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The pain-induced change in relative activation of upper trapezius muscle regions is independent of the site of noxious stimulation
Clinical Neurophysiology 120 (2009) 150–157
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The pain-induced change in relative activation of upper trapezius muscle regions is independent of the site of noxious stimulation D. Falla *, L. Arendt-Nielsen, D. Farina Center for Sensory-Motor Interaction (SMI), Department of Health Science and Technology, Aalborg University, Fredrik Bajers Vej 7, D-3, 9220 Aalborg, Denmark
a r t i c l e
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Article history: Accepted 12 October 2008 Available online 22 November 2008 Keywords: Experimental muscle pain Multi-channel electromyography Muscle topography Upper trapezius muscle
a b s t r a c t Objective: To assess the effect of local excitation of nociceptors at different locations of the upper trapezius muscle on the spatial distribution of upper trapezius electromyographic (EMG) amplitude during sustained contraction. Methods: Surface (EMG) signals were recorded from the upper trapezius muscle with a grid of 10 5 electrodes from nine healthy men during 90° shoulder abduction sustained for 60 s. In one experimental session, the subjects received separate injections of 0.4 ml of hypertonic saline (experimental muscle pain) into the cranial and caudal region of the upper trapezius. In a separate experimental session the same subjects received two injections of 0.2 ml each of hypertonic saline simultaneously in the cranial and caudal region. The EMG root mean square (RMS) values were computed for each electrode location to provide a topographical map of EMG amplitude. Results: The RMS value averaged across all electrode locations decreased following injection of hypertonic saline (P < 0.05) by a similar amount for the two experimental sessions. The pain-induced decrease was larger in the cranial than in the caudal region for both experimental sessions, as evidenced by a shift of the EMG amplitude distribution towards the caudal region of the muscle (P < 0.0001). Conclusion: Muscle pain induces a consistent change in the spatial activation of the upper trapezius muscle which is independent of the site of noxious stimulation. Significance: Pain-induced changes in the spatial distribution of muscle activity may induce overload of specific muscle regions in the long term. Ó 2008 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved.
1. Introduction Muscle pain influences motor control via numerous reflex and central mechanisms (Arendt-Nielsen and Graven-Nielsen, 2008). Experimental muscle pain frequently results in reduced activation of the painful muscle (Graven-Nielsen et al., 1997b; Svensson et al., 1998; Farina et al., 2004; Falla et al., 2007b), which reflects decreased neural drive from the spinal cord to the muscle (Sohn et al., 2000; Farina et al., 2004). This inhibition is due to a combination of reflex mechanisms mediated by small diameter muscle afferents and reduced supraspinal drive to the muscle. Motor units in the caudal region of the upper trapezius muscle have greater discharge rates during sustained shoulder abduction than motor units in more cranial regions (Falla and Farina, 2008a,b). This observation suggests that motor units in the caudal region have lower recruitment thresholds than those in the cranial region and is in agreement with the characteristic increase in surface EMG amplitude towards the cranial region with increasing * Corresponding author. Tel.: +45 96 35 74 59; fax: +45 98 15 40 08. E-mail address: [email protected] (D. Falla).
force (Holtermann and Roeleveld, 2006). Since pain decreases the net excitatory drive to the motor neurons (Sohn et al., 2000; Wang et al., 2000; Farina et al., 2004), the presence of pain in the upper trapezius is expected to reduce muscle activity predominantly in the cranial region, where motor units have higher threshold for activation. Consistent with this hypothesis, excitation of nociceptors in the cranial region of the upper trapezius muscle by intramuscular injection of hypertonic saline has been shown to induce a relatively larger reduction of EMG amplitude in cranial compared to caudal regions during static tasks (Madeleine et al., 2006). However, this observation was limited to a single injection site which was located in the cranial region of the muscle. Therefore it could not be discriminated if the observed response corresponded to a spatial matching between the pain stimulus and inhibition or if rather it was a general response of the muscle to a painful stimulus independent of the injection site. Changes in the activation of upper trapezius have been observed in people with neck and shoulder disorders. These include reduced activation during a repetitive upper limb task (Falla et al., 2004), increased activity during computer work (Szeto et al., 2005), reduced ability to relax the upper trapezius muscles
1388-2457/$34.00 Ó 2008 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.clinph.2008.10.148
D. Falla et al. / Clinical Neurophysiology 120 (2009) 150–157
following voluntary activation (Falla et al., 2004) and reduced rest periods of the upper trapezius muscle during repetitive tasks (Veiersted et al., 1990; Hägg and Aström, 1997; Fredin et al., 1997). Given the common complaint of upper trapezius muscle pain and the alterations of upper trapezius activity which have been frequently documented in people with neck and shoulder disorders, further studies investigating the basic effect of pain on the activation of the trapezius muscle are warranted. In particular, the effect of pain on the distribution of upper trapezius activity may be relevant for interpreting changes in trapezius activity in clinical pain conditions and offer further insight into the hypothesis of overload of muscle regions and overexertion of low-threshold motor units in the presence of upper trapezius pain (Hägg, 1991). In this study it is hypothesized that experimentally induced muscle pain results in a greater reduction of EMG amplitude in the cranial region (higher threshold for activation) of the upper trapezius independent of the site of nociceptive stimulation within the muscle. Therefore, the purpose of the study was to assess the effect of experimentally induced muscle pain at different locations of the upper trapezius muscle on the spatial distribution of upper trapezius EMG amplitude.
