Peculiarities of extracellular potentials produced by deep muscles. Part 2: motor unit potentials.

The potential fields generated by single fibres far from the sources are non-propagating. This suggests that there should be differences in the features of surface motor unit (MU) potentials (MUPs) detected from deep and superficial muscles. We explored the features using a simulation approach. We have shown that the non-propagating character and similar shapes among surface MUPs recorded over a wide area above deep muscles with monopolar or longitudinal single differential (LSD) electrodes are natural. Contrary to close distances, at large radial distances single differentiation did not emphasize MUP main phase relative weight. The position of the end plate area could be estimated with LSD detections only for MUs with long (123 mm) almost symmetric fibres. With short fibres, the LSD main phase was masked by the outlined terminal phases. This could be misleading in MUP analysis since the terminal phases reflect standing sources. The highly asymmetric fibres could yield peculiar MUP shapes resembling MUPs of two distinct MUs. We have shown that the relative weight of terminal phases at large fibre-electrode distance decreases under abnormal peripheral conditions. However, the changes in membrane depolarization due to fatigue or pathology could be assessed non-invasively also from deep muscles.

Peculiarities of extracellular potentials produced by deep muscles. Part 1: single fibre potential fields.

The similarity among surface electromyography (EMG) signals recorded by the poles of electrode arrays above deep muscles like erector spinae is a substantial obstacle in determining major muscle characteristics. What makes EMG signals so different when detected at various distances from the fibres? To answer this question, we simulated and analyzed extracellular potential fields produced by a single muscle fibre. We considered the fields at a few specific time instants. They corresponded to the origination of two depolarized zones at the end-plate, their propagation along both semi-fibres, and extinction at the fibre-ends. We used intracellular action potentials and muscle fibre propagation velocities typical for non-fatigued or fatigued muscle fibres. We have shown that at relatively small distances from the fibre, the strong potential fields are concentrated mainly near the sources. The interaction between potential fields is weak and the propagation of the fields and EMG signals in relatively long fibres is clearly apparent. At large distances, the potential fields are wide and the interaction between the fields produced by the two depolarized zones is strong. The total potential field could remain non-propagating during the entire main phase. As a result, the propagation will be obscured also in EMG signals.

The spectral changes in EMG during a second bout eccentric contraction could be due to adaptation in muscle fibres themselves: a simulation study.

The mechanism of marked reduction in damage symptoms after repeated bout of similar eccentric contractions is still unknown. The neuronal adaptation leading to reduction of muscle fibre propagation velocity (MFPV) due to increased activation of slow-twitch motor units (MUs), decrease in activation of fast-twitch MUs, and/or increase in MU synchronization was suggested as a cause for lower EMG frequency characteristics. However, the repeated bout effect could occur also after electrically stimulated exercise. Prolonged elevation of cytoplasmic Ca(2+) due to the increased membrane permeability after eccentric contractions was reported. Elevated Ca(2+) induced peripheral changes that included alteration of intracellular action potential and MFPV reduction. We simulated and compared changes in EMG frequency characteristics related to effects of central nervous system (CNS) or to peripheral changes. The simulations were performed for different electrode arrangements and positions. The results showed that the peripheral effects could be similar or even stronger than the effects related to CNS. We hypothesised that the repeated bout effect was a consequence of the adaptation in muscle fibres necessary for avoiding Ca(2+)-induced protein and lipid degradation due to Ca(2+) overload resulting from the increased membrane permeability after eccentric contraction. The possibilities for noninvasive testing of this hypothesis were discussed.

Fatigue analysis of interference EMG signals obtained from biceps brachii during isometric voluntary contraction at various force levels.

The aim of the present study was to test the applicability of indices of muscle fatigue to interference EMG signals detected at various distances from the end-plate region during isometric voluntary contractions at different force levels. Bar electrode with 12 leading off surfaces and 5mm inter-pole distance was used to detect EMG from human m. biceps brachii. The sensitivity of the new spectral indices to detect muscle fatigue was higher than that of mean or median frequencies. Considerable variations in the characteristic frequencies and values of spectral indices that could reflect recruitment and/or rotation of MUs were found under submaximal efforts. The increase of the indices was considered as a sign of peripheral muscle fatigue while their decreasing could be a sign of de-recruitment of fatigued or/and recruitment of new MUs reflecting central fatigue. The sensitivity of the indices to fatigue depended on the electrode arrangement and its longitudinal position in respect of the end-plate region and ends of the muscle fibres. It was larger for the electrodes placed in the middle of the semi-fibre. To overcome the problem with inappropriate position of the electrode, one could use an electrode whose longitudinal dimension would cover the entire semi-length of the analyzed fibres.

