Effect of pain on the modulation in discharge rate of sternocleidomastoid motor units with force direction

Clinical Neurophysiology 121 (2010) 744–753

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Effect of pain on the modulation in discharge rate of sternocleidomastoid motor units with force direction Deborah Falla a,*, Rene Lindstrøm a, Lotte Rechter b,c, Dario Farina a a

Center for Sensory-Motor Interaction (SMI), Department of Health Science and Technology, Aalborg University, Denmark Multidisciplinary Pain Center, Aalborg, Denmark c Department of Occupational Therapy and Physiotherapy, Aalborg Hospital, Aarhus University Hospital, Denmark b

See Editorial, pages 634–635

a r t i c l e

i n f o

Article history: Accepted 1 December 2009 Available online 25 January 2010 Keywords: Motor unit Neck pain

a b s t r a c t Objective: To compare the behavior of sternocleidomastoid motor units of patients with chronic neck pain and healthy controls. Methods: Nine women (age, 40.4 ± 3.5 yr) with chronic neck pain and nine age- and gender-matched healthy controls participated. Surface and intramuscular EMG were recorded from the sternocleidomastoid muscle bilaterally as subjects performed isometric contractions of 10-s duration in the horizontal plane at a force of 15 N in eight directions (0–360°; 45° intervals) and isometric contractions at 15 and 30 N force with continuous change in force direction in the range 0–360°. Motor unit behavior was monitored during the 10-s contractions and the subsequent resting periods. Results: The mean motor unit discharge rate depended on the direction of force in the control subjects (P < 0.05) but not in the patients. Moreover, in three of the nine patients, but in none of the controls, single motor unit activity continued for 8.1 ± 6.1 s upon completion of the contraction. The surface EMG amplitude during the circular contraction at 15 N was greater for the patients (43.5 ± 54.2 lV) compared to controls (16.9 ± 14.9 lV; P < 0.05). Conclusions: The modulation in discharge rate of individual motor units with force direction is reduced in the sternocleidomastoid muscle in patients with neck pain, with some patients showing prolonged motor unit activity when they were instructed to rest. Significance: These observations suggest that chronic neck pain affects the change in neural drive to muscles with force direction. Ó 2009 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved.

1. Introduction The cervical spine is a complex structure responsible for the stabilization of head posture, and the control of head movement. Moreover, the cervical region is involved in proprioception and reflexes that control postural orientation, stability and oculomotor control (Roberts, 1978; Wilson, 1984; Taylor and McCloskey, 1988; Dutia, 1991). The control of the cervical spine includes a continuous demand for stabilization of the head in a three-dimensional space, in addition to the execution of voluntary movements, for example to

* Corresponding author. Address: Center for Sensory-Motor Interaction (SMI), Department of Health Science and Technology, Aalborg University, Fredrik Bajers Vej 7, D-3, DK-9220 Aalborg, Denmark. Tel.: +45 99 40 74 59; fax: +45 98 15 40 08. E-mail address: [email protected] (D. Falla).

follow a visual stimulus through coordinated control of eye and head movement (Schor et al., 1988; Dutia, 1991). The coordinated activity of all muscles influences the orientation of the cervical spine and head position (Dutia, 1991). More than 20 pairs of muscles act on the cervical vertebrae and head to generate multidirectional force and movements (Blouin et al., 2007). However, some neck muscles have similar lines of action and therefore different groups of muscles can be recruited to perform the same task (Keshner et al., 1989; Vasavada et al., 2002). A single action of the head and neck can be accomplished through a variety of muscle patterns (Keshner et al., 1989). The motor control problem in the cervical spine is the simplification or reduction of the degrees of freedom for efficient and timely production of an optimal movement pattern (Keshner, 2004). Thus, the maximal excitation of a muscle when participating in a task is related to a specific direction of motion (Keshner

1388-2457/$36.00 Ó 2009 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.clinph.2009.12.029