2. Methods 2.1. Subjects Nine men participated in the study after providing informed consent. The participants (age: 26.4 ± 4.4 year; height: 179.3 ± 9.0 cm; weight: 78.4 ± 14.5 kg) were free of shoulder and neck pain, had no past history of orthopaedic disorders affecting the shoulder or neck region and no history of neurological disorders. All participants were right hand dominant. Ethical approval for the study was granted by the local Ethics Committee (VN 2005/38) and all procedures were conducted according to the Declaration of Helsinki. 2.2. Experimental design Subjects attended two experimental sessions separated by a minimum of 48 and maximum of 72 h (Fig. 1). In both sessions experimental muscle pain was induced by injection (27G needle) of sterile hypertonic saline (5.8%) into the upper division of the trapezius on the right side. In one experimental session (session A; Fig. 1), subjects received separate injections (individual bolus) of 0.4 ml of hypertonic saline into the cranial and caudal region of the upper trapezius. The cranial and caudal locations were defined as 15 mm cranial and 40 mm caudal to the line between the acromion and the spinous process of the seventh cervical vertebra, respectively. In addition, subjects received an injection of isotonic saline (0.4 ml, 0.9%) into the trapezius muscle at either the caudal or cranial location (randomized across subjects). In the other experimental session (session B; Fig. 1) subjects received two injections of 0.2 ml of hypertonic saline (total 0.4 ml), delivered simultaneously by two investigators in the caudal and cranial region. In addition subjects received injections of isotonic saline (0.2 ml, 0.9%) at both locations simultaneously. The bolus was injected over a 10-s period for all injections. The order of the experimental sessions (simultaneous injections or individual injection) was randomized across subjects. In each experimental session the isotonic saline injection was given first. However, participants were told that each injection may or may not be painful. A rest of 10 min was provided between injections. Following the hypertonic saline injection, the rest period commenced when pain was no longer reported.
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2.3. Procedure In both experimental sessions subjects were comfortably seated in a chair with their back supported, knees in 90° of flexion and feet flat on the ground. The subjects were asked to hold both arms in 90° of abduction for 60 s, with elbows fully extended and forearms pronated with palms facing toward the ground. Two flexible bars positioned on a board behind the subject extended horizontally over the subjects shoulders to provide tactile position feedback. The bars also allowed the investigator to monitor the subjects shoulder position during the 60 s contraction to ensure that the subject did not move their arms in the transverse or coronal planes. Guides were also placed behind and on the side of the subject which were used by the investigator to ensure the same position of the neck and head in all contractions. The sustained contraction was performed before, and immediately following the injection of hypertonic and isotonic saline into the right (dominant side) upper trapezius muscle. 2.4. Sensory assessment Participants were asked to verbally rate their level of perceived pain intensity on an 11 point numerical rating scale (NRS) with ‘‘no pain” equal to 0 and ‘‘the worst possible pain imaginable” equal to 10. Pain intensity ratings were obtained immediately following the injection and every 30 s until pain was no longer reported. Peak pain intensity and duration of pain were extracted. Participants documented the area of pain on a body chart. Pain drawings were subsequently digitized (ACECAD D9000 + Taiwan) and pain areas were measured. 2.5. Multi-channel surface EMG Prior to electrode placement, the main innervation zone location of the upper trapezius along the seventh cervical vertebra (C7)–acromion line was identified with an array of eight electrodes (silver bars, 5-mm long, 1-mm diameter, 5-mm interelectrode distance), as previously described (Farina et al., 2002). During the experimental measures, surface EMG signals were detected with a semi-disposable adhesive grid of electrodes (LISiN-OT Bioelettronica, Torino, Italy). The grid consists of 10 rows and 5 columns of electrodes (1-mm diameter, 8-mm interelectrode distance in both directions) with one electrode absent from the upper right corner. The position corresponding to the absent electrode was used as the origin of the coordinate system to define the electrode location. The subject’s skin was prepared by gentle local abrasion using abrasive paste (Medic-Every, Parma, Italy) and cleaned with water. The electrode grid was placed with the fourth row along the C7–acromion line and with the most lateral electrode column 10-mm distant from the innervation zone location. Thus the injections were performed lateral to the electrode grid (10 mm) and corresponded to the second and ninth row for the cranial and caudal locations, respectively (Fig. 2). 30 ll of conductive gel was inserted into each cavity of the grid to provide electrode-skin contact. A reference electrode was placed around the right wrist. 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 by a 12-bit analog-to-digital converter. 2.6. Signal analysis Surface EMG signals were off-line band-pass filtered (second order Butterworth filter; 3 dB bandwidth, 10–400 Hz). 39 bipolar EMG signals along the direction of the muscle fibers were obtained
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Fig. 1. Schematic representation of the experimental sessions. Participants attend two experimental sessions separated by a minimum of 48 and maximum of 72 h. The locations of the injections are defined in Fig. 2.
