George V. Dimitrov

Interpretation of EMG changes with fatigue: facts, pitfalls, and fallacies

Failure to maintain the required or expected force, defined as muscle fatigue, is accompanied by changes in muscle electrical activity. Although studied for a long time, reasons for EMG changes in time and frequency domain have not been clear until now. Many authors considered that theory predicted linear relation between the characteristic frequencies and muscle fibre propagation velocity (MFPV), irrespective of the fact that spectral characteristics can drop even without any changes in MFPV, or in proportion exceeding the MFPV changes. The amplitude changes seem to be more complicated and contradictory since data on increased, almost unchanged, and decreased amplitude characteristics of the EMG, M-wave or motor unit potential (MUP) during fatigue can be found in literature. Moreover, simultaneous decrease and increase in amplitude of MUP and M-wave, detected with indwelling and surface electrodes, were referred to as paradoxical. In spite of this, EMG amplitude characteristics are predominantly used when causes for fatigue are analysed. We aimed to demonstrate theoretical grounds for pitfalls and fallacies in analysis of experimental results if changes in intracellular action potential (IAP), i.e. in peripheral factors of muscle fatigue, were not taken into consideration. We based on convolution model of potentials produced by a motor unit and detected by a point or rectangular plate electrode in a homogeneous anisotropic infinite volume conductor. Presentation of MUP in the convolution form gave us a chance to consider power spectrum (PS) of MUP as a product of two terms. The first one, PS of the input signal, represented PS of the first temporal derivative of intracellular action potential (IAP). The second term, PS of the impulse response, took into account MFPV, differences in instants of activation of each fibre, MU anatomy, and MU position in the volume conductor in respect to the detecting electrode. PS presentation through product means that not only changes in MFPV could be responsible for PS shift as is usually assumed. Changes in IAP duration and IAP after-potential magnitude, affecting the first term of the product, influence the product and thus MUP PS. Moreover, the interrelations between the two spectra and thus sensitivity of spectrum to different parameters change with MU-electrode distance because the second term depends on it. Thus, we have demonstrated that theory does not predict a linear relation between the characteristic frequencies (maximum, mean and median) and MFPV. IAP duration and after-potential magnitude are among parameters affecting MUP or M-wave PS and thus, EMG PS detected by monopolar and bipolar electrodes. Usage of single fibre action potential models instead of MUP ones can result in false dependencies of frequency characteristics. The MUP amplitude characteristics are determined not only by amplitude of IAP, but also by the length of the IAP profile and source-electrode distance. Due to the IAP profile lengthening and an increase in the negative after-potential, surface detected EMG amplitude characteristics can increase even when IAP amplitude decreases considerably during fatigue. Increase in surface detected MUP or M-wave amplitude should not be attributed to a weaker attenuation of the low-frequency components with distance. Simultaneous decrease and increase in amplitude of MUP and M-wave detected with indwelling and surface electrodes are regular, not paradoxical. Corner frequency of the high pass filter should be 0.5 or 1 Hz when muscle fatigue is analyzed. The area of MUP or M-wave normalized in respect of the amplitude of the terminal phase (that is produced during extinction of the depolarized zones at the ends of the fibres) could be useful as a fatigue index. Analysing literature data on IAP changes due to Ca(2+) increasing, we hypothesised that the ability of muscle fibres to uptake Ca(2+) back into the sarcoplasmic reticulum could be the limiting site for fatigue. If this hypothesis is valid, IAP changes are not a cause of fatigue; they are due to it.

Precise and fast calculation of the motor unit potentials detected by a point and rectangular plate electrode

To reduce the time of computation of a motor unit potential (MUP), the shape of intracellular action potential (IAP) and (or) MU anatomy are generally simplified. A method of MUP presentation is suggested. It provides accuracy of the MUPs calculated for any distance and size of rectangular electrodes together with considerably reduced computational load and time. No simplification of the IAP shape or location of muscle fibres of different diameters and lengths is required. The MUP generated by N temporally and spatially dispersed single fibre action potentials is considered to be the output signal of a linear time-shift invariant system for potential generation. The input signal is the first temporal derivative of the IAP. The common impulse response (CIR) is the sum of potentials produced at the electrode by N pairs of dipoles propagating from the motor end-plates to the ends of the corresponding fibres. The potentials of each dipole at the rectangular plate electrode are determined analytically. Thus, the MUP is calculated as a single convolution between the input signal and CIR for a rectangular electrode of any size.

