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Journal of Electromyography and Kinesiology 18 (2008) 255261 www.elsevier.com/locate/jelekin

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

3.

4.

1. Introduction
*

Corresponding author. Tel.: +45 96 35 74 59; fax: +45 98 15 40 08. E-mail address: deborahf@hst.aau.dk (D. Falla).

The cervical spine is a dynamic structure which serves to 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

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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 maintaining mechanical stability. In addition to their role in movement and support, the cervical muscles are intimately related with reex systems associated with stabilization of the head and the eyes, vestibular function and proprioceptive systems that serve general postural orientation and stability (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 paradigms to induce acute painful sensations, mimicking clinical pain, in healthy subjects (Arendt-Nielsen et al., 1996; Graven-Nielsen et al., 1997). The purpose of this brief review is to present recent evidence on the eect of experimentally-induced muscle pain on the control of cervical muscles and to discuss the mechanisms 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 underlying 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 nociceptive 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 stimulation (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 postural 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 agonists (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 amplitude ipsilateral to the side of pain (Falla et al., in pressb). 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 substance (Farina et al., 2004, 2005a). Accordingly, single motor unit studies have proven a reex-mediated adaptation 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

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Ipsilateral Upper Trapezius ARV (V)

100 80 60 40 20 0 30 60 90 120 Time (s) 150

35 30 25 20 15 10 5 30 60 90 Time (s) Pre Injection Post Injection 120 150

* * * *

Contralateral Upper Trapezius ARV ( V)

Ipsilateral Lower Trapezius ARV ( V)

100 80 60 40 20 0 30 60 90 Time (s) 120 150

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 with unchanged motor output (Falla et al., in press-a). Since peripheral muscle properties are not likely to change with injection of hypertonic saline (Farina et al., 2004), maintenance of the motor output should be due to a redistribution of load in the muscles contributing to the task. This may result in a variety of control strategies leading to the same exerted force or kinematics, especially in complex biomechanical systems such as the cervical spine. For example, during cervical exion isometric contractions of increasing force, noxious stimulation of the sternomastoid muscle results in decreased sternomastoid EMG activity with a concomitant bilateral reduction of splenius capitis and trapezius muscle activity (Falla et al., in press-b). Reduced sternomastoid muscle activity has also been reported during cervical rotation following hypertonic saline-evoked splenius capitis muscle pain (Svensson et al., 2004). In dynamic tasks of the upper limb, hypertonic salineevoked unilateral upper trapezius muscle pain induces a bilateral reorganization in the coordinated activity of the three subdivisions of the trapezius (Falla et al., in pressa) (Fig. 2A). Similarly, in low load repetitive upper limb tasks, experimental upper trapezius muscle pain results in reduced EMG in the upper trapezius, with a tendency for

increased activity of the infraspinatus muscle (Madeleine et al., 1999). Overall, these results suggest a dynamic reorganization of the coordination among muscles in order to minimize the use of the painful muscle with minimal disruption to the task. Reorganization of activity following local painful stimulation has also been reported within parts of the same muscle. Two-dimensional multi-channel surface EMG recordings of the upper trapezius demonstrated a shift in activity to the more caudal region of the upper trapezius muscle following local excitation of trapezius nociceptive aerents in the cranial region during sustained shoulder abduction (Madeleine et al., 2006) (Fig. 2B). The above observations indicate that local excitation of nociceptive aerents has an inhibitory eect on the painful muscle which is counteracted by the reorganization of the motor strategy at the level of the muscle groups involved in the task. 2.3. Potential implications of pain-induced alterations in the motor strategy Experimental pain models demonstrate that paininduced alterations of the motor strategy may be viewed as a compensatory mechanism to allow similar motor

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output in painful and non-painful conditions. Evidence for an altered motor strategy has been provided at levels ranging 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 (cortical motor drive) mechanisms. Similar adaptations may also occur in neck pain patients and may have implications for the perpetuation and worsening of symptoms. Paininduced 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 atrophy 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 concomitant with increased activation of the supercial muscles (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 isometric cervical exion contractions (Falla et al., 2004d) and during dynamic movement of the upper limb (Falla et al., 2004c). Furthermore, people with neck pain demonstrate reduced ability to relax the anterior scalene and sternomastoid 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 association 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 supercial cervical exor muscles but were most evident in the deep longus colli and longus capitis. Onset of the deep cervical 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 cervical exor muscles is direction-specic in patients with neck pain, which is consistent with a change in the strategy

A
Control Pressure DCF EMG (L) AS EMG (R) AS EMG (L) SM EMG (R) SM EMG Neck Pain 22 24 26 28 30

B
Control Neck Pain

AD EMG

DCF EMG (L) AS EMG

(R) AS EMG Pressure DCF EMG (L) AS EMG (R) AS EMG (L) SM EMG 100 ms (R) SM EMG 5s (R) SM EMG (L) SM EMG

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.

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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, omohyoid, 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 connectivetissue inltration of the deep suboccipital muscles have been documented in people with chronic neck pain (Andary 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 development 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 contraction (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 contractions 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 tissue, 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

observed in neck pain patients during repetitive shoulder elevation (Falla and Farina, 2005) cannot be reproduced in healthy subjects by experimental stimulation of the nociceptors (Falla et al., in press-a), as also conrmed at the single motor unit level (Farina et al., 2004). Therefore, ndings 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 properties, 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 strategy induced by nociceptive input contributes to muscle overload or disuse and thus induces additional adaptations at the muscle level. The large modication in relative muscle 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 underlying alterations of muscle activity in people with neck pain. Experimental pain research has convincingly demonstrated that nociception substantially alters the load sharing 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 electrophysiological 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). References
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Deborah Falla received her PhD from The University of Queensland, Australia in 2003. In 2005 she was awarded Fellowships from the International 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, Aalborg 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 mechanisms that underpin the ecacy of therapeutic exercise for the treatment of musculoskeletal pain. Dario Farina graduated summa cum laude in Electronics Engineering (equivalent to MSc) from Politecnico di Torino, Torino, Italy, in February 1998. During 1998 he was a Fellow of the Laboratory 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 teaches 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 Neuroscience 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 Kinesiology). 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.