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et al., 1989, 1992, 1997). The activation of neck musculature is based on consistent muscle synergies that generate multidirectional patterns of force and eliminate the redundancy of the system (Keshner et al., 1989; Vasavada et al., 2002; Blouin et al., 2007). Movements are executed by translating the task-level commands into muscle activation patterns that depend on the direction of force. The presence of pain induces modifications of cervical motor control. For example, patients with neck pain show different activation of the superficial neck flexor muscles with respect to healthy controls in standardized isometric contractions of cervical and cranio-cervical flexion (Jull et al., 2004; Falla et al., 2004b,d) and reduced ability to relax their neck muscles following contraction (Falla et al., 2004a; Johnston et al., 2008). Moreover, increased cocontraction of the neck muscles has been observed in headache patients (Fernandez-de-las-Penas et al., 2008). These results suggest that pain may alter the task-related modulation of neck muscle activity so that the motor control problem in the cervical spine is solved by alternative combinations of muscle synergistic activities. In this study, we investigated the neural drive to the sternocleidomastoid muscle from the discharge rate of individual motor units as a function of the direction in force production in the horizontal plane. It was hypothesized that changes in motor unit discharge rate with force direction would be different in people with neck pain with respect to controls. Based on previous observations that patients with neck pain have a reduced ability to relax their neck muscles after contraction, we also analyzed motor unit activity immediately following the contractions. It was hypothesized that motor unit activity would persist in patients. Therefore, the aim of the study was to compare the behavior of individual motor units in the sternocleidomastoid muscle of patients with chronic neck pain and healthy controls both during and immediately following multidirectional isometric tasks. 2. Methods 2.1. Subjects Nine women (age, mean ± SD: 40.4 ± 3.5 yr; height: 170.8 ± 5.5 cm; weight: 73.7 ± 10.1 kg) with chronic, non-traumatic neck pain greater than 3 months (years, mean ± SD: 12.3 ± 11.1; range: 1–33) participated in the study. Subjects were excluded if they previously had cervical spine surgery, presented with neurological signs in the upper limb or had a history of torticollis. The patients’ average score for the Neck Disability Index (0–50) (Vernon and Mior, 1991) was 16.5 ± 8.8 (range: 5–31) and their average pain intensity rated on a visual analog scale (0–10) was 4.3 ± 1.5 (range: 2.0–6.9). Nine women were recruited as controls (age, mean ± SD: 35.4 ± 7.5 yr; height: 164.8 ± 7.7 cm; weight: 65.0 ± 12.3 kg). Control subjects were free of shoulder and neck pain, had no past history of orthopedic disorders affecting the shoulder or neck region and no history of neurological disorders. The two subject groups did not differ in age, weight or height (P > 0.05). Women were not tested during menstruation or ovulation, as self-reported, to avoid times of rapid change in hormone levels (Greenspan et al., 2007). Ethical approval for the study was granted by the Ethics Committee (No. 20070045) and the procedures were conducted according to the Declaration of Helsinki. 2.2. Procedure Participants were seated with their head rigidly fixed in a device for the measurement of multidirectional neck force (Aalborg University, Denmark) with their back supported, knees and hips in 90° of flexion, their torso firmly strapped to the seat back and their hands resting comfortably in their lap (Fig. 1).

Fig. 1. Device for the measurement of multidirectional neck force. The device is equipped with force transducers (strain gauges) to measure force in the sagittal and coronal planes (A). Participants are seated with their head fixed in a head piece. The head is rigidly secured via eight contacts which are fastened around the head (B). Surface and intramuscular EMG was acquired from the sternocleidomastoid muscle bilaterally (C). The subjects back and torso are firmly strapped to the seat back (D).

The device is equipped with eight adjustable contacts which are fastened around the head to stabilize the head and provide resistance during isometric contractions of the neck. The force device is equipped with force transducers (strain gauges) to measure force in the sagittal and coronal planes. The electrical signals from the strain gauges were amplified (LISiN – OT Bioelettronica, Torino, Italy) and their output was displayed on an oscilloscope as visual feedback to the subject. Following a period of familiarization with the measuring device and a period to practice the desired contractions, subjects performed two maximum voluntary contractions (MVC) of 3–4 s duration separated by 1 min of rest, for cervical flexion, extension, left lateral flexion, and right lateral flexion. Verbal encouragement was provided to the subject to promote higher forces in each trial. The highest value of force recorded over the 2 maximum contractions for each direction was selected as the maximal force. The order of the MVC contractions was randomized between movement directions. A rest of 30 min followed the MVCs. Subsequently, the subjects performed isometric contractions of 10-s duration (constant force direction) exerting a force of 15 N in eight directions (45° intervals) in the range 0–360° (0°: flexion, 90°: right lateral flexion, 180°: extension, 270°: left lateral flexion) (Fig. 2A). Upon completion of each contraction, the subject was informed to completely relax their neck muscles. An absolute level of force was selected as the target to eliminate variation due to differences in strength between the two groups. Real-time visual feedback of force direction and

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A

C

Flexion 0° 330

0° 30

330

60

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300

Left 270 Lateral Flexion

90 Right Lateral Flexion

240

60

270

120

210

90

120

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150

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30

150 180

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D

0° 330

100 µV

200 ms

30

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90 10

100 µV 240

120

20 30

200 ms

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40 180

150 µV

Fig. 2. Subjects performed two isometric tasks in the horizontal plane. (A) Ten second contractions exerting a force of 15 N in eight directions (45° intervals) of force from 0° to 360°. During these contractions intramuscular EMG was acquired and signals decomposed to obtain the discharge rate of single motor units (B). In this example the discharge of single motor units is displayed for flexion and ipsilateral lateral flexion. Subjects also performed contractions in the horizontal plane at 15 and 30 N force with change in force direction in the range 0–360° (C). During the circular contractions with change in force direction, the amplitude of the surface EMG was obtained and directional activation curves were calculated (D). The directional activation curve represents the modulation in intensity of muscle activity with the direction of force exertion. The central point of the tuning curve defined a directional vector (dashed arrow), whose length was expressed as a percent of the mean EMG average rectified value during the entire task.

