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Journal of Electromyography and Kinesiology 18 (2008) 255261

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Review

Neuromuscular adaptation in experimental and clinical neck pain

Deborah Falla *, Dario Farina
Center for Sensory-Motor Interaction (SMI), Department of Health Science and Technology, Aalborg University,
Fredrik Bajers Vej 7, D-3, DK-9220 Aalborg, Denmark

Received 6 September 2006; received in revised form 6 November 2006; accepted 6 November 2006

Abstract

The purpose of this brief review is to present evidence from experimental and clinical neck pain studies of pain-induced neuromus-
cular adaptations. It has been shown that clinical neck pain is associated with a substantial reorganization in the control strategies of
cervical muscles during static and dynamic tasks. Experimental neck pain models allow local elicitation of nociceptive aerents, mimick-
ing the sensory aspects of clinical pain, without major changes in muscle properties. These models may help understand the physiological
mechanisms underlying the observations from clinical neck pain studies. The knowledge obtained from the interpretation of clinical nd-
ings with experimental pain models has relevance for the development of therapeutic interventions for the rehabilitation of patients with
neck pain disorders.
2006 Elsevier Ltd. All rights reserved.

Keywords: Neck pain; Motor control; Motor unit; Experimental muscle pain

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 255
2. Nociception and motor control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 256
2.1. Nociceptive input and motor neuron discharge . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 256
2.2. Nociceptive input and muscle coordination . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 256
2.3. Potential implications of pain-induced alterations in the motor strategy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 257
3. Clinical neck pain . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 258
3.1. Changes in cervical motor control strategies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 258
3.2. Changes in the peripheral properties of the cervical muscles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 259
3.3. Potential relationships between altered motor control and peripheral adaptation. . . . . . . . . . . . . . . . . . . . . . . . . . 259
4. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 259
Acknowledgement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 259
References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 259

1. Introduction

*
Corresponding author. Tel.: +45 96 35 74 59; fax: +45 98 15 40 08. The cervical spine is a dynamic structure which serves to
E-mail address: deborahf@hst.aau.dk (D. Falla). support and orient the head in space and transmit forces

