Journal of Applied Biomechanics, 2014, 30, 255-261 http://dx.doi.org/10.1123/jab.2013-0178 © 2014 Human Kinetics, Inc.
An Official Journal of ISB www.JAB-Journal.com ORIGINAL RESEARCH
Mechanomyographic and Electromyographic Responses During Fatiguing Eccentric Muscle Actions of the Leg Extensors Clayton L. Camic,1 Terry J. Housh,2 Jorge M. Zuniga,3 Haley C. Bergstrom,2 Richard J. Schmidt,2 and Glen O. Johnson2 1University
of Wisconsin-La Crosse; 2University of Nebraska-Lincoln; 3Creighton University, Omaha
The purpose of the current study was to examine the patterns of responses for torque, mechanomyographic (MMG) amplitude, MMG frequency, electromyographic (EMG) amplitude, and EMG frequency across 30 repeated maximal eccentric muscle actions of the leg extensors. Eleven moderately trained females performed an eccentric fatigue protocol at 30°/s with MMG and EMG signals recorded from the vastus lateralis. The results indicated there were significant (P < .05) decreases in MMG frequency (linear, r2 = .395), EMG frequency (linear, r2 = .177), and torque (linear, r2 = .570; % decline = 9.8 ± 13.3%); increases in MMG amplitude (linear, r2 = .783); and no change in EMG amplitude (r2 = .003). These findings suggested that the neural strategies used to modulate torque during fatiguing eccentric muscle actions involved de-recruitment of motor units, reduced firing rates, and synchronization. In addition, the decreases in eccentric torque were more closely associated with changes in MMG frequency than EMG frequency. Thus, these findings indicated that MMG frequency, compared with EMG frequency, more accurately tracks fatigue during repeated maximal eccentric muscle actions. Keywords: isokinetic, fatigue, muscle lengthening, motor control Muscle actions defined as “eccentric” occur when the load torque applied against a muscle exceeds the torque generated by the muscle, thereby forcing it to lengthen in a contracted state.1 These types of muscle actions have been of significant interest to clinicians, therapists, and other health professionals based on their importance in functional movements, rehabilitation strategies, and athletic performance.1–4 In the research setting, considerable attention has also been focused on the aspects of eccentric muscle actions related to muscle soreness, fatigue-resistance, and neural activation. For example, the delayed onset muscle soreness that typically occurs 24–48 hours following an unaccustomed bout of physical activity has been attributed to the cellular damage that accompanies the eccentric phase of muscular contraction.5,6 Previous findings have also indicated that eccentric muscle actions exhibit a greater resistance to fatigue compared with other types of muscle actions. Specifically, it has been shown3,7,8 that eccentric, isokinetic torque levels can be maintained across repeated, maximal repetitions, whereas isometric9 and concentric, isokinetic10,11 torque levels decrease 50–65%. This fatigue-resistance is due, in part, to the greater mechanical efficiency associated with musclelengthening exercise as well as the unique neural strategies that involve incomplete activation, yet rotation of recruitment among all available muscle fibers.3,8 As demonstrated by Aagaard et al.,12 these mechanisms are likely responsible for the greater torque achieved during muscle-lengthening contractions compared with muscle-shortening contractions, despite lower activation levels by the nervous system. Clayton L. Camic is with Exercise and Sport Science, University of Wisconsin–La Crosse, La Crosse, WI. Jorge M. Zuniga is with Exercise Science, Creighton University, Omaha, NE. Terry J. Housh, Haley C. Bergstrom, Richard J. Schmidt, and Glen O. Johnson are with Nutrition and Health Sciences, University of Nebraska–Lincoln, Lincoln, NE. Address author correspondence to Clayton L. Camic at
[email protected].