magnitude was provided on an oscilloscope positioned in front of the subject which displayed a template with force targets for each direction. The direction of the contractions was randomized and each contraction was followed by rest periods of 2 min. Subjects then performed contractions in the horizontal plane at 15 and 30 N force with change in force direction in the range 0–360° (circular contractions) (Fig. 2C). A 15 or 30 N circular template was superimposed on the oscilloscope to guide the subjects. Following a period of 10 min to practice the task, the subjects performed the 15 and 30 N contractions in both clockwise and counter-clockwise directions with 2 min of rest between contractions. The subjects were guided by a counter to perform the circular contractions at a constant velocity in 12 s. Patients did not report that their pain was provoked by the sub-maximal contractions. 2.3. EMG recordings Surface and intramuscular EMG were acquired from the sternocleidomastoid muscle bilaterally during the contractions in constant force directions and the rest periods that followed these contractions whilst surface EMG only, was acquired during the circular contractions. Intramuscular EMG was not acquired during the circular contractions since preliminary tests showed that the decomposition of the EMG signal was not sufficiently reliable during contractions with change in force direction.

Bipolar surface EMG signals were detected from the sternal head of the sternocleidomastoid muscle bilaterally with pairs of electrodes (Neuroline 72001-k; Medicotest, Denmark) positioned 20 mm apart following skin preparation and using guidelines for electrode placement (Falla et al., 2002). The bipolar EMG signals were amplified (128-channel surface EMG amplifier, LISiN-OT Bioelettronica, Torino, Italy; 3 dB bandwidth 10–500 Hz) by a factor of 2000, sampled at 2048 Hz, and converted to digital form by a 12-bit analog-to-digital converter. Action potentials of single motor units were recorded with a pair of Teflon-coated stainless steel wires (diameter: 0.1 mm; AM Systems, Carlsborg, WA) inserted in the sternocleidomastoid muscle bilaterally 2-cm cephalad to the midpoint between the sternum and the mastoid process via a 25-gauge hypodermic needle. The wires were cut to expose only the cross section and provided one bipolar signal which was amplified (Counterpoint EMG, DANTEC Medical, Skovlunde, Denmark), band-pass filtered (500 Hz–5 kHz), sampled at 10,000 Hz, and stored after 12-bit A/ D conversion. A common reference electrode for both the surface and intramuscular EMG was placed around the right wrist. 2.4. Signal analysis Single motor unit action potentials were identified from the intramuscular EMG with a decomposition algorithm (McGill et al., 2005). The software displays a segment of the EMG signal,

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the templates of the action potentials of the identified motor units, the discharge patterns, and a close-up of the signal for resolving missed discharges and superimpositions. Accuracy of the automatic decomposition was achieved by inspection of the identified discharge patterns. Full, regular patterns provided confidence that the decomposition was correct, whereas gaps, extra discharges or uneven intervals provided an indication of possible decomposition errors. To assist in identifying missed discharges the program displays bars in the signal panel that indicate the expected discharge times of each motor unit. The signal portion can then be viewed in the close-up panel which displays the signal at an expanded scale and allows matching motor unit templates to be selected. The close-up panel also displays superimpositions at an expanded scale which allows verification of the result or allows different sets of templates to be selected and adjusted to find the correct fit. Commands are also available for undoing identifications and deleting or merging templates. The discharge rate of each identified motor unit was obtained across the 10-s contractions with constant force direction (Fig. 2B) and during the rest periods after the contractions if motor unit activity was detected. The interspike interval (ISI) variability was computed as the ratio (%) between SD and mean ISI. Discharge rate and ISI variability were computed from the entire duration of the contractions. During the circular contractions, the amplitude of the surface EMG was estimated as the average rectified value (ARV) of the signal in non-overlapping intervals of 250 ms. The ARV of the EMG as a function of the angle of force direction will be referred to in the following as directional activation curves. The directional activation curves represent the modulation in intensity of muscle activity with the direction of force exertion and represent a closed area when expressed in polar coordinates (Fig. 2D). The line connecting the origin with the central point of this area defined a directional vector, whose length was expressed as a percent of the mean ARV during the entire task. This normalized vector length represents the specificity of muscle activation: it is equal to zero if the muscle is active in the same way in all directions and, conversely, it corresponds to 100% if the muscle is active in exclusively one direction. In addition, the EMG amplitude was averaged across the entire circular contraction to provide an indicator of the overall muscle activity. Since no significant differences were observed for the data extracted from the circular contractions in the clockwise and counter-clockwise directions when the data were compared for the same direction of force, the data were combined to obtain an average. The coefficient of variation of force (SD divided by mean, %) was obtained from both the 10-s contractions with constant force direction and the circular contractions with change in force direction. 2.5. Statistical analysis Two-way analyses of variance (ANOVA) were used to evaluate differences between patients and controls for maximum neck strength and the coefficient of variation of force. For maximum neck strength the factors were group (patient, control) and direction (flexion, extension, right lateral flexion, left lateral flexion). For the coefficient of variation of force during the circular contractions the factors were force (15 N, 30 N) and group (patient, control) and for the coefficient of variation of force during the brief isometric contractions the factors were direction (0–360° in 45° intervals) and group (patient, control). Three-way ANOVAs was conducted to assess differences in the directional specificity of sternocleidomastoid muscle activity (vector length) and the average ARV obtained across the entire circular contraction. In both cases the factors were force (15 N, 30 N), side (left and right sternocleidomastoid) and group (patient, control).

