Motor unit activity within the depth of the masseter characterized by an adapted scanning EMG technique.

OBJECTIVE: To study motor unit activity in the medio-lateral extension of the masseter using an adapted scanning EMG technique that allows studying the territories of multiple motor units (MUs) in one scan. METHODS: We studied the m. masseter of 10 healthy volunteers in whom two scans were performed. A monopolar scanning needle and two pairs of fine-wire electrodes were inserted into the belly of the muscle. The signals of the fine wire electrodes were decomposed into the contribution of single MUs and used as a trigger for the scanning needle. In this manner multiple MU territory scans were obtained simultaneously. RESULTS: We determined 161 MU territories. The maximum number of territories obtained in one scan was 15. The median territory size was 4.0mm. Larger and smaller MU territories were found throughout the muscle. CONCLUSIONS: The presented technique showed its feasibility in obtaining multiple MU territories in one scan. MUs were active throughout the depth of the muscle. SIGNIFICANCE: The distribution of electrical and anatomical size of MUs substantiates the heterogeneous distribution of MUs throughout the muscle volume. This distributed activity may be of functional significance for the stabilization of the muscle during force generation.

Accuracy assessment of CKC high-density surface EMG decomposition in biceps femoris muscle.

The aim of this study was to assess the accuracy of the convolution kernel compensation (CKC) method in decomposing high-density surface EMG (HDsEMG) signals from the pennate biceps femoris long-head muscle. Although the CKC method has already been thoroughly assessed in parallel-fibered muscles, there are several factors that could hinder its performance in pennate muscles. Namely, HDsEMG signals from pennate and parallel-fibered muscles differ considerably in terms of the number of detectable motor units (MUs) and the spatial distribution of the motor-unit action potentials (MUAPs). In this study, monopolar surface EMG signals were recorded from five normal subjects during low-force voluntary isometric contractions using a 92-channel electrode grid with 8 mm inter-electrode distances. Intramuscular EMG (iEMG) signals were recorded concurrently using monopolar needles. The HDsEMG and iEMG signals were independently decomposed into MUAP trains, and the iEMG results were verified using a rigorous a posteriori statistical analysis. HDsEMG decomposition identified from 2 to 30 MUAP trains per contraction. 3 ± 2 of these trains were also reliably detected by iEMG decomposition. The measured CKC decomposition accuracy of these common trains over a selected 10 s interval was 91.5 ± 5.8%. The other trains were not assessed. The significant factors that affected CKC decomposition accuracy were the number of HDsEMG channels that were free of technical artifact and the distinguishability of the MUAPs in the HDsEMG signal (P < 0.05). These results show that the CKC method reliably identifies at least a subset of MUAP trains in HDsEMG signals from low force contractions in pennate muscles.

Automatic decomposition of multichannel intramuscular EMG signals.

We describe an automatic algorithm for decomposing multichannel EMG signals into their component motor unit action potential (MUAP) trains, including signals from widely separated recording sites in which MUAPs exhibit appreciable interchannel offset and jitter. The algorithm has two phases. In the clustering phase, the distinct, recurring MUAPs in each channel are identified, the ones that correspond to the same motor units are determined by their temporal relationships, and multichannel templates are computed. In the identification stage, the MUAP discharges in the signal are identified using matched filtering and superimposition resolution techniques. The algorithm looks for the MUAPs with the largest single channel components first, using matches in one channel to guide the search in other channels, and using information from the other channels to confirm or refute each identification. For validation, the algorithm was used to decompose 10 real 6-to-8-channel EMG signals containing activity from up to 25 motor units. Comparison with expert manual decomposition showed that the algorithm identified more than 75% of the total 176 MUAP trains with an accuracy greater than 95%. The algorithm is fast, robust, and shows promise to be accurate enough to be a useful tool for decomposing multichannel signals. It is freely available at http://emglab.stanford.edu.

Surface electromyogram signal modelling.

The paper reviews the fundamental components of stochastic and motor-unit-based models of the surface electromyogram (SEMG). Stochastic models used in ergonomics and kinesiology consider the SEMG to be a stochastic process whose amplitude is related to the level of muscle activation and whose power spectral density reflects muscle conduction velocity. Motor-unit-based models for describing the spatio-temporal distribution of individual motor-unit action potentials throughout the limb are quite robust, making it possible to extract precise information about motor-unit architecture from SEMG signals recorded by multi-electrode arrays. Motor-unit-based models have not yet been proven as successful, however, for extracting information about recruitment and firing rates throughout the full range of contraction. The relationship between SEMG and force during natural dynamic movements is much too complex to model in terms of single motor units.

Estimating motor-unit architectural properties by analyzing motor-unit action potential morphology.

