Neuromuscular adjustments that constrain submaximal EMG amplitude at task failure of sustained isometric contractions

The amplitude of the surface EMG does not reach the level achieved during a maximal voluntary contraction force at the end of a sustained, submaximal contraction, despite near-maximal levels of voluntary effort. The depression of EMG amplitude may be explained by several neural and muscular adjustments during fatiguing contractions, including decreased net neural drive to the muscle, changes in the shape of the motor unit action potentials, and EMG amplitude cancellation. The changes in these parameters for the entire motor unit pool, however, cannot be measured experimentally. The present study used a computational model to simulate the adjustments during sustained isometric contractions and thereby determine the relative importance of these factors in explaining the submaximal levels of EMG amplitude at task failure. The simulation results indicated that the amount of amplitude cancellation in the simulated EMG (～ 40%) exhibited a negligible change during the fatiguing contractions. Instead, the main determinant of the submaximal EMG amplitude at task failure was a decrease in muscle activation (number of muscle fiber action potentials), due to a reduction in the net synaptic input to motor neurons, with a lesser contribution from changes in the shape of the motor unit action potentials. Despite the association between the submaximal EMG amplitude and reduced muscle activation, the deficit in EMG amplitude at task failure was not consistently associated with the decrease in neural drive (number of motor unit action potentials) to the muscle. This indicates that the EMG amplitude cannot be used as an index of neural drive.     

Sensitivity of the cross-correlation between simulated surface EMGs for two muscles to detect motor unit synchronization.

The purpose of the study was to evaluate the use of cross-correlation analysis between simulated surface electromyograms (EMGs) of two muscles to quantify motor unit synchronization. The volume conductor simulated a cylindrical limb with two muscles and bone, fat, and skin tissues. Models of two motor neuron pools were used to simulate 120 s of surface EMG that were detected over both muscles. Short-term synchrony was established using a phenomenological model that aligned the discharge times of selected motor units within and across muscles to simulate physiological levels of motor unit synchrony. The correlation between pairs of surface EMGs was estimated as the maximum of the normalized cross-correlation function. After imposing four levels of motor unit synchrony across muscles, five parameters were varied concurrently in the two muscles to examine their influence on the correlation between the surface EMGs: 1) excitation level (5, 10, 15, and 50% of maximum); 2) muscle size (350 and 500 motor units); 3) fat thickness (1 and 4 mm); 4) skin conductivity (0.1 and 1 S/m); and 5) mean motor unit conduction velocity (2.5 and 4 m/s). Despite a constant and high level of motor unit synchronization among pairs of motor units across the two muscles, the cross-correlation index ranged from 0.08 to 0.56, with variation in the five parameters. For example, cross-correlation of EMGs from pairs of hand muscles, each having thin layers of subcutaneous fat and mean motor unit conduction velocities of 4 m/s, may be relatively insensitive to the level of synchronization across muscles. In contrast, cross-correlation of EMGs from pairs of leg muscles, with larger fat thickness, may exhibit a different sensitivity. These results indicate that cross correlation of the surface EMGs from two muscles provides a limited measure of the level of synchronization between motor units in the two muscles.     

Amplitude cancellation reduces the size of motor unit potentials averaged from the surface EMG.

The purpose of the study was to evaluate the influence of selected physiological parameters on amplitude cancellation in the simulated surface electromyogram (EMG) and the consequences for spike-triggered averages of motor unit potentials derived from the interference and rectified EMG signals. The surface EMG was simulated from prescribed recruitment and rate coding characteristics of a motor unit population. The potentials of the motor units were detected on the skin over a hand muscle with a bipolar electrode configuration. Averages derived from the EMG signal were generated using the discharge times for each of the 24 motor units with lowest recruitment thresholds from a population of 120 across three conditions: 1) excitation level; 2) motor unit conduction velocity; and 3) motor unit synchronization. The area of the surface-detected potential was compared with potentials averaged from the interference, rectified, and no-cancellation EMGs. The no-cancellation EMG comprised motor unit potentials that were rectified before they were summed, thereby preventing cancellation between the opposite phases of the potentials. The percent decrease in area of potentials extracted from the rectified EMG was linearly related to the amount of amplitude cancellation in the interference EMG signal, with the amount of cancellation influenced by variation in excitation level and motor unit conduction velocity. Motor unit synchronization increased potentials derived from both the rectified and interference EMG signals, although cancellation limited the increase in area for both potentials. These findings document the influence of amplitude cancellation on motor unit potentials averaged from the surface EMG and the consequences for using the procedure to characterize motor unit properties.     

