Professional Documents
Culture Documents
Rehabilitation Center “Her Roessingh,” and *Biomedical Engineering Division, Department of Electrical
Engineering, University of Twente, Enschede, The Netherlands
The noisy character of surface EMG records a broadly accepted parameter to monitor muscle
makes statistical signal analysis the most appropri- fatigue (6). Therefore, it has been applied in clinical
ate technique to obtain a quantitative description of (24,33) as well as in more basic (l&32) studies of
the signal. In the frequency domain, the power fatigue. The use of special hardware makes it pos-
spectral density function (power spectrum) is often sible to monitor MF even on-line (15), which seems
used, one of its more explored parameters being the especially useful in ergonomic studies. Recently it
median frequency (MF). It has been shown that this was shown that the MF can also be used to identify
parameter deviates from its normal value in a num- recruitment control strategies (26).
ber of neuromuscular disorders (2,9,17). MF is also Model studies have linked motor unit character-
istics, like the firing process statistics and the motor
unit action potential (MUAP), to properties of the
Accepted October 11, 1991. power spectrum. A usual approach is to model sin-
Address correspondence and reprint requests to Dr. H. J.
Hermens at Roessingh Research and Development, Roessingh- gle motor unit firing as a point process and an
bleekweg 33, 7522 AH Enschede, The Netherlands. MUAP train as the convolution of this point process
15
16 H. J. HERMENS ET AL.
Firing instants
Figure 1 shows the basic concepts of the model.
The EMG signal was obtained by addition of a num-
ber (N) of MUAP trains. In calculating each train,
we distinguished three stages. First the MUAP was MUAP train
calculated, then the firing instants were determined. FIG. 1. Generation of one MUAP train. First a MUAP shape
is chosen from a library. Then values for MUAP PPV and
Finally generation of the MUAP at the firing in- MUAP PPT are drawn from Gaussian distributions (mean CL,,
stants created a MUAP train. resp. Pr, SD w,, resp. UT) and used to create an MUAP. An
mlPl is drawn from a distribution function (pLM, uM), repre-
senting the variability in mlPl among MUAP trains. The mlPl
MUAP Generation value is used as a mean value for the Gaussian distribution
function (CL,,u,) from which subsequent IPls are drawn. Con-
volution of the MUAP with the pulse train results in an MUAP
Each MUAP was described with three parame- train.
ters: an MUAP shape normalized with respect to
amplitude and duration, an amplitude, and a dura-
tion (see Fig. 1). The MUAP shapes were stored in sumed to be constant, its shape, amplitude, and du-
a library that could contain up to 16 different ration not being changed during the simulation.
shapes. During simulation each MUAP shape was
assigned to a given percentage of the total number Firing Patterns
of MUAP trains.
The peak-peak voltage (PPV) of the biphasic For each MUAP train a mean IPI (mIP1) was
MUAP was defined as the voltage (difference) be- drawn from a Gaussian distribution (JL~, aM>. This
tween the positive and negative peak of the MUAP. distribution function expressed the variation in
The duration of the MUAP was parameterized by mIP1 values among the different MUAP trains. As a
the peak-peak time (PPT), i.e., the time difference next step the drawn mIP1 was used as the mean
between the occurrence of the two peak values. All value of a second distribution function (pi, ui).
MUAP shapes in the library had equal (unity) val- From this distribution function the subsequent IPIs
ues of PPT and PPV. During simulation, actual val- for the MUAP train were drawn.
ues of PPV and PPT were drawn from two indepen- The IPI values were assumed to behave like in-
dent Gaussian distribution functions (mean value dependent samples of a Gaussian distribution
t.~v and pr; standard deviation uv and u-r). These (22,23). According to experimental findings, a
values were used to multiply and resample the Gaussian distribution is justified (4) when the mean
MUAP shapes. The MUAP properties were as- firing rate exceeds -10 Hz (21).
55
1
50 -
i7 45- ,+++++s+,:+++++,++++8r +
+A
I, -: + +
l.L FIG. 3. The relation between MF and the stan-
I 40- dard deviation of the IPI distribution function
~)~im$;ion parameters: N = 1, PLT= 10 ms,
1 , M = 100 ms, (T,,,= O%, Ns = 0).
