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Original Research

Time Course of Changes in Neuromuscular Parameters During Sustained Isometric Muscle Actions

Smith, Cory M.; Housh, Terry J.; Herda, Trent J.; Zuniga, Jorge M.; Camic, Clayton L.; Bergstrom, Haley C.; Smith, Doug B.; Weir, Joseph P.; Hill, Ethan C.; Cochrane, Kristen C.; Jenkins, Nathaniel D.M.; Schmidt, Richard J.; Johnson, Glen O.

Author Information
The Journal of Strength & Conditioning Research: October 2016 - Volume 30 - Issue 10 - p 2697-2702
doi: 10.1519/JSC.0000000000001547

Abstract

Erratum

In the October 2016 issue of the in the article by Smith, CM, Housh, TJ, Herda, TJ, Zuniga, JM, Camic, CL, Bergstrom, HC, Smith, DB, Weir, JP, Hill, EC, Cochrane, KC, Jenkins, NDM, Schmidt, RJ, and Johnson, GO, “Time Course of Changes in Neuromuscular Parameters During Sustained Isometric Muscle Actions”, the incorrect image was used for . The appropriate figure should have been shown as follows:

Figure 1
5+ images

The Journal of Strength & Conditioning Research. 31(12):e86, December 2017.

Introduction

Simultaneous assessments of electromyographic (EMG) and mechanomyographic (MMG) time and frequency domain parameters have been used to examine the motor unit activation strategies during fatiguing isometric muscle actions. Recording the EMG and MMG signals during a fatiguing isometric muscle action allows for the identification of changes in muscle activation (EMG amplitude), motor unit action potential conduction velocity (EMG frequency), motor unit recruitment (MMG amplitude), and global motor unit firing rate (MMG frequency) (2,25,26). Typically, during a fatiguing submaximal isometric muscle action, there are increases in muscle activation and motor unit recruitment and decreases in motor unit action potential conduction velocity and global motor unit firing rate (24,31,33). For example, Vaz et al. (34) reported decreases in EMG frequency (25%) and MMG frequency (50%) but increases in EMG amplitude (35%) and MMG amplitude (48%) from the vastus lateralis (VL) after a fatiguing isometric muscle action of the leg extensors that began at 70% maximal voluntary isometric contraction (MVIC) and ended when the subjects could not maintain 50% MVIC. Furthermore, previous EMG and MMG studies (19,24,26) have reported that the motor unit activation strategies that modulate torque production are specific to the mode of muscle action (i.e., isometric, concentric, or eccentric) (5,6,16) and protocol performed (continuous isometric, intermittent isometric, or dynamic) (4,22,26). In addition, neuromuscular parameters are often measured at the beginning and end of a fatiguing workbout, and the direction and magnitude of changes have been used to infer about the motor unit activation strategy used to control force production (16,30,36). Fatigue, however, is a process that occurs over time, and therefore, it is possible that the time course of changes in neuromuscular responses may better identify what maintains force production during fatigue than measuring neuromuscular parameters at the beginning and end of a fatiguing workbout (7,8,11). No previous studies, however, have simultaneously assessed the time and frequency domain parameters of EMG and MMG signals to identify the time course of changes in motor unit activation strategies during a sustained isometric muscle action of the leg extensors. By examining the time course of changes in the EMG and MMG time and frequency domain parameters, it is possible to determine when changes in specific aspects of motor unit activation strategies begin (percent time to exhaustion) and the patterns of changes (linear, quadratic, or cubic). The time course of changes in neuromuscular parameters may also give greater insight into the fatiguing process than measurements at the beginning and end of the fatiguing workbout alone. Therefore, the purpose of the present study was to identify the time course of changes in EMG amplitude, EMG frequency, MMG amplitude, and MMG frequency from the VL during a sustained isometric muscle action of the leg extensors at 50% MVIC.

Methods

Experimental Approach to the Problem

This study examined the time course of changes in EMG and MMG time and frequency domain responses from the VL during a sustained isometric muscle action of the leg extensors at 50% MVIC (Figure 1). The subjects performed 2 MVICs and then a sustained isometric muscle action at 50% MVIC to exhaustion. The neuromuscular parameters were recorded from the VL every 10% of the time to exhaustion during the sustained isometric muscle action, and polynomial regression analyses were used to examine the time course of changes in the neuromuscular responses.

