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Are there mode-specific and fatigue-related electromechanical delay responses for maximal isokinetic and isometric muscle actions?
Journal of Electromyography and Kinesiology 37 (2017) 9–14
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Are there mode-specific and fatigue-related electromechanical delay responses for maximal isokinetic and isometric muscle actions? Cory M. Smith ⇑, Terry J. Housh, Ethan C. Hill, Joshua L. Keller, Glen O. Johnson, Richard J. Schmidt University of Nebraska – Lincoln, Lincoln, NE, United States
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Article history: Received 9 March 2017 Received in revised form 2 August 2017 Accepted 8 August 2017
Keywords: EMD Excitation-contraction coupling Series elastic component Fatigue Recovery
a b s t r a c t This study used a combined electromyographic, mechanomyographic, and force approach to identify electromechanical delay (EMD) from the onsets of the electromyographic to force signals (EMDE-F), onsets of the electromyographic to mechanomyogrpahic signals (EMDE-M), and onsets of mechanomyographic to force signals (EMDMF). The purposes of the current study were to examine: (1) differences in EMDE-M, EMDMF, and EMDE-F from the vastus lateralis between maximal isokinetic and maximal concentric isometric leg extensions; and (2) the effects of fatigue and recovery on EMDE-M, EMDMF, and EMDE-F. These EMD measures were obtained from twelve men during maximal concentric isokinetic and isometric leg extensions pretest, posttest, and after 3-min and 5-min of recovery from 25 maximal isokinetic leg extensions at 60° s1. The results indicated no differences between maximal isokinetic and isometric muscle actions for EMDE-M, EMDM-F, or EMDE-F during the pretest, posttest, 3-min recovery, and 5-min recovery measurements. These findings support the comparison of voluntary EMD measures between studies with different modes of exercise as long as the methodology for the determination of EMD are consistent. There were, however, fatigue-induced pretest to posttest increases in EMDE-M, EMDM-F, and EMDE-F which remained elongated after 3-min of recovery, but returned to pretest values after 5-min of recovery. Ó 2017 Elsevier Ltd. All rights reserved.
1. Introduction Electromechanical delay (EMD) measures the time delay between the onset of electrical activation of the muscle and the onset of force production (Norman and Komi, 1979). Typically (Vos et al., 1991; Zhou et al., 1998), EMD has been operationally defined as the time period between the onset of the electromyographic (EMG) signal and the onset of force production during a muscle contraction. More recently, however, mechanomyography (MMG) has been used to identify the onset of the lateral oscillations associated with the contraction of skeletal muscle which provides additional information regarding the factors that contribute to EMD (Cè et al., 2013; Esposito, 2013; Smith et al., 2016). Specifically, the onset of the EMG signal identifies when an electrical impulse activates the muscle and the MMG signal reflects the initiation of movement from the activated muscle fibers (Basmajian and De Luca, 1985; Orizio, 1993). The time delay between the onsets of the EMG and MMG signals is a measure of excitation⇑ Corresponding author at: Department of Nutrition and Health Sciences, 110 Ruth Leverton Hall, University of Nebraska-Lincoln, Lincoln, NE 68583-0806, United States. E-mail address: [email protected] (C.M. Smith). http://dx.doi.org/10.1016/j.jelekin.2017.08.001 1050-6411/Ó 2017 Elsevier Ltd. All rights reserved.
contraction coupling which includes the total duration of the events from the motor unit action potentials travelling along the sarcolemma to cross-bridge formation (Merletti and Parker, 2004; Orizio et al., 1997). The onset of the MMG signal to the onset of force production is a measure of the series elastic component which includes the time required to take up the muscle-tendon unit slack before force transmission can occur (Merletti and Parker, 2004; Orizio et al., 1997). Thus, simultaneous assessments of EMG, MMG, and force production allow for the identification of the onset of the EMG signal to the onset of the MMG signal (EMDE-M), the onset of the MMG signal to the onset of force production (EMDM-F), and the onset of the EMG signal to the onset of force production (EMDE-F) (Cè et al., 2015a; Smith et al., 2016, 2017). Therefore, EMDE-M and EMDM-F can measure the relative contributions of excitation-contraction coupling and the series elastic component, respectively, to the overall time duration of EMDE-F (EMDE-M + EMDM-F = EMDE-F). Fatigue-induced increases in voluntary EMD measures are thought to be influenced by a number of factors including: (1) the buildup of metabolic byproducts (Cè et al., 2013, 2015b; Smith et al., 2016; Zhou, 1996), (2) Ca2+efflux from the sarcoplasmic reticulum (Begovic et al., 2014; Cè et al., 2013; Smith et al., 2016, 2017; Zhou, 1996), (3) cross-bridge cycling rate (Begovic
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et al., 2014; Cè et al., 2013; Zhou, 1996), and (4) increases in muscle temperature (Cè et al., 2013). It has been suggested (Cè et al., 2013; Smith et al., 2016, 2017; Zhou et al., 1998) that fatigueinduced excitation-contraction coupling failure due to metabolic disturbances results in an increase in EMDE-M, while increases in the compliance of the series elastic component associated with muscle temperature result in increased EMDM-F. The effects of fatigue on these aspects of voluntary EMD measures, however, have primarily been examined using pre-fatigue versus post-fatigue measurements (Cè et al., 2013; Chan et al., 2001; Taylor et al., 1997). The few studies (Conchola et al., 2013, 2015; Rampichini et al., 2014) that have examined the recovery of EMD have performed isometric (maximal and submaximal) or stimulated muscle actions. Stimulated muscle actions have lower EMD values than those during voluntary muscle actions and do not reflect the motor unit control strategies used to voluntarily contract a muscle (Hopkins et al., 2007). In addition, the studies (Conchola et al., 2013, 2015; Zhou, 1996) which have examined the recovery of voluntary EMD measures did not examine the relative contributions of excitation-contraction coupling (EMDE-M) and the series elastic component (EMDM-F) to the total time duration of EMDE-F. Previous studies (Hopkins et al., 2007; Jenkins et al., 2013; Smith et al., 2017) have examined voluntary EMD measures during dynamic and isometric muscle actions with conflicting results. Specifically, Jenkins et al. (2013) reported greater EMDE-F during voluntary (40.73 ms) isokinetic (dynamic) muscle actions compared to those reported by Hopkins et al. (2007) (22.8 ms) during isometric muscle actions. Smith et al. (2017), however, reported no differences in absolute EMD measures or the relative contributions of EMDE-M and EMDM-F to EMDE-F between maximal isometric and dynamic constant external resistance (DCER) muscle actions in a non-fatigued or fatigued state. No previous studies, however, have examined the effects of isokinetic and isometric muscle actions on EMDE-M, EMDM-F, and EMDE-F under the same voluntary testing conditions. Identifying potential differences in EMD measures between isokinetic and isometric muscle actions will have implications for the comparisons between studies as well as possible clinical applications where most movements are dynamic. Therefore, the purposes of the current study were to identify potential mode-specific differences in EMDE-M, EMDM-F, and EMDE-F during isokinetic and isometric muscle actions as well as if there are fatigue-related differences in the responses of EMDEM, EMDM-F, and EMDE-F with different modes of EMD measures by examining: (1) the differences in EMDE-M, EMDM-F, and EMDEF from the vastus lateralis (VL) between maximal isokinetic and maximal isometric leg extensions; and (2) the effects of fatigue and recovery on EMDE-M, EMDM-F, and EMDE-F. These EMD measures were obtained from twelve men during maximal isokinetic and isometric leg extensions pretest, posttest, and after 3-min and 5-min of recovery from 25 maximal isokinetic leg extensions at 60° s1. Based on previous studies (Hopkins et al., 2007; Jenkins et al., 2013; Smith et al., 2017), we hypothesized that there will be no difference between the maximal isokinetic and isometric EMD values. In addition, we hypothesized (Conchola et al., 2013, 2015; Zhou, 1996) that there would be fatigue-induced increases in EMDE-F, EMDM-F, and EMDE-M which would recover to pretest values at 5-min of recovery.