from the grid (10 4 bipolar recordings with one absent electrode). Root mean square (RMS) values were computed from each bipolar recording from adjacent, non-overlapping signal epochs of 1-s duration, as described previously (Merletti et al., 1990). For graphical representation, the 39 values were interpolated by a factor of 8 but only the original values were used for data processing and statistical analysis. To characterize the spatial distribution of muscle activity, the following variables were extracted from the
39 bipolar signals: RMS averaged over the 39 signals and the two coordinates of the centroid of the root mean square map (x- and y-axis coordinates for the medial-lateral and cranial-caudal direction, respectively) (Farina et al., 2008). Consecutive values over time of RMS, x- and y-axis coordinates of the centroid were averaged to obtain mean values corresponding to 5-s intervals of the sustained contraction. In addition, the difference in the position of the y-axis coordinate of the centroid
Fig. 2. Surface EMG signals were detected using a semi-disposable adhesive grid of electrodes over the right upper trapezius muscle. The grid consists of 10 rows and 5 columns of electrodes with one electrode absent at the upper right corner. The electrode grid was placed with the fourth row along the C7–acromion line. Injections were performed lateral to the electrode grid (10 mm) and corresponded to the second row of the grid for the cranial location and ninth row for the caudal location. For the simultaneous injection condition, injections were performed in the cranial and caudal locations simultaneously.
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between the painful conditions and baseline conditions was obtained for each epoch. The shift of the centroid over time was defined as the modulus of the centroid displacement in the medial-lateral and cranial-caudal direction with respect to the position at the beginning of the contraction. 2.7. Statistical analysis One-way ANOVA were applied to parameters of pain intensity, duration and area with injection (hypertonic cranial, hypertonic caudal, hypertonic combined, isotonic individual and isotonic combined) as repeated measures. Two-way ANOVA were applied to values of RMS, and x- and y-axis coordinates for the combined injection condition with factors, condition (baseline, isotonic, hypertonic) and time (12 time intervals of 5 s) as repeated measures. Moreover, two-way ANOVA were applied to values of RMS, and x- and y-axis coordinates for the individual injection condition with factors, condition (baseline, isotonic, hypertonic cranial, hypertonic caudal) and time (12 time intervals of 5 s) as repeated measures. Differences in the position of the y-axis coordinate between the baseline and painful condition were compared using a two-way ANOVA with condition (hypertonic cranial, hypertonic caudal, hypertonic combined) and time (12 time intervals of 5 s) as repeated measures. A two-way ANOVA was utilized to compare the shift of the centroid of the RMS map across the sustained contraction for both the individual and simultaneous injection conditions with factors, condition and time (11 time instants) as repeated measures. Significant differences revealed by ANOVA were followed by post-hoc Student–Newman–Keuls (SNK) pair-wise comparisons. Results are reported as mean and standard deviation (SD) in the text and standard error (SE) in the figures. Statistical significance was set at P < 0.05. 3. Results 3.1. Sensory characteristics Peak pain intensity was greater following the injection of hypertonic (simultaneous injections: 4.6 ± 1.7, caudal: 4.1 ± 1.7, cranial: 4.2 ± 0.9) compared to isotonic saline in all conditions (F = 32.4, P < 0.00001; Fig. 1). No differences in peak pain intensity were identified between the hypertonic saline injections given at
3.2. EMG amplitude RMS values averaged over all locations of the grid were reduced across the entire duration of the 60 s shoulder abduction contraction following the simultaneous hypertonic saline injections compared to both baseline and isotonic saline conditions (ANOVA: F = 5.1, P < 0.05, SNK both P < 0.05; Fig. 5A). Moreover, individual injections of hypertonic saline in the cranial or caudal region of the upper trapezius resulted in lower RMS values compared to baseline and isotonic conditions (ANOVA: F = 9.2, P < 0.001; SNK: all P < 0.01; Fig. 5A). The average RMS remained constant across the duration of the contraction for the baseline and isotonic conditions. However, a condition by time interaction revealed that the average RMS increased over time following injection of hypertonic saline in either the caudal or cranial region of upper trapezius or following the injections performed simultaneously (ANOVA: F = 2.4, P < 0.0001; SNK: P < 0.05). 