Motor unit number estimation by decomposition-enhanced spike-triggered averaging: control data, test-retest reliability, and contractile level effects

Decomposition-enhanced spike-triggered averaging (DE-STA) has been developed as a method for obtaining a motor unit number estimate (MUNE). We describe the method and report control data for the first dorsal interosseous/adductor pollicis and thenar muscles and reliability in the thenar muscles. Seventeen subjects (ages 20-50 years) took part in the study. The maximum M potential was elicited with supramaximal stimulation of the ulnar or median nerve at the wrist. Surface and intramuscularly detected electromyographic signals were then collected simultaneously during mild to moderate contractions. Decomposition algorithms were used to detect and sort the individual motor unit potential (MUP) occurrences of several concurrently active motor units in the needle-detected signals. The MUP occurrences were used as triggering sources to estimate their corresponding surface-detected MUPs (S-MUPs) using STA. The mean S-MUP size was calculated and divided into the maximum M-potential size to derive a MUNE. The MUNE values were consistent with those previously reported with other methods, and thenar MUNEs for the two trials were similar (249 +/- 78 and 246 +/- 90), with high test-retest reliability (r = 0.94, P < 0.05). DE-STA thus appears to be a valid and reliable method to obtain MUNEs.     

Effect of motor unit firing pattern on twitches obtained by spike-triggered averaging

The spike-triggered averaging technique (STA) was used to determine the twitch profile of single motor units in human masseter during a voluntary isometric contraction. The effect of the immediate firing pattern of the unit on the twitch was assessed with a computer program which scanned the unit discharge records and selected valid trigger spikes for the averager on the basis of the interspike intervals preceding and following the trigger spike. Successive averages from the same data using different interval parameters revealed progressively more fusion of twitches as the instantaneous firing rate increased. When the data were averaged with interval parameters similar to those used in earlier studies, some fusion of the twitch profile was also evident. It is therefore likely that the degree of fusion of human motor unit twitches obtained by STA has been underestimated in the past. It is further concluded that masseter motor units are sufficiently fast-contracting to allow a relatively unfused twitch profile to be obtained with STA, provided trigger spikes are subjected to appropriate rate control.     

Decomposition-based quantitative electromyography: effect of force on motor unit potentials and motor unit number estimates

Decomposition-based quantitative electromyography (DQEMG) allows for the collection of motor unit potentials (MUPs) over a broad range of force levels. Given the size principle of motor unit recruitment, it may be necessary to control for force when using DQEMG for the purpose of deriving a motor unit number estimate (MUNE). Therefore, this study was performed to examine the effect of force on the physiological characteristics of concentric needle- and surface-detected MUPs and the subsequent impact on MUNEs obtained from the first dorsal interosseous (FDI) muscle sampled using DQEMG. Maximum M waves were elicited in 10 subjects with supramaximal stimulation of the ulnar nerve at the wrist. Intramuscular and surface-detected EMG signals were collected simultaneously during 30-s voluntary isometric contractions performed at specific percentages of maximal voluntary contraction (MVC). Decomposition algorithms were used to identify needle-detected MUPs and their individual MU firing times. These MU firing times were used as triggers to extract their corresponding surface-detected MUPs (S-MUPs) using spike-triggered averaging. A mean S-MUP was then calculated, the size of which was divided into the maximum M-wave size to derive a MUNE. Increased levels of contraction had a significant effect on needle- and surface-detected MUP size, firing rate, and MUNE. These results suggest that force level is an important factor to consider when performing quantitative EMG, including MUNEs with this method.     

Reliability of spike triggered averaging of the surface electromyogram for motor unit action potential estimation

Introduction: The reliability of estimated motor unit parameters using spike triggered averaging (STA) of the surface electromyogram (sEMG) has not been tested thoroughly. We investigated factors that may induce amplitude bias in estimated motor unit action potentials (MUAPs) and shape variations. Methods: An sEMG record was simulated. MUAPs were then estimated from the STA of the simulated EMG. Results: Variations in MUAP duration led to under‐estimation of real MUAP amplitude, while synchronized firing led to over‐estimation of amplitude. Spurious firing resulted in over‐estimation of the amplitude of small motor units but under‐estimation of the amplitude of large ones. Variability in amplitude and high firing rates had minimal influence on amplitude estimation. High firing rates and variation in MUAP duration led to large variations in MUAP shape. Estimation errors also correlated with shape variations. Conclusions: Recommendations to enhance the accuracy of the STA estimates have been proposed. Muscle Nerve 48 : 557–570, 2013     

The effect of contraction intensity on motor unit number estimates of the tibialis anterior.