2. Methods 2.1. Subjects Twelve men (mean ± SD age 23 ± 3 yr; body mass 79.3 ± 8.2 kg; height 173.1 ± 3.9 cm) volunteered to participate in this study. The subjects were recreationally trained (greater than 6-months of
resistance training at least 3 times per week with approximately 50% of their training consisting of lower body exercises), and free from any musculoskeletal injuries or neuromuscular disorders. This study was approved by the Institutional Review Board, and all subjects signed a written informed consent and completed a health history questionnaire prior to participation. 2.2. Experimental approach The study consisted of 2 visits, separated by at least 48-h. The first visit was a familiarization visit which consisted of maximal and submaximal concentric isokinetic and isometric leg extension muscle actions of the dominant leg (based on kicking preference). Emphasis was placed on contracting and relaxing as quickly as possible on command. This was continued until each subject indicated that they were comfortable performing these muscle actions. During both visits, the subjects were able to visualize their muscle activation on a monitor placed in front of them. The visualization of the muscle actions helped emphasize the importance of contracting and relaxing as quickly as possible. During the testing visit, the subjects performed 2 pretest leg extension maximal voluntary isometric contractions (MVIC) and 2 maximal concentric isokinetic leg extension muscle actions at 60° s1 with the dominant leg. The subjects then performed 25 maximal concentric isokinetic leg extension muscle actions at 60° s1. Immediately following the 25 maximal concentric isokinetic leg extension muscle actions, the subjects performed a posttest MVIC and a maximal concentric isokinetic leg extension muscle action at 60° s1. Recovery MVICs and maximal concentric isokinetic leg extension muscle actions at 60° s1 were measured after 3- and 5-min of recovery (Fig. 1). 2.3. Protocol A warmup consisting of 5–7 isokinetic and isometric leg extension muscle actions were performed at approximately 50–70% of their maximal effort. All isometric muscle actions were performed with the dominant leg at a knee joint angle of 120 ° (180 ° being full extension) (Kulig et al., 1984). Following the warmup, the subjects performed 2, randomly ordered, pretest MVIC and maximal concentric isokinetic leg extension muscle actions at 60° s1 with 1-min of rest between each pretest muscle action. The greatest strength of the 2 trials were used for analysis. All isokinetic and isometric muscle actions were performed on a calibrated Cybex II isokinetic dynamometer. After the pretest muscle actions, subjects were given 1-min of rest and then performed the fatiguing protocol consisting of 25 maximal concentric isokinetic leg extension muscle actions at 60° s1. Immediately after the fatiguing protocol, subjects performed a randomly ordered posttest MVIC and maximal concentric isokinetic leg extension muscle action at 60° s1. During the 5-min recovery phase, an MVIC and maximal concentric isokinetic leg extension muscle action at 60° s1 were performed at the 3- and 5-min of recovery time-points following the posttest muscle actions (Fig. 1). 2.4. Electromyographic, mechanomyographic, and force signal acquisition A surface bipolar electrode arrangement (Ag/AgCl, AccuSensor, Lynn Medical, Wixom, MI, USA) was placed on the VL of the dominant leg with an interelectrode distance of 30 mm. The skin was dry shaven, abraded, and cleaned with isopropyl alcohol prior to placing the electrodes. The bipolar electrode arrangement was placed 66% of the distance between the anterior superior iliac spine (ASIS) and the lateral border of the patella and orientated at a 20°
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Fig. 1. Depiction of the order of muscle actions during the protocol. The order of the maximal voluntary isometric contractions (MVIC) and maximal concentric isokinetic leg extension muscle actions were randomized during the pretest, posttest, and recovery measurements. No rest was given between the randomly ordered MVIC and maximal isokinetic leg extensions during the posttest and recovery measurements.
angle to approximate the pennation angle of the muscle fibers (Abe et al., 2000; Hermens et al., 1999). A reference electrode was placed over the ASIS. The EMG signals were zero-meaned, bandpass filtered (fourth-order Butterworth) at 10–500 Hz. The MMG signal was measured using a triaxial accelerometer (EGAS-FT-10/V05, Measurement Specialties Inc., Hampton, VA) placed between the bipolar electrode arrangement on the VL using double-sided adhesive foam tape. The MMG signals were zero-meaned and bandpass filtered (fourth-order Butterworth) at 5–100 Hz. Force was measured using a low-profile pancake load cell (Honeywell Model 41, Morris Plains, NJ) attached to the lever arm. All signals were simultaneously collected through a BioPac MP150 (BioPac System Inc., Goleta, CA) at a sampling frequency of 10,000 Hz. All signal processing and EMD measurements were performed using custom programs written with LabVIEW software (Version 15.0, National Instruments, Austin TX). 2.5. Electromechanical delay The EMD measurements were determined as the time periods from the onset of the EMG signal to the onset of force (EMDE-F), onset of the MMG signal to the onset of force (EMDM-F), and the onset of the EMG signal to the onset of the MMG signal (EMDEM). The onset of EMG, MMG, and force were determined by the condition of 3 standard deviations (SDs) from the mean baseline noise observed for each signal, determined from a 10,000 Hz sample to increase accuracy for determination of the onset of the signals (Begovic et al., 2014; Costa et al., 2012; Stock et al., 2015) and were selected off-line by the primary investigator using a custom written LabVIEW program that provided interactive graphical viewing of each signal (Fig. 2) (Smith et al., 2016, 2017). 2.6. Statistical analysis A 3 (EMD: EMDE-M, EMDM-F, and EMDE-F) 3 (Mode: Isokinetic and Isometric) 4 (Time: pretest, posttest, 3-min recovery, and 5-min recovery) repeated measures ANOVA was performed. Follow-up 2- and 1-way repeated measures ANOVAs and paired sampled t-tests with Tukey’s LSD were performed when appropriate. In addition, partial eta squared values were calculated from the ANOVAs and was calculated as the sums of squared between/sums of squared total. If the assumption of sphericity was violated, the Huynh-Feldt correction was used. An alpha of p 0.05 was considered statistically significant for all statistical analyses (SPSS Version 22.0, Armonk, NY). 3. Results The 3 (EMD: EMDE-M, EMDM-F, and EMDE-F) 3 (Mode: Isokinetic and Isometric) 4 (Time: pretest, posttest, 3-min recovery, and 5-min recovery) repeated measures ANOVA indicated no significant 3-way interaction (p = 0.43, g2p = 0.49) or 2-way interactions for Mode Time (p = 0.97, g2p = 0.03) or EMD Mode
Fig. 2. Graphical representation of the electromyographic, mechanomyographic, and force combination for the determinations of electromechanical delay (EMD). Together, these signals allowed for the identification of the onset of the electromyographic signal to the onset of the mechanomyographic signal (EMDE-M), onset of the mechanomyographic signal to the onset of force production (EMDM-F), and onset of the electromyographic signal to the onset of force production (EMDE-F). This Figure was used with permission from the Primary Investigator (Smith et al., 2017).
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Table 1 Descriptive statistics (mean and standard error) for the electromechanical delay (EMD) measures for the maximal isokinetic and maximal isometric leg extension muscle actions during pretest, posttest, 3-min recovery, and 5-min recovery measurements. The EMD measurements were determined from the onset of the electromyographic signal to the onset of the mechanomyographic signal (EMDE-M), onset of the mechanomyographic signal to the onset of force production (EMDM-F), and the onset of the electromyographic signal to the onset of force production (EMDE-F).