Figure 1
Figure 1:
Figure shows the relationships (linear, quadratic, or cubic) for the normalized electromyographic (EMG) and mechanomyographic (MMG) signals vs. percent time to exhaustion. The EMG root mean square (RMS) [Black Square] had a positive linear relationship (p = 0.018, r 2 = 0.77, standard error of the estimate (SEE) = 10.88), which began to increase immediately from 10% of the time to exhaustion to task failure. The EMG mean power frequency (MPF) (p = 0.002, R 2 = 0.99, SEE = 0.80) and MMG MPF [Black up-pointing triangle] (p = 0.015, R 2 = 0.94, SEE = 2.29) had negative quadratic relationships, which began to decrease at 30% of the time to exhaustion and continued to decrease to task failure. The MMG RMS ● had a cubic relationship (p = 0.001, R 2 = 0.94, SEE = 7.90), which increased from 10 to 30% of the time to exhaustion, decreased from 40 to 70% of the time to exhaustion, and then markedly increased from 70% of the time to exhaustion to task failure.

Subjects

Eleven healthy adults (9 men and 2 women, mean ± SD age = 22.5 ± 2.1 years; age range: 20 to 24 years; body mass = 81.2 ± 13.4 kg; height = 180.0 ± 9.9 cm) volunteered to participate in the investigation. The subjects regularly participated in physical activities, such as running, bicycling, and resistance training. The study was approved by the University Institutional Review Board for Human Subjects, and all subjects completed a health history questionnaire and signed an informed consent document before testing.

Procedures

The orientation session was used to determine the location of the innervation zone (IZ) and the pennation angle of the muscle fibers of the VL. Each subject's skin was dry shaven and cleaned with a damp cloth before applying a probe of 8 silver bar electrodes (5 × 1 mm, 10 mm interelectrode distance; Ottino Bioelectronica, Torino, Italy) over the VL on a reference line between the anterior spina iliac superior and the anterior border of the medial ligament (29). The reference electrodes were placed around the subject's wrist according to the procedures described by the EMG 16 User Manual (2006). The subjects were instructed to perform a submaximal isometric muscle action of their leg extensors to identify their IZ. The location of the IZ was identified by the EMG channel with minimal amplitude and phase reversal (20). The probe was then moved along the muscle until the IZ was in the center of the electrode array. The pennation angle of the muscle fibers of the VL was determined by rotating the probe around the IZ until the slopes of the 2 lines connecting the EMG waveforms from the channels above and below the IZ had symmetrical propagation of motor unit action potentials according to the EMG 16 User Manual. An outline of the probe was traced with a nonwashable marker before removing the probe so the same electrode position could be obtained in the subsequent session.

All isometric leg extension testing was performed on the dominant leg (based on kicking preference) using a calibrated Cybex II dynamometer at a knee joint angle of 120°. Before the isometric testing, each subject performed a warm-up of five 6-second submaximal isometric muscle actions, followed by a 2-minute rest period. The subjects were instructed to provide an effort corresponding to approximately 50% of their maximum during each muscle action.

After completing the warm-up, each subject performed two 6-second pretest MVIC trials. A 2-minute rest was given between each trial. Strong verbal encouragement was provided for both trials. The MVIC was calculated for a 2-second time period corresponding to the middle 33% of each 6-second trial. The highest torque value of the 2 MVIC trials was used to calculate 50% MVIC for the subsequent sustained isometric task. In addition, a 6-second posttest MVIC was performed immediately after the sustained isometric muscle action.

Each subject performed a sustained isometric muscle action to exhaustion at 50% MVIC. Exhaustion was operationally defined as the subject being unable to maintain a torque value within ±5% of their 50% MVIC despite strong verbal encouragement. The subjects tracked their torque production on a computer monitor placed in front of them that displayed the real-time digitalized torque signal overlaid onto a programmed template identifying their target torque value. The isometric template and real-time torque signal overlay were programmed using LabVIEW (LabVIEW version 7.1; National Instruments, Austin, TX, USA).