35 -
0 5 10 15 20 25 30
that links the firing instants in the different synchro- changed its shape. With lower values of Ns, the
nized MUAP trains. This relation was calculated for minimum of MF was reached at lower values of us.
different sizes of the subpopulation with synchro-
nized activity (Ns). Sensitivity to MUAP Characteristics
When all MUAP trains were involved in synchro-
nous tiring (Ns = lOO%), an increase of us from Figure 6 shows the relation between MF and the
zero lowered MF substantially. However, above a reciprocal value of the mean MUAP PPT (kr) for
certain value of us, MF was found to increase again two different MUAP shapes. MF was found to be
up to its original value. This means that in case of linearly related to the reciprocal value of u-r, the
perfect synchronization, as during electrical stimu- MUAP shape thus affecting only the slope of this
lation of the muscle, MF has approximately the relation. This finding made it possible to quantify an
same value as without synchronization. MUAP shape as the slope of this relation.
When only part of the motor unit pool was as- Figure 7 shows the relation between MF and the
sumed to fire synchronously, not only the effect on variability in MUAP PPT (or) in the motor unit
MF was found to be less, but also the curve pool. Increasing or caused a slight shift of MF to
60 ,
1
60 - + * +
+ ++
+ +++
+ + + +
+ + +
77
I
- 40-
FIG. 4. The relation between MF and the mean
5 of the mlPl distribution function &,,) (simula-
tion parameters: N = 100, k = 10 ms, cr, = 5%,
0 M = 5%, (T, = lo%, N, = 0).
20 -
45
lower values. This shift was -10% for the whole With each MUAP shape, the results of 30 simu-
range of UT (0, 25% t.+) used during simulation. lations, using the individual MUAP statistics, were
averaged to obtain one MF value. The relative
Comparison Between Simulation Results and width of the 95% confidence interval of these MF
EMG Recordings values was 5%. The results are shown in the graphs
of Fig. 8 as histograms of MF values.
MF values obtained from simulations, using ex- An estimate of MF of the actual EMG recordings
perimental MUAPs, were compared with MF val- was obtained by averaging the MF values obtained
ues directly calculated from EMG recordings. With from 10 recordings of each subject. The 95% confi-
each subject, the experimental MUAPs were con- dence intervals of the mean MF values were calcu-
verted to input data (PT, UT, l.~v, uv, and MUAP lated to compare the results. These are shown as
shapes) for the model and the values of the other bars in the graphs of Fig. 8. Assuming a correct
input parameters were chosen within physiological estimation of all model parameters, including p,r
ranges (N = 100, l.~~ = 100 ms, oM = 20%, uI = from the limited amount of MUAPs, the bar should
13%). It was assumed that no synchronization (Ns be in the middle of the histogram (e.g., Fig. 8B).
= 0) occurred. The results in Fig. 8 indicate that the estimated
160 ,
20 25 30
value of MF from actual recordings is equal to or relative variations in SH and PPT, this indicates
higher than predicted by simulation. that both MUAP parameters contribute in a similar
way to variations in MF.
Inter-individual and Intraindividual Differences The statistics concerning the whole set of mea-
sured MUAPs reveal some information on interin-
Considering the relations found between the dividual variations in SH and PPT. For SH the
model input parameters and MF, it can be predicted overall standard deviation is in the same range as
that, in absence of synchronization, variations in the three individual standard deviation values. This
MF will be largely caused by variations in mean indicates a large overlap of the individual distribu-
MUAP PPT (pr) and MUAP shape. To investigate tion functions of the MUAP shape parameter. In
the role of l~r and MUAP shape in interindividual contrast to this, the overall standard deviation for
and intraindividual differences in MF, first the ef- PPT is two to three times larger than the individual
fect of a particular MUAP shape was defined as the standard deviations, which indicates that these dis-
slope (H-J) of the MF vs. l/p,, relationship. Thus; tribution functions do overlap only for a small part
(Figs. 8 and 9). These findings were confirmed by
SH = MF . ,kT (6) the p values resulting from two identical analysis of
It then follows from the results illustrated in Fig. 6, variance tests (df = 2,21), one applied to the set of
showing a linear relation with zero axis intercepts, PPT data and one applied to the set of SH data. The
that SH does not depend on e and MF. Calculated p value for the SH data was 0.75 > pSH > 0.5 and
SH values of three subjects are shown in the histo- that for the PPT data was 0.25 > pppT > 0.10, indi-
grams in Fig. 9. cating stronger evidence for interindividual differ-
As a next step, the relative standard deviations of ences in PPT than for interindividual differences
the three individual distribution functions of PPT in SH.