*
y à R
R
EMDE-M (ms)
EMDM-F (ms)à
EMDE-F (ms)
Isokinetic Isometric
20.7 (2.1) 20.5 (1.4)
29.9 (1.9) 28.2 (1.6)
50.6 (3.4) 48.7 (2.2)
Posttest*,y Isokinetic Isometric
30.7 (2.0) 32.0 (1.3)
41.2 (3.6) 35.9 (2.7)
71.9 (4.6) 67.9 (3.0)
3-Min Recovery*,y Isokinetic 25.5 (3.5) Isometric 27.7 (1.8)
36.3 (2.6) 32.6 (2.5)
61.8 (2.9) 60.3 (3.2)
5-Min Recovery* Isokinetic Isometric
32.8 (4.1) 32.3 (2.0)
56.9 (4.4) 54.0 (3.6)
Pretest*
24.1 (2.4) 21.7 (1.8)
No differences between isokinetic and isometric EMDE-M, EMDM-F, or EMDE-F (p > 0.05). Posttest and 3-Min of Recovery were greater than Pretest EMD values (p < 0.01). EMDM-F was greater than EMDE-M at all time-points for both modes (p < 0.01). EMDE-F was greater than EMDE-M and EMDM-F at all time-points for both modes (p < 0.01).
(p = 0.29, g2p = 0.24). There was, however, a significant 2-way interaction for EMD Time (p = 0.03, g2p = 0.89). The follow-up 3 (EMD: EMDE-M, EMDM-F, and EMDE-F) 4 (Time: pretest, posttest, 3-min recovery, and 5-min recovery) repeated measures ANOVA (collapsed across Mode) indicated a significant 2-way interaction (p < 0.01, g2p = 0.69). Post-hoc analyses indicated that for EMDE-M, EMDM-F, and EMDE-F values pretest < posttest (p < 0.01) = 3-min recovery (p = 0.68) > 5-min posttest (p < 0.01) (Table 1 and Fig. 3). In addition, post hoc analyses indicated that EMDE-M < EMDM-F < EMDE-F (p < 0.01) (Table 1 and Fig. 3).
4. Discussion 4.1. Mode-specific differences in electromechanical delay A primary finding in the present study was that there were no differences between modes (isokinetic and isometric) for EMDE-M, EMDM-F, or EMDE-F during the pretest, posttest, 3-min recovery, and 5-min recovery measurements (Table 1 and Fig. 3). These findings were similar to those of Smith et al. (2017) who reported no differences between MVIC and maximal DCER leg extensions for EMDE-M, EMDM-F, or EMDE-F values from the VL measured pretest or following 70% 1 repetition maximum (1-RM) DCER leg extensions to failure. Thus, current and previous findings of Smith et al. (2017) indicated that the mode of muscle action did not influence EMD measures in non-fatigued (pretest), fatigued (posttest), or recovery states. Furthermore, these findings indicated that the time duration for excitation-contraction coupling (EMDE-M) and series elastic component (EMDM-F) were not influenced by the mode of the muscle action performed (isometric, isokinetic, or DCER) (Smith et al., 2017). Therefore, studies which utilized different modes (isometric, isokinetic, and DCER) of maximal voluntary muscle actions can be compared to one another. It is important to note that these findings should not be applied to studies which utilized stimulated or submaximal muscle actions. Future studies are required to further examine these methodological differences and how they relate to EMD measures. In addition, there are potential differences in methodology may result in different absolute EMD measures between studies (Begovic et al., 2014; Jenkins et al., 2013; Zhou et al., 1998, 1995). Some methodological differences which may influence EMD include: sampling frequency, signal conditioning (i.e. filters), definition of the onset of a signal, and the muscle tested (Begovic et al., 2014; Jenkins et al., 2013; Zhou et al., 1998, 1995). Thus, comparison of voluntary EMD measures between studies with different modes of exercise can be made, however, caution should be taken when there are different methodological factors present which may influence the EMD measures.
Fig. 3. The mean electromechanical delay (EMD) measurements from the vastus lateralis during pretest, posttest, 3-min, and 5-min of recovery during the maximal concentric isokinetic and isometric muscle actions. The EMD measurements were determined from the onset of the electromyographic signal to the onset of the mechanomyographic signal (EMDE-M), onset of the mechanomyographic signal to the onset of force production (EMDM-F), and the onset of the electromyographic signal to the onset of force production (EMDE-F).
C.M. Smith et al. / Journal of Electromyography and Kinesiology 37 (2017) 9–14
4.2. Pretest to posttest electromechanical delay In the current study, there were fatigue-induced pretest to posttest increases in EMDE-M, EMDM-F, and EMDE-F for both the maximal concentric isokinetic and isometric muscle actions (Table 1 and Fig. 3). These findings were in agreement with previous studies (Conchola et al., 2013, 2015; Smith et al., 2016, 2017; Zhou et al., 1996) which suggested that fatigue resulted in an increase in EMD measures. For example, Smith et al. (2017) reported pretest to posttest increases in EMDE-M, EMDM-F, and EMDE-F from VL during maximal isometric and DCER muscle actions following 70% 1-RM DCER leg extensions. In addition, Smith et al. (2016) reported pretest to posttest increases in EMDE-M, EMDM-F, and EMDE-F measures from the VL during MVIC muscle actions following 30% 1-RM DCER leg extensions to failure. Conchola et al. (2013), (Conchola et al., 2015) also reported pretest to posttest increases in maximal isometric EMDE-F from the VL after intermittent 50 and 60% MVIC muscle actions to exhaustion. It has been suggested (Cè et al., 2013; Smith et al., 2016) that an increase in EMDE-M indicated the occurrence of excitationcontraction coupling failure. That is, the fatigue-induced buildup of metabolic byproducts altered the metabolic state of the muscle and resulted in a greater time duration for motor unit action potentials to propagate along the sarcolemma and cause physical movement of the muscle (MMG onset). In addition, the increased time duration for EMDM-F suggested increases in the compliance of the series elastic component, perhaps due to an increase in muscle temperature (Cè et al., 2013; Smith et al., 2016). Thus, in the current study, there were fatigue-induced pretest to posttest increases in EMDE-M, EMDM-F, and EMDE-F which suggested the occurrence of excitation-contraction coupling failure and increased compliance of the series elastic component during both maximal concentric isokinetic and isometric muscle actions. 4.3. Recovery electromechanical delay During recovery in the current study, EMDE-M, EMDM-F, and EMDE-F remained elongated after 3-min of recovery, but returned to pretest values after 5-min of recovery (Table 1 and Fig. 3). These findings were similar to those of Conchola et al. (2013), (Conchola et al., 2015) who reported increases in maximal isometric EMDE-F from the VL after a fatiguing protocol which returned to pretest values after 7-min of recovery. These findings were not in agreement, however, with Zhou et al. (1996) who reported that maximal isometric EMDE-F from the VL remained greater than pretest values after 5-min of recovery, but returned to pretest values after 10-min of recovery following 25 MVIC leg extensions. It is possible that the differences between the current study and those of Zhou et al. (1996) were due to methodological differences (signal conditioning, signal onset, and equipment). In the current study, at 3-min of recovery, excitation-contraction coupling failure and increased compliance of the series elastic component were still evident during both the maximal concentric isokinetic and isometric muscle actions (Table 1 and Fig. 3). After 5-min of recovery, however, the EMD values returned to pretest levels for both the maximal concentric isokinetic and isometric muscle actions (Table 1 and Fig. 3). These findings suggested that the effects of the buildup of metabolic byproducts were affecting excitation-contraction coupling failure at 3-min of recovery, but not at 5-min of recovery. In addition, the series elastic component returned to pretest levels of compliance at 5-min of recovery, but not at 3-min of recovery. 4.4. Relative contributions of electromechanical delay measures There were no differences in the relative contributions from EMDE-M and EMDM-F to EMDE-F during the maximal concentric