Task-Dependent Intermuscular Motor Unit Synchronization between Medial and Lateral Vastii Muscles during Dynamic and Isometric Squats

Purpose

Motor unit activity is coordinated between many synergistic muscle pairs but the functional role of this coordination for the motor output is unclear. The purpose of this study was to investigate the short-term modality of coordinated motor unit activity–the synchronized discharge of individual motor units across muscles within time intervals of 5ms–for the Vastus Medialis (VM) and Lateralis (VL). Furthermore, we studied the task-dependency of intermuscular motor unit synchronization between VM and VL during static and dynamic squatting tasks to provide insight into its functional role.

Methods

Sixteen healthy male and female participants completed four tasks: Bipedal squats, single-leg squats, an isometric squat, and single-leg balance. Monopolar surface electromyography (EMG) was used to record motor unit activity of VM and VL. For each task, intermuscular motor unit synchronization was determined using a coherence analysis between the raw EMG signals of VM and VL and compared to a reference coherence calculated from two desynchronized EMG signals. The time shift between VM and VL EMG signals was estimated according to the slope of the coherence phase angle spectrum.

Results

For all tasks, except for singe-leg balance, coherence between 15–80Hz significantly exceeded the reference. The corresponding time shift between VM and VL was estimated as 4ms. Coherence between 30–60Hz was highest for the bipedal squat, followed by the single-leg squat and the isometric squat.

Conclusion

There is substantial short-term motor unit synchronization between VM and VL. Intermuscular motor unit synchronization is enhanced for contractions during dynamic activities, possibly to facilitate a more accurate control of the joint torque, and reduced during single-leg tasks that require balance control and thus, a more independent muscle function. It is proposed that the central nervous system scales the degree of intermuscular motor unit synchronization according to the requirements of the movement task at hand.     

Limitations of the surface electromyography technique for estimating motor unit synchronization

Motor unit synchronization was estimated from the surface electromyograms (EMG) of the first dorsal interosseus muscle of human volunteers by a simplified surface-EMG technique (Milner-Brown et al. 1973, 1975). Single motor units were identified from intramuscular recordings and were used to obtain a spike-triggered average of the surface-EMG. The discharge rate of a reference motor unit was controlled at two levels (high and low), and the effect of motor unit activity on the surface-EMG estimate of synchronization was studied in 56 motor units. The surface-EMG estimate of motor unit synchronization was significantly higher when the reference motor unit discharged at the high rate than when it discharged at the low rate. A regression analysis indicated that the synchronization ratio calculated from the surface EMG was significantly correlated with the level of EMG activity in the muscle. Motor unit synchronization was also estimated from surface-EMG measurements that were derived by computer simulation. The simulation permitted manipulation of motor unit activity (discharge rate and recruitment) with a complete absence of synchrony among the units in the pool. The stimulated surface-EMG index was influenced by an artifact associated with signal rectification, and this effect changed non-monotonically with motor unit activity. Furthermore, the increase in the motor unit activity reduced the signal-to-noise ratio of the spike-triggered surface EMG average, and consequently decreased the sensitivity of the surface-EMG index as an estimate of motor unit synchronization. We conclude that the simplified surface-EMG method (Milner-Brown et al. 1973, 1975) does not provide a useful index of motor unit synchronization due to its inability to accurately distinguish the synchronization from methodological effects related to a rectification artifact and variation in the signal-to-noise ratio.     

Motor unit firing rates during isometric voluntary contractions performed at different muscle lengths

Firing rates of motor units and surface EMG were measured from the triceps brachii muscles of able-bodied subjects during brief submaximal and maximal isometric voluntary contractions made at 5 elbow joint angles that covered the entire physiological range of muscle lengths. Muscle activation at the longest, midlength, and shortest muscle lengths, measured by twitch occlusion, averaged 98%, 97%, and 93% respectively, with each subject able to achieve complete activation during some contractions. As expected, the strongest contractions were recorded at 90 degrees of elbow flexion. Mean motor unit firing rates and surface EMG increased with contraction intensity at each muscle length. For any given absolute contraction intensity, motor unit firing rates varied when muscle length was changed. However, mean motor unit firing rates were independent of muscle length when contractions were compared with the intensity of the maximal voluntary contraction (MVC) achieved at each joint angle.     