OBJECTIVE: To examine the effect of contractile level on motor unit number estimates (MUNEs) and establish the contraction intensity that will yield the most representative MUNE for the tibialis anterior (TA) muscle. METHODS: Surface and intramuscular electromyographic (EMG) signals were collected during a range of submaximal (threshold, 10, 20, 30 and 40% MVC) isometric dorsiflexion contractions using decomposition-enhanced spike-triggered averaging (DE-STA). Six MUNEs were calculated, one for each of the five intensities, and an ensemble sixth MUNE that had equal MU contributions from all intensities. RESULTS: Mean surface-motor unit potential sizes increased significantly (26-69 microV) and MUNEs decreased accordingly (226-91) as contraction intensity increased from threshold to 40% MVC, respectively (P<0.05). The ensemble MUNE was 153, and extrapolated to approximately 25% MVC. CONCLUSIONS: There was a significant and progressive decline in the MUNE as contraction intensity increased, confirming the importance of monitoring torque during data collection. The ensemble MUNE suggests that collecting EMG signals at a contraction intensity of approximately 25% MVC provides the most representative sample of the actual number and sizes of MUs in the TA. SIGNIFICANCE: Establishing appropriate contraction intensities improves the utility of DE-STA as a useful method for tracking changes to the MU pool in disease states and healthy aging.     

Continuous motor unit activity confined to the upper extremities

We report a patient with clinical vermiform motor activity, muscle cramps, delayed relaxation of grip, and continuous motor unit discharges who developed mild symmetric symptoms in the upper extremities following a viral infection. Treatment with carbamazepine produced considerable symptomatic improvement. Needle electromyography (EMG) in several muscles showed irregular grouped spontaneous discharges composed of potentials resembling normal motor units. The discharges occurred asynchronously in distal muscles with identical and different peripheral nerve innervation but were not seen in more proximal muscles innervated by the same nerves. Our EMG findings indicate an origin of this spontaneous activity in the terminal branched motor nerves.     

Monitoring of free calcium in the neuronal endoplasmic reticulum: an overview of modern approaches

This paper describes an improved spike triggered averaging technique for the assessment of control properties and conduction velocity (CV) of single motor units (MUs) of the tibialis anterior muscle during voluntary muscle contractions. The method is based on the detection of multi-channel surface EMG signals (with linear electrode arrays) and intramuscularly recorded single MU action potentials (MUAPs). Intramuscular electrodes were inserted in the muscle taking into account the MU structural properties (innervation zone, tendon locations, length of the fibers), assessed by the linear array surface EMG detection technique. An algorithm for intramuscular EMG signal decomposition is used to identify single MUAP trains. The MUAPs detected by the intramuscular EMG decomposition algorithm were used to trigger and average the multi-channel EMG signals. CV of single averaged surface MUAPs was estimated by the use of advanced signal processing methods based on multi-channel recordings which allow to consistently reduce the variance of CV estimates compared with traditional two channel delay estimators. The number of averaged potentials can thus be limited, resulting in high temporal resolution CV estimates. The developed technique was tested on recordings from the tibialis anterior muscle in 11 volunteers during fatigue. It was shown that the method allows the assessment of single MU CV changes (fatigue) as small as 0.1 m/s with less than 2 s data epochs. The method allows reliable assessment of firing rate and conduction properties of single MUs with applications for the investigation of central and peripheral fatigue mechanisms.     

Concentric macro electromyography

Concentric EMG electrodes can record from a few (10 to 15) muscle fibers of a motor unit (MU). Macro EMG, is able to record from the majority of muscle fibers in the MU. The macro EMG electrode uses a single fiber action potential (SFAP) on one channel to trigger the time locked cannula (macro) response on the other channel. To study the concentric motor unit action potential (MUAP), alongside the macro potential, we built a needle electrode combining concentric and macro recording surfaces. The study of 240 motor units in 10 healthy subjects with the single fiber (SF macro) and concentric macro (conmac) electrodes revealed no significant differences between macro potentials areas and amplitudes obtained with either electrode. The ability to study a small and a large section of the motor unit simultaneously offers insights into the local or global nature of motor unit changes not otherwise available to the electromyographer. It also reveals which concentric parameters correlate best with the macro potential and, can even be of great help with the newer EMG signal decomposition techniques; by identifying each motor unit by its concentric and macro waveform simultaneously, it will allow for the "marking" of these motor units helping to reduce the risk of their misclassification when the concentric MUAP is used alone.     