1050-6411/$ - see front matter 2006 Elsevier Ltd. All rights reserved.
doi:10.1016/j.jelekin.2006.11.001
256 D. Falla, D. Farina / Journal of Electromyography and Kinesiology 18 (2008) 255261
arising from the trunk that will inuence the position of the
head (Keshner, 2004). Control of cervical muscles allows
three-dimensional movement of the head whilst maintain-
ing mechanical stability. In addition to their role in move-
ment and support, the cervical muscles are intimately
related with reex systems associated with stabilization of
the head and the eyes, vestibular function and propriocep-
tive systems that serve general postural orientation and sta-
bility (Dutia, 1991; Keshner, 1990; Winters and Peles,
1990).
Given the complexity of the cervical spine, it is expected
that alterations in aerent feedback from the muscles, for
instance due to pain, induce major modications of cervical
motor control. Accordingly, altered muscle activity has
been observed in individuals with neck pain during various
tasks (e.g., Falla et al., 2004a; Jull et al., 2004; Mork and
Westgaard, 2006). The mechanisms underlying these
changes are not fully understood which poses limitations
in the design of rehabilitation programs. One method to
explore the pathophysiology associated with changes in
neural control due to pain is the use of experimental para-
digms to induce acute painful sensations, mimicking clini-
cal pain, in healthy subjects (Arendt-Nielsen et al., 1996;
Graven-Nielsen et al., 1997).
The purpose of this brief review is to present recent evi-
dence on the eect of experimentally-induced muscle pain
on the control of cervical muscles and to discuss the mech-
anisms of altered motor control in individuals with neck
pain. The focus on both experimental and clinical pain
manifestations shows that an experimental pain model
may help understand the physiological mechanisms under-
lying alterations in neural control and muscle properties in
people with neck pain disorders.
2. Nociception and motor control
2.1. Nociceptive input and motor neuron discharge
Group III and IV muscle aerents are sensitive to noci-
ceptive stimuli (Mense and Meyer, 1985) and can be
experimentally elicited in humans using various exogenous
or endogenous methods, including intramuscular injection
of algogenic substances (Graven-Nielsen et al., 1997;
Stohler and Lund, 1994), ischemia (Moore et al., 1979),
exercise (Madeleine et al., 2006), repetitive mechanical
pressure stimulation (Nie et al., 2005) and electrical stim-
ulation (Marchettini et al., 1996). Nociceptive aerents in
the neckshoulder region are usually experimentally
excited by intramuscular injection of chemical substances,
such as hypertonic saline (e.g., Birch et al., 2001; Falla
et al., in press-b; Schmidt-Hansen et al., 2006) (Fig. 1).
This approach allows standardization of the intensity,
location and duration of pain (Kellgren, 1938; Svensson
and Arendt-Nielsen, 1995). In addition, injection of
hypertonic saline produces a deep pain comparable in
quality to clinical neckshoulder muscle pain (Madeleine
et al., 1998).
Fig. 1. Experimentally induced neck muscle pain: Area of perceived pain
following infusion of 0.2 ml hypertonic saline into the (A) trapezius muscle
in the middle of the muscle belly 6 cm below the external occipital
protuberance; (B) splenius capitis muscle midway between the mastoid
process and external occipital protuberance; and (C) sternomastoid muscle
in the upper 1/3 of the muscle belly. Note the presence of both local and
referred pain areas. Reprinted with permission from Schmidt-Hansen
et al. (2006) with kind permission from Blackwell Publishing.
Muscle pain inuences motor control via numerous
reex and central mechanisms (Le Pera et al., 2001,
2002). At rest, only a small and transient increase in pos-
tural electromyographic (EMG) activity has been observed
in response to deep noxious stimulation of cervical muscles
(Ashton Miller et al., 1990, 1943, 2004). On the contrary,
during voluntary contraction, cervical muscles consistently
demonstrate pain-induced inhibition when acting as ago-
nists (Falla et al., in press-a, in press-b; Ge et al., 2005;
Madeleine et al., 1999, 2006). For example, during cervical
exion contractions of linearly increasing force, injection of
hypertonic saline in the sternomastoid muscle results in a
force-dependent reduction of sternomastoid EMG ampli-
tude ipsilateral to the side of pain (Falla et al., in press-
b). Similarly, injection of hypertonic saline into the upper
trapezius muscle reduces upper trapezius EMG activity in
isometric (Ge et al., 2005; Madeleine et al., 2006) and
dynamic tasks (Falla et al., in press-a; Madeleine et al.,
1999). These results support the hypothesis of an inhibitory
eect of pain on motor neurons (Lund et al., 1991).
Inhibited activity of the painful muscle in experimental
pain studies occurs without changes in electrophysiological
membrane properties of the muscle bers, as indirectly
assessed in EMG studies (Farina et al., 2004). Thus,
decreased electrical activity from painful muscles with the
same exerted force at the joint, is not mediated by changes
in muscle properties due to injection of the painful sub-
stance (Farina et al., 2004, 2005a). Accordingly, single
motor unit studies have proven a reex-mediated adapta-
tion of motor neuron discharges to pain in the absence of
modication of muscle properties (Farina et al., 2004; Sohn
et al., 2000).
2.2. Nociceptive input and muscle coordination
In isometric contractions, pain-induced inhibition of
cervical muscles has been observed with unchanged
force (Falla et al., in press-b). Similarly, decreased EMG
 D. Falla, D. Farina / Journal of Electromyography and Kinesiology 18 (2008) 255261 257

Contralateral Upper Trapezius

Ipsilateral Lower Trapezius
100 35 100
Ipsilateral Upper Trapezius

* 30
80 80
*

ARV ( V)
ARV ( V)
25
ARV (V)

60 20 60
* *
* * * * *
40 * 15 40
* *
*
10
20 20
5
0 0
30 60 90 120 150 30 60 90 120 150 30 60 90 120 150
Time (s) Time (s) Time (s)
Pre Injection Post Injection

B
140

100

60

20
V
Baseline During 15 min post 30 min post

Fig. 2. (A) Pain induced reorganization of trapezius muscle activity during a dynamic task: Mean and standard error of EMG average rectied value
(ARV) are shown for the upper and lower trapezius ipsilateral to the side of injection of hypertonic saline and the contralateral upper trapezius during
performance of a 2.5-min repetitive upper limb task. Hypertonic saline-evoked unilateral upper trapezius muscle pain induces inhibition of the painful
muscle and a concomitant increase in EMG activity of the lower trapezius on the painful side and upper trapezius on the contralateral side. *: signicant
dierence pre to post injection (P < 0.05). Reprinted from Falla et al. (in press-a) with kind permission of Springer Science and Business Media. (B) Pain
induced reorganization of activity within the upper trapezius muscle during sustained contraction: Representative two-dimensional root mean square
maps obtained from the upper trapezius muscle during 90-s isometric shoulder abduction contractions before, during, 15 min and 30 min after
intramuscular injection of hypertonic saline. Dashed circle indicates location of the injection. d: represents the position of the center of gravity of the root
mean square map. Note the shift of activity to the more caudal region of the upper trapezius muscle following local elicitation of nociceptive aerents in
the cranial region. Reprinted with permission from Madeleine et al. (2006) with kind permission from the International Federation of Clinical
Neurophysiology.