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isokinetic or isometric muscle actions at the pretest, posttest, 3- and 5-min of recovery measurements (Table 1). The time duration for excitation-contraction coupling (EMDE-M) accounted for 40–47% of the total time delay between the onset of the EMG signal the onset of force production (Table 1). Therefore, the time duration to take up the slack of the series elastic component (EMDM-F) accounted for 53–60% of EMDE-F (Table 1). These findings were similar to those of Smith et al. (2016) who reported approximately equal contributions from EMDE-M and EMDM-F to EMDE-F during pretest and posttest MVIC muscle actions. Thus, the current and previous study of Smith et al. (2016) suggested that the fatigue-induced buildup of metabolic byproducts (EMDE-M) and increased compliance of the series elastic component (EMDM-F) contributed to EMDE-F similarly at the pretest, posttest, 3- and 5-min of recovery measurements during maximal isokinetic, isometric, and DCER muscle actions. 4.5. Summary In summary, there were no differences between modes (isokinetic and isometric) for EMDE-M, EMDM-F, and EMDE-F during the pretest, posttest, 3-min recovery, and 5-min recovery measurements. These findings support the comparison of voluntary EMD measures between studies with different modes of exercise as long as the methodology for the determination of EMD are consistent. In addition, there were fatigue-induced pretest to posttest increases in EMDE-M, EMDM-F, and EMDE-F which suggested the occurrence of excitation-contraction coupling failure and increased compliance of the series elastic component during both maximal concentric isokinetic and isometric muscle actions. After the fatiguing protocol, however, EMDE-M, EMDM-F, and EMDE-F remained elongated after 3-min of recovery and returned to pretest values after 5-min of recovery. The relative contributions from EMDE-M and EMDM-F to EMDE-F suggested that the fatigue-induced buildup of metabolic byproducts and increased compliance of the series elastic component contributed to EMDE-F similarly at the pretest, posttest, 3- and 5-min of recovery measurements during maximal concentric isokinetic and isometric muscle actions. Acknowledgements We would like to thank our subjects for their time and dedication. Conflicts of interest There are no conflicts of interest for any author involved with this research. References Abe, T., Kumagai, K., Brechue, W., 2000. Fascicle length of leg muscles is greater in sprinters than distance runners. Med. Sci. Sport Exerc. 32, 1125–1129. Basmajian, J., De Luca, C., 1985. Muscles alive: their functions revealed by electromyography, vol. 278, p. 126. Begovic, H., Zhou, G., Li, T., Wang, Y., Zheng, Y., 2014. Detection of the electromechanical delay and its components during voluntary isometric contraction of the quadriceps femoris muscle. Front. Physiol. 5, 235–239. Cè, E., Rampichini, S., Agnello, L., Limonta, E., Veicsteinas, A., Esposito, F., 2013. Effects of temperature and fatigue on the electromechanical delay components. Muscle Nerve 47, 566–576. Cè, E., Rampichini, S., Esposito, F., 2015a. Novel insights into skeletal muscle function by mechanomyography: from the laboratory to the field. Sport Sci. Health 11, 1–28. Cè, E., Rampichini, S., Venturelli, M., Limonta, E., Veicsteinas, A., Esposito, F., 2015b. Electromechanical delay components during relaxation after voluntary contraction: reliability and effects of fatigue. Muscle Nerve 51, 907–915. Chan, A., Lee, F., Wong, P., Wong, C., Yeung, S., 2001. Effects of knee joint angles and fatigue on the neuromuscular control of vastus medialis oblique and vastus lateralis muscle in humans. Eur. J. Appl. Physiol. 84, 36–41.
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m. vastus lateralis myosin heavy chain composition. Eur. J. Appl. Physiol. 75, 151–159. Vos, E., Harlaar, J., van Ingen, S., 1991. Electromechanical delay during knee extensor contractions. Med. Sci. Sport Exerc. 23, 1187–1193. Zhou, S., 1996. Acute effect of repeated maximal isometric contraction on electromechanical delay of knee extensor muscle. J. Electromyog. Kinesiol. 6, 117–127. Zhou, S., Carey, M., Snow, R., Lawson, D., Morrison, W., 1998. Effects of muscle fatigue and temperature on electromechanical delay. Electromyog. Clin. Neurophysiol. 38, 67. Zhou, S., Lawson, D., Morrison, W., Fairweather, I., 1995. Electromechanical delay in isometric muscle contractions evoked by voluntary, reflex and electrical stimulation. Eur. J. Appl. Physiol. 70, 138–145. Zhou, S., McKenna, M., Lawson, D., Morrison, W., Fairweather, I., 1996. Effects of fatigue and sprint training on electromechanical delay of knee extensor muscles. Eur. J. Appl. Physiol. 72, 410–416. Cory M. Smith is currently a PhD student in human physiology at the University of Nebraska–Lincoln and studies EMG, MMG, prosthetic control, fatigue, supplementation, and electromechanical delay. Terry J. Housh received his Ph.D. (1984) from the University of Nebraska-Lincoln. His main areas of research are muscle function, fatigue, and growth and development in young athletes. Ethan C. Hill is currently a PhD student at the University of Nebraska-Lincoln and his main research interests include sex-specific differences and eccentric interventions. Joshua L. Keller is currently a Ph.D. student University of Nebraska-Lincoln, his primary research agenda consists of using neuromuscular parameters to better understand perceived exertion during resistance training. Glen O. Johnson received his Ph.D. (1972) from the University of Iowa. He is currently a professor emeritus of Nutrition and Health Sciences at the University of Nebraska-Lincoln. Richard J. Schmidt received his Ph.D. (1972) in Education from the University of Nebraska-Lincoln. His main areas of research are exercise testing, clinical exercise physiology, and military & law enforcement sports medicine.
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Are there mode-specific and fatigue-related electromechanical delay responses for maximal isokinetic and isometric muscle actions? Cory M. Smith ⇑, Terry J. Housh, Ethan C. Hill, Joshua L. Keller, Glen O. Johnson, Richard J. Schmidt University of Nebraska – Lincoln, Lincoln, NE, United States
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Article history: Received 9 March 2017 Received in revised form 2 August 2017 Accepted 8 August 2017
Keywords: EMD Excitation-contraction coupling Series elastic component Fatigue Recovery
a b s t r a c t This study used a combined electromyographic, mechanomyographic, and force approach to identify electromechanical delay (EMD) from the onsets of the electromyographic to force signals (EMDE-F), onsets of the electromyographic to mechanomyogrpahic signals (EMDE-M), and onsets of mechanomyographic to force signals (EMDMF). The purposes of the current study were to examine: (1) differences in EMDE-M, EMDMF, and EMDE-F from the vastus lateralis between maximal isokinetic and maximal concentric isometric leg extensions; and (2) the effects of fatigue and recovery on EMDE-M, EMDMF, and EMDE-F. These EMD measures were obtained from twelve men during maximal concentric isokinetic and isometric leg extensions pretest, posttest, and after 3-min and 5-min of recovery from 25 maximal isokinetic leg extensions at 60° s1. The results indicated no differences between maximal isokinetic and isometric muscle actions for EMDE-M, EMDM-F, or EMDE-F during the pretest, posttest, 3-min recovery, and 5-min recovery measurements. These findings support the comparison of voluntary EMD measures between studies with different modes of exercise as long as the methodology for the determination of EMD are consistent. There were, however, fatigue-induced pretest to posttest increases in EMDE-M, EMDM-F, and EMDE-F which remained elongated after 3-min of recovery, but returned to pretest values after 5-min of recovery. Ó 2017 Elsevier Ltd. All rights reserved.