Chest wall muscle cross talk in canine costal diaphragm electromyogram

Sinderby, C., S. Friberg, N. Comtois, and A. Grassino.Chest wall muscle cross talk in the canine costal diaphragm electromyogram. J. Appl. Physiol.81(5): 2312-2327, 1996.The present paper describes the influenceof cross talk from the abdominal and intercostal muscles on the caninediaphragm electromyogram (EMG). The diaphragm EMG was recorded withbipolar surface electrodes placed on the costal portion of thediaphragm (abdominal side), aligned in the fiber direction, andpositioned in a region with a relatively low density of motor endplates. The results indicated that cross talk may occur in thediaphragm EMG, especially during conditions of loaded breathing andlight general anesthesia. The cross-talk signals showed characteristicsthat were entirely different from the diaphragm EMG. Although thediaphragm EMG was typical for signals recorded with electrodes alignedin the fiber direction, the cross-talk signals were characteristic ofthose obtained with electrode pairs not aligned in the direction of themuscle fibers. Alterations in electrode positioning, interelectrodedistance, and/or electrode surface area cannot guarantee theelimination of cross-talk signals, whereas spinal anesthesia at a highthoracic level will paralyze the sources of the cross talk and henceeliminate the cross-talk signals. By taking advantage of thedifferences in EMG signal characteristics for the diaphragm EMG andcross-talk signals, an index that has the capability to detect crosstalk was developed.

     

Motor unit activity and surface electromyogram power spectrum during increasing force of contraction

Twelve male subjects were tested to determine the relationship between motor unit (MU) activities and surface electromyogram (EMG) power spectral parameters with contractions increasing linearly from zero to 80% of maximal voluntary contraction (MVC). Intramuscular spike and surface EMG signals recorded simultaneously from biceps brachii were analyzed by means of a computer-aided intramuscular MU spike amplitude-frequency (ISAF) histogram and an EMG frequency power spectral analysis. All measurements were made in triplicate and averaged. Results indicate that there were highly significant increases in surface EMG amplitude (71 +/- 31.3 to 505 +/- 188 microV, p less than 0.01) and mean power frequency (89 +/- 13.3 to 123 +/- 23.5 Hz, p less than 0.01) with increasing force. These changes were accompanied by progressive increases in the firing frequency of MU's initially recruited, and of newly recruited MU's with relatively larger spike amplitudes. The group data in the ISAF histograms revealed significant increases in mean spike amplitude (412 +/- 79 to 972 +/- 117 microV, p less than 0.01) and mean firing frequency (17.8 +/- 5.4 to 24.7 +/- 4.1 Hz, p less than 0.01). These data suggest that surface EMG spectral analysis can provide a sensitive measure of the relative changes in MU activity during increasing force output.     

等长伸膝动作的运动单元放电特征分析

本研究基于表面肌电分解技术,分析伸膝动作中不同发力状态下大腿肌肉运动单元的解码准确性,并对比神经特征和肌电特征在肌肉激活程度估计中的效果. 12名大学生分别以2种发力速度和4种发力等级完成伸膝动作的等长收缩.实验同步采集受试者股内侧肌和股外侧肌处的高密度表面肌电信号和伸膝动作收缩力.基于卷积核补偿算法解码肌电信号得到运动单元动作电位,提取神经特征用于收缩力的互相关分析.结果发现,对于股内侧肌,2种任务及4种收缩力等级下平均解码得到(7±4)个运动单元,股外侧肌平均解码得到(9±5)个运动单元.它们的平均脉冲信噪比(pulse-to-noise ratio,PNR)为30.1 d B,对应解码准确率大于90%.股内侧肌的两种神经特征与力之间的平均相关性分别为(0.79±0.08)和(0.80±0.08),股外侧肌的两种神经特征与力之间的平均相关性分别为(0.85±0.05)和(0.85±0.06).综上可见,基于肌电分解技术可以准确识别不同发力状态下大腿肌肉的运动单元放电活动,并且运动单元放电频率与伸膝动作力高度相关,研究结果可用于运动康复、运动训练及人机接口等领域.     

