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Analysis of intramuscular electromyogram signals


Roberto Merletti and Dario Farina
Phil. Trans. R. Soc. A 2009 367, 357-368
doi: 10.1098/rsta.2008.0235

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Phil. Trans. R. Soc. A (2009) 367, 357368


doi:10.1098/rsta.2008.0235
Published online 11 November 2008

REVIEW

Analysis of intramuscular electromyogram


signals
B Y R OBERTO M ERLETTI 1, *

AND

D ARIO F ARINA 2

Laboratorio di Ingegneria del Sistema Neuromuscolare (LISiN), Dipartimento


di Elettronica, Politecnico di Torino, 10129 Torino, Italy
2
Center for Sensory-Motor Interaction (SMI ), Department of Health Science
and Technology, Aalborg University, 9220 Aalborg, Denmark

Intramuscular electromyographic (EMG) signals are detected with needles or wires


inserted into muscles. With respect to non-invasive techniques, intramuscular
electromyography has high selectivity for individual motor unit action potentials and
is thus used to measure motor unit activity. Decomposition of intramuscular signals into
individual motor unit action potentials consists in detection and classication, usually
followed by separation of superimposed action potentials. Although intramuscular EMG
signal decomposition is the primary tool for physiological investigations of motor unit
properties, it is rarely applied in clinical routine, because of the need for human interaction and the difculty in interpreting the quantitative data provided by EMG signal
decomposition to support clinical decisions. The current clinical use of intramuscular
EMG signals relates to the diagnosis of myopathies, of diseases of the a-motor neuron
and of the neuromuscular junction through the analysis of the interference signal or of
the shape of some motor unit action potentials, usually without a full decomposition
of the signal.
Keywords: intramuscular electromyogram; decomposition;
integration of invasive and non-invasive electromyogram analysis techniques;
muscle; peripheral nervous system

1. Introduction
The motor unit consists of a motor neuron and the muscle bres innervated by
its axonal branches. The number of muscle bres it contains ranges widely across
human muscles. The muscle bres of each motor unit are intermingled with bres
of other motor units so that bres belonging to several motor units are close to
each other. The bres of a motor unit occupy a portion of the cross section of a
muscle (motor unit territory), which has an irregular round shape (Sta
lberg et al.
1995; Sta
lberg & Falck 1997; Trontelj et al. 2004).
* Author for correspondence (roberto.merletti@polito.it).
One contribution of 13 to a Theme Issue Signal processing in vital rhythms and signs.

357

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R. Merletti and D. Farina

The electrical activity associated with the contraction of muscle bres in the
motor units can be recorded using either intramuscular or non-invasive (surface)
detection systems. The difference between the two detection modalities consists
in the effect of the volume conductor that separates the muscle bres from the
detecting electrodes; this effect can be modelled as a low-pass lter whose
selectivity depends on the distance between the electrodes and the source. As
compared with surface electromyographic (EMG) recording, the insertion of
electrodes into muscles allows the detection of electric potentials close to the
muscle bres, thus the effect of the volume conductor is limited. For this reason
the action potentials of individual motor units can be easily identied from the
interference signal, at least at moderate force levels.
The invasive recording of EMG signals also allows the measure of different
types of spontaneous activity, e.g. brillation potentials due to denervation, as
well as changes in the motor unit potentials related to disorders affecting the
muscle, the neuromuscular junction or the peripheral nerves. The traditional
clinical use of intramuscular electromyography is in the diagnosis of myopathies,
diseases of the neuromuscular junction and of the lower motor neuron through
the observation of features of the detected individual action potentials (single
bre electromyography) up to the interference signal. This analysis is based on
signal features (e.g. number of turns) that differ in healthy conditions and
diseases. Most of these features are lost in surface recordings owing to the severe
low-pass ltering and diffusion due to the volume conductor, which causes the
EMG signal bandwidth to reduce from more that 1 kHz, typical of the
intramuscular signals, to less than 400 Hz, typical of the surface recordings.
Needle or wire electrodes inserted in the contracting muscle record individual
motor unit action potentials. Depending on the type of electrode used and its
location (see gure 1), the recorded action potentials can be the result of the activity of a small (13), moderate (1520) or large (more than 20) number of muscle
bres. The action potentials generated by bres belonging to the same motor unit
are not time aligned owing to the different locations of the end-plates (gure 2).
In neurophysiologic investigations, intramuscular recordings are often used to
identify the discharge times of individual motor units (De Luca et al. 1982; Nawab
et al. 2008; Marateb & McGill in press). In this application, the shape of the action
potentials is used to identify the occurrences of the discharges of the active motor
units. Although surface EMG signals can also be decomposed into individual
motor unit activities (e.g. Gazzoni et al. 2004; Holobar & Zazula 2004), the analysis
of motor units is usually more accurate using intramuscular systems owing to the
narrower action potentials. Moreover, by contrast with surface techniques,
intramuscular electromyography allows recordings from deep muscles.
The greater selectivity of intramuscular recordings compared with surface
recordings also poses some limitations. Owing to its selectivity, intramuscular
EMG recordings reect the activity of only a small number of active motor units
whose bres are close to the position of the detection site. In addition, the identied
intramuscular action potentials are not representative of all the bres in the motor
unit, and it is difcult to extract parameters related to the membrane bre properties
by using intramuscular recordings only. Finally, intramuscular recording systems
usually have a very small detection volume and thus it is difcult to reposition a
needle to detect the same motor units in repeated insertions. Surface electromyography provides a more global assessment of muscle properties and thus overcomes
Phil. Trans. R. Soc. A (2009)