Mechanomyography (MMG) and electromyography (EMG) are commonly used tools for the noninvasive assessment of muscle function that provide information related to the low-frequency lateral oscillations of contracting skeletal muscle fibers and the electrical activity involved in their activation, respectively. In particular, the MMG signal reflects the mechanical processes that occur with muscle activation and is a function of the gross lateral movements at the beginning and end of a muscle contraction, smaller subsequent lateral oscillations generated at the resonant frequency of the muscle, and dimensional changes of the active fibers.13 The EMG signal, however, provides global information related to the action potentials of the motor units that lie within the pickup area of the recording electrodes.14 Recent investigations7,9–11,15,16 have used simultaneous MMG and EMG measurements in the evaluation of neuromuscular fatigue at various exercise intensities. For example, the fatigue-induced increases in EMG amplitude that occur during submaximal exercise have been shown to reflect increases in motor unit recruitment, firing rates, and synchronization.17 During fatigue protocols that involve repeated maximal muscle actions, however, fatigue is characterized by decreases in EMG amplitude that have been attributed to the de-recruitment of activated motor units.9,10 In the frequency domain of the EMG signal, fatigue is identified by compression of the power density spectrum and decreases in EMG frequency that are the result of decreases in muscle fiber conduction velocity.18 It has been also demonstrated that the amplitude of the MMG signal is determined by motor unit recruitment and synchronization, whereas MMG frequency reflects the global firing rates of unfused, activated motor units.13,19 Recent investigations have examined the MMG and EMG responses during repeated maximal isometric9,15 and concentric, isokinetic7,10,11,15 muscle actions. Based on the patterns (ie, linear, quadratic, cubic) of responses in torque, MMG amplitude, MMG frequency, EMG amplitude, and EMG frequency across repetition number, these authors7,9–11,15 reported decreases in torque that 255
256 Camic et al.
were the result of progressive decreases in activated type II fibers, motor unit discharge rates, muscular compliance, and muscle fiber conduction velocity. No previous studies, however, have provided comprehensive MMG and EMG data regarding the neural activation strategies that modulate torque production during fatiguing eccentric muscle actions. Therefore, the purpose of the current study was to examine the patterns of responses for torque, MMG amplitude, MMG frequency, EMG amplitude, and EMG frequency across 30 repeated maximal eccentric muscle actions of the leg extensors. Based on the findings of previous investigations,2,3,7–9 we hypothesized that the eccentric protocol would result in decreased MMG amplitude, MMG frequency, and EMG frequency, but no change in torque or EMG amplitude.
Methods Subjects Eleven moderately trained (3.0 ± 1.5 resistance training hr⋅wk–1, 4.8 ± 2.2 aerobic training hr⋅wk–1), female subjects (mean age ± SD = 21.2 ± 1.4 years; body mass = 61.9 ± 5.8 kg; height = 166.7 ± 2.4 cm) volunteered to visit the laboratory on two occasions (separated by 48–72 hours) and were instructed to avoid exercise for 48 hours before each visit. According to the American College of Sports Medicine,20 moderate training includes aerobic activity performed for a minimum of 30 minutes five times per week. The study was approved by the University Institutional Review Board for Human Subjects and all subjects completed a health history questionnaire and signed a written informed consent before testing.
Orientation Session (Visit 1) The first laboratory visit consisted of an orientation session to familiarize the subjects with the testing protocols. For warm-up, each subject practiced 10 submaximal eccentric isokinetic muscle actions of the leg extensors at 30°⋅s–1 on a calibrated Cybex 6000 isokinetic dynamometer corresponding to approximately 50% of their maximum. Following the warm-up, the subjects practiced 10 maximal eccentric muscle actions at 30°⋅s–1 for assessment of peak torque.
Fatigue Session (Visit 2) During the second laboratory visit, each subject performed a warmup of 10 eccentric isokinetic muscle actions at 30°⋅s–1 corresponding to approximately 50–75% of their maximum. After two minutes of rest, the subjects completed an eccentric isokinetic fatigue protocol of 30 consecutive maximal eccentric leg extension muscle actions at 30°⋅s–1 followed by passive leg extension movements. The range of motion was standardized from 0° to 90° of leg flexion at the knee. During each maximal muscle action, the subjects were encouraged to produce as much torque as possible.
EMG and MMG Measurements During Visit 2, a bipolar (30 mm center to center) surface electrode (circular 4 mm diameter silver/silver chloride, BIOPAC Systems, Inc., Santa Barbara, CA) arrangement was placed on the dominant thigh over the vastus lateralis according to the SENIAM Project.21 The EMG signals were amplified (gain: ×1000) using differential amplifiers (EMG 100, Biopac Systems, Inc., Santa Barbara, CA, bandwidth = 10–500 Hz) and digitally bandpass filtered (fourthorder Butterworth) at 10–500 Hz. The MMG signals from the vastus lateralis were detected using an accelerometer (Entran EGAS FT 10, bandwidth 0–200 Hz, dimensions: 1.0 × 1.0 × 0.5 cm, mass 1.0 g sensitivity 10 mV/g) placed between the EMG electrodes.