3.3. Changes in the root mean square map The x-axis coordinate of the RMS map was not dependent on time or condition (Fig. 6A). In both experimental sessions the ycoordinate of the RMS map reduced across the duration of the contraction (simultaneous and individual injection experimental sessions: F = 12.8, P < 0.00001 and F = 14.96, P < 0.00001, respectively; Fig. 6B) indicating a shift of activity towards the cranial region of the muscle. Following the injection of hypertonic saline, higher estimates of the y-axis coordinate of the RMS map were observed compared to both baseline and isotonic injection conditions indicating a shift of activity towards the caudal region (simultaneous and individual injection experimental sessions: F = 15.6, P < 0.0001 and F = 16.9, P < 0.00001, respectively; Figs. 6B and 7). Differences in the position of the y-axis coordinate 6
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single sites or when injected at both sites simultaneously (SNK: P > 0.41). Pain duration and area were not dependent on the location of the hypertonic saline injection (P = 0.83 and P = 0.76, respectively; Figs. 3 and 4). Total mapped pain areas were 5.3 ± 3.5, 4.5 ± 4.8 and 4.2 ± 3.8 (arbitrary units) for the simultaneous, caudal and cranial hypertonic saline injections, respectively. Both isotonic saline injections (simultaneous and individual) produced lower scores on all measured pain parameters compared to the hypertonic saline injections (P < 0.05).
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Fig. 3. Mean (±SE) pain intensity scores following individual injections of 0.4 ml of hypertonic saline into the cranial and caudal region of the upper trapezius and following injections of 0.2 ml of hypertonic saline in the caudal and cranial region simultaneously (total 0.4 ml). Similar injections of isotonic saline were given as control injections.
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Hypertonic Cranial and Caudal Simultaneously
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Fig. 4. Area of pain reported following individual injections of 0.4 ml of hypertonic saline into the cranial and caudal region of the upper trapezius and following injections of 0.2 ml of hypertonic saline in the caudal and cranial region simultaneously (total 0.4 ml). Area of pain is also shown following injection of 0.4 ml isotonic saline into either the cranial or caudal region of the muscle.
between the baseline and painful condition were not dependent on the location of the injection or time. The centroid of the EMG amplitude map moved in the cranial direction across the duration of the sustained contraction (simultaneous and individual injection experimental sessions: F = 8.8, P < 0.000001 and F = 7.8, P < 0.00001, respectively; Fig. 8) and was not influenced by intramuscular injection of hypertonic saline.
previous reports of hypertonic saline-induced upper trapezius muscle pain (Ge et al., 2005; Komiyama et al., 2005; Falla et al., 2007a). Previously it has been shown that four simultaneous but spatially separated injections of 0.1 ml hypertonic saline into the tibialis anterior muscle induce a greater pain intensity, distributed over a larger area compared to a single injection of 0.1 ml hypertonic saline (Graven-Nielsen et al., 1997a), consistent with an increased perceived pain intensity due to spatial summation (Price et al., 1989). However, it was also shown that the intensity of pain induced by infusion of 0.4 ml hypertonic saline at spatially separated sites or injection of 0.4 ml at a single site was comparable (Graven-Nielsen et al., 1997a), which is consistent with the observations in the present study.
4. Discussion Intramuscular injection of hypertonic saline into the upper trapezius muscle induced a relatively larger reduction of upper trapezius EMG amplitude in the cranial compared to caudal regions of the muscle independent of the location of noxious stimulation. This finding indicates that muscle regions with a higher threshold of activation are the most inhibited in the presence of pain.
4.2. Spatial distribution of EMG amplitude During the sustained contraction the cranial region became progressively more active than the caudal region consistent with observations from previous surface EMG studies (Madeleine et al., 2006; Falla and Farina, 2007; Farina et al., 2008).
