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Surface Electromyography to Study Muscle

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Surface Electromyography to Study Muscle
Coordination

Franois Hug and Kylie Tucker

Abstract
Electromyography (EMG) records the electrical activity that is generated as
action potentials propagate along the length of muscle bers. As such surface
EMG is the research tool that is used in a vast majority of the works that assess
muscle coordination in health and disease. Although surface EMG recordings can
provide valuable information regarding the neural activation of a muscle by the
nervous system, there are multiple factors that need to be considered to ensure
that the interpretation of the data is accurate. In this chapter, we have highlighted
crosstalk, signal cancellation, normalization, computation signal, detection of
the onset/offset times, and the misinterpretation of EMG to infer torque as six of
the most signicant factors that need to be considered when recording and then
interpreting EMG data. These factors need to be considered before data is
collected, to determine if EMG is the right tool and/or which processing methods
may best provide insight into the research question.

Keywords
EMG Motor control Force Torque Force sharing Crosstalk Signal
cancellation Normalization Movement Pattern Prole Activation Motor
unit Electrodes Contraction

F. Hug (*)
Laboratory Movement, Interaction, Performance (EA4334), University of Nantes, Nantes, France
NHMRC Centre of Clinical Research Excellence in Spinal Pain, Injury and Health, School of
Health and Rehabilitation Sciences, The University of Queensland, Brisbane, QLD, Australia
e-mail: francois.hug@univ-nantes.fr
K. Tucker
NHMRC Centre of Clinical Research Excellence in Spinal Pain, Injury and Health, School of
Health and Rehabilitation Sciences, The University of Queensland, Brisbane, QLD, Australia
School of Biomedical Sciences, The University of Queensland, Brisbane, QLD, Australia
e-mail: k.tucker1@uq.edu.au

# Springer International Publishing AG 2016 1

B. Mller, S.I. Wolf (eds.), Handbook of Human Motion,
DOI 10.1007/978-3-319-30808-1_184-1
2 F. Hug and K. Tucker

Contents
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
State-Of-The-Art . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
Factors that Will Inuence the Recorded Surface EMG Signal . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
Crosstalk . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
Signal Cancellation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
EMG Processing to Assess Muscle Coordination Strategies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
Normalization of the EMG Amplitude . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
From the Raw EMG Signal to the EMG Prole . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9
Sequence of Activation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11
Some Basic Misinterpretations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13
EMG Amplitude Is Not Muscle Force/Torque . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13
EMG Onset Is Not Torque Onset . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14
Relationship Between Muscle Activation and Muscle Torque-Generating Capacity . . . . . . . 14
Neuromuscular Fatigue Cannot Be Accurately Determined by Changes in EMG
Amplitude . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16
Concluding Remarks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17
Cross-References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18

Introduction

Movement is critical for our successful interaction with the world. Movement
facilitates basic and vital functions, as well as complex daily activities. However,
understanding how movement is controlled remains one of the main challenges for
many scientic elds. Part of the underlying complexity of human movement
originates from redundancy within our musculoskeletal system. Coordination
between multiple effectors at different levels (e.g., between limbs, between joints,
between individual muscles, and perhaps even between regions of a muscle) is
required to achieve the vast majority of motor tasks, even those considered the
simplest of tasks. As such, many different muscle coordination1 strategies are
theoretically possible to achieve the same goal (Bernstein 1967); although recent
works provide evidence that the range of strategies used is much smaller than
possible given the redundant nature of our motor control system (Valero-Cuevas
et al. 2015). This is because the coordination strategies used depend largely on neural
and mechanical constraints (Valero-Cuevas et al. 2015). A comprehensive under-
standing of muscle coordination has direct applications in robotics, ergonomics, and
human movement sciences, as well as informing the development of innovative and
individualized prevention and rehabilitation strategies for people with physical
disability.
In the simplest form, for a muscle to produce torque, the muscle bers within a
single motor unit (that comprises of a motoneuron, its motor axon, and all of the

1
Here we consider muscle coordination as the distribution of muscle activation or force among
individual muscles to produce a given motor task.
Surface Electromyography to Study Muscle Coordination 3

muscle bers it innervates) must receive a neural command (an action potential)
from their motoneuron. In healthy individuals, there is a one-to-one relationship
between the generation of an action potential in the motoneuron and the generation
of an action potential in the innervated muscle bers. The generation of this motor
unit action potential begins the physiological process of actin and myosin cross-
bridge attachment within the muscle ber sarcomeres and is therefore directly related
to the production of force. As electromyography (EMG) records the electrical
activity that is generated as action potentials propagate along the length of muscle
bers, EMG is the research tool that is used in a vast majority of the works that assess
muscle coordination in health and disease. Although surface EMG recordings can
provide valuable information regarding the neural activation of muscle, there are
many factors that can inuence the recorded signal. Further, there are important
limitations to consider when interpreting EMG recordings within a laboratory or
clinical environment.