Left and right sternocleidomastoid motor unit discharge rate and ISI variability during the brief isometric contractions in eight directions were assessed with a two-way ANOVA with factors direction (0–360° in 45° intervals) and group (patient, control). Finally, a three-way ANOVA was conducted to assess differences in sternocleidomastoid surface EMG amplitude (ARV) with direction (0–360° in 45° intervals), side (left and right sternocleidomastoid) and group (patient, control) as factors. Significant differences revealed by ANOVA were followed by post hoc Student–Newman–Keuls (SNK) pair-wise comparisons. Results are reported as mean and SD in the text and SE in the figures. Statistical significance was set at P < 0.05. 3. Results 3.1. Motor output The maximum voluntary neck strength was dependent on force direction (F = 31.49, P < 0.00001) with extension showing highest values of force compared to the other directions (SNK: all P < 0.001). In addition, the maximum force produced in cervical flexion was lower than in the other directions (SNK: all P < 0.05). The patient group exerted lower force across all directions compared to the control subjects (F = 4.7, P = 0.045; Table 1). Fig. 3 shows the force and surface EMG signals during a 15 N circular contraction performed in the clockwise direction by representative subjects in the two groups. In this example, the neck pain patient shows reduced force steadiness with respect to the control subject. Moreover, the patient shows a surface EMG signal with similar amplitude in all force directions. Conversely, the control subject displays a more steady maintenance of force and a greater modulation in the activity of the sternocleidomastoid muscle with force direction. From the group data analysis, the patients presented with a greater coefficient of variation of force compared to the control group during the circular contractions at 30 N (SNK: P = 0.002), whereas the two groups had similar variability in force for circular contractions at 15 N (P = 0.828; Table 2). The coefficient of variation of force was higher for the 30 N contraction compared to the 15 N contraction but only for the patient group (patients: P = 0.003; controls: P = 0.188). The patient group also showed greater values of the coefficient of variation of force during the 10-s contractions with constant force direction compared to the control subjects (P = 0.03; Table 2). 3.2. Directional activation curves Representative directional activation curves during a circular contraction performed at 15 N are illustrated in Fig. 4 for a control subject and a patient. In this example, the control subject presents with defined activation of the sternocleidomastoid with the highest amplitude of activity towards the ipsilateral anterolateral flexion direction. The sternocleidomastoid muscle is minimally active during extension or posterolateral extension, as expected. Conversely, the sternocleidomastoid directional activation curves for

Table 1 Mean and standard deviation of maximum voluntary force (N) for cervical flexion, extension, right lateral flexion and left lateral flexion in patients with neck pain (n = 9) and control subjects (n = 9). The patient group exerted lower force across all directions compared to the control subjects (P = 0.045). Force direction

Neck pain (N)

Controls (N)

Flexion Extension Right lateral flexion Left lateral flexion

102.3 ± 39.7 193.7 ± 77.2 129.6 ± 47.1 125.2 ± 46.5

151.8 ± 37.6 243.4 ± 56.6 168.8 ± 58.5 175.1 ± 48.5

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Control

Neck Pain

A

90°

90°

3N

3N

150 µV

150 µV

150 µV

150 µV

B

C

D

2s

2s

Fig. 3. Representative angle (A), force (B) and surface EMG data acquired from the left (C) and right (D) sternocleidomastoid muscle of one patient and one control subject during a 15 N circular contraction performed in the clockwise direction. Note the reduced force steadiness and similar EMG amplitude in all force directions for the patient.