Methods for estimating numbers of motor units in biceps-brachialis muscles and losses of motor units with aging

This paper presents a new method, here applied to the biceps-brachialis muscles, for estimating motor unit numbers in healthy subjects. This method combines isometric contraction, intramuscular needle electrode recordings, and spike-triggered averaging techniques to measure the sizes of motor unit potentials as recorded in the innervation zone with surface electrodes. The number of motor units is then estimated by division of the maximum biceps-brachialis "M" potential recorded with the same surface electrodes and evoked by supramaximal stimulation of the musculocutaneous nerve, by the mean of at least 10 surface-recorded motor unit potentials. The requisite intramuscular recordings provide additional information as to innervation density, incidence of linked potentials, and impulse blocking, phenomena that are particularly common in neurogenic and myogenic disorders. There was clear evidence of losses of motor units in older subjects: subjects over 60 years of age having approximately half the numbers of motor units of subjects under 60 years of age.     

Motor unit recruitment and bursts of activity in the surface electromyogram during a sustained contraction

Bursts of activity in the surface electromyogram (EMG) during a sustained contraction have been interpreted as corresponding to the transient recruitment of motor units, but this association has never been confirmed. The current study compared the timing of trains of action potentials discharged by single motor units during a sustained contraction with the bursts of activity detected in the surface EMG signal. The 20 motor units from 6 subjects [recruitment threshold, 35.3 +/- 11.3% maximal voluntary contraction (MVC) force] that were detected with fine wire electrodes discharged 2-9 trains of action potentials (7.2 +/- 5.6 s in duration) when recruited during a contraction that was sustained at a force below its recruitment threshold (target force, 25.4 +/- 10.6% MVC force). High-pass filtering the bipolar surface EMG signal improved its correlation with the single motor unit signal. An algorithm applied to the surface EMG was able to detect 75% of the trains of motor unit action potentials. The results indicate that bursts of activity in the surface EMG during a constant-force contraction correspond to the transient recruitment of higher-threshold motor units in healthy individuals, and these results could assist in the diagnosis and design of treatment in individuals who demonstrate deficits in motor unit activation.     

Effect of small motor unit potentials on the motor unit number estimate

Small surface motor unit potentials (S-MUPs) may have a negative influence on the variability of the motor unit number estimate (MUNE). According to published consensus criteria S-MUPs with a negative peak amplitude smaller than 10 muV should be omitted. The effect of omitting small S-MUPs on the MUNE was evaluated using a simulation model. The model incorporated a healthy and amyotrophic lateral sclerosis (ALS) distribution formed with real S-MUPs. Using a random drawing process the MUNE was calculated with and without small S-MUPs. In the healthy population 27% of all S-MUPs were small. MUNE determined without these S-MUPs was marginally less variable. However, MUNE values dropped about 24% at a sample size of 20. In ALS, only 12% of the total population of 130 S-MUPs were small. MUNE dropped about 12% without the small S-MUPs. By omitting small S-MUPs the differences between the healthy and ALS distributions become smaller. Therefore, incorporating small S-MUPs in the estimate is suggested.     

Quantitative comparison of motor unit potential parameters between monopolar and concentric needles

This study quantitatively compared the simultaneous recording of the "same" motor unit potentials recorded by closely positioned concentric and monopolar needles. The motor unit potentials from the anterior tibialis of 12 young subjects were analyzed independently by both needles being connected to 2 sets of EMG-computer combinations. Recordings of the same motor unit potentials were confirmed by triggering and averaging of the 2 sets of motor unit potentials with identical firing patterns on both EMG screens. Automatic analysis disclosed the monopolar recordings had a significantly higher mean amplitude (2.05 times), larger surface area (2.64 times), and longer duration (1.86 times) than the concentric recordings, while the mean number of phases (1.58 times) and turns (1.35 times) revealed no statistical differences. Both active recording and reference electrodes contributed to these differences.     

Multielectrode surface EMG for noninvasive estimation of motor unit size.

