Separation of propagating and non propagating components in surface EMG

Surface electromyogram (EMG) detected by electrode arrays along the muscle fibre direction can be approximated by the sum of propagating and non propagating components. A technique to separate propagating and non propagating components in surface EMG signals is developed. The first step is an adaptive filter, which allows obtaining an estimation of the delay between signals detected at different channels and a first estimate of propagating and non propagating components; the second step is used to optimise the estimation of the two components. The method is applicable to signals with one propagating and one non propagating component. It was optimised on simulated signals, and then applied to single motor unit action potentials (MUAP) and to electrically elicited EMG (M-waves).

The new method was first tested on phenomenological signals constituted by the sum of a propagating and a non propagating signal and then applied to simulated and experimental EMG signals. Simulated signals were generated by a cylindrical, layered volume conductor model. Experimental signals were monopolar surface EMG signals collected from the abductor pollicis brevis muscle and M-waves recorded during transcutaneous electrical stimulation of the biceps muscle. The technique may find different applications: in single motor unit (MU) studies (a) for decreasing the variability and bias of CV estimates due to the presence of the non propagating components, (b) for estimating automatically the length of the muscle fibres from only three detected channels and (c) for removal of the stimulation artifact M-waves.     

Computer simulation study of the shape of motor unit action potential

Motor unit action potentials (MUAPs) of brachial biceps were simulated. A simulated MUAP was obtained as a sum of single fibre action potentials (SFAPs) from all the muscle fibres of a motor unit (MU). The influence of the following factors on MUAP shape for different kinds of recording electrode was studied: fibre density, neuromuscular jitter, temporal dispersion and electrode displacements. The simulation confirms that typical MUAPs recorded with needle electrodes from muscles of low fibre density such as brachial biceps are usually triphasic. Increased fibre density produces MUAPs of more complex shape and higher amplitude. Normal neuromuscular jitter is responsible for the variability of shape of subsequent potentials from the same MU as well as for electromyographic shimmer. Pathologic (increased) jitter makes the shapes of subsequent potentials unrecognizable. The influence of temporal dispersion is interconnected with other factors but rather of minor importance. The simulation shows how big changes in MUAP shape can be expected due to electrode displacements during single experiment or during estimation of MU territory.     

Non-invasive detection of the single motor unit action potential by averaging the spatial potential distribution triggered on a spatially filtered motor unit action potential.

For research as well as diagnostic applications the non-invasive detection of the activity of single motor units is of interest. The most direct information is expected to be found in monopolarly recorded data. But when an array of surface electrodes is used for the monopolar recordings of the potential distribution on the skin, in most cases an additional invasive needle electrode is utilized to detect the exact points in time when a certain motor unit is firing. With this supplementary information, an averaging of the monopolar EMG tracings can be performed. In this paper, a completely non-invasive methodology is presented which replaces the invasive needle by a spatial filtering procedure. The EMG signals from the m. biceps brachii are recorded monopolarly with an electrode array. Afterwards, a spatial filtering procedure, called normal double differentiating filter, is applied to the data. The EMG signals obtained are investigated by means of an amplitude threshold to distinguish the activity of different motor units. The point of the maximum amplitude of the selected peaks then is used as trigger point to average the monopolar EMG data. The time courses of the motor unit action potential signals found after applying the described procedure show similar shapes, while two different components are to be identified: corresponding to the spread of the excitation, one is referring to stationary, the other to travelling events. These results justify the possibility to replace the needle electrode to obtain a trigger event in the future by the non-invasive spatial filtering procedure.     

Muscle functional state assessment by estimation of muscle fiber conduction velocity

In 20 healthy subjects (10 males and 10 females) aged between 24 and 45, the conduction velocity (CV) of excitation along muscle fibers was measured in m. biceps brachii muscle using level averaging of interference electromyograms (EMGs) recorded by branched and monopolar surface electrodes. The measured CV, recorded with both monopolar and branched electrodes, were essentially equal (p < 0.05) at all different muscle tensions (10, 25, 50, and 75% of maximal voluntary contractions (MVCs)) and for all investigated healthy subjects. The CV was significant higher (p < 0.05) at 50 and 75% compared to 10 and 25% of MVC. In branched averaged potentials (AvPs), the terminal positive phase was suppressed. The monopolar AvPs were with waveform similar to those of motor units potentials and the parameters of the phases of different potentials (including the terminal positive one) may give additional information on functional state of muscles.The level-triggered averaging of the interference EMG recorded from the skin surface by branched electrodes is an adequate noninvasive method for measuring the propagation velocity of excitation along muscle fibers and for evaluating changes in the muscle functional state.     

