Brain, Vol. 124, No. 2, 352-360,
February 2001
© 2001 Oxford University Press
Propagation disturbance of motor unit action potentials during transient paresis in generalized myotonia
A high-density surface EMG study
1 Department of Clinical Neurophysiology and 2 Institute of Neurology, University Medical Centre, Nijmegen, The Netherlands, and 3 Motor Research Group, Institute of Pathological Physiology, Friedrich-Schiller University Jena, Germany
Correspondence to:
Professor M. J. Zwarts, MD, Department of Clinical Neurophysiology, University Medical Centre Nijmegen, PO Box 9101, 6500 HB Nijmegen, The Netherlands E-mail: M.Zwarts{at}czzoknf.azn.nl
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Abstract |
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Patients with autosomal recessive generalized myotonia, or Becker's disease, often suffer from a peculiar transient paresis. As yet, the relationship between this transient paresis and the defect in the gene encoding for a voltage gated Cl– channel protein in the muscle membrane of these patients is unclear. In order to gain a better understanding of the electrophysiological properties of the muscle fibre membrane in these generalized myotonia patients, we have studied transient paresis with a novel high-density surface EMG (sEMG) technique. We conclude that the transient paresis is explained by a deteriorating muscle membrane function, ending in conduction block and paresis. Multi-channel sEMG during the period of force decline in transient paresis shows a decrease in peak–peak amplitude of the motor unit action potentials from endplate towards tendon. This disturbance increases with time and place, indicating a deteriorating membrane function, and ends in a complete blocking of propagation within seconds. Spatiotemporally, this leads to a V-shaped sEMG pattern. In a more general sense, this contribution shows how spatiotemporal information, available through non-invasive high-density sEMG, may provide novel insights into electrophysio- logical aspects of membrane dysfunction.
high-density surface EMG; muscle membrane electrophysiology; recessive generalized myotonia
CMAP = compound muscle action potential; IAP = intracellular action potential; MFCV= muscle fibre conduction velocity; MU = motor unit; MUAP = motor unit action potential; MVC = maximal voluntary contraction; PPA = peak–peak amplitude; sEMG = surface EMG; SFAP = single-fibre action potential
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Introduction |
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Autosomal recessive generalized myotonia is a non-dystrophic disorder of skeletal muscles. This disease was separated from the autosomal dominant myotonia congenita (Thomsen's disease) by Becker (1977). Additional to myotonia, generalized myotonia patients often suffer from a peculiar transient weakness of the muscles after a period of rest. Following an initial normal or near-normal strength, a rapid but temporary decline in muscle force occurs. This transient paresis diminishes with repetitive contractions: the `warming-up' phenomenon (Rüdel et al., 1988
).
The myotonia has its basis in an electrical instability of the muscle fibre membrane (Rüdel and Lehmann-Horn, 1985). Bryant was the first to recognize that a similar instability is produced in normal muscle fibre membranes when the chloride conductance is experimentally reduced (Bryant, 1976). Consistent with this hypothesis, it has now been established that both generalized myotonia and Thomsen's disease are caused by mutations in the gene encoding for a voltage-gated skeletal muscle chloride channel protein (Koch et al., 1992; Ptacek et al., 1993; Hudson et al., 1995). The causal relationship between this disorder of the Cl– channel and the transient paresis is unknown.
Electrophysiological changes measured during transient paresis in generalized myotonia patients were mainly studied through electrically elicited compound muscle action potentials (CMAPs). Most of these studies, using repetitive nerve stimulation, found a decremental response of the CMAP (Ricker and Meink, 1972; Brown, 1974; Aminoff et al., 1977; Deymeer et al., 1998). Using a three-channel surface EMG technique, Zwarts and van Weerden (1989) described a decline in muscle fibre conduction velocity (MFCV) during periods of transient paresis in voluntary contractions in these patients, illustrating membrane dysfunction. A satisfactory explanation of the transient paresis within the framework of these accompanying electrophysiological phenomena has not been given yet.
We have studied the electrophysiological properties of the muscle fibre membrane in generalized myotonia patients with a novel 126-channel high-density surface EMG (sEMG) technique, in order to gain a better understanding of the relation between this peculiar paresis and membrane dysfunction. With this technique, recently developed in our department (Stegman et al., 1996), it is possible to obtain detailed spatiotemporal information on the electrophysiological properties of individual motor units (MUs) non-invasively (Roeleveld et al., 1997; Kleine et al., 2000).