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Review. Analysis of intramuscular EMG signals

359

6.0

5.0

1 mm

4.0

0.5 mm

arb. units

(a)

3.0

(b)
detection volume
(c)

2.0

1.0
(d )

100
200
300
400 m
Figure 1. The different types of needle electrodes have different recording volumes covering different
portions of a motor unit territory. (a) Single bre electrode. (b) Concentric electrode whose recording
volume has a diameter of 0.51.5 mm. (c) Monopolar electrode. (d ) Macro electrode recording from the
single bre as well as from the cannula surface: the second recording is spike-triggered averaged by the
rst over a number of discharges. The amplitude (ordinate in arbitrary units) is shown versus
recording distance for simulated action potentials recorded with different types of leading-off surfaces.
Note the low amplitude obtained with large electrodes for short electrodebre distance. The curves
for point-shaped and 25 mm electrode practically overlap (modied from Ekstedt & Sta
lberg 1973;
Sta
lberg & Falck 1997, with permission). Filled circle, point-shaped; open square, circular 25 mm; lled
square, circular 100 mm; open circle, ellipsoid 580!150 mm (short diameter along the bre); triangle,
ellipsoid 580!150 mm (long diameter along the bre).

some of these limitations. For example, muscle bre conduction velocity can be
estimated during voluntary contractions with surface electromyography (Farina &
Merletti 2004), whereas it is usually assessed only with electrical stimulation of the
muscle bres with intramuscular systems (Troni et al. 1983).
This review describes the methods used for recording and processing
intramuscular EMG signals.
2. Electrodes for EMG signal detection
Since 1929 when Adrian & Bronk (1929) proposed the concentric needle
electrode, a number of systems for the detection of intramuscular EMG signals
have been developed. The concentric needle electrode detects signals between the
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360

R. Merletti and D. Farina

(a)

(b)
T
B
B
T

P
P

P
1 mV

1 ms

duration
Figure 2. (a) Single bre action potentials do not sum synchronously to form motor unit action
potentials, which thus present multiple phases (P) and turns (T) (reproduced from Sta
lberg &
Falck 1997, with permission). (b) A motor unit action potential showing an abnormal jiggle. Eight
traces are superimposed. Some of the components show an abnormal jitter, also resulting in
vertical shifts. Two components (marked with B) display intermittent blocking. A late component,
satellite (S), is generated by a muscle bre that is either innervated by a slowly conducting
terminal axon or has a slower conduction velocity due to atrophy (reproduced from Trontelj et al.
2004, with permission q (2004) IEEE).