amplitude of the painful muscle during movement occurs increased activity of the infraspinatus muscle (Madeleine
with unchanged motor output (Falla et al., in press-a). et al., 1999). Overall, these results suggest a dynamic reor-
Since peripheral muscle properties are not likely to change ganization of the coordination among muscles in order to
with injection of hypertonic saline (Farina et al., 2004), minimize the use of the painful muscle with minimal dis-
maintenance of the motor output should be due to a redis- ruption to the task.
tribution of load in the muscles contributing to the task. Reorganization of activity following local painful stimu-
This may result in a variety of control strategies leading lation has also been reported within parts of the same muscle.
to the same exerted force or kinematics, especially in com- Two-dimensional multi-channel surface EMG recordings of
plex biomechanical systems such as the cervical spine. the upper trapezius demonstrated a shift in activity to the
For example, during cervical exion isometric contrac- more caudal region of the upper trapezius muscle following
tions of increasing force, noxious stimulation of the sterno- local excitation of trapezius nociceptive aerents in the cra-
mastoid muscle results in decreased sternomastoid EMG nial region during sustained shoulder abduction (Madeleine
activity with a concomitant bilateral reduction of splenius et al., 2006) (Fig. 2B).
capitis and trapezius muscle activity (Falla et al., in The above observations indicate that local excitation of
press-b). Reduced sternomastoid muscle activity has also nociceptive aerents has an inhibitory eect on the painful
been reported during cervical rotation following hypertonic muscle which is counteracted by the reorganization of the
saline-evoked splenius capitis muscle pain (Svensson et al., motor strategy at the level of the muscle groups involved
2004). in the task.
In dynamic tasks of the upper limb, hypertonic saline-
evoked unilateral upper trapezius muscle pain induces a 2.3. Potential implications of pain-induced alterations in the
bilateral reorganization in the coordinated activity of the motor strategy
three subdivisions of the trapezius (Falla et al., in press-
a) (Fig. 2A). Similarly, in low load repetitive upper limb Experimental pain models demonstrate that pain-
tasks, experimental upper trapezius muscle pain results in induced alterations of the motor strategy may be viewed
reduced EMG in the upper trapezius, with a tendency for as a compensatory mechanism to allow similar motor
258 D. Falla, D. Farina / Journal of Electromyography and Kinesiology 18 (2008) 255261

output in painful and non-painful conditions. Evidence for
an altered motor strategy has been provided at levels rang-
ing from the motor unit (Farina et al., 2005b) and motor
unit pool (Madeleine et al., 2006) to a reorganization of
activity among agonist, synergists and antagonist muscles
(Falla et al., in press-b). Reorganization of muscle control
may be mediated by spinal (reex) and supraspinal (corti-
cal motor drive) mechanisms. Similar adaptations may also
occur in neck pain patients and may have implications for
the perpetuation and worsening of symptoms. Pain-
induced altered neural control to the muscles may indeed
dispose them to overload and as a consequence, injury
(Hagg, 1991) or to reduced activity with consequent atro-
phy of specic ber types (Uhlig et al., 1995). This may
contribute to the development of chronic symptoms and
provide an explanation for muscle morphological changes
and motor control decits in patients with chronic neck
pain.
3. Clinical neck pain
3.1. Changes in cervical motor control strategies
Altered motor control strategies have been frequently
observed in individuals with neck pain. Neck pain has been
associated with inhibition of deep muscle activation con-
comitant with increased activation of the supercial mus-
cles (Falla et al., 2004b; Jull et al., 2004) (Fig. 3A).
Increased activity of supercial cervical exor muscles in
people with neck pain has also been observed during iso-
metric cervical exion contractions (Falla et al., 2004d)
and during dynamic movement of the upper limb (Falla
et al., 2004c). Furthermore, people with neck pain demon-
strate reduced ability to relax the anterior scalene and ster-
nomastoid muscles following activation (Barton and
Hayes, 1996; Falla et al., 2004c). Upper trapezius also
shows decreased ability to relax between (Fredin et al.,
1997) and following (Falla et al., 2004c; Nederhand
et al., 2002) repetitive arm movements, has reduced muscle
rest periods during repetitive tasks (Hagg and Anstrom,
1997; Veiersted et al., 1990) and is generally susceptible
to increased activity during tasks involving mental demand
(Bansevicius and Sjaastad, 1996; Laursen et al., 2002;
Westgaard, 1999).
Altered motor control of the cervical spine in individuals
with neck pain is also evidenced by delayed activation of
the deep and supercial cervical exor muscles in associa-
tion with rapid arm movements (Falla et al., 2004a)
(Fig. 3B). Changes in the feed-forward control were
observed in these conditions in both the deep and super-
cial cervical exor muscles but were most evident in the
deep longus colli and longus capitis. Onset of the deep cer-
vical exor muscles exceeds the criteria for feed-forward
activation with movement, indicating a signicant decit
in the automatic feed-forward control of the cervical spine
(Falla et al., 2004a). Moreover, activation of the deep cer-
vical exor muscles is direction-specic in patients with
neck pain, which is consistent with a change in the strategy