Amplitude-related characteristics of motor unit and M-wave potentials during fatigue. A simulation study using literature data on intracellular potential changes found in vitro

To realize possible reasons for changes in EMG amplitude characteristics with fatigue, we analyzed motor unit potentials (MUPs) and M-waves under simultaneous variations of the intracellular action potential (IAP) amplitude, duration, and shape as well as of the muscle fiber propagation velocity and desynchronization in activation of individual muscle fibers. Analysis was performed through computer simulation of MUPs and M-waves detected at different distances from active fibers in infinite anisotropic volume conductor. Changes in the IAP spike and negative after-potential were taken from in vitro experiments reported in the literature. It was shown that the amplitudes of MUP and M-wave detected simultaneously at different distances could decrease close to the active fibers, be almost unchanged at middle distances, and increase far from the fibers even under IAP amplitude decreasing. This reflected the distance-dependent effects of changes in the IAP profile along the fiber. Electrode position affected sensitivity of MUP and M-wave durations to changes in the IAP duration and propagation velocity. Thus, the signal area and RMS depended on electrode position and could change with fatigue in a way different from that of signal amplitude. The results can help to avoid misleading interpretation of EMG changes.

Neither high-pass filtering nor mathematical differentiation of the EMG signals can considerably reduce cross-talk

Using mathematical simulation of motor unit potentials (MUPs), detected by a point and rectangular plate electrode, we have shown that the muscle tissue does not act like a low-pass frequency filter on MUPs. Depending on the electrode type and its longitudinal position, the relative weight of the terminal phases (reflecting the excitation extinction) in MUPs and thus of high frequencies in the MUP power spectrum, increase with the MU depth. Therefore, high-pass filtering or differentiating signals detected neither monopolarly nor bipolarly could eliminate the cross-talk produced by high frequency components of MUPs from deep MUs. Such methods could be effective against the main components but not against the MUP leading edge and terminal phases. To reduce the cross-talk, position of the detecting electrodes should correspond to anatomy of muscles producing the cross-talk. Monopolar electrode should be located above the ends of the muscles. Cross-talk of the muscles located beyond the muscle of interest could be higher than that produced above the end-plate of deep muscles. On the contrary, under detection by a longitudinal bipolar electrode, the cross-talk is much smaller above the end-plate region or beyond deep muscles. The cross-talk is the greatest above the ends of the deep muscles.

Interpretation of EMG integral or RMS and estimates of ''neuromuscular efficiency" can be misleading in fatiguing contraction

In occupational and sports physiology, reduction of neuromuscular efficiency (NME) and elevation of amplitude characteristics, such as root mean square (RMS) or integral of surface electromyographic (EMG) signals detected during fatiguing submaximal contraction are often related to changes in neural drive. However, there is data showing changes in the EMG integral (I(EMG)) and RMS due to peripheral factors. Causes for these changes are not fully understood. On the basis of computer simulation, we demonstrate that lengthening of intracellular action potential (IAP) profile typical for fatiguing contraction could affect EMG amplitude characteristics stronger than alteration in neural drive (central factors) defined by number of active motor units (MUs) and their firing rates. Thus, relation of these EMG amplitude characteristics only to central mechanisms can be misleading. It was also found that to discriminate between changes in RMS or I(EMG) due to alterations in neural drive from changes due to alterations in peripheral factors it is better to normalize RMS of EMG signals to the RMS of M-wave. In massive muscles, such normalization is more appropriate than normalization to either peak-to-peak amplitude or area of M-wave proposed in literature.

Simulation analysis of the ability of different types of multi- electrodes to increase selectivity of detection and to reduce cross- talk

Selectivity of different one- and two-dimensional multi-electrodes and their ability to reduce cross-talk were analyzed. Signals from an individual motor unit (MU) were calculated as a single convolution of intracellular action potential (IAP) first temporal derivative and spatially filtered MU impulse response. It was shown that the uptake area (irrespective of the way it was defined) could not characterize electrode properties reliably because its estimate depended on the source parameters. Due to the different decline of individual phases of MU signals with depth, electrode should provide higher spatial and temporal resolution of the main phases for better selectivity and greater suppression of the terminal phases for cross-talk reduction. A two-dimensional normal double differentiating (NDD) electrode provided almost the same or slightly lower selectivity but weaker reduction of cross-talk than a longitudinal double differentiating (LDD) electrode. A transversal double differentiating (TDD) electrode provided a lower selectivity and weaker reduction of cross-talk than a LDD electrode. A new, BiTDD multi-electrode (performing difference between signals detected by two TDD electrodes) provided the best selectivity and reduction of cross-talk. To obtain the smallest cross-talk, a BiTDD electrode should be positioned above the end-plate region, while LDD, TDD, or NDD electrodes-above the ends of muscle that produced it. Signal differentiation improved selectivity but increased cross-talk.