tip of a wire insulated in the cannula and the cannula. Other needle electrodes
have been proposed in more recent times (gure 1) and have been adapted to the
specic algorithms for information extraction. For example, Buchthal et al.
(1957) extended the concentric needle by placing 12 insulated wires in a slot in
the cannula. With this system it was possible to record the motor unit electrical
activity from many points in the muscle, thus analysing the decrease in signal
amplitude with distance and measuring the size of the motor unit territory.
De Luca & Forrest (1972) described the quadripolar needle, consisting of
four detecting surfaces that provide different representations of the same motor
unit activity, thus adding information for the automatic decomposition of the
EMG signal.
The size of needles used to record intramuscular EMG signals is larger than
that of the nearby muscle bres (a concentric needle, for example, has a diameter
of 0.30.5 mm), thus the insertion of the needle damages some muscle bres
generating a small local oedema. In addition, in some cases, the insertion of
needles may unintentionally damage important structures. For example, in a
study on cadavers, Haig et al. (2003) showed that when a needle was inserted into
a muscle according to standard clinical procedures, the tip was in the intended
location in only 45 per cent of the cases and within 5 mm of important structures,
such as nerves, arteries or veins, in 17 per cent of the cases.
The potential distribution in space, and therefore the signal features, is
affected by the presence of the equipotential needle surface (Gootzen et al. 1989;
Theeuwen et al. 1993; Stegeman et al. 1994). The recorded signal amplitude
depends on whether the bre is located at the same or the opposite side of the
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Review. Analysis of intramuscular EMG signals

361

electrodes leading-off surface(s). Simulations indicated that a general decrease


in EMG signal amplitude (whose magnitude depends on the thickness of the
uid layer) should be expected. However, these changes do not seem to be
relevant for diagnostic purposes (Ekstedt & Sta
lberg 1973; Gootzen et al. 1989;
Brownell & Bromberg 2007).
Needle size, type and insertion technique determine the pain or discomfort of
the patient during the insertion (Strommen & Daube 2001). Slight movements
of the concentric needle not only cause pain but modify the action potential
amplitude and area, which vary markedly when the position of the needle
changes within the motor unit territory. The ratio of motor unit action potential
area to amplitude is less affected by changes in electrode position and measures a
duration or thickness of the waveform. This ratio is also less sensitive to the
signal-to-noise ratio and inter-operator differences than other signal features
(Nandedkar et al. 1988).
In the early 1960s, Basmajian proposed wire electrodes for the detection of
intramuscular EMG signals (for review, see Basmajian & De Luca 1985). Wire
electrodes may be made from small diameter, non-oxidizing wires with
insulation. They are placed in the cannula of a needle and bent at the tip; the
needle is inserted into the muscle and then removed, with the wires left in
the muscle. The advantage with respect to needle electrodes is that the wires can
be hardly felt when the needle is removed, thus allowing strong contractions
without discomfort or pain for the subject. However, their position cannot be
adjusted after removal of the needle, whereas a needle electrode can be moved
in the muscle to search for a suitable position. Wire electrodes are usually
preferred in studies in which the EMG signals are recorded over long periods or
during movement, since they are more stable than needle electrodes.
Gydikov et al. (1986) proposed subcutaneous branched electrodes, which
consisted of two isolated parallel wires connected together to prevent relative
displacement between the wires. The isolation of one of the wires was removed at
one point and the isolation of the other wire at two points spaced by 12 mm.
The points of removal of the isolation formed the leading-off areas. The signals
recorded by the rst wire were subtracted to the signals detected by the second
wire (the two uninsulated points of the second wire detect a signal that is the
average of the potentials in the two points). These wires were inserted
subcutaneously by means of a needle and were proven to detect EMG signals
with good selectivity for single motor unit analysis (Gydikov et al. 1986).
The main limitation of wire electrodes is the difculty in placing many
detection sites with consistent site geometry into a single system. Thus, multichannel recordings are usually performed by many wires inserted into the
cannula of a single needle. Recently, indwelling systems made of thin-lm
technology have also been proposed for intramuscular recordings, following
similar technological developments as for neural interfaces. Longitudinal intrafascicular electrodes (LIFEs) are ne wire electrodes designed to be implanted
into peripheral nerves to serve as neural interfaces (Malagodi et al. 1989).
Conventional LIFEs, usually handmade, are constructed using Teon insulated
PtIr wires (Lefurge et al. 1991) or metallized and insulated polyaramid
laments (McNaughton & Horch 1996). The new generation of LIFE systems
consists in microfabricated thin-lm LIFE. Thin-lm technology allows
the design of multiple detection sites with consistent site geometry on an
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362

