimulated supramaximally to evoke the V-wave. Solstad et al.10 conducted an interday reproducibility study for SOL and MG. When the V-wave was normalized to the corresponding M-wave, both SOL and MG showed substantial reproducibility in their study. However, the reproducibility of Vsup/Msup was lower for all muscles in our study (Table 1), which may be due to the lower number of trials. Solstad et al.10 performed 8 MVCs and averaged the Vsup/Msup ratio. In our study, only 2 MVCs were performed. Therefore, 2 trials are insufficient to obtain reproducible V-waves, particularly for the SOL and LG. Thus, the V-wave can be examined in long-term studies for SOL and MG, but it must be normalized to the corresponding M-wave. The number of trials should be increased. Reproducibility of Mechanical Data. The level of voluntary activation can be determined using the twitch interpolation technique.20,28,37 For this purpose, paired stimuli (10-ms interval) are transmitted to the nerve during MVC (superimposed stimuli).38,39 After performing MVC, a second pair of stimuli (control stimuli) is evoked as a reference to the superimposed stimuli. Therefore, we tested separately whether paired stimuli and MVCs were reproducible parameters. In accordance with Clark et al.,14 we observed substantial reproducibility for the MVC. However, Clark et al.14 observed moderate reproducibility for paired stimuli (ICC 5 0.7), whereas we observed substantial correlations. Differences may be due to the longer time between test sessions (4 weeks). Based on our results, we can recommend the use of paired stimuli and MVC for the twitch interpolation technique. The determination of VAL was homoscedastic, and the CV values were 4.6%, suggesting good reproducibility. The results are comparable with those of Clark et al.14 and Todd et al.,18 who reported CV values of 3.9% and 0.9%, respectively, for VAL. Therefore, the twitch interpolation technique is a reproducible method to determine VAL for plantar flexors over time periods of several weeks. Some limitations of this study need to be addressed. The experiments were performed in a position with the knee bent (1008). In this position, the bi-articular LG and MG are shortened and thus do not work in the plateau region of the force–length relation.40 Muscle length is known to influence force output,40 H-reflex,41–43 and Mwave.44 Thus, the small changes in muscle length potentially induced by variations in knee angle would impact the force and neuromuscular parameters, particularly for MG and LG. Therefore, we documented the subject’s position to the best of our ability to ensure that the subject was placed in Reproducibility of Neuromuscular Parameters
exactly the same position during each session. In contrast to most studies that examine reproducibility on consecutive days, we examined reproducibility over time. This approach may be important for intervention studies conducted over several weeks (e.g., 2 weeks de-training45,46). However, many intervention studies proceed for >2 weeks (e.g., training studies47,48). These time periods should be examined in future studies. This study has shown substantial and moderate reproducibility for most EMG parameters and mechanical data. Previous studies recommended that H-reflexes be evoked during voluntary contraction to maximize the amplitude. Based on our results, we conclude that this method can be used for study designs that include follow-up measurements. However, the innervation zones for each muscle should be determined before neuromuscular testing to obtain reproducible results. In general, the SOL measurements were more reproducible than the MG and LG measurements. We further conclude that SOL and MG should be selected for longitudinal studies of the adaptations of the triceps surae. The authors gratefully acknowledge Dr. Nicola A. Maffiuletti (Schulthessklinik Clinic Zurich, Zurich, Switzerland) for his cooperation throughout the study, and Dr. Marco A. Minetto (Department of Medical Sciences, University of Turin, Turin, Italy) for methodological mentoring and support. REFERENCES 1. Maffiuletti NA. Physiological and methodological considerations for the use of neuromuscular electrical stimulation. Eur J Appl Physiol 2010;110:223–234. 2. Boerio D, Jubeau M, Zory R, Maffiuletti NA. Central and peripheral fatigue after electrostimulation-induced resistance exercise. Med Sci Sports Exerc 2005;37:973–978. 3. Stutzig N, Siebert T. Influence of joint position on synergistic muscle activity after fatigue of a single muscle head. Muscle Nerve 2015;51: 259–267. 