1. Introduction Electromechanical delay (EMD) measures the time delay between the onset of electrical activation of the muscle and the onset of force production (Norman and Komi, 1979). Typically (Vos et al., 1991; Zhou et al., 1998), EMD has been operationally defined as the time period between the onset of the electromyographic (EMG) signal and the onset of force production during a muscle contraction. More recently, however, mechanomyography (MMG) has been used to identify the onset of the lateral oscillations associated with the contraction of skeletal muscle which provides additional information regarding the factors that contribute to EMD (Cè et al., 2013; Esposito, 2013; Smith et al., 2016). Specifically, the onset of the EMG signal identifies when an electrical impulse activates the muscle and the MMG signal reflects the initiation of movement from the activated muscle fibers (Basmajian and De Luca, 1985; Orizio, 1993). The time delay between the onsets of the EMG and MMG signals is a measure of excitation⇑ Corresponding author at: Department of Nutrition and Health Sciences, 110 Ruth Leverton Hall, University of Nebraska-Lincoln, Lincoln, NE 68583-0806, United States. E-mail address: [email protected] (C.M. Smith). http://dx.doi.org/10.1016/j.jelekin.2017.08.001 1050-6411/Ó 2017 Elsevier Ltd. All rights reserved.
contraction coupling which includes the total duration of the events from the motor unit action potentials travelling along the sarcolemma to cross-bridge formation (Merletti and Parker, 2004; Orizio et al., 1997). The onset of the MMG signal to the onset of force production is a measure of the series elastic component which includes the time required to take up the muscle-tendon unit slack before force transmission can occur (Merletti and Parker, 2004; Orizio et al., 1997). Thus, simultaneous assessments of EMG, MMG, and force production allow for the identification of the onset of the EMG signal to the onset of the MMG signal (EMDE-M), the onset of the MMG signal to the onset of force production (EMDM-F), and the onset of the EMG signal to the onset of force production (EMDE-F) (Cè et al., 2015a; Smith et al., 2016, 2017). Therefore, EMDE-M and EMDM-F can measure the relative contributions of excitation-contraction coupling and the series elastic component, respectively, to the overall time duration of EMDE-F (EMDE-M + EMDM-F = EMDE-F). Fatigue-induced increases in voluntary EMD measures are thought to be influenced by a number of factors including: (1) the buildup of metabolic byproducts (Cè et al., 2013, 2015b; Smith et al., 2016; Zhou, 1996), (2) Ca2+efflux from the sarcoplasmic reticulum (Begovic et al., 2014; Cè et al., 2013; Smith et al., 2016, 2017; Zhou, 1996), (3) cross-bridge cycling rate (Begovic
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et al., 2014; Cè et al., 2013; Zhou, 1996), and (4) increases in muscle temperature (Cè et al., 2013). It has been suggested (Cè et al., 2013; Smith et al., 2016, 2017; Zhou et al., 1998) that fatigueinduced excitation-contraction coupling failure due to metabolic disturbances results in an increase in EMDE-M, while increases in the compliance of the series elastic component associated with muscle temperature result in increased EMDM-F. The effects of fatigue on these aspects of voluntary EMD measures, however, have primarily been examined using pre-fatigue versus post-fatigue measurements (Cè et al., 2013; Chan et al., 2001; Taylor et al., 1997). The few studies (Conchola et al., 2013, 2015; Rampichini et al., 2014) that have examined the recovery of EMD have performed isometric (maximal and submaximal) or stimulated muscle actions. Stimulated muscle actions have lower EMD values than those during voluntary muscle actions and do not reflect the motor unit control strategies used to voluntarily contract a muscle (Hopkins et al., 2007). In addition, the studies (Conchola et al., 2013, 2015; Zhou, 1996) which have examined the recovery of voluntary EMD measures did not examine the relative contributions of excitation-contraction coupling (EMDE-M) and the series elastic component (EMDM-F) to the total time duration of EMDE-F. Previous studies (Hopkins et al., 2007; Jenkins et al., 2013; Smith et al., 2017) have examined voluntary EMD measures during dynamic and isometric muscle actions with conflicting results. Specifically, Jenkins et al. (2013) reported greater EMDE-F during voluntary (40.73 ms) isokinetic (dynamic) muscle actions compared to those reported by Hopkins et al. (2007) (22.8 ms) during isometric muscle actions. Smith et al. (2017), however, reported no differences in absolute EMD measures or the relative contributions of EMDE-M and EMDM-F to EMDE-F between maximal isometric and dynamic constant external resistance (DCER) muscle actions in a non-fatigued or fatigued state. No previous studies, however, have examined the effects of isokinetic and isometric muscle actions on EMDE-M, EMDM-F, and EMDE-F under the same voluntary testing conditions. Identifying potential differences in EMD measures between isokinetic and isometric muscle actions will have implications for the comparisons between studies as well as possible clinical applications where most movements are dynamic. Therefore, the purposes of the current study were to identify potential mode-specific differences in EMDE-M, EMDM-F, and EMDE-F during isokinetic and isometric muscle actions as well as if there are fatigue-related differences in the responses of EMDEM, EMDM-F, and EMDE-F with different modes of EMD measures by examining: (1) the differences in EMDE-M, EMDM-F, and EMDEF from the vastus lateralis (VL) between maximal isokinetic and maximal isometric leg extensions; and (2) the effects of fatigue and recovery on EMDE-M, EMDM-F, and EMDE-F. These EMD measures were obtained from twelve men during maximal isokinetic and isometric leg extensions pretest, posttest, and after 3-min and 5-min of recovery from 25 maximal isokinetic leg extensions at 60° s1. Based on previous studies (Hopkins et al., 2007; Jenkins et al., 2013; Smith et al., 2017), we hypothesized that there will be no difference between the maximal isokinetic and isometric EMD values. In addition, we hypothesized (Conchola et al., 2013, 2015; Zhou, 1996) that there would be fatigue-induced increases in EMDE-F, EMDM-F, and EMDE-M which would recover to pretest values at 5-min of recovery.