The linear electrode array: a useful tool with many applications.

In this review we describe the basic principles of operation of linear electrode arrays for the detection of surface EMG signals, together with their most relevant current applications. A linear array of electrodes is a system which detects surface EMG signals in a number of points located along a line. A spatial filter is usually placed in each point for signal detection, so that the recording of EMG signals with linear arrays corresponds to the sampling in one spatial direction of a spatially filtered version of the potential distribution over the skin. Linear arrays provide indications on motor unit (MU) anatomical properties, such as the locations of the innervation zones and tendons, and the fiber length. Such systems allow the investigation of the properties of the volume conductor and its effect on surface detected signals. Moreover, linear arrays allow to estimate muscle fiber conduction velocity with a very low standard deviation of estimation (of the order of 0.1-0.2 m/s), thus providing reliable indications on muscle fiber membrane properties and their changes in time (for example with fatigue or during treatment). Conduction velocity can be estimated from a signal epoch (global estimate) or at the single MU level. In the latter case, MU action potentials are identified from the interference EMG signals and conduction velocity is estimated for each detected potential. In this way it is possible, in certain conditions, to investigate single MU control and conduction properties with a completely non-invasive approach. Linear arrays provide valuable information on the neuromuscular system properties and appear to be promising tools for applied studies and clinical research.     

Evolution of surface electromyography: From muscle electrophysiology towards neural recording and interfacing

Surface electromyography (EMG) comprises a recording of electrical activity from the body surface generated by muscle fibres during muscle contractions. Its characteristics depend on the fibre membrane potentials and the neural activation signal sent from the motor neurons to the muscles. EMG has been classically used as the primary investigation tool in kinesiology studies in a variety of applications. More recently, surface EMG techniques have evolved from single-channel methods to high-density systems with hundreds of electrodes. High-density EMG recordings can be deconvolved to estimate the discharge times of spinal motor neurons innervating the recorded muscles, with algorithms that have been developed and validated in the last two decades. Within limits and with some variability across muscles, these techniques provide a non-invasive method to study relatively large populations of motor neurons in humans. Surface EMG is thus evolving from a peripheral measure of muscle electrical activity towards a neural recording and neural interfacing signal. These advances in technology have had a major impact on our fundamental understanding of the neural control of movement and have exposed new perspectives in neurotechnologies. Here we provide an overview and perspective of modern EMG technology, as derived from past achievements, and its impact in neurophysiology and neural engineering.     

Spatial distribution of surface action potentials generated by individual motor units in the human biceps brachii muscle

This study analyses the spatial distribution of individual motor unit potentials (MUPs) over the skin surface and the influence of motor unit depth and recording configuration on this distribution. Multichannel surface (13 × 5 electrode grid) and intramuscular (wire electrodes inserted with needles of lengths 15 and 25 mm) electromyographic (EMG) signals were concurrently recorded with monopolar derivations from the biceps brachii muscle of 10 healthy subjects during 60-s isometric contractions at 20% of the maximum torque. Multichannel monopolar MUPs of the target motor unit were obtained by spike-triggered averaging of the surface EMG. Amplitude and frequency characteristics of monopolar and bipolar MUPs were calculated for locations along the fibers’ direction (longitudinal), and along the direction perpendicular (transverse) to the fibers. In the longitudinal direction, monopolar and bipolar MUPs exhibited marked amplitude changes that extended for 16–32 mm and 16–24 mm over the innervation and tendon zones, respectively. The variation of monopolar and bipolar MUP characteristics was not symmetrical about the innervation zone. Motor unit depth had a considerable influence on the relative longitudinal variation of amplitude for monopolar MUPs, but not for bipolar MUPs. The transverse extension of bipolar MUPs ranged between 24 and 32 mm, whereas that of monopolar MUPs ranged between 72 and 96 mm. The mean power spectral frequency of surface MUPs was highly dependent on the transverse electrode location but not on depth. This study provides a basis for the interpretation of the contribution of individual motor units to the interference surface EMG signal.     

Using two-dimensional spatial information in decomposition of surface EMG signals.