State-Of-The-Art

In studies focusing on muscle coordination, noninvasive recordings through surface

electrodes are generally preferred to the invasive ne-wire recordings. This is
primarily because the volume of muscle from which signals can be recorded is
relatively small when using ne-wire electrodes and thus may not be representative
of the whole muscle. Further, the insertion of ne-wires is invasive and thus requires
appropriate training of the operators, and ne-wires may cause discomfort during
movement (although this is not common). Surface EMG recordings remain the most
common technique used to provide insight into muscle coordination, and as a
consequence, the present chapter will summarize works using primarily this
modality.
The recorded EMG signal represents the summation of all of the motor unit action
potentials that are present at a given time, within the region of muscle from which the
electrical activity can be detected given the recording electrode conguration, i.e.,
the electrode recording zone (Fig. 1). The motor unit action potentials that are being
recorded may be generated from muscle bers at various distances from the elec-
trode, and the shape of each motor unit action potential is distorted by the low-pass
ltering effect of the volume conductor, i.e., the surrounding tissue.
The signal-to-noise ratio is an important factor to consider when recording
surface EMG signals. It describes the ratio of the energy of the real EMG signal
relative to the energy of the unwanted signals (i.e., the noise) within the recording.
This noise may originate from various sources such as (i) electromagnetic radiations
from the external environment, (ii) the electronic components of the recording
equipment, or (iii) movements of the recording electrodes or cables, i.e., motion
artifacts. Noise in the signal may also originate from within the body, with the
heartbeat often observed in surface EMG recordings of trunk, back, and some limb
muscles. Any noise within the recording can result in an alteration of the amplitude
and the relative contribution of the frequency components of the recorded signal.
4 F. Hug and K. Tucker

Fig. 1 Generation of the surface EMG signal. The single motor units receive a neural command
from their motoneuron, leading to the generation of muscle ber action potentials. The recorded
EMG signal represents the summation of all of the motor unit action potentials that are present at a
given time, within the region of muscle from which the electrical activity can be detected given the
recording electrode conguration. MU motor unit

Much of the noise from an EMG signal can be reduced by applying appropriate
lters [e.g., high-pass lter at 20 Hz; (De Luca et al. 2010)].
EMG ampliers have greatly evolved over the last 30 years such that an excellent
signal-to-noise ratio is now more regularly observed. In addition, recent mobile/
wireless systems have reduced the potential for movement artifacts, in part by
removing the wires/cables and by using pre-ampliers embedded within the elec-
trodes. New technologies, such as screen printing of recording electrodes on a soft
support (Fig. 2), are being used to improve the recording quality of a surface EMG
signal by improving skin to electrode contact and thereby reducing impedance
(Bareket et al. 2016). Such a system might allow for long-term recordings offering
new applications to EMG such as activity monitoring throughout a 24-h (or longer)
period.

Factors that Will Influence the Recorded Surface EMG Signal

Surface EMG signals are inuenced by many physiological (e.g., ber membrane
properties, motor unit properties) and nonphysiological factors (e.g., detection
system, conductivity of the tissue) [for review, see Farina et al. (2004)]. Although
the inuence of some of these factors on the recorded signal can be overcome by
following recommendations for recording EMG (e.g., SENIAM project: http://www.
seniam.org/), others cannot be overcome when using traditional surface EMG
recordings. When designing a study and interpreting the results, we believe that
crosstalk and signal cancellation represent the two most signicant factors that need
to be considered.
Surface Electromyography to Study Muscle Coordination 5

Fig. 2 Example of temporary tattoo for long-term EMG recordings. (a) Fabrication scheme.
(b) Electrodes placed on a hand. (c-top) EMG recording of the rst dorsal interosseous (electrode
1 versus 3). Arrows indicate (1) rest position followed by (2) force application (isometric contrac-
tions) on the rst dorsal interosseous for 2.5 s and 1 s (repeated three times). (3) Flexion of the index
nger toward the thumb, (4) from the thumb, and (5) pointing up. (c-bottom) electrode 1 versus
6. (d) Same as (c), 3 h after placement (From Bareket et al. (2016))
6 F. Hug and K. Tucker