A B
Control 22 24 26 28 30

Pressure Control Neck Pain

DCF EMG
(L) AS EMG AD EMG

(R) AS EMG
(L) SM EMG DCF EMG

(R) SM EMG
(L) AS EMG

Neck Pain
(R) AS EMG
Pressure
DCF EMG (L) SM EMG
(L) AS EMG

(R) AS EMG (R) SM EMG

(L) SM EMG
100 ms
(R) SM EMG
5s

Fig. 3. (A) Reorganization of cervical exor muscle activity during a prescribed task: Representative raw EMG data are shown for a control and person
with neck pain during a task of staged cranio-cervical exion. Data are shown for the deep cervical exors (DCF) and left (L) and right (R) anterior
scalene (AS) and sternomastoid (SM) muscles. Note the incremental increase in EMG activity for all muscles with increasing cranio-cervical exion
(recorded as an increase in pressure in a pressure sensor under the cervical spine) but with lesser activity in the deep cervical exors and greater activity in
the supercial muscles for the neck pain patient. EMG calibration: 0.5 mV. Reprinted with permission from Falla et al. (2004b). (B) Delayed activation of
the cervical exor muscles during a perturbation: Representative raw EMG data are shown for the anterior deltoid (AD), deep cervical exors (DCF), left
(L) and right (R) sternomastoid (SM) and the anterior scalene (AS) muscles for a control and person with neck pain during rapid upper limb exion. Line
indicates onset of the anterior deltoid. m: denotes onset of neck muscle activation. Note the delayed activation of the neck muscles for the neck pain
patient. Reprinted from Falla et al. (2004a) with kind permission of Springer Science and Business Media.
 D. Falla, D. Farina / Journal of Electromyography and Kinesiology 18 (2008) 255261
used by the central nervous system to control the cervical
spine (Falla et al., 2004a).
3.2. Changes in the peripheral properties of the cervical
muscles
Muscle biopsies on ventral (sternocleidomastoid, omo-
hyoid, and longus colli) and dorsal neck muscles (rectus
capitis posterior major, obliquus capitis inferior, splenius
capitis) in individuals with neck pain have demonstrated
a signicant increase in the proportion of type IIC bers
with respect to control subjects (Uhlig et al., 1995). The
observation was unrelated to the muscle investigated,
patient diagnosis or presence of neurological symptoms
(Uhlig et al., 1995). In addition, atrophy and connective-
tissue inltration of the deep suboccipital muscles have
been documented in people with chronic neck pain (And-
ary et al., 1998; Hallgren et al., 1994; McPartland et al.,
1997).
Muscle biopsies and laser Doppler owmetry have also
shown specic morphological and histological changes in
the upper trapezius muscle in people with trapezius myalgia
including, morphological signs of disturbed mitochondrial
function (ragged red and cytochrome-coxidase negative
bers, Kadi et al., 1998; Lindman et al., 1991b), reduced
ATP content (Larsson et al., 1998; Lindman et al., 1991a)
and increased cross-sectional area of type I muscle bers
despite a lower capillary to ber area ratio (Kadi et al.,
1998; Larsson et al., 1998; Lindman et al., 1991b). Such
changes may be associated with overload of low-threshold
motor units (Hagg, 1991) that may explain pain develop-
ment in individuals performing repetitive tasks at low forces
(e.g., Mork and Westgaard, 2006; Sjgaard et al., 2000).
The observed greater proportion of type IIC bers and
lower capillary to ber area in people with neck pain is
indirectly in agreement with the nding of larger changes
in surface EMG signal features during sustained contrac-
tion (myoelectric manifestations of fatigue). The mean or
median frequency of EMG were observed to vary more
in neck pain patients than in controls during isometric con-
tractions of the sternomastoid, anterior scalene (Falla
et al., 2003) and splenius capitis (Gogia and Sabbahi,
1994) and upper trapezius muscle ber conduction velocity
demonstrated a greater decrease during repetitive shoulder
elevation (Falla and Farina, 2005).
3.3. Potential relationships between altered motor control
and peripheral adaptation
Results from experimental pain studies indicate that
nociceptive stimulation, without damage to the muscle tis-
sue, causes substantial changes in load sharing within and
between muscles. These changes are also found in people
with neck pain although, in the case of chronic neck pain,
changes in motor control are probably associated with
modications in the muscle properties. For example, larger
changes in upper trapezius muscle ber conduction velocity
259
observed in neck pain patients during repetitive shoulder
elevation (Falla and Farina, 2005) cannot be reproduced