the representative patient indicate more even activation levels of the sternocleidomastoid muscle for all directions. Accordingly, overall the patient group displayed reduced values of directional specificity in the surface EMG of the sternocleidomastoid muscle bilaterally for both the 15 and 30 N circular contractions (F = 4.45; P = 0.041) (Table 3). In addition, the patients demonstrated higher values of ARV (averaged across the circular contractions) for the sternocleidomastoid bilaterally during the circular contractions performed at 15 N (P = 0.044) but not 30 N. For the 15 and 30 N circular contractions, the ARV (average across left and right sternocleidomastoid) for the patient group were 43.5 ± 54.2 and 57.6 ± 51.9 lV and for the control group 16.9 ± 14.9 and 47.6 ± 16.9 lV, respectively. In accordance, the patient group showed greater values of sternocleidomastoid ARV for the 10-s contractions in constant force directions (main effect for group; P = 0.039; Fig. 5).

Table 2 Mean and standard deviation of the coefficient of variation of force obtained during the circular contractions at both 15 and 30 N of force and during brief constant force contractions (average across all directions) for the patients with neck pain (n = 9) and control subjects (n = 9). Task

Neck pain (%)

Controls (%)

Comparison between patients and controls

Circular contraction 15 N Circular contraction 30 N Brief constant force contractions

13.3 ± 3.8 13.9 ± 5.1 2.5 ± 1.3

12.3 ± 1.9 11.7 ± 2.3 2.1 ± 0.8

P = 0.828 P = 0.002 P = 0.030

3.3. Motor unit behavior Table 4 displays the number of motor units detected for each direction of force in the patient and control subjects. Fig. 6 illustrates representative data for motor units recorded from the left sternocleidomastoid muscle during the 10-s contractions in constant force directions. For the control subject a clear modulation in the discharge rate is observed: the discharge rate was 12 pps during ipsilateral lateral flexion, 16 pps in ipsilateral anterolateral flexion, 14 pps in flexion, and 8 pps in contralateral lateral flexion. In the other force directions, motor units were not active. On the contrary, a single motor unit recorded from the left sternocleidomastoid of a neck pain patient which was tracked over several force directions showed a consistent discharge rate of 12 pps except in the directions of contralateral posterolateral extension and extension where it was derecruited. The group data confirmed the characteristics in motor unit behavior shown in the representative example of Fig. 6. The discharge rates of the left sternocleidomastoid motor units were dependent on the interaction between group and force direction (F = 2.0, P = 0.045). For the control group, motor unit discharge rate for the left sternocleidomastoid was higher in the anterior position (0°), 45°, and 315° compared to 90°, 135° and 180° (all P < 0.05; Fig. 7). The discharge rate of motor units in the right sternocleidomastoid was also dependent on the interaction between group and force direction (F = 2.9, P = 0.004). For the control group, motor unit discharge rate for the right sternocleidomastoid was higher in the 0°, 45°, 270° and 315° directions compared to 180° (all P < 0.05; Fig. 8). On the contrary there were no differences in left or right sternocleidomastoid discharge rate between directions for the patient group.

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Left Sternocleidomastoid

Right Sternocleidomastoid

0°

A

0° 330

30

330

300

300

60

270

90

60

270

90 10

10 240

30

240

120

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30

150 40 µV

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100 150 µV

Fig. 4. Representative directional activation curves for a control subject (A) and a patient (B) performing a circular contraction at 15 N.

The ISI variability was not dependent on group or direction of force. Across all directions of force the ISI variability for the left and right sternocleidomastoid was 17.8 ± 5.6% and 18.3 ± 5.6% for the patient group and 17.0 ± 4.6% and 18.2 ± 5.7% for the control subjects. The motor unit activity was also investigated in the rest periods following each contraction. In these periods, the subjects were asked to fully relax their neck muscles. During the resting periods, it was not possible to detect the activity of any motor unit in the control subjects. On the contrary, in three of the nine patients, single motor unit activity persisted upon completion of the contraction. This continuous activity of the sternocleidomastoid muscle despite ‘‘relaxation” was observed particularly following the contractions performed in the anterior or anterolateral directions (number of occurrences; flexion: 3, ipsilateral anterolateral flexion: 3, contralateral anterolateral flexion: 2, ipsilateral lateral flexion: 1). Fig. 8 illustrates this observation in representative recordings. Fig. 8A shows absence of activity prior and following a contraction

Table 3 Mean and standard deviation of the directional specificity in the surface EMG of the right and left sternocleidomastoid obtained during the circular contractions at both 15 and 30 N of force for the patients with neck pain (n = 9) and control subjects (n = 9). Circular contraction 15 N (%)

Circular Contraction 30 N (%)