R. Merletti and D. Farina

extremely exible substrate (Farina et al. 2008). These systems have the
advantage of allowing multi-channel intramuscular electromyography with a
single insertion and with a well-dened and reproducible spatial arrangement of
the detection sites.
A few techniques have been proposed to solve the problem of the very local
nature of the information extracted from intramuscular recordings. The macro
EMG electrode (Sta
lberg 1980; Sta
lberg & Fawcett 1982; g. 1D) consists in a
modied single bre EMG needle where a portion of the isolated cannula is
exposed and acts as a macro electrode. The signal recorded from the macro
electrode is averaged using single motor unit discharges as triggers, as extracted
from the single bre recording. Although the averaged action potentials recorded
using a macro needle electrode (MAEMG), should better represent the
electrical activity of a motor unit, there is a relatively high correlation between
features of the actions potentials detected from concentric needle electrodes
(CNEMG) and MAEMG (Finsterera & Fuglsang-Frederiksen 2000).
Scanning electromyography is another technique based on triggered averaging.
This method provides an electrophysiological cross section of a motor unit
(Sta
lberg & Antoni 1980). Two intramuscular electrodes are used: a single bre
electrode for triggering and a concentric electrode for acquisition, inserted at
least 2 cm away and in the direction of the bres. The muscle is voluntarily
activated and the concentric electrode is connected to a mechanical linear
actuator, controlled by the acquisition system; the concentric electrode is pulled
out in steps of 50 mm or multiples, so that a corridor of approximately 20 mm is
investigated. The signal from the concentric electrode in each position is
averaged using the single bre action potentials as trigger and therefore outlines
the thickness of the motor unit territory in each location and direction of pulling.
3. Intramuscular EMG signal decomposition
Indwelling EMG signal decomposition is the process of identication and
classication of action potentials of individual motor units from the interference
pattern (gure 3). This process is complex owing to the variability in shape of the
action potentials generated by the same motor unit and the overlapping in time
and frequency of action potentials generated by different motor units. The
changes in shape of action potentials are usually limited for isometric constant
force contractions of short duration. For longer recordings, however, it is usually
necessary to update the templates by averaging the last N identied action
potentials to account for changes due to fatigue.
Pioneer work in EMG signal decomposition was accomplished by De Luca and
co-workers (De Luca et al. 1982; LeFever & De Luca 1982; LeFever et al. 1982).
In the last two decades, these and other researchers worked towards a robust
solution to the problem of intramuscular EMG signal decomposition (McGill
et al. 1985, 2005; Stashuk & De Luca 1989; Wellig et al. 1998; Stashuk & Qu
1998; Stashuk 2001; Katsis et al. 2007; Nawab et al. 2008; Marateb & McGill
in press). Although the solutions vary greatly for the need of operators
assistance, complexity and accuracy of the results, and computational time, some
general considerations can be drawn. In general, it is not possible to accurately
decompose EMG signals detected during very high-force contractions (more than
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Review. Analysis of intramuscular EMG signals


quadrifilar
electrode

363

raw EMG (one channel)

decomposition algorithm
muscle
-motor neurons

individual motor unit action


potential trains (MUAPTs)
Figure 3. Schematic representation of the detection and decomposition of intramuscular EMG
signals. The quadrilar needle proposed by De Luca (Basmajian & De Luca 1985) is indicated in the
gure. Three raw interference signals are detected between electrode pairs (only one is indicated in
the gure). The aim of the EMG decomposition algorithm is to identify the motor unit action potential
trains and therefore the discharge times of the motor units which contribute to the interference
signals. Such discharge times represent the control signals provided by the individual motor neurons.