OBJECTIVE: We investigated the architectural organization of groups of neighboring motor units (MUs) in normal brachial biceps and tibialis anterior muscles by analyzing morphological landmarks of their MU action potentials (MUAPs). METHODS: EMG signals containing multiple MUAPs were recorded using a monopolar needle electrode during moderate isometric voluntary contractions. The MUAPs were identified using computer-aided decomposition, and averaged. For each MUAP the onset, spike, terminal wave, and slow afterwave were identified; then the location of the MU's endplate and muscle/tendon junction were estimated from the latencies of the spike and terminal wave with respect to the MUAP onset. RESULTS: The analysis revealed a variety of architectural organizations, including single and multiple endplate zones, MU fractions, pennation, intramuscular aponeuroses, and centrally and non-centrally located endplates. CONCLUSIONS: This type of morphological analysis of the MUAP promises to be informative for studying normal MU properties as well as evaluating MU reorganization in disease.

A model of the muscle action potential for describing the leading edge, terminal wave, and slow afterwave.

The leading edge, terminal wave, and slow afterwave of the motor-unit action potential (MUAP) are produced by changes in the strength of electrical sources in the muscle fibers rather than by movement of sources. The latencies and shapes of these features are, therefore, determined primarily by the motor-unit (MU) architecture and the intracellular action potential (IAP), rather than by the volume-conduction characteristics of the limb. We present a simple model to explain these relationships. The MUAP is modeled as the convolution of a source function related to the IAP and a weighting function related to the MU architecture. The IAP waveform is modeled as the sum of a spike and a slow repolarization phase. The MU architecture is modeled by assuming that the individual fibers lie along a single equivalent axis but that their action potentials have dispersed initiation and termination times. The model is illustrated by simulating experimentally recorded MUAPs and compound muscle action potentials.

A model of the muscle-fiber intracellular action potential waveform, including the slow repolarization phase.

Recent studies have shown that the slow repolarization phase or "negative afterpotential" of the intracellular muscle-fiber action potential (IAP) plays an important role in determining the shape of the extracellularly recorded motor-unit action potential (MUAP). This paper presents a model of the IAP waveform as the sum of a spike and an afterpotential, both represented by simple analytical expressions. The model parameters that specify the sizes of the spike and afterpotential are shown to be proportional to the quadrupole and dipole moments of the transmembrane current distribution associated with the spike of the wave of excitation. The model provides a computationally efficient method for simulating the MUAP, and it can be reliably inverted to estimate the model parameters from empirical IAP and MUAP waveforms.

Satellite potentials of motor unit action potentials in normal muscles: a new hypothesis for their origin.

OBJECTIVE: A satellite potential is a late component of the motor unit action potential (MUAP) that occurs both in pathologic and normal muscle. We investigated the physiological mechanisms responsible for satellite potentials in normal muscle by relating the latencies of MUAP features to the timing of the underlying electrical events. METHODS: We analyzed 21 MUAPs with satellite potentials that had been recorded using a monopolar needle electrode from brachial biceps and tibialis anterior muscles in 10 normal subjects. We estimated the endplate-to-electrode, endplate-to-tendon, and satellite propagation times from the latencies, with respect to the MUAP onset, of the MUAP spike, terminal wave, and satellite. RESULTS: Satellite latencies ranged from 8.8 to 32 ms, too long to be explained by mechanisms involving regenerating axons or atrophic muscle fibers. The spike-to-satellite time intervals approximated either twice the spike-to-terminal-wave interval (17 MUAPs) or twice the terminal-wave latency (4 MUAPs). CONCLUSIONS: These results are consistent with the hypothesis that satellite potentials are due to retrograde propagation in a non-innervated muscle fiber that is connected with an innervated muscle fiber at one of the muscle/tendon junctions. Such a configuration could arise as a result of longitudinal muscle-fiber splitting.

The contribution of the interosseous muscles to the hypothenar compound muscle action potential.

The contributions of the various ulnar-innervated muscles of the hand to the hypothenar compound muscle action potential (CMAP) were estimated by directly stimulating individual muscles and by analyzing CMAP shape changes resulting from manipulations that changed individual muscle lengths. The results show that the first peak of the negative phase of the hypothenar CMAP comes from the hypothenar muscles, but that the second peak is due to a large volume-conducted potential from the interosseous muscles. The interosseous contribution affects both the amplitude and the area of the CMAP, and makes these parameters sensitive to changes in the configuration of the fingers and the temperature gradient in the hand. To reduce the interosseous contribution, a "balanced reference" consisting of two reference electrodes, one over each tendon, is proposed.

The physiological origin of the slow afterwave in muscle action potentials.