To noninvasively estimate the motor unit size, we present a novel surface electromyographic (EMG) measurement system consisting of a surface multielectrode with four-pin electrodes and a pair of surface-disk electrodes. Surface motor unit action potentials (MUAPs) were recorded with the multielectrode, in the so-called multielectrode surface EMG (MSEMG), which was spatially filtered to localize the sensing area and reduce the noise. In addition, a modified decomposition algorithm, considering the geometrical configuration of the multielectrode, was designed to identify the individual MUAPs in the measured MSEMG. The identified MUAP was subsequently used as the triggering source for the EMG signals recorded by the surface-disk electrodes. From a pool of 34 subjects with neuromuscular diseases and 14 normal subjects, the median amplitudes of surface-disk EMG after spike-triggered averaging, called MSEMG-MUAP, correlated well (r = 0.82, P < 0.0001) with those of macro EMG. Moreover, the MSEMG-MUAP recording during a ramp force contraction exhibited the common size principle phenomenon during motor unit recruitment. The results of this study demonstrate that the MSEMG-MUAP measurement is a feasible approach for estimating the motor unit size from the skin surface.     

Changes of the average muscle fiber conduction velocity during a varying force contraction

The average conduction velocity of muscle fibers measured with a surface electrode has been reported to increase with the level of contraction force. To clarify the factors causing this increase, the authors decomposed the interference surface EMG signal into its constituent motor unit action potentials and compared the average conduction velocity with the conduction velocity measured at the individual discharges of motor units. The conduction velocity within individual motor units increased with the contraction force and contributed to the increase of the average conduction velocity. However, the increase of the conduction velocity within motor units was relatively small and was insufficient to cause the increase of the average conduction velocity. This result indicates that the motor units recruited at higher thresholds of force should have higher conduction velocities.     

Two-dimensional spatial distribution of surface mechanomyographical response to single motor unit activity

In order to better understand the mechanisms of generation of mechanomyography (MMG) signals, the two-dimensional distribution of surface MMG produced by the activity of single motor units was analyzed by a novel two-dimensional recording method. Motor unit action potentials were identified from intramuscular electromyographic (EMG) signals and used to trigger the averaging of MMG signals detected over the tibialis anterior muscle of 11 volunteers with a grid of 5x3 accelerometers (20-mm inter-accelerometer distance). The intramuscular wires were inserted between the first and second accelerometer in the middle column of the grid, proximal to the innervation zone. The subjects performed three contractions with visual feedback of the intramuscular EMG signals. In each contraction, a new motor unit was recruited at the minimum stable discharge rate (mean+/-S.D., N = 11 subjects, 7.3+/-2.3 pulse/s), resulting in torque of 2.4+/-2.8% of the maximal voluntary contraction (MVC), 4.6+/-2.7% MVC, and 6.3+/-3.1% MVC (all different, P < 0.01). For 23 out of 33 detected motor units, it was possible to extract the motor unit surface acceleration map (MUAM). A negative MUAM peak (-2.7+/-2.2 mm/s2) was detected laterally and a positive MUAM peak (4.1+/-2.4 mm/s2) medially (P < 0.001). The time-to-peak was shorter in the medial part of the muscle (2.9+/-0.4 ms) than in the other locations (3.4+/-0.5 ms, P < 0.001). The double integrated signals (muscle displacement) indicated negative deflection in the lateral part and inflation close to the tibia bone. The maps of acceleration showed spatial dependency in single motor unit MMG activities. The technique provides a new insight into motor unit contractile properties.     

The estimation of conduction velocity in human skeletal muscle in situ with surface electrodes.

In the present study new methods were developed for estimation of conduction velocity using surface electrodes. The subjects were 4 healthy male volunteers, aged 23-29 years. EMGs were recorded from m. biceps brachii by several surface electrodes and a fine-wire bipolar electrode during weak isometric contraction with the elbow positioned at 90 degrees. Surface electrodes, 8 mm in diameter, were spaced along the course of muscle fibers at 20 mm intervals, while the bipolar fine-wire electrode was inserted in the middle of the muscle. The EMGs recorded on the magnetic tape were analyzed through a mini-computer system (ATAC-2300). Triggering a signal averager by spike potentials of single motor unit recorded by the inserted electrode, the average contribution of the single motor unit to the surface EMG could be extracted. The conduction velocity in m. biceps brachii determined from the averaged waves of each surface electrode was 4.6 +/- 0.5 m/sec (mean +/- S.D.). The conduction velocity estimated from the cross-correlation analysis between the EMGs of two different surface electrodes agreed well with the value obtained by the averaging technique mentioned above.     