4.1. Sensory responses Injection of hypertonic saline in the upper trapezius muscle resulted in muscle pain of moderate intensity, consistent with
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Fig. 5. Mean (±SE) of the average root mean square (RMS) estimated at 5-s intervals throughout sustained shoulder abduction before and following individual injections of 0.4 ml isotonic and hypertonic saline into the cranial and caudal region of the upper trapezius and following injections of 0.2 ml of isotonic and hypertonic saline in the caudal and cranial region simultaneously (total 0.4 ml). Significant difference of hypertonic saline conditions compared to baseline and isotonic condition: *P < 0.05.
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Fig. 6. Mean (±SE) of the x-axis coordinate (A) and y-axis coordinate (B) of the centroid of the RMS map, estimated at 5-s intervals throughout sustained shoulder abduction before and following individual injections of 0.4 ml isotonic and hypertonic saline into the cranial and caudal region of the upper trapezius and following injections of 0.2 ml of isotonic and hypertonic saline in the caudal and cranial region simultaneously (total 0.4 ml). Significant difference of hypertonic saline condition compared to baseline and isotonic condition: *P < 0.0001.
It has been shown that excitation of nociceptors in the cranial region of the upper trapezius muscle results in a relatively larger reduction in EMG amplitude in cranial compared to caudal regions which was revealed by a shift of the EMG amplitude distribution towards the caudal fibers of the upper trapezius muscle (Madeleine et al., 2006). A novel finding of the current study is that the same change in activation occurred following excitation of nociceptive afferent fibers in the caudal region of the upper trapezius or in both the caudal and cranial locations simultaneously. Thus, the pattern of inhibition was the same regardless of the site of nociceptive stimulation. Several studies have shown a reduction in interference EMG amplitude when a localized noxious stimulus is applied to a muscle (e.g. Graven-Nielsen et al., 1997b; Svensson et al., 1998). The results of this study also show a global reduction in upper trapezius EMG amplitude following injection of hypertonic saline. However, assessment of the EMG amplitude distribution across the upper trapezius muscle revealed that the greatest reduction in EMG amplitude was not always local to the site of noxious stimulation. Thus, a shift of the distribution of muscle activity towards the painful region was observed when hypertonic saline was injected into the caudal region of the upper trapezius muscle.
The task performed in this study corresponded to 15–20% of the maximum voluntary contraction of the trapezius muscle (Mathiassen et al., 1995). At this contraction intensity it is likely that only type I motor units were active (Stephens and Usherwood, 1977). Across these motor units, those in the caudal region of the upper trapezius have been observed to discharge at higher rates for a given force (Falla and Farina, 2008a) and to be recruited at lower forces than motor units in the cranial region (Holtermann and Roeleveld, 2006). Thus, the results of this study suggest that nociceptive input reduces the net excitatory input to the population of motor neurons, resulting in reduced activation and derecruitment, with derecruitment following the reverse order of recruitment. Reduced excitatory input may be due to decreased descending drive to the painful muscle or to pure spinal mechanisms, or more likely, a combination of both. In the present study the electrode was positioned in order to be within the region of the upper trapezius and achieve coverage of a large proportion of the upper trapezius in the longitudinal direction. It may be argued that in some cases (e.g. smaller subjects) the caudal region of the electrode grid covered a portion of the middle division of trapezius. However, this possibility would not affect the main result of this study; that muscle regions with a
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Fig. 7. Representative topographical maps (interpolation by a factor 8) of the EMG root mean square value recorded for one subject for the first 5 s of the sustained shoulder abduction contraction performed at baseline and following individual injections of 0.4 ml of hypertonic saline into the cranial and caudal region of the upper trapezius (session A). Topographical maps are also displayed for the same subject from a separate experimental session (session B) for the sustained contraction performed at baseline and following injections of 0.2 ml of hypertonic saline in the caudal and cranial region simultaneously (total 0.4 ml). Colors are scaled between the minimum and maximum RMS values. Areas of dark blue correspond to areas of low EMG amplitude and dark red to areas of high EMG amplitude. Note the greatest reduction in EMG amplitude is consistently for the cranial location. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this paper.)
higher threshold of activation are the most inhibited in the presence of pain.
This finding offers some support to the hypothesis that low-threshold motor units are continuously active even in the presence of pain (Cinderella Hypothesis) (Hägg, 1991) and may have implications for the development of chronic neck and shoulder pain. Although the cranial region of the upper trapezius showed the greatest pain-induced reduction in activity for the task of shoulder abduction, other regions of the muscle may show a greater inhibition in different tasks with different biomechanical demands.