Crosstalk

Crosstalk is dened as the contamination of the EMG signal by the myoelectric

activity generated in a nearby muscle. For example, crosstalk has been demonstrated
between leg muscles (tibialis anterior and peroneus longus) during gait (Campanini
et al. 2007). This study showed that the shape of the EMG signal recorded over the
tibialis anterior muscle varied depending on the location of the electrodes. More
precisely, the electrodes placed closer toward the boundary of the peroneus longus
recorded a second burst of activity that was not present in the other locations. This
burst likely originated from the peroneus longus. Such an effect of crosstalk on the
EMG signals could explain, at least in part, the high variability of activation proles
of the lower leg muscles often reported between participants during pedaling (Hug
et al. 2008, 2010) or during gait (Guidetti et al. 1996); although true differences in
the motor patterns of individuals are also highly possible.
In more extreme cases, crosstalk can make a muscle appear to be generating
myoelectric activity when it is not. For example, during quiet breathing, Chiti et al.
(2008) observed signicant myoelectrical activity recorded by surface EMG elec-
trodes placed over the sternomastoid muscle when ne-wire recordings inserted
within the same muscle recorded no activity. More recently, an EMG amplitude of
approximately 20% of the maximal amplitude observed during a maximal
plantarexion was recorded from the plantarexor muscles when they acted as
antagonists during a maximal dorsiexion. This signicant EMG amplitude was
recorded while no other evidence of an active contraction of the plantarexor
muscles was detected through ultrasound imaging (Raiteri et al. 2015) or
elastography (Raiteri et al. 2016).
Crosstalk remains one of the most important sources of error in interpreting
surface EMG because (i) it is difcult to quantify the amount of crosstalk by
noninvasive methods, and (ii) while crosstalk can be reduced, it cannot be totally
removed (Farina et al. 2004). Although cross-correlation has been used to quantify
crosstalk (Winter et al. 1994), results from simulation provided evidence that this
method is not accurate (Lowery et al. 2003). Attempts to quantify crosstalk using
selective electrical muscle stimulation have also been made (De Luca and Merletti
1988). However, due to the different strategies of motor unit recruitment between
voluntary and electrically elicited contractions, results obtained through application
of electrical stimulation may not be easily extended to voluntary contractions
(Lowery et al. 2003). As an accurate method to quantify crosstalk does not exist,
efforts should be made to minimize its inuence on the recorded EMG signal. To this
end, a double-differential electrode conguration (van Vugt and van Dijk 2001)
associated with a low skin-electrode impedance (Mesin et al. 2009) is recommended.
Crosstalk may be further reduced by a proper localization of the surface electrodes
on the muscle (Hermens et al. 2000) and reducing the inter-electrode distance. Care
should be taken to place the electrodes in the center of the belly of the muscle, away
from the borders, although this may be challenging for the smaller muscles. Most
Surface Electromyography to Study Muscle Coordination 7

importantly, if it remains likely that crosstalk will inuence the data being recorded,
this should be acknowledged within the manuscript discussion and reected in the
conclusions drawn.

Signal Cancellation

Signal cancellation refers to the cancellation of positive and negative phases of

motor unit action potentials (Farina et al. 2004). As such, estimation of EMG
amplitude from a raw EMG signal is less than that obtained by summing the
amplitudes of the individual motor unit action potentials. Signal cancellation can
lead to an underestimation of the neural drive by up to 62 % of maximal drive, during
a maximal voluntary contraction (Keenan et al. 2005). This phenomenon therefore
confounds the interpretation of neural drive from absolute EMG amplitude. Impor-
tantly, signal cancellation is also increased with fatigue (Keenan et al. 2005). This is
because the conduction velocity of the motor unit action potentials along muscle
bers decreases as the muscle fatigues, and therefore the duration of the action
potentials increases. This increased duration leads to greater overlap between poten-
tials recorded. That means that the increase in drive with fatigue (and therefore the
greater number of motor unit action potentials) is likely to be underestimated if
considering only the amplitude of the EMG signal. Signal cancellation can therefore
partly explain why EMG amplitude at the end of the limit time to exhaustion remains
signicantly lower than that measured during an isometric maximal voluntary
contraction (Fuglevand et al. 1993).

EMG Processing to Assess Muscle Coordination Strategies

Given that muscle coordination may be dened as the distribution of muscle

activation or force among individual muscles to produce a given motor task,
studying muscle coordination with EMG should address one or both of the following
questions: (i) Which muscles are active and what is the magnitude of this activation?
(ii) When are these muscles active during the task being performed?