in healthy subjects by experimental stimulation of the noci-
ceptors (Falla et al., in press-a), as also conrmed at the
single motor unit level (Farina et al., 2004). Therefore, nd-
ings from experimental pain studies indicate that pain by
itself does not explain the electrophysiological observations
in patients.
Modications of muscle activity in people with neck
pain must therefore be the result of a combination of
altered neural input to muscles and changed muscle prop-
erties, in agreement with biopsy studies (Kadi et al.,
1998; Lindman et al., 1991b; Uhlig et al., 1995). It can be
hypothesized that perpetuation of an altered control strat-
egy induced by nociceptive input contributes to muscle
overload or disuse and thus induces additional adaptations
at the muscle level. The large modication in relative mus-
cle activation observed with experimental pain paradigms
demonstrates that alterations in the level of muscle activity
induced by nociception are sucient to produce chronic
changes in the long term (Falla et al., 2006).
4. Conclusion
Experimental pain models may provide a means to
increase our understanding of the basic mechanisms under-
lying alterations of muscle activity in people with neck
pain. Experimental pain research has convincingly demon-
strated that nociception substantially alters the load shar-
ing among muscles which may lead to subsequent muscle
overuse or disuse in functional activities. It is also evident
from experimental neck pain studies that the electrophysi-
ological dierences which have been observed in patients
with neck pain cannot be solely explained by altered neural
strategies. However, altered motor control strategies may
enhance the changes in the peripheral properties of the
cervical muscles. This knowledge has relevance for the
design and implementation of therapeutic strategies for
the rehabilitation of people with neck pain disorders.
Acknowledgement
Deborah Falla is supported by the National Health and
Medical Research Council of Australia (ID 351678). The
Danish Technical Research Council partly supported this
work (Dario Farina).
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261
Deborah Falla received her PhD from The Uni-
versity of Queensland, Australia in 2003. In 2005
she was awarded Fellowships from the Interna-
tional Association for the Study of Pain and the
National Health and Medical Research Council
of Australia to undertake postdoctoral research at
the Center for Sensory-Motor Interaction, Aal-
borg University, Denmark. Her research focus
involves the integration of physiological and
clinical research to evaluate altered neuromotor
control in people with neck pain. In this eld, she
received the Delsys Prize for Electromyography Innovation in 2004. Her
research interests also include investigation of the physiological mecha-
nisms that underpin the ecacy of therapeutic exercise for the treatment
of musculoskeletal pain.
Dario Farina graduated summa cum laude in Elec-
tronics Engineering (equivalent to MSc) from
Politecnico di Torino, Torino, Italy, in February
1998. During 1998 he was a Fellow of the Labo-
ratory for Neuromuscular System Engineering in
Torino. In 2001 and 2002 he obtained PhD degrees
in Automatic Control and Computer Science and
in Electronics and Communications Engineering
from the Ecole Centrale de Nantes, Nantes,
France, and Politecnico di Torino, respectively. In
19992004 he taught courses in Electronics and
Mathematics at Politecnico di Torino and in 20022004 he was Research
Assistant Professor at the same University. Since 2004, he is Associate
Professor in Biomedical Engineering at the Department of Health Science
and Technology of Aalborg University, Aalborg, Denmark, where he tea-
ches courses on biomedical signal processing, modeling, and neuromuscular
physiology. He regularly acts as referee for approximately 20 scientic
International Journals, is an Associate Editor of IEEE Transactions on
Biomedical Engineering, is on the Editorial Boards of the Journal of Neu-
roscience Methods, the Journal of Electromyography and Kinesiology, and
Medical and Biological Engineering and Computing, and member of the
Council ISEK (International Society of Electrophysiology and Kinesiol-
ogy). His main research interests are in the areas of signal processing applied
to biomedical signals, modeling of biological systems, basic and applied
physiology of the neuromuscular system, and brain-computer interfaces.
Within these elds he has authored or co-authored more than 100 papers in
peer-reviewed Journals. He is a Registered Professional Engineer in Italy.