4. 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. 5. Tucker KJ, Turker KS. Muscle spindle feedback differs between the soleus and gastrocnemius in humans. Somatosens Motil Res 2004;21: 189–197. 6. Tucker KJ, Tuncer M, Turker KS. A review of the H-reflex and M-wave in the human triceps surae. Hum Mov Sci 2005;24:667–688. 7. Christie A, Lester S, LaPierre D, Gabriel DA. Reliability of a new measure of H-reflex excitability. Clin Neurophysiol 2004;115:116–123. 8. Palmieri RM, Hoffman MA, Ingersoll CD. Intersession reliability for H-reflex measurements arising from the soleus, peroneal, and tibialis anterior musculature. Int J Neurosci 2002;112:841–850. 9. Hoch MC, Krause BA. Intersession reliability of H:M ratio is greater than the H-reflex at a percentage of M-max. Int J Neurosci 2009;119: 345–352. 10. Solstad GM, Fimland MS, Helgerud J, Iversen VM, Hoff J. Test-retest reliability of v-wave responses in the soleus and gastrocnemius medialis. J Clin Neurophysiol 2011;28:217–221. 11. Brinkworth RS, Tuncer M, Tucker KJ, Jaberzadeh S, Turker KS. Standardization of H-reflex analyses. J Neurosci Methods 2007;162: 1–7. 12. Zehr PE. Considerations for use of the Hoffmann reflex in exercise studies. Eur J Appl Physiol 2002;86:455–468. 13. Young A, Getty J, Jackson A, Kirwan E, Sullivan M, Parry CW. Variations in the pattern of muscle innervation by the L5 and S1 nerve roots. Spine (Phila Pa 1976) 1983;8:616–624. 14. Clark BC, Cook SB, Ploutz-Snyder LL. Reliability of techniques to assess human neuromuscular function in vivo. J Electromyogr Kinesiol 2007;17:90–101.
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15. Aagaard P, Simonsen EB, Andersen JL, Magnusson P, Dyhre-Poulsen P. Neural adaptation to resistance training: changes in evoked V-wave and H-reflex responses. J Appl Physiol 2002;92:2309–2318. 16. DeLuca CJ. The use of surface electromyography in biomechanics. J Appl Biomech 1997;13:135–163. 17. Merletti R, Rainoldi A, Farina D. Surface electromyography for noninvasive characterization of muscle. Exerc Sport Sci Rev 2001;29: 20–25. 18. Todd G, Gorman RB, Gandevia SC. Measurement and reproducibility of strength and voluntary activation of lower-limb muscles. Muscle Nerve 2004;29:834–842. 19. Myrer JW, Schulthies SS, Fellingham GW. Relative and absolute reliability of the KT-2000 arthrometer for uninjured knees. Testing at 67, 89, 134, and 178 N and manual maximum forces. Am J Sports Med 1996;24:104–108. 20. Gandevia SC. Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 2001;81:1725–1789. 21. Crivelli G, Borrani F, Capt R, Gremion G, Maffiuletti NA. Actions of beta2-adrenoceptor agonist drug on human soleus muscle contraction. Med Sci Sports Exerc 2013;45:1252–1260. 22. Rainoldi A, Bullock-Saxton JE, Cavarretta F, Hogan N. Repeatability of maximal voluntary force and of surface EMG variables during voluntary isometric contraction of quadriceps muscles in healthy subjects. J Electromyogr Kinesiol 2001;11:425–438. 23. Hermens HJ, Freriks B, Merletti R, Stegeman D, Blok J, Rau G, et al. European recommendations for surface ElectroMyoGraphy—results of the SENIAM project. Enschede, The Netherlands: Roessingh Research and Development; 1999. 24. Pierrot-Deseilligny E, Burke DJ. The circuitry of the human spinal cord: neuroplasticity and corticospinal mechanisms. Cambridge, UK: Cambridge University Press; 2012. 25. Fimland MS, Helgerud J, Gruber M, Leivseth G, Hoff J. Functional maximal strength training induces neural transfer to single-joint tasks. Eur J Appl Physiol 2009;107:21–29. 26. Allen GM, Gandevia SC, McKenzie DK. Reliability of measurements of muscle strength and voluntary activation using twitch interpolation. Muscle Nerve 1995;18:593–600. 27. Cohen J. Statistical power analysis for the behavioral sciences. Hillsdale, NJ: Lawrence Erlbaum Associates; 1988. 28. Place N, Maffiuletti NA, Martin A, Lepers R. Assessment of the reliability of central and peripheral fatigue after sustained maximal voluntary contraction of the quadriceps muscle. Muscle Nerve 2007;35: 486–495. 29. Atkinson G, Nevill AM. Statistical methods for assessing measurement error (reliability) in variables relevant to sports medicine. Sports Med 1998;26:217–238. 30. Baumgarter TA. Norm-referenced measurement: reliability. In: Safrit MJ, Wood TM, editors. Measurement concepts in physical education and exercise science. Champaign, IL: Human Kinetics; 1989. p 45–72. 31. Shrout PE. Measurement reliability and agreement in psychiatry. Stat Methods Med Res 1998;7:301–317.