4.3. Implications Injection of hypertonic saline into the caudal region of the upper trapezius muscle resulted in a greater inhibition of activity at a site distant to the location of the injection compared to the actual site of noxious stimulation. This observation indicates that the painful region of a muscle is not always the most ‘‘protected”. The consistent change in the motor strategy which was observed suggests that regions of the muscle with a higher threshold for activation are the first to be inhibited. As a consequence the region of the upper trapezius muscle which is first to be activated during shoulder abduction remains continuously active in the presence of pain.
5. Conclusion Muscle pain induces a decrease in the net excitatory input to the motor neuron pool innervating the painful muscle, which causes reduced muscle activity. Motor neurons with a higher threshold for activation and lower discharge rate at a given force
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Fig. 8. Mean (±SE) of the displacement of the centroid estimated from the surface EMG signals during 60 s sustained shoulder abduction before and following individual injections of 0.4 ml isotonic and hypertonic saline into the cranial and caudal region of the upper trapezius and following injections of 0.2 ml of isotonic and hypertonic saline in the caudal and cranial region simultaneously (total 0.4 ml).
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are those first derecruited by the decreased synaptic input. As a consequence, pain induces a change in the spatial distribution of muscle activity for muscles characterized by non-uniform spatial recruitment of motor units, such as the upper trapezius. Acknowledgments Deborah Falla is supported by the National Health and Medical Research Council of Australia (ID 351678). References Arendt-Nielsen L, Graven-Nielsen T. Muscle pain: sensory implications and interaction with motor control. Clin J Pain 2008;24:291–8. Falla D, Farina D. Periodic increases in force during sustained contraction reduce fatigue and facilitate spatial redistribution of trapezius muscle activity. Exp Brain Res 2007;182:99–107. Falla D, Farina D. Motor units in cranial and caudal regions of the upper trapezius muscle have different discharge rates during brief static contractions. Acta Physiol (Oxf) 2008a;192:551–8. Falla D, Farina D. Non-uniform adaptation of motor unit discharge rates during sustained static contraction of the upper trapezius muscle. Exp Brain Res 2008b;191:363–70. 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 2004;29:1436–40. 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. Farina D, Madeleine P, Graven-Nielsen T, Merletti R, Arendt-Nielsen L. Standardising surface electromyogram recordings for assessment of activity and fatigue in the human upper trapezius muscle. Eur J Appl Physiol 2002;86:469–78. Farina D, Arendt-Nielsen L, Merletti R, Graven-Nielsen T. Effect of experimental muscle pain on motor unit firing rate and conduction velocity. J Neurophysiol 2004;91:1250–9. Farina D, Leclerc F, Arendt-Nielsen L, Buttelli O, Madeleine P. The change in spatial distribution of upper trapezius muscle activity is correlated to contraction duration. J Electromyogr Kinesiol 2008;18:16–25. Fredin Y, Elert J, Britschgi N, Nyberg V, Vaher A, Gerdle B. A decreased ability to relax between repetitive muscle contractions in patients with chronic symptoms after whiplash trauma of the neck. J Musculoskel Pain 1997;5:55–70. Ge HY, Arendt-Nielsen L, Farina D, Madeleine P. Gender-specific differences in electromyographic changes and perceived pain induced by experimental
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muscle pain during sustained contractions of the upper trapezius muscle. Muscle Nerve 2005;32:726–33. Graven-Nielsen T, Arendt-Nielsen L, Svensson P, Jensen TS. Quantification of local and referred muscle pain in humans after sequential i.m. injections of hypertonic saline. Pain 1997a;69:111–7. Graven-Nielsen T, Svensson P, Arendt-Nielsen L. Effects of experimental muscle pain on muscle activity and co-ordination during static and dynamic motor function. Electroenc Clin Neurogr 1997b;105:156–64. Hägg GM. Static work loads and occupational myalgia – a new explanation model. In: Anderson PA, Hobart DJ, Danoff JV, editors. Electromyographical kinesiology. Amsterdam: Elsevier; 1991. p. 141–3. Hägg GM, Aström A. Load pattern and pressure pain threshold in the upper trapezius muscle and psychosocial factors in medical secretaries with