50% of the maximal force). Moreover, the number of identied motor units is
limited to 38, with peaks of 1112 with recent algorithms (Nawab et al. 2008)
or multi-channel recordings (McGill et al. 2005). Despite this limitation,
intramuscular EMG signal decomposition currently offers the possibility of
accurate in vivo analysis of the neural drive to muscles and has allowed the
construction of conceptual models of motor unit control strategies.
In classic approaches, the decomposition of a composite EMG signal requires
two steps of (i) detecting action potentials (segmentation) and (ii) recognizing
detected action potentials as members of a class (classication). For
segmentation, the characteristics that differentiate the action potential shapes
from the background noise should be explored. Various manifestation variables
can be adopted for solving this detection problem, such as amplitude, signal
derivatives, coefcients of a transformation (e.g. wavelet transform). To classify
the detected action potentials, it is essential that the action potentials produced
by the same motor unit are more similar in shape than action potentials
generated by different motor units. The differences in shape should be quantied
(feature space) in order to compare action potentials. Various features have been
used for this purpose, including morphological statistics (e.g. peak-to-peak
voltage, number of phases, duration, number of turns), Fourier transformation
coefcients, coefcients obtained from other transformations (e.g. a wavelet
basis), the time samples of the band-pass ltered signal and the time samples of
the low-pass differentiated signal (for review, see Stashuk 2001).
In most decomposition methods, the rst classication step is performed only
on action potentials that do not overlap in time. The overlapping potentials,
which form compound waveforms that do not repeat (therefore forming classes
with single elements), should be decomposed into the basic single unit potentials.
This operation is usually the most difcult in EMG signal decomposition and
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364

R. Merletti and D. Farina

algorithms often differ in their performance owing to their different sensitivity,


accuracy and ability to resolve superimposed action potentials (Nawab et al.
2008; Marateb & McGill in press).
There are two basic strategies for resolving superimposed action potentials.
The rst is based on matching the action potentials identied in the classication
phase, one at a time, with the superimposed waveform or a residual form of it
until nding the best match. Once the best match is found, a residual waveform
is created, which is the difference between the initial waveform and the identied
action potential. The procedure is repeated until the residual is below an energy
threshold. This strategy is called peel-off or sequential approach. The second
strategy synthesizes superimposed waveform models by adding up combinations
of templates shifted in time by different amounts and searches for an optimal or
acceptable match between a model-superimposed waveform and the actual
combination of action potentials. This method is called modelling approach and,
although it is theoretically capable of resolving all types of superimposed
waveforms, it is computationally demanding. More details can be found in
Sornmo & Laguna (2005), LeFever et al. (LeFever & De Luca 1982; LeFever
et al. 1982) and Stashuk et al. (Stashuk & Qu 1998; Stashuk et al. 2004).
The verication of the accuracy of an intramuscular EMG signal decomposition
requires the availability of a gold standard for which the decomposition result is
known a priori and the denition of quantitative indexes that allow comparison
of performance (Farina et al. 2001a,b). The reference result can be obtained by
manual decomposition of a number of experimental signals by expert operators, if
it can be assumed that these decompositions are (almost) error free. Alternatively,
it is possible to independently decompose two signals that comprise the activity of
the same motor units but are detected from different locations in the muscle. The
results of the two independent decompositions can then be compared. The
probability of incorrectly decomposing the two signals and yet obtaining the same
discharge pattern for a given motor unit is very small, thus when the two
decomposition results agree the decomposition is considered correct. Finally, the
reference signal for testing performance can be obtained from a mathematical model
that includes all the relevant characteristics of experimental signals, either by
generating action potentials or by combining experimental action potentials. Each
of these approaches has limitations that currently cause difculties in comparing
different algorithms and thus in selecting a standard decomposition algorithm.
4. Spike-triggered averaging
Once the signal has been decomposed, all control properties of the identied
motor units can be directly measured, such as recruitment and derecruitment
thresholds, discharge rate and interspike interval variability. In addition, with
the joint recording of other signals, such as force and surface EMG signals,
contractile and bre membrane properties can be measured.
The joint recording of intramuscular and surface EMG signals may be useful
to investigate peripheral and control properties of the neuromuscular system.
The discharge times identied from the intramuscular EMG signals are used
to trigger the averaging of the surface EMG signal and thus to estimate the
surface representation of the single unit action potentials. From the surface
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Review. Analysis of intramuscular EMG signals


channels 1 8
(a) insulated
intramuscular single differential
wires amplifiers
electrode array