Signal Processing

Surface EMG signals were recorded from the dominant VL muscle with an 8-channel linear electrode array and EMG 16 data acquisition system (EMG 16; LISiN-Prima Biomedical and Sport, Treviso, Italy). The skin over the VL was carefully abraded and cleaned with rubbing alcohol before securing the 8-channel linear electrode array to the VL using a double-sided adhesive strip. The adhesive strip had small holes that were cut for each silver bar electrode, and each hole was filled with 30 μl of conductive gel with a gel dispenser (AG22331; Eppendorf, Hamburg, Germany) (EMG 16, 2006). The raw EMG signals from each electrode of the probe were recorded in a monopolar signal acquisition mode (gain × 500) and analog filtered (fourth-order Bessel, bandwidth = 10–500 Hz) with the surface EMG 16 data acquisition system. The monopolar EMG signals were converted to a digital form with a 12-bit analog-to-digital converter at a sampling frequency of 2,048 Hz and stored on a personal computer for subsequent analyses. Electrodes 6 and 7 were differentiated to make a bipolar electrode arrangement that was located 20 mm distal to the IZ with an interelectrode distance of 10 mm. The surface MMG signals were recorded using a miniature accelerometer (Entran EGAS FT 10, bandwidth 0–200 Hz, dimensions 1.0 × 1.0 × 0.5 cm, mass 1.0 g, sensitivity 649.5 mV·g−1) placed over the muscle belly of the VL using double-sided adhesive tape.

The EMG and MMG signals were zero-meaned and band-pass filtered (fourth-order Butterworth) at 10–500 and 5–100 Hz, respectively. The EMG amplitude (root mean square: RMS), EMG frequency (mean power frequency: MPF), MMG RMS, and MMG MPF values for the sustained isometric muscle action were calculated from 0.25-second epochs extracted every 10% of the time to exhaustion. The first 10% of the time to exhaustion was omitted to account for the time it took for each subject to stabilize their isometric torque at 50% MVIC. Therefore, the EMG RMS, EMG MPF, MMG RMS, and MMG MPF values were normalized as a percentage of the value at 10% of the time to exhaustion to examine the patterns of responses across the remaining 10–100% of the time to exhaustion of the sustained isometric muscle action where all subjects were at 50% MVIC. Time was normalized as a percentage of the total time to exhaustion. All signal processing was performed using custom programs written with LabVIEW programming software (Version 13.0; National Instruments).

Statistical Analyses

Polynomial regression analyses were used to determine whether there were significant linear, quadratic, or cubic relationships for the normalized EMG RMS, EMG MPF, MMG RMS, and MMG MPF vs. normalized time to exhaustion relationships for the composite of all subjects (28,35). A paired sample t-test was used to compare the mean MVIC values from the pretest vs. posttest measurement (35). An alpha of p ≤0.05 was considered statistically significant for all regression and t-test comparisons (Version 22.0; SPSS, Armonk, NY, USA).

Results

The mean ± SD for the time to exhaustion was 102.2 ± 17.9 seconds for the 11 subjects. Figure 1 shows the results of the polynomial regression analyses for the normalized EMG RMS, EMG MPF, MMG RMS, and MMG MPF vs. normalized time to exhaustion relationships during the sustained isometric muscle action. There was a significant positive linear relationship (p = 0.018, r2 = 0.77) for the EMG RMS vs. time to exhaustion throughout the sustained isometric muscle action (Figure 1). There were significant negative quadratic relationships for EMG MPF (p = 0.002, R2 = 0.99) and MMG MPF (p = 0.015, R2 = 0.94) vs. time to exhaustion that began to decrease at approximately 30% of the time to exhaustion (Figure 1). There was a significant cubic, but not linear or quadratic, relationship (p = 0.001, R2 = 0.94) between MMG RMS and time to exhaustion during the sustained isometric muscle action (Figure 1). From the initiation of the muscle action to the time to exhaustion, there were 48 and 81% increases in EMG RMS and MMG RMS but 23 and 27% decreases in EMG MPF and MMG MPF, respectively. In addition, there was a significant decrease in MVIC torque from pretest ±SD (287.2 ± 83.5 N·m) to posttest ±SD (145.6 ± 42.1 N·m).