2. Methods 2.1. Subjects Twelve men (mean ± SD age 23 ± 3 yr; body mass 79.3 ± 8.2 kg; height 173.1 ± 3.9 cm) volunteered to participate in this study. The subjects were recreationally trained (greater than 6-months of
resistance training at least 3 times per week with approximately 50% of their training consisting of lower body exercises), and free from any musculoskeletal injuries or neuromuscular disorders. This study was approved by the Institutional Review Board, and all subjects signed a written informed consent and completed a health history questionnaire prior to participation. 2.2. Experimental approach The study consisted of 2 visits, separated by at least 48-h. The first visit was a familiarization visit which consisted of maximal and submaximal concentric isokinetic and isometric leg extension muscle actions of the dominant leg (based on kicking preference). Emphasis was placed on contracting and relaxing as quickly as possible on command. This was continued until each subject indicated that they were comfortable performing these muscle actions. During both visits, the subjects were able to visualize their muscle activation on a monitor placed in front of them. The visualization of the muscle actions helped emphasize the importance of contracting and relaxing as quickly as possible. During the testing visit, the subjects performed 2 pretest leg extension maximal voluntary isometric contractions (MVIC) and 2 maximal concentric isokinetic leg extension muscle actions at 60° s1 with the dominant leg. The subjects then performed 25 maximal concentric isokinetic leg extension muscle actions at 60° s1. Immediately following the 25 maximal concentric isokinetic leg extension muscle actions, the subjects performed a posttest MVIC and a maximal concentric isokinetic leg extension muscle action at 60° s1. Recovery MVICs and maximal concentric isokinetic leg extension muscle actions at 60° s1 were measured after 3- and 5-min of recovery (Fig. 1). 2.3. Protocol A warmup consisting of 5–7 isokinetic and isometric leg extension muscle actions were performed at approximately 50–70% of their maximal effort. All isometric muscle actions were performed with the dominant leg at a knee joint angle of 120 ° (180 ° being full extension) (Kulig et al., 1984). Following the warmup, the subjects performed 2, randomly ordered, pretest MVIC and maximal concentric isokinetic leg extension muscle actions at 60° s1 with 1-min of rest between each pretest muscle action. The greatest strength of the 2 trials were used for analysis. All isokinetic and isometric muscle actions were performed on a calibrated Cybex II isokinetic dynamometer. After the pretest muscle actions, subjects were given 1-min of rest and then performed the fatiguing protocol consisting of 25 maximal concentric isokinetic leg extension muscle actions at 60° s1. Immediately after the fatiguing protocol, subjects performed a randomly ordered posttest MVIC and maximal concentric isokinetic leg extension muscle action at 60° s1. During the 5-min recovery phase, an MVIC and maximal concentric isokinetic leg extension muscle action at 60° s1 were performed at the 3- and 5-min of recovery time-points following the posttest muscle actions (Fig. 1). 2.4. Electromyographic, mechanomyographic, and force signal acquisition A surface bipolar electrode arrangement (Ag/AgCl, AccuSensor, Lynn Medical, Wixom, MI, USA) was placed on the VL of the dominant leg with an interelectrode distance of 30 mm. The skin was dry shaven, abraded, and cleaned with isopropyl alcohol prior to placing the electrodes. The bipolar electrode arrangement was placed 66% of the distance between the anterior superior iliac spine (ASIS) and the lateral border of the patella and orientated at a 20°
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Fig. 1. Depiction of the order of muscle actions during the protocol. The order of the maximal voluntary isometric contractions (MVIC) and maximal concentric isokinetic leg extension muscle actions were randomized during the pretest, posttest, and recovery measurements. No rest was given between the randomly ordered MVIC and maximal isokinetic leg extensions during the posttest and recovery measurements.
angle to approximate the pennation angle of the muscle fibers (Abe et al., 2000; Hermens et al., 1999). A reference electrode was placed over the ASIS. The EMG signals were zero-meaned, bandpass filtered (fourth-order Butterworth) at 10–500 Hz. The MMG signal was measured using a triaxial accelerometer (EGAS-FT-10/V05, Measurement Specialties Inc., Hampton, VA) placed between the bipolar electrode arrangement on the VL using double-sided adhesive foam tape. The MMG signals were zero-meaned and bandpass filtered (fourth-order Butterworth) at 5–100 Hz. Force was measured using a low-profile pancake load cell (Honeywell Model 41, Morris Plains, NJ) attached to the lever arm. All signals were simultaneously collected through a BioPac MP150 (BioPac System Inc., Goleta, CA) at a sampling frequency of 10,000 Hz. All signal processing and EMD measurements were performed using custom programs written with LabVIEW software (Version 15.0, National Instruments, Austin TX). 2.5. Electromechanical delay The EMD measurements were determined as the time periods from the onset of the EMG signal to the onset of force (EMDE-F), onset of the MMG signal to the onset of force (EMDM-F), and the onset of the EMG signal to the onset of the MMG signal (EMDEM). The onset of EMG, MMG, and force were determined by the condition of 3 standard deviations (SDs) from the mean baseline noise observed for each signal, determined from a 10,000 Hz sample to increase accuracy for determination of the onset of the signals (Begovic et al., 2014; Costa et al., 2012; Stock et al., 2015) and were selected off-line by the primary investigator using a custom written LabVIEW program that provided interactive graphical viewing of each signal (Fig. 2) (Smith et al., 2016, 2017). 2.6. Statistical analysis A 3 (EMD: EMDE-M, EMDM-F, and EMDE-F) 3 (Mode: Isokinetic and Isometric) 4 (Time: pretest, posttest, 3-min recovery, and 5-min recovery) repeated measures ANOVA was performed. Follow-up 2- and 1-way repeated measures ANOVAs and paired sampled t-tests with Tukey’s LSD were performed when appropriate. In addition, partial eta squared values were calculated from the ANOVAs and was calculated as the sums of squared between/sums of squared total. If the assumption of sphericity was violated, the Huynh-Feldt correction was used. An alpha of p 0.05 was considered statistically significant for all statistical analyses (SPSS Version 22.0, Armonk, NY). 3. Results The 3 (EMD: EMDE-M, EMDM-F, and EMDE-F) 3 (Mode: Isokinetic and Isometric) 4 (Time: pretest, posttest, 3-min recovery, and 5-min recovery) repeated measures ANOVA indicated no significant 3-way interaction (p = 0.43, g2p = 0.49) or 2-way interactions for Mode Time (p = 0.97, g2p = 0.03) or EMD Mode
Fig. 2. Graphical representation of the electromyographic, mechanomyographic, and force combination for the determinations of electromechanical delay (EMD). Together, these signals allowed for the identification of the onset of the electromyographic signal to the onset of the mechanomyographic signal (EMDE-M), onset of the mechanomyographic signal to the onset of force production (EMDM-F), and onset of the electromyographic signal to the onset of force production (EMDE-F). This Figure was used with permission from the Primary Investigator (Smith et al., 2017).
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Table 1 Descriptive statistics (mean and standard error) for the electromechanical delay (EMD) measures for the maximal isokinetic and maximal isometric leg extension muscle actions during pretest, posttest, 3-min recovery, and 5-min recovery measurements. The EMD measurements were determined from the onset of the electromyographic signal to the onset of the mechanomyographic signal (EMDE-M), onset of the mechanomyographic signal to the onset of force production (EMDM-F), and the onset of the electromyographic signal to the onset of force production (EMDE-F).
*
y à R
R
EMDE-M (ms)
EMDM-F (ms)à
EMDE-F (ms)
Isokinetic Isometric
20.7 (2.1) 20.5 (1.4)
29.9 (1.9) 28.2 (1.6)
50.6 (3.4) 48.7 (2.2)
Posttest*,y Isokinetic Isometric
30.7 (2.0) 32.0 (1.3)
41.2 (3.6) 35.9 (2.7)
71.9 (4.6) 67.9 (3.0)
3-Min Recovery*,y Isokinetic 25.5 (3.5) Isometric 27.7 (1.8)
36.3 (2.6) 32.6 (2.5)
61.8 (2.9) 60.3 (3.2)
5-Min Recovery* Isokinetic Isometric
32.8 (4.1) 32.3 (2.0)
56.9 (4.4) 54.0 (3.6)
Pretest*
24.1 (2.4) 21.7 (1.8)
No differences between isokinetic and isometric EMDE-M, EMDM-F, or EMDE-F (p > 0.05). Posttest and 3-Min of Recovery were greater than Pretest EMD values (p < 0.01). EMDM-F was greater than EMDE-M at all time-points for both modes (p < 0.01). EMDE-F was greater than EMDE-M and EMDM-F at all time-points for both modes (p < 0.01).