Signal Processing The raw MMG and EMG signals were digitized at 1000 samples/ second with a 12-bit analog-to-digital converter (Model MP100, Biopac Systems, Inc.). All signal processing was performed using LabVIEW programming software (version 7.1, National Instruments, Austin, TX). The MMG (m⋅s–2) and EMG (microvolts root mean square, μVrms) amplitude values as well as the MMG and EMG mean power frequency values (Hz) were calculated for a time period that corresponded to a 30° range of motion from approximately 30° to 60° of leg flexion. For the mean power frequency analyses, each data segment was processed with a Hamming window and the discrete Fourier transform algorithm, and was selected to represent the power spectrum in accordance with Hermens et al.21
Table 1 The results of the polynomial regression analyses on a subject-by-subject basis for torque, MMG amplitude, MMG frequency, EMG amplitude, and EMG frequency (n = 11) Subject 1
Torque Linear
R2 0.386
MMG Amplitude Linear
R2 0.174
MMG Frequency Linear
R2 0.204
EMG Amplitude NS
R2 0.054
EMG Frequency Quadratic
R2 0.273
2
Linear
0.187
Linear
0.551
Linear
0.269
NS
0.001
Linear
0.248
3
Linear
0.329
Quadratic
0.509
NS
0.102
Quadratic
0.362
NS
0.005
4
NS
0.008
Linear
0.335
Linear
0.206
Linear
0.472
Linear
0.123
5
Quadratic
0.558
Quadratic
0.337
NS
0.005
NS
0.001
Quadratic
0.292
6
Quadratic
0.155
Linear
0.415
Cubic
0.286
Linear
0.162
Linear
0.150
7
Linear
0.600
Linear
0.612
Linear
0.294
NS
0.099
NS
0.075
8
Linear
0.163
Linear
0.194
Linear
0.128
NS
0.017
Linear
0.418
9
NS
0.001
Linear
0.389
Cubic
0.246
Quadratic
0.591
NS
0.099
10
Quadratic
0.397
Linear
0.252
Linear
0.517
Linear
0.724
Linear
0.722
11
Linear
0.260
NS
0.053
Linear
0.275
NS
0.016
Linear
0.184
Eccentric Fatigue 257
Statistical Analyses The relationships for torque, MMG amplitude, MMG frequency, EMG amplitude, and EMG frequency versus repetition number during each eccentric muscle action were examined using polynomial regression analysis (SPSS software program). An alpha of P < .05 was considered statistically significant for all comparisons.
Results The results indicated there were significant decreases across the 30 eccentric muscle actions for mean (± SE) torque (linear, r2 = .570; % decline = 9.8 ± 13.3%) (Figure 1), MMG frequency (linear, r2 = .395) (Figure 2), and EMG frequency (linear, r2 = .177) (Figure 3), increases in MMG amplitude (linear, r2 = .783) (Figure 2), and no change in EMG amplitude (r2 = .003) (Figure 3). In addition, the patterns of responses on a subject-by-subject basis indicated that the majority of the subjects (at least 6 of the 11) exhibited changes in torque, MMG amplitude, MMG frequency, EMG amplitude, and EMG frequency versus repetition number that were consistent with those of the mean (± SE) (Table 1).