and SH were calculated, regarding them as a mea-
sure of their relative variation. Also the standard DISCUSSION
deviations of all PPT and SH values, pooled into
one set, were calculated. The results are shown in In comparison with previous models (5,13,19,22,
Table 1. From this table it can be seen that within a 23,30,31), a number of changes were made to make
muscle, MUAPs show a variation in both SH and the model more realistic. These include the library
PPT. The ratio between the relative standard devi- of MUAP shapes and the use of distribution func-
ations in SH and PPT show that the variability of tions to account for the natural variability in mean
PPT ranges between 1.00 and 1.78 times the vari- firing rates, MUAP PPT, and MUAP peak-peak am-
ability of SH. Because MF is equally sensitive to plitude. The model input parameters were not cor-
31 34 37 40 43 46 49 52 55 50
MF [Hz]
3
FIG. 9. Histograms of MF values obtained by
simulation. For each MF value, an experimental
MUAP shape was used as input. Pooled, individ-
=: ual MUAP data were used to estimate the PPT
2
w- parameters (simulation parameters: N = 100,
j~,~= 100 ms, uM = 20%, u, = 13%, Ns = 0). The
95% confidence interval of a mean MF, calcu-
lated from MF values of 10 experimental EMG
1 recordings in the same subject, is shown as a
horizontal bar. The curve shows a best fit with a
second-order spline. A-C: Data of, respectively,
subjects A, B, and C.
0
30 34 38 42 46 50 54 58 62 66 68
MF [Hz]
c 5
30 33 36 39 42 45 40 51 54 57 60
MF (Hz]
SH 11
related because the nature of such correlation is at variance with the observations of Tanzi and
largely unknown. In addition, it is relatively simple Taglietti (27). They found a linear relation (negative
to predict the effect of a possible correlation from slope) between the estimated duration of experi-
the predicted effect of variation of isolated param- mentally obtained MUAPs and the frequency of
eters. maximal power density. The seeming difference
The results obtained by simulation clearly predict with our results may be only apparent and due to
that variability in MF is caused by variations in their limited number of samples (9), which allowed
MUAP shape (SH), mean MUAP PPT (t+), and them to fit their data with a linear curve instead of
synchronization (Ns and us). This is in agreement with a l/x relation.
with findings of Person and Libkind (22). They com- Our results predict that MF is hardly sensitive to
puted the dominating frequency (frequency of max- variation of the firing process parameters. This in-
imum power density) to be linearly related to the dicates that variations in Sj$ have little influence in
reciprocal value of the duration of their artificial the first term on the right of Eq. 4. Apparently,
MUAP shape. The ratio between the duration of despite overlap of the power spectra of the MUAPs
their MUAP shape and the mean PPT is constant, and the firing processes, the power density of the
while also their dominating frequency is compara- MUAP spectra is low at those frequencies where
ble to MF owing to the rather symmetrical shape of peaks occur in the spectra of the firing processes.
their power spectrum. This result, however, seems From the figure given by Pan et al. (19), it can be
derived that MF increases as little as 5 Hz while the
mean firing rate is varied from 10 to 50 Hz. This
TABLE 1. Mean values of MUAP PPT, relative shift is even less than indicated by our results, prob-
standard deviations of MUAP PPT (UPTIPPT), ably owing to the higher value of the MUAP PPT
relative standard deviations of MUAP shape parameter they used during simulation.
(dSH/SH), calculated from experimental MUAP data in
three subjects, and relative standard deviations ofall
We also varied the other part of the first term in
PPT and SH values pooled into one set Eq. 4, which is the function [M,(o)] that describes
the MUAP properties. When we regard the varia-
dpPT/PPT dSH/SH
z
tion of l/t+ as a compression/expansion of the
(%I cm
MUAP power spectrum along the frequency axis, a
Subject A 8.9 13.0 9.6 linear relation over such a wide range as shown in
Subject B 7.6 15.1 8.5
Subject C 9.6 14.7 14.7 Fig. 6 could be obtained only when the power spec-
trum of the firing process was rather flat in the area
Pooled A + B + C - 37.1 12.2
involved.
The analysis of the experimentally obtained tion was predicted to be able to decrease MF con-
MUAPs indicated that within one muscle differ- siderably, depending on the number of motor units
ences in PPT and MUAP shape (SH) are present, involved (N,) and the spread in the firing instants
both contributing to variations in MF. Such differ- (us). MF was predicted to be equal for EMG signals
ences may result in a correlation between MF and with perfect (us = 0) and with no synchronized
the level of contraction if one or both parameters motor unit activity. This means that the M-wave
are related to the recruitment level of motor units. equals the mean MUAP with respect to shape and
Solomonow et al. (26) found a linear increase of MF PPT. This prediction coincides with experimental
of the M-wave with stimulation level (normal re- finding of Knaflitz et al. (12), as their figures do not
cruitment order). Also in experimental studies in show systematic differences in MFs obtained dur-
humans, a relatiorrbetween force level and MF has ing voluntary and electrically elicited contractions.