The extraction of neural strategies from the surface EMG.

This brief review examines some of the methods used to infer central control strategies from surface electromyogram (EMG) recordings. Among the many uses of the surface EMG in studying the neural control of movement, the review critically evaluates only some of the applications. The focus is on the relations between global features of the surface EMG and the underlying physiological processes. Because direct measurements of motor unit activation are not available and many factors can influence the signal, these relations are frequently misinterpreted. These errors are compounded by the counterintuitive effects that some system parameters can have on the EMG signal. The phenomenon of crosstalk is used as an example of these problems. The review describes the limitations of techniques used to infer the level of muscle activation, the type of motor unit recruited, the upper limit of motor unit recruitment, the average discharge rate, and the degree of synchronization between motor units. Although the global surface EMG is a useful measure of muscle activation and assessment, there are limits to the information that can be extracted from this signal.     

The cross-correlation and phase-difference methods are not equivalent under noninvasive estimation of the motor unit propagation velocity.

Noninvasive estimation of motor unit propagation velocity (MUPV) was reduced to that of the time delay between signals detected by two surface EMG electrodes placed along the muscle fibres. When the cross-correlation function between the signals was used, the problem with temporal resolution arose. Estimation of the time delay in the frequency domain was proposed to overcome this problem. To check whether the cross-correlation and phase-difference methods give the same estimates, the results obtained by both methods were compared through simulation. A different sensitivity of the two methods to the effects of the excitation origin and extinction was found. Besides, the quality of the estimate depended on the electrode arrangement. The longitudinal double difference electrodes were preferable with the phase-difference method, while the MUPV estimates obtained by the cross-correlation technique were more correct when the longitudinal single difference or bipolar transversal double difference electrodes were used. In addition, the estimates obtained by the phase-difference method were more sensitive to the longitudinal scattering of motor end-plates and ends of the fibres, to the fibre lengths and to the negative after-potential magnitude. Such sensitivity could make MUPV estimates incorrect even under a relatively small distance between the motor unit axis and electrode.     

Nonlinear surface EMG analysis to detect changes of motor unit conduction velocity and synchronization.

Amplitude and frequency content of the surface electromyographic (EMG) signal reflect central and peripheral modifications of the neuromuscular system. Classic surface EMG spectral variables applied to assess muscle functions are the centroid and median power spectral frequencies. More recently, nonlinear tools have been introduced to analyze the surface EMG; among them, the recurrence quantification analysis (RQA) was shown to be particularly promising for the detection of muscle status changes. The purpose of this work was to analyze the effect of motor unit short-term synchronization and conduction velocity (CV) on EMG spectral variables and two variables extracted by RQA, the percentage of recurrence (%Rec) and determinism (%Det). The study was performed on the basis of a simulation model, which allowed changing the degree of synchronization and mean CV of a number of motor units, and of an experimental investigation of the surface EMG signal properties detected during high-force-level isometric fatiguing contractions of the biceps brachii muscle. Simulations and experimental results were largely in agreement and show that 1) spectral variables, %Rec, and %Det are influenced by CV and degree of synchronization; 2) spectral variables are highly correlated with %Det (R = -0.95 in the simulations and -0.78 and -0.75 for the initial values and normalized slopes, respectively, in the experimental signals), and thus the information they provide on muscle properties is basically the same; and 3) variations of %Det and %Rec in response to changes in muscle properties are significantly larger than the variations of spectral variables. This study validates RQA as a means for fatigue assessment with potential advantages (such as the higher sensitivity to changes of muscle status) with respect to the classic spectral analysis.     