Discussion

In the present study, during the sustained isometric muscle action, there were mean increases in EMG RMS (48%) and MMG RMS (81%) and decreases in EMG MPF (23%) and MMG MPF (27%) from the initial 10% of the time to exhaustion (Figure 1). In addition, there was a 50% decrease in mean torque production from the pretest to posttest MVIC measurements. These findings were in agreement with Neyroud et al. (24) who reported a 58% increase in EMG RMS and Smith et al. (31) who reported 22–30% decreases in EMG MPF from the VL after a sustained isometric muscle action of the leg extensors at 50% MVIC. Tarata (32) and Madeleine et al. (19) reported 30–60% increases in MMG RMS and 15–30% decreases in MMG MPF from the biceps brachii during sustained isometric muscle actions at 25 and 30% MVIC. In addition, Hendrix et al. (15) showed 17–25% decreases in MMG MPF from the VL during sustained isometric muscle actions of the leg extensors at 35–75% MVIC. Fatigue-induced increases in EMG RMS and MMG RMS and decreases in EMG MPF and MMG MPF during sustained isometric muscle actions have been attributed to the occlusion of muscle blood flow and decreases in muscle pH caused by the buildup of metabolic by-products (hydrogen ions, inorganic phosphate, potassium, and ammonia), which alter muscle contractility and lead to greater muscle activation to maintain a constant force or torque (10,18,23). In addition to a decrease in muscle pH, fatigue-induced decreases in EMG MPF have been associated with increases in extracellular potassium, which results in a progressive loss of membrane excitability and slows motor unit action potential conduction velocity (1,14,17). Thus, it is likely that the buildup of metabolic by-products associated with blood flow occlusion were responsible for the increases in EMG RMS and MMG RMS and the decreases in EMG MPF and MMG MPF during the sustained isometric muscle action of the leg extensors in the present study.

During a sustained isometric muscle action, task failure occurs when the desired force output can no longer be maintained (1). The purpose of the present study was to examine the EMG RMS, EMG MPF, MMG RMS, and MMG MPF responses from the VL during a sustained isometric muscle action at 50% MVIC to task failure to determine the time course of fatigue-induced changes in motor unit activation strategies. In the present study, there was a linear increase in EMG throughout the sustained isometric muscle action (Figure 1). From 10 to 30% of the time to exhaustion, there were increases in EMG RMS and MMG RMS, but no changes in EMG MPF and MMG MPF. The EMG MPF and MMG MPF values began to decrease nonlinearly at approximately 30% of the time to exhaustion and continued to decrease to task failure (Figure 1). The MMG RMS had a cubic relationship that increased from 10 to 30% of the time to exhaustion but then decreased from 40 to 70% of the time to exhaustion. After 70% of the time to exhaustion, however, MMG RMS increased precipitously to task failure (Figure 1). Thus, from 10 to 30% of the sustained isometric muscle action, the increases in muscle activation (EMG RMS) and motor unit recruitment (MMG RMS) did not coincide with changes in global motor unit firing rate (MMG MPF) or motor unit action potential conduction velocity (EMG MPF). These responses suggested that during the initial 30–40% of the sustained isometric muscle action, the increase in muscle activation was likely because of motor unit recruitment, but not changes in firing rate. Between 40 and 70% of the time to exhaustion, muscle activation (EMG RMS) continued to increase linearly but MMG RMS and MMG MPF decreased. The decreases in MMG MPF likely reflected a fatigue-induced decrease in the global firing rate of the activated motor units (25–27). The decreases in MMG RMS from 40 to 70% of the time to exhaustion may have reflected a balance between the competing effects of motor unit recruitment (which increases MMG RMS) and intramuscular pressure (which decreases MMG RMS) on the MMG signal. That is, a fatigue-induced increase in motor unit recruitment would increase MMG RMS, whereas an increase in intramuscular fluid pressure can limit the lateral oscillation of the activated muscle fibers and, thereby, decrease MMG RMS. It is possible that from 40 to 70% of the time to exhaustion, the influence of intramuscular fluid pressure on the MMG signal was greater than that associated with the increase in motor unit recruitment, and therefore, MMG RMS decreased. These findings were in agreement with previous studies (3,9) that suggested the effects of intramuscular fluid pressure during a fatiguing workbout can affect the MMG signal, resulting in a decrease in MMG RMS despite an increase in motor unit recruitment. After approximately 70% of the time to exhaustion, muscle activation (EMG RMS) continued to increase linearly, whereas EMG MPF and MMG MPF decreased at greater rates than between 30 and 70% of the time to exhaustion. Thus, muscle activation (EMG RMS) increased despite a decrease in global motor unit firing rate (MMG MPF). Furthermore, the 17-fold increase in MMG RMS after 70% of the time to exhaustion was likely because of an increase in motor unit recruitment and a plateau in intramuscular fluid pressure. Moalla et al. (21) found that during a sustained isometric muscle action of the leg extensors at 50% MVIC, intramuscular pressure of the VL plateaued at 50% of the time to exhaustion. Thus, unlike between 40 and 70% of the time to exhaustion, it is likely that between 70% of the time to exhaustion and task failure, motor unit recruitment accounted for the increases in muscle activation (EMG RMS) and had a greater effect on MMG RMS than did intramuscular fluid pressure.