been observed (3,12). A broadly accepted theory on the mechanism of
The analysis of interindividual differences in MF synchronization as well as on its role during volun-
values indicated that these are caused primarily by tary contractions is missing. In a number of studies
differences in mean PPT (TV.=) rather than by differ- (8,16), it has been shown that motor units tend to
ences in MUAP shape (SH). The relatively low fire synchronously more often than can be expected
variability in SH may be explained by considering from coincidence. In other studies, the existence of
that the MUAP shape changes especially when the synchronization was questioned (28). Synchroniza-
electrodes are moved along the direction of the tion is also mentioned to explain part of the shift of
muscle fibers (25). This variability was diminished the power spectrum toward lower frequencies as
during the experiments by placement of the elec- observed in muscle fatigue (3,18,32).
trodes halfway between the distal tendon and the Part of the differences in literature may be ex-
motor endplate zone, a region where the MUAP plained by considering Ns, the number of motor
shape is relatively constant. units involved in synchronization, as a statistical
The other MUAP parameter, the PPT, is deter- time-varying parameter. It then describes a popula-
mined by factors like muscle fiber conduction ve- tion of motor units that may change constantly, but
locity, the spatial dispersion of the endplates, and with an average size equal to Ns. As a conse-
anatomical properties of the muscle (14). These fac- quence, the effect of synchronization will be ob-
tors are merely dependent on the subject rather served always in the surface EMG signal, but it
than on the recording method. This seems in agree- may be missed or underestimated easily when only
ment with experimental findings of Broman et al. a small number of motor units is observed.
(3), who observed intersubject differences in MF,
which correlated with subject muscle fiber conduc-
REFERENCES
tion velocity and limb circumference.
The use of experimental MUAPs as input for the 1. Blinowska A, Verroust J, Cannet G: An analysis of synchro-
model resulted in lower or equal values of MF in nization and double discharge effects on low frequency elec-
tromyographic power spectra. Electromyogr Clin Neuro-
comparison with the confidence interval of MF ob- physiol20465480, 1980.
tained from EMG recordings in the same subject. 2. Boukes R: Force and surface EMG measurements in pa-
Differences might be due to the limited amount of tients with neuromuscular disorders. MD thesis, Vrije Uni-
versiteit Amsterdam, Krips Repro Meppel, Amsterdam,
MUAPs (7, 7, and 10) used to estimate the mean 1982.
PPT in each subject. Another cause could be an 3. Broman H, Bilotto G, De Luca CJ: Myoelectric signal con-
underrepresentation of MUAPs with a low PPT, duction velocity and spectral parameters: influence of force
and time. .I Appl Physiol58:14211437, 1985.
probably belonging to motor units with higher re-
4. Clamann HP: Statistical analysis of motor unit firing patterns
cruitment levels. When the needle was manipu- in a human skeletal muscle. Biophys J 9: 1233-1251, 1969.
lated, subjects often tended to lower the force level 5. De Luca CJ: Physiology and mathematics of myoelectric
to avoid pain. signals. IEEE Trans Biomed Eng 26:313-325, 1979.
6. De Luca CJ: Myoelectrical manifestations of localized mus-
The results of this study indicate clearly which cular fatigue in humans. CRC Crit Rev Biomed Enn 11:251-
parameters at the motor unit level contribute signif- 279, 1984:
icantly to changes in MF and which parameters do 7. De Luca CJ and Forrest WJ: Some properties of motor unit
action potential trains recorded during constant force iso-
not. Two of the relevant parameters, MUAP shape
metric contractions in man. Kybernetik 12:160-168, 1973.
and mean PPT, are well understood in terms of the 8. Dietz V, Bischofberger E, Wita C, Freund HJ: Correlation
underlying physiological processes. Synchroniza- between the discharges of two simultaneously recorded mo-
tor units and physiological tremor. Electroencephalogr Clin tractions of muscle. Electroencephalogr Clin Neurophysiol
Neurophysiol40:97-105, 1976. 32:471-483, 1972.