Normalization of the EMG Amplitude

Amplitude of the EMG signal is one of the most straightforward and commonly used
measures of muscle activation. Normalization of EMG amplitude is a generally
considered a requirement for studies that aim to compare the level of activation
between muscles or between participants (Winter and Brookes 1991; Soderberg and
Knutson 2000). To this end, EMG amplitude is often expressed relative to that
measured during a brief isometric maximal voluntary contraction (IMVC) performed
at a given muscle length (Dubo et al. 1976; Arsenault et al. 1986). However, there are
multiple limitations to this method that must be considered. First, the region of
8 F. Hug and K. Tucker

muscle under a surface electrode will change when the length of a muscle changes,
e.g., during dynamic contractions or during isometric contractions at different joint
angles. To illustrate this point, amplitude of an M-wave (muscle compound action
potential) recorded using surface electrodes is affected by joint position and thus
muscle length (Frigon et al. 2007). Second, the ability to voluntarily activate some
muscles is inuenced by joint angle/muscle length. For example, maximal voluntary
activation of the quadriceps muscle is higher when the knee is positioned at 90
compared to a more exed or more extended position (Becker and Awiszus 2001).
However this length-dependent change in voluntary activation is not observed for
other muscle groups such as the biceps brachii (Leedham and Dowling 1995).
Therefore, the maximal EMG amplitude recorded during an IMVC performed at a
specic muscle length does not systematically represent the maximal EMG ampli-
tude that would be obtained at other muscle lengths. This is in line with EMG
amplitude values higher than that obtained during the IMVC that are often observed
during a dynamic task. For example, Hautier et al. (2000) reported an activity level
of 126.2% IMVC for Vastus lateralis during a brief maximal pedaling exercise, and
Jobe et al. (1984) reported an EMG activity up to 226% IMVC during a baseball
pitch. In addition to the region of muscle being recorded changing with changes in
muscle length, and the ability to fully activate a muscle changing with joint angle
limiting the usefulness of this normalization method for some studies, it is important
to consider the time required to obtain reliable IMVCs. Not all participants have the
same ability to maximally activate their muscles during standardized tasks (Dorel
et al. 2012), and some participants require repeated training sessions to be able to
produce a consistent IMVC. This is particularly problematic in clinical populations
as pain may be associated with decreased voluntary drive during maximal tasks
(Salomoni et al. 2016). It is therefore recommended to verify that participants
produce true maximal efforts by using the twitch interpolation technique (Hug
et al. 2015a). Further, muscle coordination is often studied by recording a large
number of muscles simultaneously, and as such IMVCs must be performed on each
muscle/muscle group with adequate rest time given between each maximal
contraction.
To reduce the time needed for the normalization procedures and to consider the
specicity of the dynamic task, some authors suggested normalizing EMG amplitude
to that measured during a maximal dynamic exercise similar to the task being
studied. For example, Rouffet and Hautier (2007) recommended the normalization
of the EMG amplitude measured during a submaximal cycling task to that measured
during an all-out sprint cycling task. This approach makes the assumption that an
all-out sprint requires maximal muscle activation, which is true for some but not all
muscles (Dorel et al. 2012). Indeed, while the quadriceps muscle group is maximally
activated during an all-out cycling sprint, hamstrings and hip extensors are not
(Dorel et al. 2012). Furthermore, not all of the participants have the same ability to
maximally activate all the muscles during such a specic exercise (Dorel et al. 2012).
This latter point is important because it could lead to misinterpretations of the
interindividual variability of the normalized EMG values.
Surface Electromyography to Study Muscle Coordination 9