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Reproducibility of Neuromuscular Parameters
32. Saitou K, Masuda T, Michikami D, Kojima R, Okada M. Innervation zones of the upper and lower limb muscles estimated by using multichannel surface EMG. J Hum Ergol (Tokyo) 2000;29:35–52. 33. Enoka RM. Neuromechanics of human movement. Champaign, IL: Human Kinetics; 2008. 34. Rainoldi A, Melchiorri G, Caruso I. A method for positioning electrodes during surface EMG recordings in lower limb muscles. J Neurosci Methods 2004;134:37–43. 35. Alrowayeh HN, Sabbahi MA, Etnyre B. Similarities and differences of the soleus and gastrocnemius H-reflexes during varied body postures, foot positions, and muscle function: multifactor designs for repeated measures. BMC Neurol 2011;11:65. 36. Burke D, Adams RW, Skuse NF. The effects of voluntary contraction on the H reflex of human limb muscles. Brain 1989;112:417–433. 37. Stutzig N, Siebert T. Muscle force compensation among synergistic muscles after fatigue of a single muscle. Hum Mov Sci 2015;42:273– 287. 38. Folland JP, Williams AG. Methodological issues with the interpolated twitch technique. J Electromyogr Kinesiol 2007;17:317–327. 39. Herbert RD, Gandevia SC. Twitch interpolation in human muscles: mechanisms and implications for measurement of voluntary activation. J Neurophysiol 1999;82:2271–2283. 40. 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. 41. Garland SJ, Gerilovsky L, Enoka RM. Association between muscle architecture and quadriceps femoris H-reflex. Muscle Nerve 1994;17: 581–592. 42. Hayashi R, Tako K, Tokuda T, Yanagisawa N. Comparison of amplitude of human soleus H-reflex during sitting and standing. Neurosci Res 1992;13:227–233. 43. Pinniger GJ, Nordlund M, Steele JR, Cresswell AG. H-reflex modulation during passive lengthening and shortening of the human triceps surae. J Physiol 2001;534:913–923. 44. Patikas DA, Kotzamanidis C, Robertson C, Koceja D. The effect of the ankle joint angle in the level of soleus Ia afferent presynaptic inhibition. Electromyogr Clin Neurophysiol 2004;44:503–511. 45. Trappe SW, Trappe TA, Lee GA, Widrick JJ, Costill DL, Fitts RH. Comparison of a space shuttle flight (STS-78) and bed rest on human muscle function. J Appl Physiol 2001;91:57–64. 46. Widrick JJ, Trappe SW, Romatowski JG, Riley DA, Costill DL, Fitts RH. Unilateral lower limb suspension does not mimic bed rest or spaceflight effects on human muscle fiber function. J Appl Physiol 2002;93:354–360. 47. Maffiuletti NA, Dugnani S, Folz M, Di Pierno E, Mauro F. Effect of combined electrostimulation and plyometric training on vertical jump height. Med Sci Sports Exerc 2002;34:1638–1644. 48. Gondin J, Brocca L, Bellinzona E, D’Antona G, Maffiuletti NA, Miotti D, et al. Neuromuscular electrical stimulation training induces atypical adaptations of the human skeletal muscle phenotype: a functional and proteomic analysis. J Appl Physiol 2011;110:433–450.
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