Recently, high-density surface EMG electrode grids and multi-channel amplifiers became available for non-invasive recording of human motor units (MUs). We present a way to decompose surface EMG signals into MU firing patterns, whereby we concentrate on the importance of two-dimensional spatial differences between the MU action potentials (MUAPs). Our method is exemplified with high-density EMG data from the vastus lateralis muscle of a single subject. Bipolar and Laplacian spatial filtering was applied to the monopolar raw signals. From the single recording in this subject six different simultaneously active MUs could be distinguished using the spatial differences between MUAPs in the direction perpendicular to the muscle fiber direction. After spike-triggered averaging, 125-channel two-dimensional MUAP templates were obtained. Template-matching allowed tracking of all MU firings. The impact of spatial information was measured by using subsets of the MUAP templates, either in parallel or perpendicular to the muscle fiber direction. The use of one-dimensional spatial information perpendicular to the muscle fiber direction was superior to the use of a linear array electrode in the longitudinal direction. However, to detect the firing events of the MUs with a high accuracy, as needed for instance for estimation of firing synchrony, two-dimensional information from the complete grid electrode appears essential.     

Fibre conduction velocity and fibre composition in human vastus lateralis

The relationship between muscle fibre composition and fibre conduction velocity was investigated in 19 male track athletes, 12 sprinters and 7 distance runners, aged 20-24 years, using needle biopsy samples from vastus lateralis. Cross sectional areas of the fast twitch (FT) and slow twitch (ST) fibres were determined by histochemical analysis. The percentage of FT fibre areas ranged from 22.6 to 93.6%. Sprinters had a higher percentage of FT fibres than distance runners. Muscle fibre conduction velocity was measured with a surface electrode array placed along the muscle fibres, and calculated from the time delay between 2 myoelectric signals recorded during a maximal voluntary contraction. The conduction velocity ranged from 4.13 to 5.20 m.s-1. A linear correlation between conduction velocity and the relative area of FT fibres was statistically significant (r = 0.84, p less than 0.01). This correlation indicates that muscle fibre composition can be estimated from muscle fibre conduction velocity measured noninvasively with surface electrodes.     

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.     

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.     

Extracellular recording of localized electrical activity in denervated frog slow muscle fibres

Pyriformis muscles of Rana temporaria were denervated by cutting the sciatic nerve in the pelvis. Slow muscle fibres were depolarized with intracellular current pulses, and the electrical activity was recorded simultaneously with intracellular and extracellular recording electrodes. When the extracellular electrode was moved along the fibre surface, outward and inward currents of variable amplitude were recorded. Inward currents coincided with the fast rising phase of the intracellularly recorded action potential; up to four inward current peaks could be detected in single fibres investigated over 3.4--8 mm of their length. The distance between inward current peaks was generally 1--2 mm, but greater distances were also observed. Composite action potentials could be shown to be due to inward currents arising in separate areas of the slow fibre membrane. It is concluded that after denervation Na-channels are incorporated into spatially limited areas of the membrane of slow muscle fibres.     

Reliability of muscle fibre conduction velocity distribution estimation from surface EMG

Most of the neuromuscular diseases induce changes in muscle fibre characteristics. For example, Duchenne dystrophy is characterized by a specific loss of fast fibres, and an increase in small diameter fibres. These morphological changes may lead to large modifications in the distribution of fibre diameters, possibly producing bimodal distributions. It has already been shown that it is possible to reveal these morphological modifications through the distribution of muscle fibre conduction velocity (MFCV) as estimated from needle electromyography (EMG) recordings. In this paper, we investigate whether such changes can be extracted from surface EMG signals.

Simulation allows generation of surface EMG signals in which features are well described especially at a morphological level. Therefore, we generated a database of simulated signals both in voluntary and electrically elicited contraction conditions using a bimodal distribution of muscle fibre diameters. MFCV distributions were computed using two short-term methods based on cross-correlation and peak-to-peak techniques for voluntary contraction signals, and using a deconvolution method in time domain for electrically elicited signals. MFCV distributions were compared with true ones, as generated from modelling.

This work reveals that estimating MFCV distribution through these methods does not appear yet as precise and robust enough to accurately characterize changes in redistribution of various muscle fibre diameters. However, it opens to new experimental protocols that can be explored in order to improve the robustness of MFCV distribution estimation for the follow-up of patients suffering from neuromuscular disorders.     

Comparison of force and EMG measures in normal and reinnervated tibialis anterior muscles of the rat.