Effect of recording electrode position along a muscle fibre on surface potential power spectrum

Extracellular action potentials produced by a muscle fibre of finite length were calculated for recordings at the skin surface. The sensitivity of power spectra to variations in propagation velocity (ν) and intracellular action potential (IAP) duration (T(in)) was studied theoretically. The magnitude and distribution of the spectral power of muscle fibre potentials depend on the electrode longitudinal position. The relative shifts of the spectra in dB induced by variation in ν or T(in) hardly depend on the longitudinal position of the electrode. A variation in ν affects only the power spectrum positive slope and the initial part of the high-frequency roll-off and a variation in T(in) affects only the remaining part of the high-frequency roll-off. The total spectral amplitude is practically non-sensitive to variations in the wavelength, b = ν.T(in). The total power is sensitive to variations in ν, T(in) as well as in b, and its relative changes depend on the electrode longitudinal position. The whole power spectrum is shifted along the frequency axis and mode (F(max)), median (F(med)) and mean (F(mean)) frequencies have practically equal percentage changes only when ν and T(in) vary jointly in such a way that the product ν.T(in) keeps unchanged.

Fundamentals of power spectra of extracellular potentials produced by a skeletal muscle fibre of finite length: Part I: Effect of fibre anatomy

To provide a thorough understanding of the changes in the power spectrum of electromyographic (EMG) signals, the formation of the power spectrum (PS) of extracellular potentials (EPs) produced by a skeletal muscle fibre of finite length was analysed. It was shown that, as in the case of an infinite fibre, the PS could be represented as the product of power spectra of the input signal (the first temporal derivative of the intracellular action potential, IAP) and of the impulse response (IR) of the fibre of finite length as a system of EP generation. The interrelations between the two multipliers determine the sensitivity of the EP power spectrum to alterations in parameters. The anatomical parameters of the fibre (length, depth, position of the end-plate in respect of the fibre ends) affect the EP power spectrum through IR power spectrum. Variations of the EP characteristic frequencies along the fibre length as well as oscillations in the PS are intrinsic properties of the fibre of finite length.

Effects of changes in intracellular action potential on potentials recorded by single-fiber, macro, and belly–tendon electrodes

Some myopathies are accompanied by abnormal calcium homeostasis. Electromyography (EMG) in such patients shows signs of normal or myopathic EMG when detected by a single‐fiber electrode and abnormally increased values in macro EMG. As calcium accumulation might be accompanied by changes in intracellular action potential (IAP) and muscle‐fiber propagation velocity, we simulated the effects of such changes on motor unit potentials (MUPs) recorded by different kinds of electrodes. We found that: (1) the requirements for what potential can be accepted as a single‐fiber action potential (SFAP) are too rigorous; (2) macro MUP amplitude can increase while SFAP amplitude can decrease when there is an increase in the spatial length of IAP spike; and (3) changes in the second phase of a belly–tendon‐detected MUP or M wave could be used for noninvasive detection of increased IAP depolarizing (negative) after‐potential. Muscle Nerve 37: 700–712, 2008

Simulation analysis of the ability to estimate motor unit propagation velocity non-invasively by different two-channel methods and types of multi-electrodes

Ability to estimate motor unit propagation velocity correctly using different two-channel methods for delay estimation and different non-invasive spatial filters was analysed by simulation. It was established that longitudinal double difference electrodes could be not a better choice than simple bipolar parallel electrodes. Spatial filtration with a new multi-electrode (performing difference between signals detected by two transversal double difference electrodes positioned along the muscle fibres) promises to give the best estimate. Delay estimation between reference points is more preferable than that based on the cross-correlation technique, which is considerably sensitive to the fundamental properties of the muscle fibre extracellular fields. Preliminary averaging and approximation of the appropriate parts of the signals around chosen reference points could reduce the larger noise sensitivity and the effects of local tissue inhomogeneities as well as eliminate the sampling problem. A correct estimate of the propagation velocity could be impossible, even in the case of not very deep motor units (15 or 10 mm, depending on the spatial filter used) with relatively long (about 120 mm) muscle fibres. In the case of fibres with asymmetrical location of the end-plates in respect to the fibre ends, the propagation velocity estimates could be additionally biased above the longer semilength of the motor unit fibres.