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Subjects and methods |
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Patients and normal subjects
We have studied seven patients with generalized myotonia, diagnosed according to established criteria (Lehmann-Horn and Rüdel, 1997
): two brothers, a brother and a sister of another family and three sporadic cases (one female and two males). The mode of inheritance was compatible with an autosomal recessive trait and first symptoms were present in the first decade of childhood. All patients had muscle stiffness, myotonic runs on needle EMG, transient paresis, warming-up phenomena and muscle hypertrophy (more pronounced in male patients). The patients were drug-free for >1 month before and during the experiments. The disease was stable for >5 years. Mean age of the generalized myotonia patients was 38 years (range 22–57 years). We compared our results with data from five normal subjects, one female and four males, with a mean age of 39 years (range 22–64 years). The UMC Nijmegen Medical Ethical Committee approved the study. All patients and normal subjects gave their informed consent.
Recording of force and sEMG
The left arm was fixed in a horizontal position in an arm flexor dynamometer supplied with strain gauges, with the elbow in a 90° abduction. The hand was in a middle position. Force was recorded isometrically and was visually fed back to the subject on a PC monitor. Simultaneously with the force, sEMG was measured with a two-dimensional electrode grid developed at our department. One-hundred-and-thirty commercially available printed circuit board testing probes (Farnell Inc., type `serrated contact') were stripped of their spring and used as gold-coated electrodes. These probes, of 1.5 mm diameter, were mounted directly onto a specially designed flexible printed circuit board (Fig. 1). The print was wrapped around a foam base to ensure flexibility and adequate contact with the skin for each electrode. Electrodes were arranged in a 10 x 13 rectangular matrix with an interelectrode distance of 5 mm in both directions. Signals were recorded monopolarly with a reference electrode on the olecranon. The electrode grid was carefully placed over the m. biceps with the 10 columns parallel to the muscle fibres (Fig. 2). To avoid short-circuiting between electrodes, no electrode paste was applied. The serrated contact structure of the electrodes ensured a sufficiently low contact impedance between electrodes and skin (Blok et al., 1998). A total of 126 monopolar signals were amplified (corner electrodes were not connected), bandpass filtered (3–400 Hz) and simultaneously AD-converted (16 bits with a resolution of 0.5 µV/bit at a rate of 2000 samples/s/channel) using a multi-channel amplifier system (Mark 6, Biosemi Inc., Amsterdam, The Netherlands). Data were stored on the hard disk of a 180 MHz Pentium PC for off-line analysis. During the measurement, the signals of any one of the columns could be selected for on-line visualization, both in monopolar and higher order (e.g. bipolar) montages.
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Experimental protocol
The patients' and subjects' maximal voluntary contractions (MVC) were taken as the peak force of three short performances. Next, isometric contractions were performed at different percentages of the MVC: 5, 20, 40, 60 and 100% MVC, each sustained for 30 s. After each measurement, a period of 10 min of rest was taken. For illustrative purposes, a single measurement was performed in which a normal subject imitated the irregular force pattern as in transient paresis, starting from a 60% MVC force level.
Data analysis
The sEMG signals were analysed off-line. For optimal detection of single motor unit action potentials (MUAPs), a bipolar montage was constructed by subtracting the signals from electrodes in consecutive positions along the columns (fibre direction). For all our generalized myotonia patients, the paresis was most pronounced at the 60% MVC level. Therefore, in this paper, the sEMG data from the first period of monotonic force decline after exercise onset will be described for this force level. One column of the grid was selected for analysis (e.g. the rectangular strip in Fig. 2
), on the basis of good signal quality and the presence of many isolated single MUAP firings.
Amplitude measurement
To determine the topography of the sEMG amplitude in the direction of the muscle fibres, we visually isolated MUAPs in the signal from an electrode pair adjacent to the endplate zone. When the available spatiotemporal information indicated that this MUAP remained isolated (no interference from other MUAPs) during its propagation towards the tendon, it was included in the analysis. For each electrode position where the peak was visible, the peak–peak amplitude (PPA) of the bipolar signal was determined. This process ended either when the last electrode in the column was reached or when the signal became so small that it was indistinguishable from background activity (<50 µV). The procedure was repeated for each isolated peak that could be detected during the selected period of monotonic force decline.
Muscle fibre conduction velocity (MFCV)
MFCV estimates were made using a standard cross-correlation technique after signal interpolation (Naeije and Zorn, 1983). MFCV was estimated during transient paresis by dividing the period of transient paresis in segments of 250 ms, over which the cross-correlation was determined. A sliding window of 100 ms was used to step through the signals. This was done for the same column that was used in the amplitude analysis. Signal pairs with a cross-correlation coefficient of <0.7 were not accepted for MFCV determination.