V1

V2

V3

V4

V5

V6

V7

V8

+ +

subcutaneous tissue (fat)

skin
muscle tissue
3 fibre
motor unit

uron

depolarized zone

tor ne

-mo

uninsulated
wire tips

(b)

innervation zone

intramuscular
signals

ch 1

MU1
ch 1

MU2
2 ms

surface signal array 1


ch 15
surface signal array 2

ch 15

0.5 mV 5 ms

Figure 4. (a) Schematic (not in proper scale) of a motor unit, of a pair of intramuscular wires and of
a surface electrode array, (b) intramuscular signal from two motor units (each line is the average
of 20 discharges obtained from decomposition of the wire recordings) and spike-triggered averages
of signals recorded from an electrode array placed on the skin on one side of the innervation zone of
the muscle. Each set of surface signals is the spike-triggered average of 20 discharges (120, 221,
322, etc.) to show the moving average of the surface multichannel action potential during a
sustained contraction. Muscle: tibialis anterior. Contraction level: 25% MVC. Interelectrode
distance of the surface array: 5 mm ( modied from Farina et al. 2002, with permission).

action potentials, motor unit properties, such as muscle bre conduction


velocity, can be measured (Farina et al. 2002; gures 4 and 5). Surface recordings can also be used jointly with intramuscular recordings to enlarge the
number of motor units that are concurrently investigated (Holobar & Zazula
2004). Spike-triggered averaging is also applied to the joint torque for estimating
the torque contribution of individual units (Stein et al. 1972), although the
approach has several limitations (Taylor et al. 2002).
5. Interference signal analysis
In clinical practice the precise decomposition of intramuscular EMG signals has
still limited applications, owing to the difculties in accurate electrode placement
and proper interpretation of the results by the clinician. In the diagnosis of
neuromuscular disorders, the shape of motor unit action potentials recorded with
intramuscular electrodes is often used to differentiate pathological versus healthy
conditions. In most cases, the signal is not fully decomposed but rather analysed
as an interference signal and characterized by global descriptors, or only a few
representative action potentials are extracted. The turns and amplitude analysis
is an example of these methods (Fuglsang-Frederiksen 1981). A turn in the EMG
signal is dened as a change in the slope sign, with some special features (e.g. the
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R. Merletti and D. Farina


(b)

(c) 4.3
4.2
4.1
4.0
3.9
3.8
3.7
3.6
3.5

(d)

CV (m s 1)

discharge rate (pps)

(a) 20
18
16
14
12
10
8
6
4
2
0

20

40

60 80 100 120
time (s)

20

40 60 80 100 120
time (s)

Figure 5. (ad ) Estimated discharge rates and conduction velocity of two motor units during 120 s
recordings using the technique described in gure 4. Discharge rates are obtained from wire signals,
whereas conduction velocity is estimated from the surface electrode array ( reproduced from Farina
et al. 2002, with permission).

maximum and minimum slope, the separation between turns, etc.) to distinguish
a true turn from noise. The portion of signal included between two subsequent
turns is referred to as a segment and described by its duration and amplitude.
Other parameters, such as the number of turns per second, mean segment
duration and amplitude, spectral variables (e.g. mean or median frequency and
spectral moments), and coefcients of wavelet expansions are also applied.
Number and amplitude of turns as well as other variables are often reported in
scatter plots versus time or force and compared with typical plots of healthy or
pathological subjects for diagnostic inference and classication of disorders.
This work was supported by grants provided by the European Community (CyberManS, contract
no. 016712), the European Space Agency (MESM, contract no. 15097/01/NL/SH), the Italian
Space Agency (OSMA), and the Bank Foundations Compagnia di San Paolo and Fondazione CRT.

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