Discussion Muscular fatigue has traditionally been defined as a failure to maintain the required or expected force.22 In the present investigation, there was a significant negative torque versus repetition number relationship (linear, r2 = .570) for the 30 repeated eccentric muscle actions that was associated with a percent decline of 9.8 ± 13.3%. These findings indicated that the 30 repeated maximal eccentric muscle actions of the leg extensors at 30°⋅s–1 used in the current study resulted in effects on torque that were consistent with muscular fatigue. Previous investigations2,3,7,8,23 have reported conflicting data regarding the changes in torque across repeated maximal eccentric muscle actions of the leg extensors. For example, the studies
that have examined repeated maximal eccentric muscle actions at velocities ranging from 60°⋅s–1 to 180°⋅s–1 have shown increases3,7 or no changes2,8 in torque across repetitions. Grabiner and Owings,23 however, reported decreases in torque across 25 maximal eccentric muscle actions at the same isokinetic velocity (30°⋅s–1) used in the current study. Tesch et al3 proposed that eccentric muscle actions have a greater metabolic demand at slower isokinetic velocities, whereas eccentric muscle actions performed at faster velocities may be associated with a greater rotation of activated motor units. This suggestion3 was consistent with the findings of Chapman et al24 that indicated there were greater decreases in eccentric torque across 30 maximal repeated muscle actions of the elbow flexors at 30°⋅s–1 (–29%) compared with 210°⋅s–1 (–18%). In conjunction, the findings of the current investigation and those of others2,3,7,8,23 suggested that the fatigue-resistant characteristics of eccentric muscle actions may be greater at faster compared with slower isokinetic velocities. The physiological mechanisms of fatigue associated with eccentric muscle actions appear to be different compared with those of isometric or concentric muscle actions. For example, the fatigue-induced decreases in isometric and concentric torque have been attributed to increased intramuscular pressure that restricts blood flow to the muscle, results in lower oxygen availability, and promotes the accumulation of metabolic byproducts that have been shown to interfere with the processes of muscular contraction.25 It has been suggested1 that the fatigue-related processes of eccentric muscle actions, however, are less metabolic in nature and more likely the result of mechanical failure. This characteristic of eccentric muscle actions explains, in part, the greater resistance to fatigue exhibited by muscle-lengthening contractions than muscle-shortening contractions. For example, it has been shown that 30–50 repeated maximal isometric or concentric muscle actions were associated with decreases in torque of 23–65%.9–11,15 In the current study, however, the 30 repeated maximal eccentric muscle actions resulted in a decline of 9.8 ± 13.3%. Enoka1 suggested that the fatigue resistance of eccentric muscle actions may also be the result of unique activation strategies by the nervous system. In particular, Beltman et al26 demonstrated that only 80% of maximum eccentric torque of the leg extensors could be attained by voluntary
Figure 1 — The patterns of responses for torque versus repetition number during the repeated maximal eccentric muscle actions. Values expressed as mean (± SE).
258 Camic et al.
Figure 2 — The patterns of responses for mechanomyographic (MMG) amplitude and mean power frequency versus repetition number during the repeated maximal eccentric muscle actions. Values expressed as mean (± SE).
effort compared with the torque production when electrical stimulation was superimposed on the maximal contraction. In contrast, it has also been shown through this technique that approximately 92–93% of maximal torque can be achieved during voluntary isometric and concentric muscle actions.26 Theoretically, incomplete voluntary activation would allow greater rotation of activated motor units during repeated maximal efforts and thus, promote the maintenance of torque.3 This suggestion3 has been supported by the findings of Hortobágyi et al27 that indicated six weeks of eccentric training lead to significant increases in muscle activation and percent declines during eccentric fatigue protocols. These findings suggested that developing the increased ability to fully activate the leg extensors during repeated
eccentric muscle actions results in greater torque, but also greater relative fatigability (% decline). Thus, the fatigue-resistant aspects of eccentric muscle actions may partially be related to incomplete muscle activation and the subsequent greater amount of rotation through the available motor unit pool. Furthermore, these findings27 explain the decline in torque (9.8 ± 13.3%) in the current sample of moderately-trained subjects (3.0 ± 1.5 resistance training hr⋅wk–1) compared with previous studies2,3,7,8 that have shown increases or no change across repetitions in untrained individuals. In the present investigation, the patterns of responses for the amplitude and frequency contents of MMG and EMG signals were examined to assess the neural strategies associated with fatiguing
Eccentric Fatigue 259
Figure 3 — The patterns of responses for electromyographic (EMG) amplitude and mean power frequency versus repetition number during the repeated maximal eccentric muscle actions. Values expressed mean (± SE).