The current findings should be viewed within the limitations of the study's methodology. The neuromuscular parameters assessed in the present study are indirect indicators of muscle activation (EMG RMS), motor unit action potential conduction velocity (EMG MPF), motor unit recruitment (MMG RMS), and global motor unit firing rate (MMG MPF). That is, the surface EMG signal is affected by a number of physiological and nonphysiological factors that are not reflective of motor unit activation strategies (12,13). The MMG signal is also affected by many factors, including motor unit synchronization, intramuscular pressure, and muscle stiffness (21,25,26). Furthermore, the current findings are limited to sustained isometric muscle actions of the VL and should not be applied to other muscles or dynamic muscle actions.

In the present study there were increases in EMG RMS and MMG RMS and decreases in EMG MPF and MMG MPF that may be attributable to the buildup of metabolic by-products associated with blood flow occlusion. The motor unit activation strategies changed throughout the sustained isometric muscle action of the leg extensors at 50% MVIC. From 10 to 30% of the time to exhaustion, an increase in muscle activation (EMG RMS) and motor unit recruitment (MMG RMS) were the main contributors to maintaining the required torque production. Beginning at 30% of the time to exhaustion, however, muscle activation (EMG RMS) and motor unit recruitment (MMG RMS) continued to increase but global motor unit firing rate (MMG MPF) and motor unit action potential conduction velocity (EMG MPF) began to decrease nonlinearly. Between 40 and 70% of the time to exhaustion, the required force was maintained by increases in muscle activation (EMG RMS), despite fatigue-induced decreases in motor unit action potential conduction velocity (EMG MPF) and global motor unit firing rate (MMG MPF). Between 70% of the time to exhaustion and task failure, there were increases in muscle activation (EMG RMS) and motor unit recruitment (MMG RMS) and decreases in motor unit action potential conduction velocity (EMG MPF) and global motor unit firing rate (MMG MPF). These findings indicated that the motor unit activation strategies changed throughout the sustained isometric muscle action of the leg extensors at 50% MVIC to maintain the production of torque.

Practical Applications

These findings have applications to a variety of fields, including strength training, supplementation, and clinical practices. Specifically, the identification of the time course of changes in neuromuscular responses as a result of training-induced adaptations may provide additional information regarding the process of fatigue during submaximal compared with maximal measurements. Typically, maximal measurements are taken before and after submaximal workbouts and are used to make inferences regarding the process of fatigue. These maximal measurements, however, may not provide complete information regarding the process of fatigue during a submaximal workbout. Because most sports require repetitive submaximal muscle actions, the time course of changes in neuromuscular responses may provide additional information regarding the process of fatigue compared with maximal measurements alone. Thus, the time course of changes in neuromuscular responses may be applied to research, clinical, and training applications to examine the effects of a fatiguing workbout, training program, or the effectiveness of supplements on the process of fatigue by comparing the changes in time, direction, and magnitude of neuromuscular parameters.

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Keywords:

fatigue; recruitment; neurophysiological; resistance training; quadriceps muscle; skeletal

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