Neck pain Right sternocleidomastoid Left sternocleidomastoid

22.1 ± 9.7 21.0 ± 9.6

27.0 ± 9.8 28.7 ± 9.2

Controls Right sternocleidomastoid Left sternocleidomastoid

33.3 ± 18.4 32.1 ± 21.7

37.3 ± 11.5 35.3 ± 14.7

in a control subject; the same behavior was observed in all control subjects and in all force directions. Representative data from the 3 patients who showed post-contraction activity are presented in Fig. 8B–D. Some motor units remained active when the patient was asked to relax post-contraction even if the patient was able to achieve relaxation of the muscle at baseline. In most cases (Fig. 8B and D) this activity only sustained for short intervals (<10 s) and in each case lasted no longer than 20 s (average duration, 8.1 ± 6.1 s). The discharge rate and ISI variability of the motor units active after completion of the contraction were not different during (12.6 ± 1.6 pps and 17.1 ± 7.1%, respectively) or after (12.1 ± 1.9 pps and 19.0 ± 8.2%) the contraction. 4. Discussion In the presence of chronic neck pain the modulation in discharge rate of individual motor units in the sternocleidomastoid muscle differed with respect to control subjects. The neural drive to the muscle was tuned selectively with direction of force production in the control subjects whereas in neck pain patients it was similar for a large range of directions. Further, some patients but not controls showed prolonged motor unit activity following a contraction when they were instructed to rest. Patients with neck pain exhibited reduced neck strength, which is consistent with previous studies (e.g., Ylinen et al., 2004; O’Leary et al., 2007). Furthermore, patients with neck pain showed reduced force steadiness during brief constant force contractions and circular contractions performed at 30 N. It may be argued that the increased coefficient of variation of force for the patients was due to the larger relative intensity of the load, however poor accuracy in maintaining a steady low-load contraction has also been observed for neck pain patients when producing the same relative force compared to controls (O’Leary et al., 2007).

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Left Sternocleidomastoid

Right Sternocleidomastoid

60

60

50

50

* Control NeckPain

40

* * * *

30

*

*

*

*

20

Average Rectified Value (µV)

Average Rectified Value (µV)

*

* *

40

* *

30

*

*

135

180

20

10

10

0

0 0

45

90

135

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225

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315

Directionof Force (°)

0

45

90

225

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315

Directionof Force (°)

Fig. 5. Mean and standard deviation of left and right sternocleidomastoid EMG average rectified value (lV) obtained for the control (n = 9) and patient groups (n = 9) across the 10-s contractions performed at 15 N of force in eight directions (45° intervals from 0° to 360°) in the horizontal plane. The symbols at the top of the image illustrate the directions of force. The patient group showed higher values of sternocleidomastoid average rectified value in all force directions (main effect for group; *P < 0.05).

The surface EMG amplitude of the sternocleidomastoid muscle depended on the direction of activity in asymptomatic individuals, which is consistent with previous studies (Keshner et al., 1989; Vasavada et al., 2002; Blouin et al., 2007). Moreover, the muscle activity was more selectively tuned with increasing load, as shown previously for a similar continuous force sweep in the horizontal plane (Blouin et al., 2007). Conversely, studies that analyzed a discrete set of directions in static contractions reported reduced selectivity in the direction of muscle activity with increasing load (Keshner et al., 1989; Vasavada et al., 2002), indicating differences in the control strategy between continuous sweeps and discrete changes in direction. The main contribution of this study is the analysis of the behavior of individual motor units for multiple force directions in women with neck pain and controls. The discharge rates of the active motor units during a task depend on the net excitatory input to the motor neuron pool and the intrinsic excitability of the motor neurons. It was expected that the excitatory input changed with direction of force with a consistent modulation that reflects the biomechanical efficiency in force production. The results obtained in this study for the control subjects confirmed this hypothesis by revealing a consistent modulation in discharge of motor units across the subject sample. Table 4 Number of motor units detected from the right and left sternocleidomastoid muscle for both groups during 10-s isometric contractions in eight directions of force (0°: flexion, 90°: right lateral flexion, 180°: extension, 270°: left lateral flexion). Force direction