Submaximal isometric or dynamic tasks are also used to normalize the EMG
signal (Dankaerts et al. 2004; Chapman et al. 2010). The underlying assumption is
that the relationship between muscle activation and contraction intensity is linear,
such that 20% of maximal EMG amplitude should correspond to 20% of maximal
force. Despite being true for some muscles during specic tasks [e.g., exor
digitorum interosseous during isometric abduction of the index nger; (Lawrence
and De Luca 1983)], there is considerable evidence that the relationship between
muscle activation and joint torque is not linear for other muscles such as the biceps
brachii and the deltod (Lawrence and De Luca 1983). This is because contribution
of individual muscles to the joint torque may change with contraction intensity
during a task in which multiple synergist muscles are involved (Bouillard et al.
2012). As a consequence, normalization to submaximal tasks may lead to misinter-
pretation of the role of some muscles in a given task, as illustrated in Fig. 3. The
submaximal normalization method is further compromised when used in studies that
include clinical populations as the motor coordination strategies used to complete
submaximal tasks are often altered in people with pain and/or musculoskeletal
disease (Hodges and Tucker 2011; Hodges et al. 2013).
In summary, when focusing on submaximal isometric contractions, accurate
information regarding the level of muscle activation can be obtained by normalizing
the EMG amplitude to that measured during an IMVC performed at the same muscle
length. However, it is more challenging when studying a dynamic task for which
there is no agreement on the best normalization procedure to be used (Burden and
Bartlett 1999). Importantly, information about the level of muscle activation is not
always needed. To study the shape of the EMG envelope, to determine muscle
activation timing, or to extract muscle synergies, EMG signals can be normalized
to the peak [named peak dynamic method; (Ryan and Gregor 1992)] or to the mean
[named mean dynamic method; (Winter and Yack 1987)] value measured over a
cycle. Despite being appropriate for these purposes, these normalization procedures
provide no information about the degree of muscle activation relative to the maximal
muscle activation.

From the Raw EMG Signal to the EMG Profile

During isometric tasks, muscle coordination can be assessed by determining the

distribution of activation between muscles. To this end, the normalized EMG
amplitude is averaged over a given time period to provide a representative EMG
amplitude value for the task being performed. However, when focusing on a
dynamic task, the mean EMG amplitude over a cycle or a specic part of the
movement may conceal important information about coordination strategies. As
illustrated in Fig. 4, two EMG signals obtained in two different conditions may
exhibit the same mean EMG amplitude over the cycle, while the EMG proles
demonstrate some alterations in coordination strategies. For a deeper understanding
of muscle coordination strategies during dynamics tasks, the computation of the
linear envelope and the EMG prole is therefore recommended.
10 F. Hug and K. Tucker

Fig. 3 Drawbacks associated with the normalization of EMG amplitude to submaximal

values. Here we have the theoretical relationship between EMG amplitude and muscle force for
two muscles (red and blue). If EMG measured during a contraction performed at 60% of maximal
joint torque is normalized to that measured at 20% of maximal joint torque, the muscle in red would
exhibit a normalized EMG amplitude of 300%, and the muscle in blue would exhibit a normalized
EMG amplitude of 600%. However, the muscle in blue would be actually activated at a much lower
intensity. This is because of a different EMG amplitude-force relationship of these muscles. Note
that this same limitation exists between individuals for the same muscle (i.e., red and blue lines
could represent the same muscle but from different individuals) as it does between muscles within
an individual

To represent the linear envelope, the raw EMG signal is generally rectied and
low-pass ltered (Kleissen 1990; Shiavi et al. 1998; Hug and Dorel 2009). One
major methodological consideration when computing linear envelope of the EMG
signal is the choice of the smoothing level (Hug et al. 2012), which is mainly
determined by the low-pass cutoff frequency, the movement velocity, and to a lesser
extent, by the number of cycles that are averaged (Fig. 5). In biomechanical studies
that use EMG as an estimate of muscle force, a relatively low cutoff frequency
(below 410 Hz depending on the movement velocity) is often used. However, the
choice of the low-pass lter is less trivial in neurophysiological studies where EMG
is used as an indicator of the input to the motoneurons. The level of smoothing
should be chosen such that there is a neurophysiological basis for interpreting the
EMG linear envelope. A wide range of low-pass lters has been used in the literature,
e.g., from 3 Hz in Winter and Yack (1987) during walking to 40 Hz in Guidetti et al.
(1996) during running. Results from Shiavi et al. (1998) suggested that a cutoff
frequency of about 9 Hz is appropriate for gait analysis at fast walking speed (about
1.8 m.s 1). The logic behind this recommendation is that the frequency of muscle
control cannot lie outside the frequency of movement. It means that to compare the
linear envelope of a movement performed at different velocities, the low-pass lter
Surface Electromyography to Study Muscle Coordination 11