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Results |
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Force
At a low force (5% MVC, not shown) level, force profiles in generalized myotonia patients were not different from those in normal subjects, who smoothly reached and maintained the desired force level. At higher force levels, a specific pattern emerged in generalized myotonia patients. In the 20% MVC measurements, the force profiles remained almost normal in four patients (e.g. Fig. 3A
, upper panel). In three patients we observed a small initial force `dip' just after reaching the desired level (e.g. Fig. 3B, upper panel). At 40 and 60% MVC, all seven patients showed an irregular force pattern with intermittent decline in force (Fig. 3, middle and lower panels). As stated before, since transient paresis was most pronounced and uniform during the 60% MVC experiment, we analysed sEMG data before and during the first period of transient paresis in the 60% MVC experiment. Mean MVC in the seven patients was 202 N (range 125–298 N) and 330 N (range 133–430 N) in normal subjects. Normal subjects were able to maintain force without any problem during the first 10 s of 60% MVC, in which the transient paresis in patients occurred. Initially, generalized myotonia patients were able to reach the desired force level (mean 59% MVC, range 43–73% MVC). However, immediately thereafter, force declined despite our call to continue the contraction. On average, the force dropped to 29% (range 4–45%) of the initial—nearly 60% MVC—force level. Mean duration of the first period of monotonic force decline, over which we analysed the sEMG pattern, was 3.3 s (range 1.9–6.8 s).
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SEMG
During the phase of the first transient paresis of the 60% MVC measurement, the sEMG recordings of the seven patients basically showed the same aberrant pattern.
Amplitude
In normal subjects, we found a sEMG pattern in which MUAPs can be seen to propagate from the motor endplates in both directions along the muscle fibres. Motor endplate zones can easily be detected in the bipolar signals of a column using low amplitude and inversion of the signal polarity as main indicators (Masuda et al., 1983; Yamada et al., 1987). Our results are consistent with results from other investigators who used electrode arrays in the examination of normal subjects (Masuda et al., 1983; Yamada et al., 1987; Masuda and Sadoyama, 1988). The MUAPs in normal subjects are conducted undisturbed along the muscle fibres from the motor endplate zone towards the tendon (Fig. 4B, lower panel, and Fig. 5D). Before the transient paresis, the sEMG recordings of the generalized myotonia patients show a nearly normal EMG pattern (Fig. 4A, lower panel, and Fig. 5A, at 6.4–6.6 s). With the involuntary force decline in generalized myotonia patients, the pattern along the membrane changes in a peculiar way. In Fig. 4A and in its time-zoomed version in Fig. 5A, an example of such behaviour in one of our patients is shown. At first, MUAP amplitudes drop at the fibre ends. Then, more and more electrodes show a strong decline in MUAP amplitude, with a later onset of this decline when the electrode is closer to the motor endplate (Fig. 4A, lower panel, Fig. 5A and C). The activity around the endplate never completely vanishes. This results in a `V'-shaped (or rather a `>'-shaped) appearance of the signals in the bipolar montage. In the monopolar montage (see Methods), this drop of MUAP amplitude can also be observed (Fig. 5E).
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In healthy muscles, we have never observed such an EMG pattern. Normally, during decrease in voluntary effort, the EMG is characterized by a physiological decrease in MU recruitment in all channels simultaneously (Fig. 4B
, and Fig. 5B and D), with no or only a marginal decrease in signal amplitude along the fibre.
Figure 6 shows PPAs of all isolated MUAPs that were detected during the first phase of paresis after force onset. MUAP propagation was followed from one electrode to the next, thus yielding an amplitude profile from the endplate to the tendon. All amplitudes are scaled to the PPA of the MUAPs in the bipolar trace just adjacent to the endplate (e.g. trace 32 in Fig. 5A). This trace is indicated as `1' on the x-axis of Fig. 6. When the signal becomes so small that it is indistinguishable from noise, PPA is set to zero. Figure 6A and B give examples of the PPAs of one generalized myotonia patient and of one normal subject, respectively (patient and normal subject as in Figs 4 and 5). Figure 6C shows the results of the mean amplitude behaviour in the five male patients (solid lines) compared with the five normal subjects (dotted lines), including the subject imitating the force decline (S 1) and the patient of Figs 4 and 5 (Pt 4). The data of the female patients did not allow the selection of a sufficient number of isolated peaks (>20) to yield a reliable estimate of the amplitude topography. The PPA in generalized myotonia patients is halved at a distance of only 1 cm from the endplate (at electrode `3' in Fig. 6C), while in the normal subjects, this amplitude remains constant, shows a very slight decrease or even increases over the muscle (Fig. 6C, dotted lines). As may be deduced from Figs 4A and 5A, the action potentials early in the paresis are rather undisturbed (`+' symbols in Fig 6A, for the earliest 50% of all MUAPs). They keep a relatively large PPA along the fibre. The later peaks, marked with the `o' symbol, show a rapid decline (below-average PPA). This systematic behaviour of the early 50% (+) and the late 50% (o) of the firings is in contrast with the mixed pattern (Fig. 6B) shown by the healthy subject (Fig. 4B), which is not correlated with time.