eccentric muscle actions. The results indicated there was no significant relationship (r2 = .003) for EMG amplitude versus repetitions during the repeated eccentric muscle actions. These findings demonstrated that despite a constant level of muscle activation, eccentric torque (linear, r2 = .571) could not be maintained across the 30 repetitions. Other studies3,8 have reported inconsistent data regarding the relationship between EMG amplitude and changes in torque during repeated eccentric muscle actions of the leg extensors. For example, Tesch et al3 found no changes in EMG amplitude that was associated with increases in torque across 32 repeated maximal eccentric muscle actions at 180°⋅s–1. In addition, Kay et al8 reported that both EMG amplitude and torque remained unchanged during
32 repeated maximal eccentric muscle actions at 60°⋅s–1. Therefore, EMG amplitude has been shown to remain constant during eccentric fatigue protocols that result in increases, decreases, or no changes in torque across repetitions. Thus, the present findings and those of others3,8 suggested that there is dissociation between muscle activation as indicated by EMG amplitude and torque during repeated maximal eccentric muscle actions of the leg extensors. Recent investigations9,10,15 have further examined the components of muscle activation through analysis of the amplitude and frequency responses of the MMG signal during fatiguing isometric and isokinetic protocols. Specifically, the decreases in MMG amplitude during repeated maximal isometric9 and concentric10
260 Camic et al.
muscle actions have been attributed to a fatigue-induced impaired contractility and subsequent de-recruitment of motor units as well as increased intramuscular pressure that impairs the dimensional changes of the active muscle fibers. In the current study, however, the repeated eccentric muscle actions led to significant increases (linear, r2 = .783) in MMG amplitude. Orizio et al19 suggested that increases in MMG amplitude may due to factors related to muscle activation such as motor unit recruitment, increased firing rates, or synchronization. In the current study, there is considerable, although indirect, evidence that MMG amplitude increased as the result of motor unit synchronization. Specifically, it has been demonstrated that synchronized motor unit activity is enhanced: 1) during slowlengthening contractions;28 2) with the progression of fatigue;29 3) in slow compared with fast twitch motor units;30 and 4) in those that participate in strength training.31 Therefore, as fatigue progressed across the repeated maximal eccentric muscle actions in the current sample of moderately-trained individuals, there was likely a fatigue-induced de-recruitment of type II motor units that lead to the slow, but progressive decrease in torque, greater reliance on slow twitch fibers, and associated increase in motor unit synchronization as well as MMG amplitude. These factors related to eccentrically induced fatigue were also consistent with changes in the frequency of the MMG and EMG signals. In particular, the de-recruitment of type II motor units as the result of fatigue explains the decreases in MMG frequency (linear, r2 = .395) that reflects the global firing rate and contractile properties of unfused activated motor units.19 In contrast to parallel decreases in EMG frequency and torque that typically occur during isometric and concentric muscle actions, the decreases in eccentric torque were more closely associated with changes in MMG frequency than EMG frequency. Thus, the present findings also indicated that when compared with EMG frequency, MMG frequency more accurately tracks decreases in torque during fatiguing eccentric muscle actions. The polynomial regression analyses indicated there were significant decreases in EMG frequency (linear, r2 = .177) across the repeated eccentric muscle actions. Other investigations3,32 have reported no change in EMG frequency during fatiguing eccentric muscle actions of the leg extensors at 60 and 180°⋅s–1. It is possible that the slower velocity (30°⋅s–1) used in the current study compared with velocities (60 and 180°⋅s–1) used previously3,32 resulted in greater metabolic demand, thereby leading to decreases in EMG frequency.3,24 In particular, fatigue is identified by decreases in EMG frequency that are primarily due to decreases in muscle fiber conduction velocity.17 The underlying mechanism responsible for both has been attributed to a fatigue-induced increase in interstitial potassium that leads to a progressive loss of membrane excitability and subsequent inactivation of motor units.33,34 Due to the accumulation of metabolic byproducts such as potassium that are associated with fatigue, concurrent decreases in EMG frequency and torque during slow eccentric muscle actions may be expected. Provided the fatigue-resistant aspects of eccentric muscle actions related to greater mechanical efficiency and lower metabolic demand (ie, potassium accumulation), however, the findings of the current investigation suggested that EMG frequency should not be used as an indicator of fatigue during muscle-lengthening exercise. In summary, the patterns of responses for torque (decreases, r2 = .570), MMG amplitude (increases, r2 = .783), MMG frequency (decreases, r2 = .395), EMG amplitude (no change, r2 = .003), and EMG frequency (decreases, r2 = .177) suggested that the neural strategies used to modulate torque during repeated maximal eccentric muscle actions involved de-recruitment of fatigued motor units,
reduced firing rates, and increased motor unit synchronization. The present findings also indicated that MMG frequency, not EMG frequency, closely tracked decreases in torque across the fatiguing eccentric muscle actions.