The relationship between motor unit force and the recorded voltage produced by activated muscle unit fibres (electromyogram, EMG) was examined in normal and reinnervated rat tibialis anterior muscles. The number, cross-sectional area, and radial distance from the recording electrode of muscle fibres in a given unit, obtained directly from a sample of glycogen-depleted motor units, were analysed in relation to the magnitude of the EMG signal produced by that unit. EMG peak to peak amplitude and area varied as approximately the square root of twitch force in both normal and reinnervated units. Furthermore, the EMG amplitude increased approximately as the total cross-sectional area of the motor unit (number of muscle fibres x the average cross-sectional area of the fibres) and inversely with approximately the square root of the distance of fibres from the recording electrodes on the surface of the muscle.     

Comparison of the duration and power spectral changes of monopolar and bipolar M waves caused by alterations in muscle fibre conduction velocity

The muscle compound action potential (M wave) recorded under monopolar configuration reflects both the propagation of the action potentials along the muscle fibres and their extinction at the tendon. M waves recorded under a bipolar configuration contain less cross talk and noise than monopolar M waves, but they do not contain the entire informative content of the propagating potential. The objective of this study was to compare the effect of changes in muscle fibre conduction velocity (MFCV) on monopolar and bipolar M waves and how this effect depends on the distance between the recording electrodes and tendon. The study was based on a simulation approach and on an experimental investigation of the characteristics of surface M waves evoked in the vastus lateralis during 4-s step-wise isometric contractions in knee extension at 10%, 20%, 30%, 40%, 50%, 60%, 70%, 80%, and 90% MVC. The peak-to-peak duration (Durpp) and median frequency (Fmedian) of the M waves were calculated. For monopolar M waves, changes in Durpp and Fmedian produced by MFCV depended on the distance from the electrode to the tendon, whereas, for bipolar M waves, changes in Durpp and Fmedian were largely independent of the electrode-to-tendon distance. When the distance between the detection point and tendon lay between approximately 15 and 40 mm, changes in Durpp of bipolar M waves were more pronounced than those of distal monopolar M waves but less marked than those of proximal monopolar M waves, and the opposite occurred for Fmedian. Since, for bipolar M waves, changes in duration and power spectral features produced by alterations in MFCV are not influenced by the electrode-to-tendon distance, the bipolar electrode configuration is a preferable choice over monopolar arrangements to estimate changes in conduction velocity.     

Surface electromyography and peak torque of repetitive maximum isokinetic plantar flexions in relation to aspects of muscle morphology.

This study investigates the relationships between surface electromyography (EMG [Mean frequency of the power spectrum (MNF)]) and peak torque variables obtained during 100 maximum concentric plantar flexions with the right limb at 60 degrees s(-1) and different muscle morphological variables. Surface EMG was recorded from the right gastrocnemius lateralis and muscle biopsies were taken from the same site as the EMG electrodes were positioned. Muscle fibre area and fibre type composition were determined on serial muscle cross sections using both histochemistry (myofibrillar adenosine triphosphatase) and immunohistochemistry (monoclonal antibodies against specific myosin heavy chain isoforms). Forty-three female and nine male students participated in the study. Gastrocnemius lateralis contained predominantly type I fibres (50%) and type IIA fibres (40%) in both sexes and large individual differences were found. Principal component analysis (PCA) was used for the intercorrelation analyses, and projection to latent structures (PLS) was used for the multivariate regression analysis. MNF correlated positively with different fibre areas and with the proportion of type I fibres. Fibre areas and sex were the most important factors in the regression of maximum peak torque. High proportion of type I fibres and sex were the most important regressors of peak torque endurance normalised for lean body mass. More studies are needed to understand the complex interrelationships between intrinsic muscle properties and the frequency content of the surface EMG before theoretical models can be formulated that incorporate both fibre areas and fibre type proportions.     

Estimation of the muscle fibre semi-length under varying joint positions on the basis of non-invasively extracted motor unit action potentials.

Changes in muscle fibre length and surface electrode position with respect to the muscle fibres affect the amplitude and frequency characteristics of surface electromyography (SEMG) in different ways. Knowledge of changes in muscle fibre length would help towards a better interpretation of the signals. The possibility of estimating the length through SEMG during voluntary contractions was checked in this study. The fibres' semi-length was estimated from the product of the conduction velocity and conduction time during which the wave of excitation propagated from the end-plate region to the ends of the fibres. Short (10 s), moderate (30% of maximum voluntary contraction) isometric contractions were performed by 10 subjects at different elbow joint angles (80-140 degrees in steps of 20 degrees ). Monopolar signals were detected non-invasively, using a two-dimensional electrode array. High spatial resolution EMG and a decomposition technique were utilised to extract single motor unit activities for triggered averaging and to estimate conduction velocity. A significant increase with joint angle was found in conduction time and estimated fibre semi-length. Changes in conduction velocity with joint angle were found to be not significant. The methodology described allows the relative changes in fibres' semi-length to be estimated from SEMG data.     