(p = 0.29, g2p = 0.24). There was, however, a significant 2-way interaction for EMD Time (p = 0.03, g2p = 0.89). The follow-up 3 (EMD: EMDE-M, EMDM-F, and EMDE-F) 4 (Time: pretest, posttest, 3-min recovery, and 5-min recovery) repeated measures ANOVA (collapsed across Mode) indicated a significant 2-way interaction (p < 0.01, g2p = 0.69). Post-hoc analyses indicated that for EMDE-M, EMDM-F, and EMDE-F values pretest < posttest (p < 0.01) = 3-min recovery (p = 0.68) > 5-min posttest (p < 0.01) (Table 1 and Fig. 3). In addition, post hoc analyses indicated that EMDE-M < EMDM-F < EMDE-F (p < 0.01) (Table 1 and Fig. 3).
4. Discussion 4.1. Mode-specific differences in electromechanical delay A primary finding in the present study was that there were no differences between modes (isokinetic and isometric) for EMDE-M, EMDM-F, or EMDE-F during the pretest, posttest, 3-min recovery, and 5-min recovery measurements (Table 1 and Fig. 3). These findings were similar to those of Smith et al. (2017) who reported no differences between MVIC and maximal DCER leg extensions for EMDE-M, EMDM-F, or EMDE-F values from the VL measured pretest or following 70% 1 repetition maximum (1-RM) DCER leg extensions to failure. Thus, current and previous findings of Smith et al. (2017) indicated that the mode of muscle action did not influence EMD measures in non-fatigued (pretest), fatigued (posttest), or recovery states. Furthermore, these findings indicated that the time duration for excitation-contraction coupling (EMDE-M) and series elastic component (EMDM-F) were not influenced by the mode of the muscle action performed (isometric, isokinetic, or DCER) (Smith et al., 2017). Therefore, studies which utilized different modes (isometric, isokinetic, and DCER) of maximal voluntary muscle actions can be compared to one another. It is important to note that these findings should not be applied to studies which utilized stimulated or submaximal muscle actions. Future studies are required to further examine these methodological differences and how they relate to EMD measures. In addition, there are potential differences in methodology may result in different absolute EMD measures between studies (Begovic et al., 2014; Jenkins et al., 2013; Zhou et al., 1998, 1995). Some methodological differences which may influence EMD include: sampling frequency, signal conditioning (i.e. filters), definition of the onset of a signal, and the muscle tested (Begovic et al., 2014; Jenkins et al., 2013; Zhou et al., 1998, 1995). Thus, comparison of voluntary EMD measures between studies with different modes of exercise can be made, however, caution should be taken when there are different methodological factors present which may influence the EMD measures.
Fig. 3. The mean electromechanical delay (EMD) measurements from the vastus lateralis during pretest, posttest, 3-min, and 5-min of recovery during the maximal concentric isokinetic and isometric muscle actions. The EMD measurements were determined from the onset of the electromyographic signal to the onset of the mechanomyographic signal (EMDE-M), onset of the mechanomyographic signal to the onset of force production (EMDM-F), and the onset of the electromyographic signal to the onset of force production (EMDE-F).
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4.2. Pretest to posttest electromechanical delay In the current study, there were fatigue-induced pretest to posttest increases in EMDE-M, EMDM-F, and EMDE-F for both the maximal concentric isokinetic and isometric muscle actions (Table 1 and Fig. 3). These findings were in agreement with previous studies (Conchola et al., 2013, 2015; Smith et al., 2016, 2017; Zhou et al., 1996) which suggested that fatigue resulted in an increase in EMD measures. For example, Smith et al. (2017) reported pretest to posttest increases in EMDE-M, EMDM-F, and EMDE-F from VL during maximal isometric and DCER muscle actions following 70% 1-RM DCER leg extensions. In addition, Smith et al. (2016) reported pretest to posttest increases in EMDE-M, EMDM-F, and EMDE-F measures from the VL during MVIC muscle actions following 30% 1-RM DCER leg extensions to failure. Conchola et al. (2013), (Conchola et al., 2015) also reported pretest to posttest increases in maximal isometric EMDE-F from the VL after intermittent 50 and 60% MVIC muscle actions to exhaustion. It has been suggested (Cè et al., 2013; Smith et al., 2016) that an increase in EMDE-M indicated the occurrence of excitationcontraction coupling failure. That is, the fatigue-induced buildup of metabolic byproducts altered the metabolic state of the muscle and resulted in a greater time duration for motor unit action potentials to propagate along the sarcolemma and cause physical movement of the muscle (MMG onset). In addition, the increased time duration for EMDM-F suggested increases in the compliance of the series elastic component, perhaps due to an increase in muscle temperature (Cè et al., 2013; Smith et al., 2016). Thus, in the current study, there were fatigue-induced pretest to posttest increases in EMDE-M, EMDM-F, and EMDE-F which suggested the occurrence of excitation-contraction coupling failure and increased compliance of the series elastic component during both maximal concentric isokinetic and isometric muscle actions. 4.3. Recovery electromechanical delay During recovery in the current study, EMDE-M, EMDM-F, and EMDE-F remained elongated after 3-min of recovery, but returned to pretest values after 5-min of recovery (Table 1 and Fig. 3). These findings were similar to those of Conchola et al. (2013), (Conchola et al., 2015) who reported increases in maximal isometric EMDE-F from the VL after a fatiguing protocol which returned to pretest values after 7-min of recovery. These findings were not in agreement, however, with Zhou et al. (1996) who reported that maximal isometric EMDE-F from the VL remained greater than pretest values after 5-min of recovery, but returned to pretest values after 10-min of recovery following 25 MVIC leg extensions. It is possible that the differences between the current study and those of Zhou et al. (1996) were due to methodological differences (signal conditioning, signal onset, and equipment). In the current study, at 3-min of recovery, excitation-contraction coupling failure and increased compliance of the series elastic component were still evident during both the maximal concentric isokinetic and isometric muscle actions (Table 1 and Fig. 3). After 5-min of recovery, however, the EMD values returned to pretest levels for both the maximal concentric isokinetic and isometric muscle actions (Table 1 and Fig. 3). These findings suggested that the effects of the buildup of metabolic byproducts were affecting excitation-contraction coupling failure at 3-min of recovery, but not at 5-min of recovery. In addition, the series elastic component returned to pretest levels of compliance at 5-min of recovery, but not at 3-min of recovery. 4.4. Relative contributions of electromechanical delay measures There were no differences in the relative contributions from EMDE-M and EMDM-F to EMDE-F during the maximal concentric
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isokinetic or isometric muscle actions at the pretest, posttest, 3- and 5-min of recovery measurements (Table 1). The time duration for excitation-contraction coupling (EMDE-M) accounted for 40–47% of the total time delay between the onset of the EMG signal the onset of force production (Table 1). Therefore, the time duration to take up the slack of the series elastic component (EMDM-F) accounted for 53–60% of EMDE-F (Table 1). These findings were similar to those of Smith et al. (2016) who reported approximately equal contributions from EMDE-M and EMDM-F to EMDE-F during pretest and posttest MVIC muscle actions. Thus, the current and previous study of Smith et al. (2016) suggested that the fatigue-induced buildup of metabolic byproducts (EMDE-M) and increased compliance of the series elastic component (EMDM-F) contributed to EMDE-F similarly at the pretest, posttest, 3- and 5-min of recovery measurements during maximal isokinetic, isometric, and DCER muscle actions. 4.5. Summary In summary, there were no differences between modes (isokinetic and isometric) for EMDE-M, EMDM-F, and EMDE-F during the pretest, posttest, 3-min recovery, and 5-min recovery measurements. These findings support the comparison of voluntary EMD measures between studies with different modes of exercise as long as the methodology for the determination of EMD are consistent. In addition, there were fatigue-induced pretest to posttest increases in EMDE-M, EMDM-F, and EMDE-F which suggested the occurrence of excitation-contraction coupling failure and increased compliance of the series elastic component during both maximal concentric isokinetic and isometric muscle actions. After the fatiguing protocol, however, EMDE-M, EMDM-F, and EMDE-F remained elongated after 3-min of recovery and returned to pretest values after 5-min of recovery. The relative contributions from EMDE-M and EMDM-F to EMDE-F suggested that the fatigue-induced buildup of metabolic byproducts and increased compliance of the series elastic component contributed to EMDE-F similarly at the pretest, posttest, 3- and 5-min of recovery measurements during maximal concentric isokinetic and isometric muscle actions. Acknowledgements We would like to thank our subjects for their time and dedication. Conflicts of interest There are no conflicts of interest for any author involved with this research. References Abe, T., Kumagai, K., Brechue, W., 2000. Fascicle length of leg muscles is greater in sprinters than distance runners. Med. Sci. Sport Exerc. 32, 1125–1129. Basmajian, J., De Luca, C., 1985. Muscles alive: their functions revealed by electromyography, vol. 278, p. 126. Begovic, H., Zhou, G., Li, T., Wang, Y., Zheng, Y., 2014. Detection of the electromechanical delay and its components during voluntary isometric contraction of the quadriceps femoris muscle. Front. Physiol. 5, 235–239. Cè, E., Rampichini, S., Agnello, L., Limonta, E., Veicsteinas, A., Esposito, F., 2013. Effects of temperature and fatigue on the electromechanical delay components. Muscle Nerve 47, 566–576. Cè, E., Rampichini, S., Esposito, F., 2015a. Novel insights into skeletal muscle function by mechanomyography: from the laboratory to the field. Sport Sci. Health 11, 1–28. Cè, E., Rampichini, S., Venturelli, M., Limonta, E., Veicsteinas, A., Esposito, F., 2015b. Electromechanical delay components during relaxation after voluntary contraction: reliability and effects of fatigue. Muscle Nerve 51, 907–915. Chan, A., Lee, F., Wong, P., Wong, C., Yeung, S., 2001. Effects of knee joint angles and fatigue on the neuromuscular control of vastus medialis oblique and vastus lateralis muscle in humans. Eur. J. Appl. Physiol. 84, 36–41.