Right sternocleidomastoid

Left sternocleidomastoid

Neck pain

Control

Neck pain

Control

0° 45° 90° 135° 180° 225° 270° 315°

21 18 23 10 5 11 5 20

34 37 28 20 7 5 7 23

33 27 13 8 10 23 34 26

50 28 18 9 4 7 29 36

Total

113

161

175

180

The patient data showed reduced specificity of sternocleidomastoid muscle activation with respect to the controls, resulting in increased activation of the muscle when acting as an antagonist. This result supports the consistent finding of augmented activity of the sternocleidomastoid muscle in patients with neck pain, regardless of the task examined, e.g., cervical flexion (Falla et al., 2004b), cranio-cervical flexion (Jull et al., 2004; Falla et al., 2004d) and movements of the upper limb (Falla et al., 2004a; Johnston et al., 2008). The findings on motor unit behavior confirmed differences between patients and controls in the modulation of the neural drive to the muscle with multidirectional force and indicate a potential change in motor neuron excitability (Fig. 8). Possible explanations for these findings include the direct effects of nociception on motor neuron output, effects of pain on sympathetic activity, and changes in motor planning. Among these mechanisms, an effect of nociceptive input from the sternocleidomastoid muscle is unlikely since patients reported pain in the posterior aspect of their neck and not anteriorly. Furthermore, experimental pain studies have shown that local excitation of splenius capitis nociceptive afferents or sternocleidomastoid afferents following injection of hypertonic saline, results in a consistent reduction in sternocleidomastoid muscle activity (Falla et al., 2007b) and not augmented activity. The reduced modulation in discharge rate of individual motor units in the sternocleidomastoid muscle and enhanced sternocleidomastoid muscle activity for the patient group may be due to an increased sympatho-adrenal outflow as a consequence of pain. Although no direct recordings of sympathetic activity were obtained in this study, neck pain is frequently associated with psychosocial stress which implies sympathetic nervous system activation (e.g., Sterling et al., 2005; Holm et al., 2006). Increased sympathetic activity as a consequence of pain (Janig, 1985), affects muscle function and motor control by modulating local muscle blood flow, muscle contractility and proprioceptive activity from muscle spindle afferents (reviewed by Passatore and Roatta, 2006). More specifically, sympathetic activation depresses the sensitivity of muscle spindles to muscle length changes, especially in jaw and neck muscles (Hunt, 1960; Hunt et al., 1982; Matsuo et al., 1995; Roatta et al., 2002; Hellström et al., 2005), which re-

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Fig. 6. Representative single motor unit recordings from the left sternocleidomastoid muscle of one control subject and one patient with neck pain during the 10-s contractions in constant force directions. The symbols in the center of the image illustrate the directions of force. Segments (500 ms) of intramuscular EMG signals are presented with the identified motor unit discharge represented by circles above each trace. The corresponding template of the identified motor unit is presented to confirm that the same motor unit has been tracked in the different force directions. Note the modulation in the discharge rate for the control subject but consistent discharge rate for the patient.

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Fig. 7. Mean and standard deviation of left and right sternocleidomastoid motor unit discharge rate (pps: pulses per second) for the control (n = 9) and patient groups (n = 9) during 10-s contractions performed at 15 N of force in eight directions (45° intervals from 0° to 360°) in the horizontal plane. The symbols at the top of the image illustrate the directions of force. No differences in left or right sternocleidomastoid discharge rate were identified between the different directions of force for the patient group. The horizontal bars indicate significant differences (*P < 0.05) in motor unit discharge rate between different directions of force in the control group.

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Fig. 8. Representative single motor unit recordings from the sternocleidomastoid muscle of one control subject (A) and three patients with neck pain (B–D) obtained at rest, during a 10-s contraction in a constant force directions and immediately following the contraction when the subjects have been asked to relax completely. Ten second recordings of intramuscular EMG signals are presented with the identified motor unit discharges represented by circles above each trace together with the corresponding template of the identified motor units. Note that the control subject and patients were able to fully relax their sternocleidomastoid muscle prior to contraction. Although the control subject was able to fully relax the sternocleidomastoid muscle following the 10-s contraction at 15 N of force, the patient data illustrate examples of persistent single motor unit activity even though the patients have been instructed to relax.

sults in impaired proprioception and reduced efficiency and precision of movements. The increased neural drive to the sternocleidomastoid muscle in the patient group may therefore reflect an attempt to enhance kinesthetic sense by muscular contraction since increased muscle activity can enhance the acuity of movement detection (Gandevia et al., 1992). Increased sympatho-adrenal outflow can also induce changes in the input–output relations for motor neurons by providing metabotropic input. Noradrenaline facilitates the generation of persistent inward currents in spinal motor neurons which affects their excitability (Lee and Heckman, 1999). Increased motor neuron excitability produces higher motor unit discharge rates with similar excitatory input which is in agreement with the observed higher activity of antagonist muscles in the patient group. In the present study motor unit activity was also recorded during the rest periods as it was hypothesized that motor unit activity would persist in patients. In the rest periods, some but not all of the patients showed motor unit activity despite the instruction to fully relax their muscles. Although this observation was not consistent across all patients, it does partly support our hypothesis and the possibility of a contribution of persistent inward currents to the results shown since during relaxation the input to motor neurons should be null. This interpretation is supported by the