OBJECTIVE: Both intramuscularly-recorded motor unit action potentials (MUAPs) and surface recorded MUAPs and compound muscle action potentials (CMAPs) have slow afterwaves which can contribute as much as half their measured duration. This study tested the hypothesis that the slow afterwave has its physiological origin in the negative afterpotential of the muscle fiber intracellular action potential (IAP). METHODS: We investigated the slow afterwave in MUAPs and CMAPs from brachial biceps, tibialis anterior, first dorsal interosseous, thenar and hypothenar muscles in 15 normal subjects, and using computer simulations. RESULTS: The slow afterwaves did not match the time constant of the amplifier's high-pass filter, and so were not filtering artifacts. They lasted long after propagation had terminated at the muscle/tendon junction, and so were not due to the temporal or spatial dispersion of propagating single-fiber potentials. Their amplitude and polarity varied with the recording site as predicted by computer simulations that modeled the IAP as having a negative afterpotential. They also changed with double-pulse stimulation and decreasing temperature in ways consistent with the results of intracellular studies of the IAP negative afterpotential. CONCLUSIONS: The presented results support our hypothesis that the slow afterwave is a manifestation of the IAP negative afterpotential.

Anatomical and electrophysiological determinants of the human thenar compound muscle action potential.

Clinical interpretation of the compound muscle action potential (CMAP) requires a precise understanding of its underlying mechanisms. We recorded normal thenar CMAP5 and motor unit action potentials using different electrode configurations and different thumb positions. Computer simulations show that the CMAP has four parts: rising edge, negative phase, positive phase, and tail which correspond to four distinct stages of electrical activity in the muscle: initiation at the end-plate, propagation, termination at the muscle/tendon junctions, and slow repolarization. The shapes of volume-conducted signals recorded beyond the muscle are also explained by these four stages. Changes in CMAP shape associated with thumb abduction are due to changes in termination times resulting from changes in muscle-fiber lengths. These findings demonstrate that the negative and positive phases of the CMAP are due to different mechanisms, and that anatomical factors, particularly muscle-fiber lengths, play an important role in determining CMAP shape.

Action potentials of curved nerves in finite limbs.

Previous simulations of volume-conducted nerve-fiber action-potentials have modeled the limb as semi-infinite or circularly cylindrical, and the fibers as straight lines parallel to the limb surface. The geometry of actual nerves and limbs, however, can be considerably more complicated. This paper presents a general method for computing the potentials of fibers with arbitrary paths in arbitrary finite limbs. It involves computing the propagating point-source response (PPSR), which is the potential arising from a single point source (dipole or tripole) travelling along the fiber. The PPSR can be applied to fibers of different conduction velocities by simple dilation or compression. The method is illustrated for oblique and spiralling nerve fibers. Potentials from oblique fibers are shown to be different for orthodromic and antidromic propagation. Such results show that the straight-line models are not always adequate for nerves with anatomical amounts of curvature.

The nerve gap dilemma: a comparison of nerves repaired end to end under tension with nerve grafts in a primate model.

The objective of this study was to compare, in a clinically relevant primate model, axon regeneration after epineurial repair under tension (15 mm gap) with interfascicular nerve grafts with the use of either standard microsuture techniques or a new interfascicular nerve graft technique termed fascicular tubulization that uses a hypoantigenic collagen membrane formed into a tube to approximate nerve ends. Electrophysiologic analysis demonstrated that the percentage of proximal axons that conducted across the repair site was greater in those nerves repaired under tension with epineurially placed sutures than in either of the tensionless repairs involving interfascicular graft techniques. The mean diameters of the regenerated axons repaired under tension with epineurial sutures were greater than those of the nerves repaired with interfascicular grafts, although the difference was not statistically significant. Interfascicular nerve grafting with tubulization using the current collagen tube resulted in regeneration equal to the sutured interfascicular nerve grafts. For modest defects (perhaps up to 3 to 4 cm in the adult), it seems advantageous to accept the modest tension associated with an epineurial repair rather than to use an autograft (or artificial graft) to achieve a tension-free repair.

A comparison of suture and tubulization nerve repair techniques in a primate.

This study compared standard methods of nerve repair, epineurial or perineurial sutures with a technique termed fascicular tubulization using a biodegradable polyglycolic acid tube in a nonhuman primate model. Electrophysiologic analysis demonstrated that the percentage of proximal axons that conducted across the repair site did not significantly differ among the three techniques while epineurial suture repairs were associated with significantly longer conduction delays across the repair site compared with the other two techniques. Even though fascicular tubulization using the current polyglycolic acid tube resulted in regeneration equal to the currently perceived best suture repair technique, associated technical problems with the current tube design indicate that this fascicular tubulization technique cannot, at present, be considered as an alternative to present clinically used nerve suture techniques.

A comparison of turns analysis and motor unit analysis in electromyography.