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Conchola, E., Thompson, B., Smith, D., 2013. Effects of neuromuscular fatigue on the electromechanical delay of the leg extensors and flexors in young and old men. Eur. J. Appl. Physiol. 113, 2391–2399. Conchola, E., Thiele, R., Palmer, T., Smith, D., Thompson, B., 2015. Effects of neuromuscular fatigue on electromechanical delay of the leg extensors and flexors in young men and women. Muscle Nerve 52, 844–851. Costa, P., Ryan, E., Herda, T., Walter, A., Hoge, K., Cramer, J., 2012. Acute effects of passive stretching on the electromechanical delay and evoked twitch properties: a gender comparison. J. Appl. Biomech. 28, 645–654. Esposito, F., 2013. Reliability of the electromechanical delay components assessment during the relaxation phase. Physiol. J. 2013. Hermens, H., Freriks, B., Merletti, R., Stegeman, D., Blok, J., Rau, G., et al., 1999. European recommendations for surface electromyography. Roessingh Res. Dev. 8, 13–54. Hopkins, J., Feland, J., Hunter, I., 2007. A comparison of voluntary and involuntary measures of electromechanical delay. Int. J. Neurosci. 117, 597–604. Jenkins, N., Palmer, T., Cramer, J., 2013. Comparisons of voluntary and evoked rate of torque development and rate of velocity development during isokinetic muscle actions. Isokin. Exerc. Sci. 21, 253–261. Kulig, K., Andrews, J., Hay, J., 1984. Human strength curves. Exerc. Sport Sci. Rev. 12, 417–466. Merletti, R., Parker, P., 2004. Electromyography: Physiology, Engineering, and Non-Invasive Applications. John Wiley & Sons. Norman, R., Komi, P., 1979. Electromechanical delay in skeletal muscle under normal movement conditions. Acta Physiol. Scand. 106, 241–248. Orizio, C., 1993. Muscle sound: bases for the introduction of a mechanomyographic signal in muscle studies. Crit. Rev. Biomed. Eng. 21, 201–243. Orizio, C., Esposito, F., Paganotti, I., Marino, L., Rossi, B., Veicsteinas, A., 1997. Electrically-elicited surface mechanomyogram in myotonic dystrophy. Ital. J. Neurol. Sci. 18, 185–190. Rampichini, S., Cè, E., Limonta, E., Esposito, F., 2014. Effects of fatigue on the electromechanical delay components in gastrocnemius medialis muscle. Eur. J. Appl. Physiol. 114, 639–651. Smith, C., Housh, T., Hill, E., Johnson, G., Schmidt, R., 2016. Changes in electromechanical delay during fatiguing dynamic muscle actions. Muscle Nerve 56 (2), 315–320. Smith, C., Housh, T., Hill, E., Johnson, G., Schmidt, R., 2017. Dynamic versus isometric electromechanical delay in non-fatigued and fatigued muscle: a combined electromyographic, mechanomyographic, and force approach. J. Electromyog. Kinesiol. 33, 34–38. Stock, M., Olinghouse, K., Mota, J., Drusch, A., Thompson, B., 2015. Muscle group specific changes in the electromechanical delay following short-term resistance training. J. Sci. Med. Sport. 19, 761–765. Taylor, A., Bronks, R., Smith, P., Humphries, B., 1997. Myoelectric evidence of peripheral muscle fatigue during exercise in severe hypoxia: some references to
m. vastus lateralis myosin heavy chain composition. Eur. J. Appl. Physiol. 75, 151–159. Vos, E., Harlaar, J., van Ingen, S., 1991. Electromechanical delay during knee extensor contractions. Med. Sci. Sport Exerc. 23, 1187–1193. Zhou, S., 1996. Acute effect of repeated maximal isometric contraction on electromechanical delay of knee extensor muscle. J. Electromyog. Kinesiol. 6, 117–127. Zhou, S., Carey, M., Snow, R., Lawson, D., Morrison, W., 1998. Effects of muscle fatigue and temperature on electromechanical delay. Electromyog. Clin. Neurophysiol. 38, 67. Zhou, S., Lawson, D., Morrison, W., Fairweather, I., 1995. Electromechanical delay in isometric muscle contractions evoked by voluntary, reflex and electrical stimulation. Eur. J. Appl. Physiol. 70, 138–145. Zhou, S., McKenna, M., Lawson, D., Morrison, W., Fairweather, I., 1996. Effects of fatigue and sprint training on electromechanical delay of knee extensor muscles. Eur. J. Appl. Physiol. 72, 410–416. Cory M. Smith is currently a PhD student in human physiology at the University of Nebraska–Lincoln and studies EMG, MMG, prosthetic control, fatigue, supplementation, and electromechanical delay. Terry J. Housh received his Ph.D. (1984) from the University of Nebraska-Lincoln. His main areas of research are muscle function, fatigue, and growth and development in young athletes. Ethan C. Hill is currently a PhD student at the University of Nebraska-Lincoln and his main research interests include sex-specific differences and eccentric interventions. Joshua L. Keller is currently a Ph.D. student University of Nebraska-Lincoln, his primary research agenda consists of using neuromuscular parameters to better understand perceived exertion during resistance training. Glen O. Johnson received his Ph.D. (1972) from the University of Iowa. He is currently a professor emeritus of Nutrition and Health Sciences at the University of Nebraska-Lincoln. Richard J. Schmidt received his Ph.D. (1972) in Education from the University of Nebraska-Lincoln. His main areas of research are exercise testing, clinical exercise physiology, and military & law enforcement sports medicine.