Fig. 4 EMG proles obtained during a pedaling task. The two EMG proles were obtained
from the same muscle in two different experimental conditions and are depicted as a function of
crank angle. Although the EMG amplitude averaged over the cycle does not change between
conditions (dashed lines), the EMG proles exhibit some differences demonstrating an alteration
of muscle coordination strategies. This example demonstrates that mean EMG amplitude value may
conceal important information about coordination strategies

should be adapted to each velocity condition. For instance, considering that 9 Hz is

appropriated for a cycle movement performed at 1.8 Hz, 5 Hz should be used for a
slower cycle movement performed at 1 Hz.
The EMG prole is calculated by ensemble averaging the linear envelope for a
number of cycles or trials (Shiavi et al. 1981; Hug and Dorel 2009; Hug et al. 2010).
First, mechanical events (e.g., foot switches, force signal) are used to determine the
start and the end of each cycle. Second, the cycles interpolated such that they have an
equal number of points. Finally, all the interpolated cycle are averaged together. Note
that this averaging process may also improve the signal-to-noise ratio by reducing
the amplitude of occasional or noisy events that is not occurring in synchrony with
the motor task being performed (Bruce et al. 1977).

Sequence of Activation

Clinical interpretation of EMG signals is often based on the determination of the onset
and offset times. For example, delayed EMG onset of the medial head of the quadriceps
relative to the lateral head of the quadriceps (of 20 ms) has been reported in individuals
with patellofemoral pain during various tasks such as stepping (Crossley et al. 2002) and
postural tasks (Cowan et al. 2002). This delayed activity of the medial head is thought to
contribute to patellar maltracking and development of patellofemoral pain.
There are various methods that can be used detect EMG onset and offset time. The
most common method used involves determining at what time the EMG amplitude
increases past a pre-determined EMG amplitude threshold. This threshold is often xed
12 F. Hug and K. Tucker

Fig. 5 Individual example

of the inuence of the
low-pass cutoff frequency on
the EMG envelope. Three
low-pass lters (4, 10, and
15 Hz) were applied on a
rectied EMG signal recorded
during pedaling. This example
highlights the effect of the
low-pass lter on the
smoothing level of the EMG
envelopes (From Hug et al.
2012 reproduced with
permission from Elsevier)

at 1525% of the peak EMG or 1, 2, or 3 standard deviations above the baseline EMG
amplitude measured during a resting condition (Staude 2001). This threshold method is
also often associated with a minimum duration criterion during which the EMG
amplitude must remain above the threshold. Despite being easy to implement in
processing routines, this method provides results that are highly dependent on the
signal-to-noise ratio and the choice of the amplitude/duration thresholds. As such
comparisons between studies may be difcult. To overcome these drawbacks, more
complicated statistical methods have been developed to differentiate EMG from back-
ground noise (Staude and Wolf 1999). Further, because EMG frequency content
changes occur at the onset of muscular activation, other methods based on local analysis
of the EMG frequency content using wavelet transform have been proposed (Merlo
et al. 2003). Li and Aruin (2005) proposed a method that takes advantage of the Teager-
Kaiser energy operator (TKEO) to decrease the background noise of the signal.
Although this method shows a higher accuracy than classical methods when the signal-
to-noise ratio of the raw EMG signal is low, it does induce a time delay of the onset
detection of about 20 ms (Li and Aruin 2005).
Although numerous automatic methods have been proposed to detect EMG onset/
offset times, it should be kept in mind that they provide different outcomes (Fig. 6). As
such, care should be taken when comparing results obtained with different methods.
Further, as proposed by Hodges and Bui (1996), visual inspection of the detected onset/
offset times remains important following any automatic detection process, to reduce the
potential for an unusual occurrence of artefact/noise in the EMG signal to inuence the
reported data.
Surface Electromyography to Study Muscle Coordination 13

Fig. 6 Example of EMG onset detection obtained using different automatic methods. The raw
EMG signal recorded during an elbow exion was rectied and subsequently smoothed with a
50-Hz, fourth-order zero-lag low-pass Butterworth lter. Different automatic methods were used to
detect the onset time. The results greatly differ depending on the detection method used. SD
standard deviation

Some Basic Misinterpretations

EMG Amplitude Is Not Muscle Force/Torque

A strong linear relationship between EMG amplitude and joint torque has been
demonstrated for some (but not all) muscles (Lawrence and De Luca 1983). Because
of this, EMG amplitude normalized to a maximum voluntary isometric contraction is
often considered as an index of torque. As such, if two synergist muscles A and B are
activated at 30% and 70% of their maximum, respectively, it is often assumed that
muscle B contributes more than muscle A to the global joint torque. However,
beyond limitations inherent to the surface EMG technique to accurately quantify
neural drive, muscle torque cannot be inferred from only neural drive. This is
because torque also depends on several biomechanical factors such as the physio-
logical cross-sectional area (PCSA), the force-length and force-velocity relation-
ships, the specic tension, and the moment arm. For example, for the same activation
level, a muscle with a bigger PCSA will produce more force than a smaller muscle.
In addition, because of the well-known force-length and force-velocity relationship,
higher muscle force can be produced for the same activation level if the muscle
operates at a more optimal length and/or velocity. Although moment arms and PCSA
can be estimated through imaging techniques, in vivo estimation of both the specic
tension (maximal force per unit area) and force-length and force-velocity relation-
ships is not a trivial task. This is mainly because there is no experimental technique
to estimate individual muscle force (Erdemir et al. 2007).
14 F. Hug and K. Tucker