References 1. Enoka RM. Eccentric contractions require unique activation strategies by the nervous system. J Appl Physiol. 1996;81(6):2339–2346. PubMed 2. Gray JC, Chandler JM. Percent decline in peak torque production during repeated concentric and eccentric contractions of the quadriceps femoris muscle. J Orthop Sports Phys Ther. 1989;10(8):309–314. PubMed doi:10.2519/jospt.1989.10.8.309 3. Tesch PA, Dudley GA, Duvoisin MR, Hather BM, Harris RT. Force and EMG signal patterns during repeated bouts of concentric or eccentric muscle actions. Acta Physiol Scand. 1990;138(3):263–271. PubMed doi:10.1111/j.1748-1716.1990.tb08846.x 4. Westing SH, Seger JY. Eccentric and concentric torque-velocity characteristics, torque output comparisons, and gravity effect torque corrections for the quadriceps and hamstring muscles in females. Int J Sports Med. 1989;10(3):175–180. PubMed doi:10.1055/s-2007-1024896 5. Clarkson PM, Tremblay I. Exercise induced muscle damage, repair and adaptation in humans. J Appl Physiol. 1988;65(1):1–6. PubMed 6. Tiidus PM, Ianuzzo CD. Effects of intensity and duration of muscular exercise on delayed soreness and serum enzyme activities. Med Sci Sports Exerc. 1983;15(6):461–465. PubMed doi:10.1249/00005768198315060-00004 7. Perry-Rana SR, Housh TJ, Johnson GO, Bull AJ, Cramer JT. MMG and EMG responses during 25 maximal, eccentric, isokinetic muscle actions. Med Sci Sports Exerc. 2003;35(12):2048–2054. PubMed doi:10.1249/01.MSS.0000099090.73560.77 8. Kay D, St. Clair Gibson A, Mitchell MJ, Lambert MI, Noakes TD. Different neuromuscular recruitment patterns during eccentric, concentric and isometric contractions. J Electromyogr Kinesiol. 2000;10(6):425–431. PubMed doi:10.1016/S1050-6411(00)00031-6 9. Kouzaki M, Shinohara M, Fukunaga T. Non-uniform mechanical activity of quadriceps muscle during fatigue by repeated maximal voluntary contraction in humans. Eur J Appl Physiol. 1999;80(1):9–15. PubMed doi:10.1007/s004210050551 10. Ebersole KT, O’Connor KM, Wier AP. Mechanomyographic and electromyographic responses to repeated concentric muscle actions of the quadriceps femoris. J Electromyogr Kinesiol. 2006;16:149–157. PubMed doi:10.1016/j.jelekin.2005.05.005 11. Perry-Rana SR, Housh TJ, Johnson GO, Bull AJ, Berning JM, Cramer JT. MMG and EMG responses during fatiguing isokinetic muscle contractions at different velocities. Muscle Nerve. 2002;26(3):367–373. PubMed doi:10.1002/mus.10214 12. Aagaard P, Simonsen EB, Andersen JL, Magnusson SP, HalkjærKristensen J, Dyhre-Poulsen P. Neural inhibition during maximal eccentric and concentric quadriceps contraction: effects of resistance training. J Appl Physiol. 2000;89(6):2249–2257. PubMed 13. Orizio C. Muscle sound: bases for the introduction of a mechanomyographic signal in muscle studies. Crit Rev Biomed Eng. 1993;21(3):201–243. PubMed 14. Lynn PA. Direct on-line estimation of muscle fiber conduction velocity by surface electromyography. IEEE Trans Biomed Eng. 1979;26(10):564–571. PubMed doi:10.1109/TBME.1979.326444 15. Camic CL, Housh TJ, Zuniga JM, et al. Electromyographic and mechanomyographic responses across repeated maximal isometric and concentric muscle actions of the leg extensors. J Electromyogr Kinesiol. 2013;23(2):342–348. PubMed doi:10.1016/j.jelekin.2012.09.010