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Muscle fibre conduction velocity
From visual inspection, a decline of the MFCV along the muscle fibres seemed to be present, but it appeared that the MFCV could not be reliably estimated in the phase of transient paresis in generalized myotonia patients. In general, a reliable quantification is impossible without a high resemblance between the consecutive wave shapes (the correlation coefficients between subsequent traces should be >0.7). During transient paresis, this condition is not met because of the changing signal wave shapes of the MUAPs from one trace to the next (see Fig. 5C
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Discussion |
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The occurrence of transient paresis is force dependent. At 5% MVC force levels, generalized myotonia patients had no problem maintaining an isometric contraction for a period of at least 30 s. This can be considered an unexpected finding. When stimulating a nerve supramaximally with 5 or 10 Hz, patients already show a decline in force and EMG amplitude after 5 s (Aminoff et al., 1977
; Deymeer et al., 1998). Frequency of voluntary drive to MUs is in this order of magnitude [exceeds 6–8 firings/s (Freund, 1983)], so a rapid decline could be anticipated for all voluntary force levels as well. The lack of transient paresis at the lowest levels can be explained by a rapid and smooth switchover to other, not yet recruited MUs (MU rotation). Preliminary analysis of the sEMG data of the 20% MVC force in the generalized myotonia patients indeed shows an alternating recruitment of MUs. The central nervous motor drive can cope with the functional limitation of the not fully activated muscles. The typical electrical phenomenon, i.e. the typical V-shaped decay of activity, was observed in individual MUs after some seconds. However, this was always followed by the immediate recruitment of new MUs, as determined by a varying position of endplate zones. Patient dependent coping mechanisms also determine the way in which restoration of force after transient paresis occurs `electrophysiologically'. They point to the existence of interindividual differences in the way by which the central nervous motor drive overcomes the functional limitation. So a study of both low force and the restoration phase will need the incorporation of central drive mechanisms in the explanation of the observations.
At the highest force levels, when a large fraction of the available MUs or all MUs have to be recruited [at 50% MVC, 90% of the MUs in hand muscles are active (Grillner and Udo, 1971)], MU rotation or other coping mechanisms can hardly compensate for the peripheral neuromuscular problem. In between high and low force levels, there is a transition of behaviour. In the upper panel of Fig. 3A, the force pattern still is `like normal' (successful rotation at 20% MVC), whereas in the upper panel of Fig. 3B, the insufficiency of this rotation turns up already. From supramaximal electrical nerve stimulation experiments (Wagner and Zett, 1982; Streib, 1987; Deymeer et al., 1998), it is known that MU force drops more dramatically in patients when stimulus (i.e. firing) frequency increases. This explains the further deterioration of the transient paresis with still higher force levels (60–100% MVC; not shown), also documented by Zwarts and van Weerden (Zwarts and van Weerden, 1989).
Recording surface EMG with a large number of densely packed electrodes offers a novel view on electrophysiological phenomena of the sarcolemma as observed in this study. In the electrophysiological changes of the MUAPs of generalized myotonia patients during the force decline a temporal and a spatial aspect can be distinguished.
Initially, generalized myotonia patients show a normal interference pattern of the sEMG and a normal force rise. In the course of time, our results basically show the same characteristics as reported by nerve stimulation studies: an unusual lowering of amplitudes, indicating disturbed membrane function (Brown, 1974; Aminoff et al., 1977; Streib, 1987; Deymeer et al., 1998).
With respect to spatial characteristics, we confirmed the general observations of other investigators who used an sEMG array in normal subjects, i.e. the determination of the motor endplate zone in the bipolar lead and the undisturbed propagation of MUAPs over the muscle fibre from endplate towards tendon (Masuda et al., 1983; Yamada et al., 1987; Masuda and Sadoyama, 1988).