A Simulation Study to Examine the Effect of Common Motoneuron Inputs on Correlated Patterns of Motor Unit Discharge

The influence of common oscillatory inputs to the motoneuron pool on correlated patterns of motor unit discharge was examined using model simulations. Motor unit synchronization, in-phase fluctuations in mean firing rates known as ‘common drive’, and the coefficient of variation of the muscle force were examined as the frequency and amplitude of common oscillatory inputs to the motoneuron pool were varied. The amount of synchronization, the peak correlation between mean firing rates and the coefficient of variation of the force varied with both the frequency and amplitude of the common input signal. Values for ‘common drive’ and the force coefficient of variation were highest for oscillatory inputs at frequencies less than 5 Hz, while synchronization reached a maximum when the frequency of the common input was close to the average motor unit firing rate. The frequency of the common input signal for which the highest levels of synchronization were observed increased as motoneuron firing rates increased in response to higher target force levels. The simulation results suggest that common low-frequency oscillations in motor unit firing rates and short-term synchronization result from oscillatory activity in different bands of the frequency spectrum of shared motoneuron inputs. The results also indicate that the amount of synchronization between motor unit discharges depends not only on the amplitude of the shared input signal, but also on its frequency in relation to the present firing rates of the individual motor units.     

Training adaptations in the behavior of human motor units.

The purpose of this brief review is to examine the neural adaptations associated with training, by focusing on the behavior of single motor units. The review synthesizes current understanding on motor unit recruitment and rate coding during voluntary contractions, briefly describes the techniques used to record motor unit activity, and then evaluates the adaptations that have been observed in motor unit activity during maximal and submaximal contractions. Relatively few studies have directly compared motor unit behavior before and after training. Although some studies suggest that the voluntary activation of muscle can increase slightly with strength training, it is not known how the discharge of motor units changes to produce this increase in activation. The evidence indicates that the increase is not attributable to changes in motor unit synchronization. It has been demonstrated, however, that training can increase both the rate of torque development and the discharge rate of motor units. Furthermore, both strength training and practice of a force-matching task can evoke adaptations in the discharge characteristics of motor units. Because the variability in discharge rate has a significant influence on the fluctuations in force during submaximal contractions, the changes produced with training can influence motor performance during activities of daily living. Little is known, however, about the relative contributions of the descending drive, afferent feedback, spinal circuitry, and motor neuron properties to the observed adaptations in motor unit activity.     

Agonist-antagonist common drive during fatiguing knee extension efforts using surface electromyography.

AIM: This study examined the electromyographic (EMG) activity of knee extensor agonists and a knee extensor antagonist muscle during fatiguing isometric extensions across a range of force levels. METHODS: Five female subjects performed isometric knee extensions at 25%, 50%, 75% and 100% of their maximal voluntary contraction (MVC) with the knee flexed to 75 degrees. Surface EMG (SEMG) was recorded with bipolar electrodes from the vastus lateralis (VL), vastus medialis (VM), rectus femoris (RF) and biceps femoris (BF) and the root-mean-squared (RMS) amplitude and the percentage frequency compression of these recordings were calculated. Commonality and cross talk between recordings were also examined. RESULTS: Cross talk between recordings was deemed negligible despite significant levels of commonality between the agonist and antagonist SEMG, which was attributed to common drive. SEMG RMS amplitude increased significantly for all muscles during the 25%, 50%, 75% MVC knee extensions until task failure, and decreased significantly for 100% MVC. The frequency spectrum of the SEMG compressed significantly for all muscles and % MVC levels. The VM, VL and BF SEMG recordings responded similarly to fatigue. The RF's frequency spectrum compressed to a significantly higher degree. CONCLUSIONS: The VM, VL, RF, and BF fatigue in parallel, with high similarity between VM, VL and BF, giving support to the concept of a shared agonist-antagonist motoneuron pool.     

Validation of estimated muscle fiber conduction velocity with the normalized peak-averaging technique.

To estimate muscle fiber conduction velocity (MFCV), the normalized peak-averaging technique was developed along with complementary software and reported in a previous study. Electromyograms were recorded from the vicinity of end-plate zones (EMG data 1) and a site farther from the end-plates and distal tendons (EMG data 2) of biceps brachii muscles using surface array electrodes during 50% maximal voluntary isometric contractions in ten healthy volunteers. The MFCV values obtained with normalized peak-averaging technique were compared to those obtained with the cross-correlation technique and examined by computer simulation of the MFCV distribution. The MFCV values obtained with normalized peak-averaging technique highly correlated with those obtained with cross-correlation technique in both EMG data 1 and EMG data 2. It was also confirmed that MFCV values obtained from EMG data 1 were distributed much more widely than those obtained from EMG data 2. These results show the clinical usefulness of normalized peak-averaging technique for the detailed assessment of MFCV.     