and without shoulder/neck disorders. Int Arch Occup Environ Health 1997;69:423–32. Holtermann A, Roeleveld K. EMG amplitude distribution changes over the upper trapezius muscle are similar in sustained and ramp contractions. Acta Physiol 2006;186:159–68. Komiyama O, Arai M, Kawara M, Kobayashi K, De Laat A. Pain patterns and mandibular dysfunction following experimental trapezius muscle pain. J Orofac Pain 2005;19:119–26. Madeleine P, Leclerc F, Arendt-Nielsen L, Ravier P, Farina D. Experimental muscle pain changes the spatial distribution of upper trapezius muscle activity during sustained contraction. Clin Neurophysiol 2006;117:2436–45. Mathiassen SE, Winkel J, Hagg GM. Normalisation of surface EMG amplitude from the upper trapezius muscle in ergonomic studies – a review. J Electromyogr Kinesiol 1995;5:197–226. Merletti R, Knaflitz M, De Luca CJ. Myoelectric manifestations of fatigue in voluntary and electrically elicited contractions. J Appl Physiol 1990;69:1810–20. Price DD, McHaffie JG, Larson MA. Spatial summation of heat-induced pain: influence of stimulus area and spatial separation of stimuli on perceived pain sensation intensity and unpleasantness. J Neurophysiol 1989;62:1270–9. Sohn MK, Graven-Nielsen T, Arendt-Nielsen L, Svensson P. Inhibition of motor unit firing during experimental muscle pain in humans. Muscle Nerve 2000;23:1219–26. Stephens JA, Usherwood TP. The mechanical properties of human motor units with special reference to their fatigability and recruitment threshold. Brain Res 1977;125:91–7. Svensson P, Arendt-Nielsen L, Houe L. Muscle pain modulates mastication: an experimental study in humans. J Orofac Pain 1998;12:7–16. Szeto GP, Straker LM, O’Sullivan PB. A comparison of symptomatic and asymptomatic office workers performing monotonous keyboard work 1: neck and shoulder muscle recruitment patterns. Man Ther 2005;10:270–80. Veiersted KB, Westgaard RH, Andersen P. Pattern of muscle activity during stereotyped work and its relation to muscle pain. Int Arch Occup Environ Health 1990;62:31–41. Wang K, Arima T, Arendt-Nielsen L, Svensson P. EMG-force relationships are influenced by experimental jaw-muscle pain. J Oral Rehabil 2000;27:394–402.
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Clinical Neurophysiology journal homepage: www.elsevier.com/locate/clinph
The pain-induced change in relative activation of upper trapezius muscle regions is independent of the site of noxious stimulation D. Falla *, L. Arendt-Nielsen, D. Farina Center for Sensory-Motor Interaction (SMI), Department of Health Science and Technology, Aalborg University, Fredrik Bajers Vej 7, D-3, 9220 Aalborg, Denmark
a r t i c l e
i n f o
Article history: Accepted 12 October 2008 Available online 22 November 2008 Keywords: Experimental muscle pain Multi-channel electromyography Muscle topography Upper trapezius muscle
a b s t r a c t Objective: To assess the effect of local excitation of nociceptors at different locations of the upper trapezius muscle on the spatial distribution of upper trapezius electromyographic (EMG) amplitude during sustained contraction. Methods: Surface (EMG) signals were recorded from the upper trapezius muscle with a grid of 10 5 electrodes from nine healthy men during 90° shoulder abduction sustained for 60 s. In one experimental session, the subjects received separate injections of 0.4 ml of hypertonic saline (experimental muscle pain) into the cranial and caudal region of the upper trapezius. In a separate experimental session the same subjects received two injections of 0.2 ml each of hypertonic saline simultaneously in the cranial and caudal region. The EMG root mean square (RMS) values were computed for each electrode location to provide a topographical map of EMG amplitude. Results: The RMS value averaged across all electrode locations decreased following injection of hypertonic saline (P < 0.05) by a similar amount for the two experimental sessions. The pain-induced decrease was larger in the cranial than in the caudal region for both experimental sessions, as evidenced by a shift of the EMG amplitude distribution towards the caudal region of the muscle (P < 0.0001). Conclusion: Muscle pain induces a consistent change in the spatial activation of the upper trapezius muscle which is independent of the site of noxious stimulation. Significance: Pain-induced changes in the spatial distribution of muscle activity may induce overload of specific muscle regions in the long term. Ó 2008 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved.