EMG Onset Is Not Torque Onset

As mentioned above, there is some evidence that the relative onset of muscle
activation is altered in people with painful musculoskeletal conditions. For example,
there is a positive correlation between delayed onset of vastus medialis EMG
compared to vastus lateralis EMG during gait, and the magnitude of patella tilt
observed with MRI during weight bearing, in a subgroup of people with
patellofemoral pain who were classied as having abnormal patella tilt (Pal et al.
2011). However, the classical interpretation that altered EMG onset is associated
with altered onset of torque production requires some considerations (Fig. 7). First,
the onset of the recorded EMG signal is dependent on both the onset of muscle
activation and the time it takes for the motor unit action potentials to reach the
recording volume (Hug et al. 2011). EMG onset is therefore dependent on the
position of the recording electrodes relative to the muscles motor point. Assuming
an average conduction velocity of the action potentials of 5 m/s, for every 1 cm the
recording electrodes are from the motor point, a 2 ms delay will be erroneously
introduced into the recorded data. Second, there is also a time lag (referred to as
electromechanical delay) between onset of neural drive to a muscle and torque
production. This electromechanical delay depends on both electrochemical (e.g.,
excitation-contraction coupling) and mechanical (e.g., force transmission along the
connective tissues) processes that can greatly vary between muscles and individuals
(Nordez et al. 2009). Taking the aforementioned example of patellofemoral pain, the
relatively small delayed onset of vastus medialis EMG compared to vastus lateralis
(about 20 ms), and the highly variable nature of this outcome measure as reported
between studies could be explained by different electrode positioning in respect to
the motor points and/or different electromechanical delay between the muscles (Hug
et al. 2015b).

Relationship Between Muscle Activation and Muscle Torque-

Generating Capacity

The two previous paragraphs emphasize the need to consider the torque-generating
capacity of individual muscles for biomechanical interpretation of the EMG signal.
Surprisingly, little is known about the coupling between muscle activation and
muscle torque-generating capacity. There is preliminary evidence that the mechan-
ical advantage of a muscle (due to its moment arm) and the neural drive it receives
during a voluntary task are coupled (De Troyer et al. 2005; Hudson et al. 2009). For
example, respiratory-related muscles such as the intercostal muscles are recruited
during the breathing cycle according to their relative mechanical advantages
(De Troyer et al. 2005). Similarly, during a task where the mechanical advantage
of the exor digitorum interosseous is increased by modifying thumb position and
thus the moment arm, there is an adaptive increase in the neural drive to that muscle
(Hudson et al. 2009). However, it remains unclear how the nervous system accounts
for the force-generating capacity of individual agonist muscles surrounding the same
Surface Electromyography to Study Muscle Coordination 15

Fig. 7 Schematic representation of the inuence of electromechanical delay on the onset of

force production. (a) The time lag between onset of myoelectrical activity and force production
(electromechanical delay) reects both electrochemical processes (i.e., synaptic transmission,
excitation-contraction coupling) and mechanical processes (i.e., force transmission along the
muscle and tendon). (b) Although the electromechanical delay has been shown to be similar
between the VM and VL in pain-free participants (about 25 ms), longer delay has been reported
in the VM (about 38 ms) than in the VL (about 18 ms) in people with patellofemoral pain (Chen
et al. 2012). With consideration of this difference, this example illustrates that an absence of
difference of EMG onset times might still lead to difference in onset of force production. VL vastus
lateralis, VM vastus medialis (From Hug et al. 2015b reproduced with permission)

joint. There are three possible alternatives for how neural drive of synergists may be
regulated (Fig. 8):

1. Neural drive is adjusted to balance force between synergist muscles of differing

force-generating capacities; thus the muscle with the lower force-generating
capacity would receive greater neural drive.
2. Neural drive is targeted to reduce the overall energy cost; thus the muscle with the
higher force-generating capacity would receive greater drive.
3. There is no relationship between neural drive and force-generating capacity.
16 F. Hug and K. Tucker