Sources of error in the spike-triggered averaging method of motor unit number estimation (MUNE)

Motor unit number estimation (MUNE) is an electrophysical technique to estimate the number of motor units innervating a muscle or muscle group. MUNE may be useful as a measure of progression of lower motor neuron loss in amyotrophic lateral sclerosis (ALS). Several methods of MUNE have been developed. The spike-triggered averaging method can be readily performed on EMG machines with signal averaging capabilities and is suitable for estimating the number of motor neurons innervating proximal muscles. We have used MUNE as a measure of disease state in a drug efficacy trial for ALS. From our experience with this method we have identified sources of error which can affect MUNE accuracy. We have investigated these sources and report their effect on MUNE.© 1995 John Wiley & Sons, Inc.     

Pathophysiology of fasciculations in ALS as studied by electromyography of single motor units

Electromyographic potentials of fasciculations were studied in ten patients with amyotrophic lateral sclerosis (ALS). The EMG recordings were made from the extensor digitorum brevis muscle. The EMG recording was so selective that only one motor unit potential appeared on maximal voluntary effort and on supramaximal electrical stimulation of the peroneal nerve. In a series of fasciculations, the shapes of the EMG potentials varied, while in a series of voluntary twitch activations of electrical nerve stimulations the EMG potentials were mainly constant. Fasciculations were followed by antidromic impulses in the test unit axon as judged from collision tests, and they persisted after lidocaine blockades of the nerve to the muscle. The findings are compatible with a conclusion of distal multifocal triggering of fasciculation. Fasciculating motor units had voluntary firing properties close to those of normal low-threshold motor units. Widespread fasciculations were abolished by a nonparalytic dose of a synthetic curare derivative (Pavulon) and augmented by administration of neostigmine in two cases. The fasciculations in ALS thus have the same characteristics as experimental fasciculations evoked by cholinesterase inhibitors, and there is reason to believe that the underlying pathophysiological mechanism is similar in the two cases.     

Decomposition-based quantitative electromyography: methods and initial normative data in five muscles

Quantitative electromyographic (EMG) techniques provide clinically useful information to aid in the diagnosis and follow the course or response to treatment of diseases affecting the motor system. The purpose of this study was to describe a decomposition-based quantitative electromyography method (DQEMG) designed to obtain clinically applicable information relating to motor unit potential (MUP) size and configuration, and motor unit (MU) firing characteristics. Additionally, preliminary normative data were obtained from the deltoid, biceps brachii, first dorsal interosseous, vastus medialis, and tibialis anterior muscles of 13 control subjects. DQEMG was capable of efficiently and accurately extracting MUP data from complex interference patterns during mild to moderate contractions. MUP amplitude, surface-detected MUP (S-MUP) amplitude, MUP duration, number of phases, and MU firing frequencies varied significantly across muscles. The mean parameter values for the individual muscles studied were similar to previous reports based on other quantitative methods. The main advantages of this method are the speed of data acquisition and processing, the ability to obtain MUPs from MUs with low and higher recruitment thresholds, and the ability to obtain both S-MUP or macro-MUP data as well as MU firing rate information.     

Decomposition-enhanced spike-triggered averaging: Contraction level effects

Decomposition-enhanced spike-triggered averaging (DE-STA) was applied to the vastus medialis muscle to examine size distributions of surface-detected motor unit action potentials (S-MUAPs) at various force levels. Using DE-STA, 15–20 S-MUAPs were identified during 5%, 10%, 20%, and 30% of maximum voluntary contraction. Average S-MUAPs showed increase in peak to peak (and negative peak) amplitude with force (in μV): 5% = 37.9 ± 6.1 (16.6 ± 2.5), 10% = 44.0 ± 4.0 (20.4 ± 1.8), 20% = 80.7 ± 9.3 (41.3 ± 4.5), and 30% = 102.5 ± 10.3 (53.6 ± 5.0). Test-retest variability of peak to peak (and negative peak amplitude) between repeated trials was 0.10 (0.14), 0.14 (0.14), 0.17 (0.15), and 0.21 (0.20) at 5%, 10%, 20%, and 30% respectively. A relationship was found between the S-MUAP amplitude and force (r² = 0.78, df = 90, F = 160, P < 0.001). Increase in average S-MUAP amplitude with force suggests that STA performed only at low levels of contraction may result in a biased sampling and small average S-MUAP amplitudes. © 1997 John Wiley & Sons, Inc. Muscle Nerve 20: 976–982, 1997