observations that these patients could voluntarily relax before a contraction but not immediately after a contraction, and is in agreement with the presence of activity-induced persistent inward currents (Heckman et al., 2008). In addition to these effects, experimental pain studies suggest that the central motor strategy is different in the presence of neck pain. When pain is acutely induced in the neck muscles of healthy subjects, the coordination among neck muscles is substantially altered (Falla et al., 2007b). Previous clinical data also show the presence of altered motor strategies suggestive of changes in motor planning. For example, when people with neck pain perform rapid shoulder flexion or extension, the onset of the neck flexors is delayed and is not a preplanned response contrary to healthy controls (Falla et al., 2004c). Thus, the differences in modulation of motor unit discharge in the patients and control subjects observed in this study are likely to be partly due to different control strategies. The strategy adopted by the patients, despite being inefficient, may reflect an attempt to voluntarily increase the stability of the head for the fear of performing potentially painful movements or the need to compensate for decreased activity of the deep cervical muscles (Falla et al., 2004d). Various theories have been proposed to explain the link between pain and alterations in motor activity. The pain-adaptation

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model predicts an inhibitory effect of pain on motor neurons during agonist activity and an excitatory effect during antagonist action (Lund et al., 1991). Although experimental neck pain studies support this model by showing a consistent pain-induced inhibition of agonist muscle activity (Falla et al., 2007a,b), the results of the present clinical study do not fully support this model since increased activity of the sternocleidomastoid muscle was observed for the patients during contractions in flexion and anterolateral flexion, even though increased antagonist activity was observed. However, the patients in this study did not report pain in the sternocleidomastoid muscle, thus a direct comparison with experimental pain models is not possible. Contrary to the painadaptation model, the vicious cycle theory suggests an increased muscle activity as a consequence of activation of group III and IV muscle afferents (Travell et al., 1942; Johansson and Sojka, 1991). This theory has been supported by several animal experiments (Johansson et al., 1993; Djupsjobacka et al., 1994; Thunberg et al., 2001). In this clinical study, augmented activity of the sternocleidomastoid muscle was observed for the patient group regardless of the direction of force which seems in agreement with the vicious cycle theory. Nevertheless, reduced activity of other neck muscles (e.g., the deeper cervical flexors) has been shown in patients with neck pain (Falla et al., 2004c). In conclusion, reduced modulation of the discharge rate of individual motor units in the sternocleidomastoid muscle was observed in women with chronic neck pain with some women showing prolonged motor unit activity when instructed to relax. These observations indicate a change in the modulation of the neural drive to muscles in the presence of pain. The results are compatible with either an increase in input to the motor neurons when the sternocleidomastoid acts as an antagonist or increased excitability of the motor neurons. Acknowledgments Supported by the Danish Medical Research Council, Kiropraktorfonden, Denmark and Østifterne, Denmark. References Blouin JS, Siegmund GP, Carpenter MG, Inglis JT. Neural control of superficial and deep neck muscles in humans. J Neurophysiol 2007;98:920–8. Djupsjobacka M, Johansson H, Bergenheim M. Influences on the gamma-muscle spindle system from muscle afferents stimulated by increased intramuscular concentrations of arachidonic acid. Brain Res 1994;663:293–302. Dutia MB. The muscles and joints of the neck: their specialisation and role in head movement. Prog Neurobiol 1991;37:165–78. Falla D, Bilenkij G, Jull G. Patients with chronic neck pain demonstrate altered patterns of muscle activation during performance of a functional upper limb task. Spine 2004a;29:1436–40. Falla D, Dall’Alba P, Rainoldi A, Merletti R, Jull G. Location of innervation zones of sternocleidomastoid and scalene muscles – a basis for clinical and research electromyography applications. Clin Neurophysiol 2002;113:57–63. Falla D, Farina D, Graven-Nielsen T. Experimental muscle pain results in reorganization of coordination among trapezius muscle subdivisions during repetitive shoulder flexion. Exp Brain Res 2007a;178:385–93. Falla D, Farina D, Kanstrup Dahl M, Graven-Nielsen T. Muscle pain induces taskdependent changes in cervical agonist/antagonist activity. J Appl Physiol 2007b;102:601–9. Falla D, Jull G, Edwards S, Koh K, Rainoldi A. Neuromuscular efficiency of the sternocleidomastoid and anterior scalene muscles in patients with chronic neck pain. Disabil Rehabil 2004b;26:712–7. Falla D, Jull G, Hodges PW. Feedforward activity of the cervical flexor muscles during voluntary arm movements is delayed in chronic neck pain. Exp Brain Res 2004c;157:43–8. Falla D, Jull G, Hodges PW. Patients with neck pain demonstrate reduced electromyographic activity of the deep cervical flexor muscles during performance of the craniocervical flexion test. Spine 2004d;29:2108–14. Fernandez-de-las-Penas C, Falla D, Arendt-Nielsen L, Farina D. Cervical muscle coactivation in isometric contractions is enhanced in chronic tension-type headache patients. Cephalalgia 2008;28:744–51.

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