Fig. 8 Relationship between the neural drive and force-generating capacity (determined here
from muscle physiological cross-sectional area, PCSA). There are three possible alternatives for
how neural drive of synergists may be regulated: (1) neural drive is adjusted to balance force
between synergist muscles of differing force-generating capacities; thus the muscle with the lower
force-generating capacity would receive greater neural drive (panel 1); (2) neural drive is targeted to
reduce the overall energy cost; thus the muscle with the higher force-generating capacity would
receive greater drive (panel 2); or (3) there is no relationship between neural drive and force-
generating capacity (panel 3)

Hug et al. (2015a) determined the relationship between the ratio of activation
during an isometric task and the ratio of muscle force-generating capacity between
two synergist muscles [vastus lateralis (VL) and vastus medialis (VM)]. Neither
force capacity nor activation was balanced between VL and VM. There was a strong
correlation between the ratio of VL/VM EMG amplitude and the ratio of VL/VM
PCSA. These results provided evidence that muscle activation is biased by muscle
force-generating capacity; the greater the force-generating capacity of VL compared
to VM, the stronger bias of the activation to the VL. Despite providing evidence of a
positive relationship between neural drive and muscle force-generating capacity,
these results cannot explain the origin of this relationship. It is possible that an
individuals muscle morphology and architecture underlies the relationship, such
that the nervous system develops/adapts optimally to bias drive to the muscle with
larger physiological cross-sectional area. Alternatively, muscle coordination strate-
gies may underpin muscle morphology and architecture, such that the muscle with
greater drive leads to biased development of PCSA.

Neuromuscular Fatigue Cannot Be Accurately Determined by

Changes in EMG Amplitude

If we consider a submaximal force-matched task that involves only one muscle (e.g.,
little nger abduction or index nger abduction), an increase in the EMG amplitude
may be considered as a sign of neuromuscular fatigue. In this case, the increased
Surface Electromyography to Study Muscle Coordination 17

EMG amplitude might be explained by (i) an additional recruitment of motor units

(MU) to compensate for the decrease in the force of contraction that occurs in fatigued
muscle bers (Edwards and Lippold 1956), (ii) an increased ring frequency and/or
synchronization of motor unit recruitment (Gandevia 2001), and/or (iii) the slowing of
muscle ber action potential conduction velocity (Linstrom et al. 1970). However, this
interpretation of increased EMG amplitude as a sign of neuromuscular fatigue does
not hold true during tasks that involve synergist and antagonist muscles (Hug 2011).
This is because it is difcult to dissociate the effects of neuromuscular fatigue and the
possible changes of muscle coordination strategies. For example, an increased EMG
amplitude of a lower leg muscle during a constant-load pedaling exercise could be
explained by (i) a change of muscle coordination strategy that consists of an increase
in muscle force produced by this muscle to compensate for fatigue in other muscles
(in this case the recorded muscle does not fatigue); (ii) a change of motor units
recruitment such as an additional recruitment, an increased ring frequency, and
synchronization and slowing of muscle ber action potential conduction velocity
(in this case the recorded muscle exhibits fatigue); or (iii) both. In order to better
isolate the direct effects of neuromuscular fatigue from the changes of muscle
coordination, it is possible to measure neural (M-wave, voluntary activation, maximal
activation level) and contractile (muscular twitch) properties of a muscle group at
various instants of a fatiguing exercise. Unfortunately, this information can be
obtained simultaneously only from a limited number of muscles.

Concluding Remarks

EMG is a powerful research tool that has provided many remarkable insights into the
control of movement. To facilitate the appropriate reporting and interpretation of
data, and drive new discoveries in human movement studies, it is essential that
researchers and clinicians understand the limitations to this technique. There are
many excellent technical reviews on EMG recording and processing that have come
before this (Merlo et al. 2003; Farina et al. 2004, 2014). Rather than replicate this
information, we have highlighted crosstalk, signal cancellation, normalization,
computation signal, detection of the onset/offset times, and the misinterpretation of
EMG to infer torque as six of the most signicant factors that need to be considered
when recording and then interpreting EMG data. These factors need to be considered
before data is collected, to determine if EMG is the right tool and/or which pro-
cessing methods may best provide insight into the research question. Further, these
factors may be important to consider when determining the validity of the conclu-
sions made from previously published research.

Cross-References

EMG Activity in Gait: The Inuence of Motor Disorders

Optimal Control Strategies for Human Movement
18 F. Hug and K. Tucker

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