Comparison of electromyographic signals from monopolar current and potential amplifiers derived from a penniform muscle,the gastrocnemius medialis

Electromyograms (EMGs) are measured by bipolar surface electrodes that quantify potential differences. Bipolar potentials over penniform muscles may be associated with errors. Our assumption was that muscle activity can be quantified more reliably and with a higher spatial resolution using current measurements.The purpose of this work is: (a) to introduce the concept of current measurements to detect muscle activity, (b) to show the coherences observed over a segment of a typical penniform muscle, the gastrocnemius medialis where one would expect a synchronicity of the activation, and (c) to show the amount of mixing that is caused by the finite inter electrode resistance.A current amplifier was developed. EMGs were recorded at 40% of maximum voluntary contraction during isometric contractions of the gastrocnemius medialis. EMGs of twelve persons were recorded with an array of four peripheral and one central electrode. Monopolar EMGs were recorded for “all-potential”, “center at current” and “all-current” conditions. Coherence revealed the similarity of signals recorded from neighboring electrodes.Coherence was high for the “all-potential”, significant for the “current at center” condition and disappeared in the “all-current” condition.It was concluded that EMG array recordings strongly depends on the measurement configuration. The proposed current amplifier significantly improves spatial resolution of EMG array recordings because the inter-electrode cross talk is reduced.     

Recording Large Extracellular Spikes in Microchannels along Many Axonal Sites from Individual Neurons

The numerous connections between neuronal cell bodies, made by their dendrites and axons, are vital for information processing in the brain. While dendrites and synapses have been extensively studied, axons have remained elusive to a large extent. We present a novel platform to study axonal physiology and information processing based on combining an 11,011-electrode high-density complementary metal-oxide semiconductor microelectrode array with a poly(dimethylsiloxane) channel device, which isolates axons from somas and, importantly, significantly amplifies recorded axonal signals. The combination of the microelectrode array with recording and stimulation capability with the microfluidic isolation channels permitted us to study axonal signal behavior at great detail. The device, featuring two culture chambers with over 30 channels spanning in between, enabled long-term recording of single spikes from isolated axons with signal amplitudes of 100 μV up to 2 mV. Propagating signals along axons could be recorded with 10 to 50 electrodes per channel. We (i) describe the performance and capabilities of our device for axonal electrophysiology, and (ii) present novel data on axonal signals facilitated by the device. Spontaneous action potentials with characteristic shapes propagated from somas along axons between the two compartments, and these unique shapes could be used to identify individual axons within channels that contained many axonal branches. Stimulation through the electrode array facilitated the identification of somas and their respective axons, enabling interfacing with different compartments of a single cell. Complex spike shapes observed in channels were traced back to single cells, and we show that more complicated spike shapes originate from a linear superposition of multiple axonal signals rather than signal distortion by the channels.     

Simulation analysis of interference EMG during fatiguing voluntary contractions. Part II--changes in amplitude and spectral characteristics.

Capabilities of amplitude and spectral methods for information extraction from interference EMG signals were assessed through simulation and preliminary experiment. Muscle was composed of 4 types of motor units (MUs). Different hypotheses on changes in firing frequency of individual MUs, intracellular action potential (IAP) and muscle fibre propagation velocity (MFPV) during fatigue were analyzed. It was found that changes in amplitude characteristics of interference signals (root mean square, RMS, or integrated rectified value, IEMG) detected by intramuscular and surface electrodes differed. RMS and IEMG of surface detected interference signals could increase even under MU firing rate reduction and without MU synchronisation. IAP profile lengthening can affect amplitude characteristics more significantly than MU firing frequency. Thus, an increase of interference EMG amplitude is unreliable to reflect changes in the neural drive. The ratio between EMG amplitude and contraction response can hardly characterise the so-called 'neuromuscular efficiency'. The recently proposed spectral fatigue indices can be used for quantification of interference EMG signals. The indices are practically insensitive to MU firing frequency. IAP profile lengthening and decrease in MFPV enhanced the index value, while recruitment of fast fatigable MUs reduced it. Sensitivity of the indices was higher than that of indices traditionally used.