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.

Simulation analysis of interference EMG during fatiguing voluntary contractions. Part I: What do the intramuscular spike amplitude-frequency histograms reflect?

Decline in amplitude of EMG signals and in the rate of counts of intramuscularly recorded spikes during fatigue is often attributed to a progressive reduction of the neural drive only. As a rule, alterations in intracellular action potential (IAP) are not taken into account. To test correctness of the hypothesis, the effect of various discharge frequency patterns as well as changes in IAP shape and muscle fibre propagation velocity (MFPV) on the spike amplitude-frequency histogram of intramuscular interference EMG signals were simulated and analyzed. It was assumed that muscle was composed of four types of motor units (MUs): slow-twitch fatigue resistant, fast-twitch fatigue resistant, fast intermediate, and fast fatigable. MFPV and IAP duration at initial stage before fatigue as well as their changes differed for individual MU types. Fatigability of individual MU types in normal conditions as well as in the case of ischaemic or low oxygen conditions due to restricted blood flow was also taken into account. It was found that spike amplitude-frequency histogram is poorly sensitive to MU firing frequency, while it is highly sensitive to IAP profile lengthening. It is concluded that spike amplitude-frequency analysis can hardly provide a correct measure of MU rate-coding pattern during fatigue.

Estimate of M-wave changes in human biceps brachii during continuous stimulation.

The purpose of the present study was to validate the capability of new fatigue indexes (in the time and frequency domain) applied to experimental recordings and thus, to test some assumptions made in previous simulations. The indexes were applied to M-waves detected non-invasively from human m.biceps brachii during repetitive slightly above threshold stimulations. It was found that distance between the motor point and middle of the end-plate region could be relatively large. Under identical conditions (signals detected by monopolar electrodes and high-pass filtered at 1 Hz), the relative changes of the indexes obtained in electrophysiological experiments and simulations were similar. Changes of the intracellular action potential profile during fatigue used in the simulations were consequently supposed to be close to the actual ones for the muscle analyzed. When the high-pass cut-off frequency was higher than 1 Hz, the sensitivity of the index in the time domain was higher, while that in the frequency domain was lower. If the normalizing spectral moment was of higher order, the sensitivity of the spectral index could be even 150-times greater than that of the fatigue indexes traditionally used. Thus, the spectral index promises high capability to assess fatigue during functional electrical stimulation.

Simulation analysis of the performance of a novel high sensitive spectral index for quantifying M-wave changes during fatigue.

A high sensitive fatigue index is desired to improve stimulation strategy and to prevent muscle damage in functional electrical simulations. The great number of indexes used shows that there is no index that satisfies all investigators. A way to develop a high sensitive index for quantifying M-wave changes during fatigue and to estimate its performance was analyzed. The changes in M-wave and its frequency distribution due to variations of intracellular action potential (IAP) and muscle fibre propagation velocity (MFPV) with fatigue were simulated. It was found that the ratio between the spectral moments of order -1 and 2 was considerably more sensitive to peripheral muscle fatigue than the mean (the ratio between the spectral moments of order 1 and 0) and median frequency traditionally used. The sensitivity of the new index depended on the electrode arrangement and position in respect to the active fibres. The belly-tendon detection promised the highest index sensitivity. The length of the active fibres also affected the index sensitivity. The shorter the fibres the lower was the index sensitivity. The sensitivity of the new index could be relatively high even in the case of traditionally used high-pass cut-off frequencies that could distort the M-wave shape.

Intracellular action potential generation and extinction strongly affect the sensitivity of M-wave characteristic frequencies to changes in the peripheral parameters with muscle fatigue.

Changes in muscle fibre propagation velocity (MFPV) and shape of intracellular action potentials (IAPs) accompany peripheral muscle fatigue. We have shown through mathematical simulations that the effects of IAP generation and extinction reduced the sensitivity of the mean (fmean) and median (fmed) frequency of M-wave power spectra to individual changes in MFPV. Due to the differences in weighting of the spectral components used for calculation of the characteristic frequencies, the highest spectral components of the M-wave affected the fmean more than the fmed. These components are related to the M-wave leading edge that reflects the IAP depolarization phase. They reduced the sensitivity of the spectral moment of order 1 to individual changes in MFPV and increased its sensitivity to IAP changes. Since the changes of the IAP depolarization phase during the final stages of peripheral muscle fatigue affected the fmean more, the range of the relative reductions of the fmean and fmed were approximately the same under combined changes in IAP and MFPV. The sensitivities of M-wave characteristic frequencies depended also on the electrode arrangement and position as well as on the length of active muscle fibres.

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.

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.