Our most important and unique finding is that there are peculiar spatial changes in the MUAPs during transient paresis. The topographical aspects of the measurements with the 10 x 13 electrode grid clearly indicate increasing abnormalities in the propagation of the action potentials from motor endplate zone towards tendon. It is shown that during transient paresis, the amplitude of an MUAP declines when it propagates along the fibres. Eventually MUAPs even vanish. The further away from the endplate zone, the sooner this becomes visible. A V-shape emerges in the spatiotemporal presentation of the EMG, indicating a gradual deterioration of action potential propagation from the endplate towards the tendon in time. The resulting decrease in PPA along the fibre is dramatic: while in normal subjects the PPA remains more or less constant, the PPA is halved over a distance of only 1 cm in generalized myotonia patients. Abnormal morphological features, such as focal necrosis, cannot explain the spatially distributed character of membrane dysfunction during transient paresis, because initially normal activity is seen along the whole fibre length. Therefore, it must be a physiological phenomenon. One can think of three underlying mechanisms bringing about the MUAP wave shape and amplitude changes: (i) dispersion between action potentials of fibres of a single MU; (ii) amplitude decline of single-fibre action potentials (SFAPs) because of MFCV decrease; and (iii) decline and eventually blocking of intracellular action potentials (IAPs). As can be deduced from simulation studies (e.g. using the SiMyo simulation model) (Duchene and Hogrel, 2000), dispersion alone is insufficient by far as an explanation for the amplitude decline observed. The second possibility (a decrease of MFCV and an associated reduction of the spatial extension of the IAP) would affect bipolarly recorded signals much more than monopolar signals (also confirmed by simulations with the SiMyo model). From the example in Fig. 5E, this possibility can also be ruled out as a sufficient explanation. This is further supported by single-fibre EMG studies in generalized myotonia patients (Stalberg and Trontelj, 1994) that showed a dramatic drop in signal amplitude without an obvious relation to an MFCV decrease. Therefore, amplitude decline of IAPs and a subsequent propagation blocking of SFAPs seem to be required as an explanatory mechanism at a single-fibre level for the electrophysiological response during transient paresis.
At a more basic physiological level, the phenomenon can be explained by a disturbed repolarization capacity of the fibre membrane (Hudson et al., 1995). The reduced chloride conductance in generalized myotonia patients is thought to build up a membrane depolarization, caused by an only partial repolarization after each action potential. This results in hyperexcitability, causing myotonia and, when severe, in hypoexcitability because of K+ accumulation in the T-tubules (Coonan and Lamb, 1998; Wallinga et al., 1999). The diminution and eventual blocking of MUAP peaks is consistent with such a mechanism. Focal block of conduction was already observed by Trontelj and Stalberg (1995) with stimulated single-fibre EMG in generalized myotonia patients. Last but not least, single-fibre action potential blocking offers a persuasive explanation for the observed decrease in force during transient paresis. Failing membrane propagation prevents the activation of a growing part of the contractile mechanism. The nature of the improvement after some time could be explained by the induction of a strongly increased Na+–K+ pump activity, which develops within seconds (Everts and Clausen, 1994).
The particular spatial distribution of the observations can, at the level of the sarcolemmal structure, be interpreted in two ways. One possible interpretation is that ion channels are inhomogeneously distributed along the sarcolemma. For Na+ channels this indeed has been shown in some animal muscles. A high Na+ channel concentration was found near the endplate zone with a strong, gradual decline towards the tendon (Almers et al., 1983; Caldwell et al., 1986). The shape of this curve is similar to our V-shaped sEMG pattern. The low Na+ channel concentrations near the tendon give rise to a lower safety factor for action potential generation. In combination with the disturbed sarcolemma function of generalized myotonia patients, this could easily give rise to a more pronounced expression of the disturbance further away from the endplate. Another possibility is that the excitation of the generated action potentials gradually deteriorates due to the abnormal, but as such homogeneously, distributed chloride conductivity. This leads to single-fibre action potential amplitude decrease, MFCV decrease and eventually propagation blocking. As yet, detailed information concerning these topographical aspects of ion channels in human muscle fibres is lacking, and the pathophysiological mechanism therefore remains partly speculative.
In conclusion, high-density surface EMG provides basic and unique information about electrophysiological and topographical aspects of the sarcolemma. Surprising as it may seem, recording at some distance from the muscle thus provides a more precise view of the electrical activity of the muscle fibre membrane.
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Acknowledgments |
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This research is supported by the Technology Foundation (STW, Utrecht, The Netherlands), grant no. NGN.3818.
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Received July 4, 2000. Revised October 3, 2000. Accepted October 23, 2000.
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