9. Hermens HJ, Boon KL, Zilvold G: The clinical use of sur- 22. Person RS and Libkind MS: Simulation of electromyograms
face EMG. Electromyogr Clin Neurophysiol 241243-265, showing interference patterns. Electroencephalogr Clin
1984. Neurophysiol28z625-632, 1970.
10. Hermens HJ, van Bruggen TAM, Rutten WLC, Wilts G: A 23. Piotrkiewicz M: A study of surface electromyograms by
stochastic model for simulation of surface EMG patterns. In: means of digital simulation. Electromyogr Clin Neurophysiol
Electrophysiological Kinesiology, International Congress 18:83-94, 1978.
Series 804, Elseviers Science Publishers, Amsterdam, pp 24. Roy SH, De Luca CJ, Casavant DA, Emley MS: EMG as-
231-234, 1988. sessment of muscular deficits associated with chronic low
11. Kirkwood PA and Sears TA: The synaptic connexions to back pain. In: Electrophysiological Kinesiology, Interna-
intercostal motoneurones as revealed by the average com- tional Congress Series 804, Elseviers Science Publishers,
mon excitation potential. J Physiol 275: 103-134, 1978. Amsterdam, pp 451-454, 1988.
12. Knaflitz M, Merletti R, De Luca CJ: Inference of motor unit 25. Sollie G, Hermens HJ, Boon KL, Wallinga de Jonge W,
recruitment order in voluntary and electrically elicited con- Zilvold G: The boundary conditions for measurement of the
tractions. J Appl Physiol 68:1657-1667, 1990. conduction velocity of muscle libres with surface EMG.
13. Lago PJ and Jones NB: Effect of motor unit firing time sta- Electromyogr Clin Neurophysiol25:45-56, 1985.
tistics on EMG spectra. Med Biol Eng Comput 15648-655, 26. Solomonow M, Baten CTM, Smit J, Baratta R, Hermens HJ,
1977. D’ Ambrosia R, Shoji H: Electromyogram power spectra fre-
14. Lindstrom LH and Magnusson RI: Interpretation of myo- quencies associated with motor unit recruitment strategies. J
electric power spectra: a model and its applications. IEEE Appl Physiol68:1177-1185, 1990.
Trans Biomed Eng 65:653-662, 1977. 27. Tanzi F and Taglietti V: Spectral analysis of surface motor
unit action potentials and surface interference electromyo-
15. Merletti R, Biey D, Biey M, Prato G, Orusa A: On-line mon-
itoring of the median frequency of the surface EMG power gram. IEEE Trans Biomed Eng 28:318-324, 1981.
28. Taylor A: The significance of grouping of motor unit activ-
spectrum. IEEE Tram Biomed Eng 32~1-7, 1985.
ity. J Physiol 162:259-269, 1962.
16. Milner-Brown HS, Stein RB, Lee RG: Synchronization of
29. Ten Hoopen M: Examples of power spectra of uni-variate
human motor units: possible roles of exercise and supraspi-
point processes. Electroencephalogr Clin Neurophysiol
nal reflexes. Electroencephalogr Clin Neurophysiol38:245-
70~68-72, 1974.
254. 1975.
30. Weytjens JLF and van Steenberghe D: Spectral analysis of
17. Muro M, Nagata A, Murakami K, Moritani T: Surface EMG the surface electromyogram as a tool for studying rate mod-
power spectral analysis of neuromuscular disorders during ulation: a comparison between theory, simulation, and ex-
isometric and isotonic contractions. Am J Phys Med 61:24& periment. Biol Cybern 50:95-103, 1984.
254, 1982. 31. Weytjens JLF and van Steenberghe D: The effects of motor
18. Naeije M, Zom H: Relation between EMG power spectrum unit synchronisation on the power spectrum of the electro-
shifts and muscle fibre action potential conduction velocity myogram. Biol Cybern 51:71-77, 1984.
changes during local muscular fatigue in man. Eur J Appl 32. Zwarts MJ, van Weerden TW, Haenen HTM: Relationship
Physiol50:23-33, 1982. between average muscle tibre conduction velocity and EMG
19. Pan ZS, Zhang Y, Parker PA: Motor unit power spectrum power spectra during isometric contraction, recovery and
and firing rate. Med Biol Eng Comput 27:14-18, 1989. applied ischemia. Eur J Appl Physiol 56:212-216, 1987.
20. Papoulis A: Probability, Random Variables, and Stochastic 33. Zwarts MJ, van Weerden TW, Links TP, Haenen HTM,
Processes. McGraw-Hill, Kogakusha, 1965. Oosterhuis HJGH: The muscle libre conduction velocity and
21. Person RS and Kudina LP: Discharge frequency and dis- power spectrum in familial hypokalemic periodic paralysis.
charge pattern in human motor units during voluntary con- Muscle Nerve 11: 166-173, 1988.