We compared the results of turns analysis and motor unit analysis on 4056 electromyographic interference patterns (IPs) from normal subjects and patients with neuromuscular disorders. The motor unit analysis involved decomposing the IPs into their component motor unit action potentials (MUAPs) using automatic decomposition electromyography (ADEMG). We checked the accuracy of the decompositions by attempting to reconstruct some of the IPs from their identified MUAPs using computer simulations. The simulations revealed that ADEMG typically identified more than 60% (but not all) of the MUAPs in a given IP. Both turns and MUAP properties showed regular and related changes with force, age, muscle, and recording electrode type. The number of turns in each IP was highly correlated with the number of active MUAPs (r = 0.65), the mean MUAP firing rate (r = 0.72), the mean number of turns per MUAP (r = 0.34), and the product of these 3 properties (r = 0.83). The mean amplitude change per turn was highly correlated with the mean MUAP amplitude (r = 0.82), but also depended on the number of turns per MUAP. Due to the lack of a one-to-one relationship between the turns analysis properties and the MUAP properties, the turns analysis properties by themselves did not provide sufficient information to infer unambiguous physiological information about motor unit morphology or firing behavior.

Triphasic behavioral response of motor units to submaximal fatiguing exercise.

We have measured the firing rate and amplitude of 4551 motor unit action potentials (MUAPs) recorded with concentric needle electrodes from the brachial biceps muscles of 10 healthy young adults before, during, and after 45 minutes of intermittent isometric exercise at 20% of maximum voluntary contraction (MVC), using an automatic method for decomposition of electromyographic activity (ADEMG). During and after exercise, MUAPs derived from contractions of 30% MVC showed progressive increase in mean firing rate (P less than or equal to .01) and amplitude (P less than or equal to .05). The firing rate increase preceded the rise in mean amplitude, and was evident prior to the development of fatigue, defined as reduction of MVC. Analysis of individual potentials revealed that the increase in firing rate and in amplitude reflected different MUAP subpopulations. A short-term (less than 1 minute) reduction in MUAP firing rates (P less than or equal to .05) was also observed at the onset of each test contraction. These findings suggest that motor units exhibit a triphasic behavioral response to prolonged submaximal exercise: (1) short-term decline and stabilization of onset firing rates, followed by (2) gradual and progressive increase in firing rates and firing variability, and then by (3) recruitment of additional (larger) motor units. The (2) and (3) components presumably compensate for loss of force-generating capacity in the exercising muscle, and give rise jointly to the well-known increase in total surface EMG which accompanies muscle fatigue.

Motor unit firing rates and firing rate variability in the detection of neuromuscular disorders.

We have used automatic decomposition electromyography (ADEMG) to study 41 muscles in 29 patients with well-defined peripheral and central motor disorders. In motor neuron diseases motor unit action potentials (MUAPs) showed increased amplitudes, firing rates and firing variability. Relatively large MUAPs sometimes were not identified by the computer program if they lacked sufficient high-frequency signal content, or were too variable in shape. In myopathies the MUAPs showed reduced amplitudes, durations and turns, and sometimes dramatic increases in firing rates. Also, the mean number of MUAPs per recording site was often increased, indicating excessive recruitment. In polymyositis (the best studied myopathy) the nature and magnitude of the MUAP shape and firing abnormalities were usually similar at different levels of contractile force, suggesting that motor units are affected without regard to recruitment order. In upper motor neuron paresis (multiple sclerosis), the shape properties of the MUAPs were normal, but mean firing rates were reduced, and firing variability increased. These findings confirm many of the traditional criteria for distinguishing neurogenic from myopathic disease electrophysiologically at the level of the individual MUAP. In addition, they demonstrate the potential diagnostic sensitivity of MUAP firing rate measurements for detecting neuromuscular dysfunction, and for differentiating between some cases of central and peripheral paresis, but not for distinguishing peripheral neurogenic from myopathic weakness, since firing rates tend to increase in both. Increased firing rate variability may be a marker of central or peripheral neurogenic weakness.

Properties of motor unit action potentials recorded with concentric and monopolar needle electrodes: ADEMG analysis.

We compared the configurational and firing properties of 7270 motor unit action potentials (MUAPs) recorded with either concentric (CNE) or monopolar (MNE) needle electrodes from the brachial biceps and anterior tibial muscles of 10 healthy young adults (mean age 27 +/- 4.5 years) using automatic decomposition electromyography (ADEMG). In both muscles, mean MUAP amplitude, rise rate, and number of turns were significantly greater when recorded with MNE (paired t-test, P less than 0.001 in each case). Similar findings were observed at all three tested levels of isometric contractile force: threshold, 10% of maximum voluntary contraction (MVC), and 30% MVC. In contrast, there was no significant difference between electrode types on measurements of mean MUAP duration or firing rate (P greater than 0.05 in each case). These findings indicate that it is acceptable to generalize normative data on MUAP duration and firing rate from one electrode type to another, but that measures of MUAP amplitude and complexity require independent normative databases.