Eccentric Fatigue 261 16. Hendrix CR, Housh TJ, Johnson GO, et al. Comparison of critical force to EMG fatigue thresholds during isometric leg extenson. Med Sci Sports Exerc. 2009;41(4):956–964. PubMed doi:10.1249/ MSS.0b013e318190bdf7 17. Basmajian JV, DeLuca CJ. Muscles alive: their functions revealed by electromyography. Baltimore, MD: Williams & Wilkins; 1985. 18. Broman H, Bilotto G, De Luca CJ. A note on the noninvasive estimation of muscle fiber conduction velocity. IEEE Trans Biomed Eng. 1985;32(5):341–344. PubMed doi:10.1109/TBME.1985.325550 19. Orizio C, Gobbo M, Diemont B, Esposito F, Veicsteinas A. The surface mechanomyogram as a tool to describe the influence of fatigue on biceps brachii motor unit activation strategy. Historical basis and novel evidence. Eur J Appl Physiol. 2003;90(3-4):326–336. PubMed doi:10.1007/s00421-003-0924-1 20. Thompson WR, Gordon NF, Pescatello LS. American College of Sports Medicine. ACSM’s Guidelines for Testing and Prescription. 8th ed. Philadelphia, PA: Lippincott, Williams, & Wilkins; 2010:84–87. 21. Hermens HJ, Freriks B, Merletti R, et al. SENIAM European recommendations for surface electromyography: results of the SENIAM project. Enschede, The Netherlands: Roessingh Research and Development; 1999. 22. Edwards RH. Human muscle function and fatigue. Ciba Found Symp. 1981;82:1–18. PubMed 23. Grabiner MD, Owings TM. Effects of eccentrically and concentrically induced unilateral fatigue on the involved and uninvolved limbs. J Electromyogr Kinesiol. 1999;9(3):185–189. PubMed doi:10.1016/ S1050-6411(98)00031-5 24. Chapman D, Newton M, Sacco P, Nosaka K. Greater muscle damage induced by fast versus slow velocity eccentric exercise. Int J Sports Med. 2006;27(8):591–598. PubMed doi:10.1055/s-2005-865920 25. Edwards RH, Hill DK, Jones DA. Heat production and chemical changes during isometric contractions of the human quadriceps muscle. J Physiol. 1975;251(2):303–315. PubMed
26. Beltman JGM, Sargeant AJ, van Mechelen W, de Haan A. Voluntary activation level and muscle fiber recruitment of human quadriceps during lengthening contractions. J Appl Physiol. 2004;97(2):619–626. PubMed doi:10.1152/japplphysiol.01202.2003 27. Hortobágyi T, Barrier J, Beard D, et al. Greater initial adaptations to submaximal muscle lengthening than maximal shorterning. J Appl Physiol. 1996;81(4):1677–1682. PubMed 28. Semmler JG, Kornatz KW, Dinenno DV, Zhou S, Enoka RM. Motor unit synchronization is enhanced during slow lengthening contractions of a hand muscle. J Physiol. 2002;545(Pt. 2):681–695. PubMed doi:10.1113/jphysiol.2002.026948 29. Kleine BU, Stegeman DF, Mund D, Anders C. Influence of motoneuron firing synchronization on SEMG characteristics in dependence of electrode position. J Appl Physiol. 2001;91(4):1588–1599. PubMed 30. Schmied A, Descarreaux M. Reliability of EMG determinism to detect changes in motor unit synchrony and coherence during submaximal contraction. J Neurosci Methods. 2011;196(2):238–246. PubMed doi:10.1016/j.jneumeth.2011.01.005 31. Semmler JG, Nordstrom MA. Motor unit discharge and force tremor in skill- and strength-trained individuals. Exp Brain Res. 1998;119(1):27–38. PubMed doi:10.1007/s002210050316 32. Denis R, Bringard A, Perrey S. Vastus lateralis oxygenation dynamics during maximal fatiguing concentric and eccentric isokinetic muscle actions. J Electromyogr Kinesiol. 2011;21(2):276–282. PubMed doi:10.1016/j.jelekin.2010.12.006 33. Fortune E, Lowery MM. The effect of extracellular potassium concentration on muscle fiber conduction velocity examined using model simulation. Conf Proc IEEE Eng Med Biol Soc. 2007;2007:2726– 2729. 34. Van Dieën JH, Westebring-van der Putten EP, Kingma I, de Looze MP. Low-level activity of the trunk extensor muscles causes electromyographic manifestations of fatigue in absence of decreased oxygenation. J Electromyogr Kinesiol. 2009;19(3):398–406. PubMed doi:10.1016/j.jelekin.2007.11.010