Influence of amplitude cancellation on the accuracy of determining the onset of muscle activity from the surface electromyogram

The purpose of the study was to quantify the influence of amplitude cancellation on the accuracy of detecting the onset of muscle activity based on an analysis of simulated surface electromyographic (EMG) signals. EMG activity of a generic lower limb muscle was simulated during the stance phase of human gait. Surface EMG signals were generated with and without amplitude cancellation by summing simulated motor unit potentials either before (cancellation EMG) or after (no-cancellation EMG) the potentials had been rectified. The two sets of EMG signals were compared at forces of 30% and 80% of maximum voluntary contraction (MVC) and with various low-pass filter cut-off frequencies. Onset time was determined both visually and by an algorithm that identified when the mean amplitude of the signal within a sliding window exceeded a specified standard deviation (SD) above the baseline mean. Onset error was greater for the no-cancellation conditions when determined automatically and by visual inspection. However, the differences in onset error between the two cancellation conditions appear to be clinically insignificant. Therefore, amplitude cancellation does not appear to limit the ability to detect the onset of muscle activity from the surface EMG.     

Influence of amplitude cancellation on the simulated surface electromyogram.

The purpose of the study was to quantify the influence of selected motor unit properties and patterns of activity on amplitude cancellation in the simulated surface electromyogram (EMG). The study involved computer simulations of a motor unit population with physiologically defined recruitment and rate coding characteristics that activated muscle fibers whose potentials were recorded on the skin over the muscle. Amplitude cancellation was quantified as the percent difference in signal amplitude when motor unit potentials were summed before and after rectification. The simulations involved varying the level of activation for the motor unit population, the recording configuration, the upper limit of motor unit recruitment, peak discharge rates, the amount of motor unit synchronization, muscle fiber length, the thickness of the subcutaneous tissue, and the motor unit properties that change with advancing age. The results confirmed a previous experimental report (Day SJ and Hulliger M, J Neurophysiol 86: 2144-2158, 2001) that amplitude cancellation in the surface EMG can reach 62% at maximal activation. A decrease in the range of amplitudes of the motor unit potentials, as can occur during fatiguing contractions, increased amplitude cancellation up to approximately 85%. Differences in the amount of amplitude cancellation were observed across all simulated conditions, and resulted in substantial changes in the absolute magnitude of the EMG signal. The most profound factors influencing amplitude cancellation were the number of active motor units and the duration of the action potentials. The effects of amplitude cancellation were minimal (<5%) when the EMG amplitude was normalized to maximal values, with the exception of variations in peak discharge rate and recruitment range, which resulted in differences up to 17% in the normalized EMG signal across conditions. These results indicate the amount of amplitude cancellation that can occur in various experimental conditions and its influence on absolute and relative measures of EMG amplitude.     

Motor unit recruitment strategies investigated by surface EMG variables.

During isometric contractions of increasing strength, motor units (MUs) are recruited by the central nervous system in an orderly manner starting with the smallest, with muscle fibers that usually show the lowest conduction velocity (CV). Theory predicts that the higher the velocity of propagation of the action potential, the higher the power at high frequencies of the detected surface signal. These considerations suggest that the power spectral density of the surface detected electromyogram (EMG) signal may give indications about the MU recruitment process. The purpose of this paper is to investigate the potential and limitations of spectral analysis of the surface EMG signal as a technique for the investigation of muscle force control. The study is based on a simulation approach and on an experimental investigation of the properties of surface EMG signals detected from the biceps brachii during isometric linearly increasing torque contractions. Both simulation and experimental data indicate that volume conductor properties play an important role as confounding factors that may mask any relation between EMG spectral variables and estimated CV as a size principle parameter during ramp contractions. The correlation between spectral variables and CV is thus significantly lower when the MU pool is not stable than during constant-torque isometric contractions. Our results do not support the establishment of a general relationship between spectral EMG variables and torque or recruitment strategy.