1. Introduction Muscle pain influences motor control via numerous reflex and central mechanisms (Arendt-Nielsen and Graven-Nielsen, 2008). Experimental muscle pain frequently results in reduced activation of the painful muscle (Graven-Nielsen et al., 1997b; Svensson et al., 1998; Farina et al., 2004; Falla et al., 2007b), which reflects decreased neural drive from the spinal cord to the muscle (Sohn et al., 2000; Farina et al., 2004). This inhibition is due to a combination of reflex mechanisms mediated by small diameter muscle afferents and reduced supraspinal drive to the muscle. Motor units in the caudal region of the upper trapezius muscle have greater discharge rates during sustained shoulder abduction than motor units in more cranial regions (Falla and Farina, 2008a,b). This observation suggests that motor units in the caudal region have lower recruitment thresholds than those in the cranial region and is in agreement with the characteristic increase in surface EMG amplitude towards the cranial region with increasing * Corresponding author. Tel.: +45 96 35 74 59; fax: +45 98 15 40 08. E-mail address: [email protected] (D. Falla).
force (Holtermann and Roeleveld, 2006). Since pain decreases the net excitatory drive to the motor neurons (Sohn et al., 2000; Wang et al., 2000; Farina et al., 2004), the presence of pain in the upper trapezius is expected to reduce muscle activity predominantly in the cranial region, where motor units have higher threshold for activation. Consistent with this hypothesis, excitation of nociceptors in the cranial region of the upper trapezius muscle by intramuscular injection of hypertonic saline has been shown to induce a relatively larger reduction of EMG amplitude in cranial compared to caudal regions during static tasks (Madeleine et al., 2006). However, this observation was limited to a single injection site which was located in the cranial region of the muscle. Therefore it could not be discriminated if the observed response corresponded to a spatial matching between the pain stimulus and inhibition or if rather it was a general response of the muscle to a painful stimulus independent of the injection site. Changes in the activation of upper trapezius have been observed in people with neck and shoulder disorders. These include reduced activation during a repetitive upper limb task (Falla et al., 2004), increased activity during computer work (Szeto et al., 2005), reduced ability to relax the upper trapezius muscles
1388-2457/$34.00 Ó 2008 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.clinph.2008.10.148
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following voluntary activation (Falla et al., 2004) and reduced rest periods of the upper trapezius muscle during repetitive tasks (Veiersted et al., 1990; Hägg and Aström, 1997; Fredin et al., 1997). Given the common complaint of upper trapezius muscle pain and the alterations of upper trapezius activity which have been frequently documented in people with neck and shoulder disorders, further studies investigating the basic effect of pain on the activation of the trapezius muscle are warranted. In particular, the effect of pain on the distribution of upper trapezius activity may be relevant for interpreting changes in trapezius activity in clinical pain conditions and offer further insight into the hypothesis of overload of muscle regions and overexertion of low-threshold motor units in the presence of upper trapezius pain (Hägg, 1991). In this study it is hypothesized that experimentally induced muscle pain results in a greater reduction of EMG amplitude in the cranial region (higher threshold for activation) of the upper trapezius independent of the site of nociceptive stimulation within the muscle. Therefore, the purpose of the study was to assess the effect of experimentally induced muscle pain at different locations of the upper trapezius muscle on the spatial distribution of upper trapezius EMG amplitude.
2. Methods 2.1. Subjects Nine men participated in the study after providing informed consent. The participants (age: 26.4 ± 4.4 year; height: 179.3 ± 9.0 cm; weight: 78.4 ± 14.5 kg) were free of shoulder and neck pain, had no past history of orthopaedic disorders affecting the shoulder or neck region and no history of neurological disorders. All participants were right hand dominant. Ethical approval for the study was granted by the local Ethics Committee (VN 2005/38) and all procedures were conducted according to the Declaration of Helsinki. 2.2. Experimental design Subjects attended two experimental sessions separated by a minimum of 48 and maximum of 72 h (Fig. 1). In both sessions experimental muscle pain was induced by injection (27G needle) of sterile hypertonic saline (5.8%) into the upper division of the trapezius on the right side. In one experimental session (session A; Fig. 1), subjects received separate injections (individual bolus) of 0.4 ml of hypertonic saline into the cranial and caudal region of the upper trapezius. The cranial and caudal locations were defined as 15 mm cranial and 40 mm caudal to the line between the acromion and the spinous process of the seventh cervical vertebra, respectively. In addition, subjects received an injection of isotonic saline (0.4 ml, 0.9%) into the trapezius muscle at either the caudal or cranial location (randomized across subjects). In the other experimental session (session B; Fig. 1) subjects received two injections of 0.2 ml of hypertonic saline (total 0.4 ml), delivered simultaneously by two investigators in the caudal and cranial region. In addition subjects received injections of isotonic saline (0.2 ml, 0.9%) at both locations simultaneously. The bolus was injected over a 10-s period for all injections. The order of the experimental sessions (simultaneous injections or individual injection) was randomized across subjects. In each experimental session the isotonic saline injection was given first. However, participants were told that each injection may or may not be painful. A rest of 10 min was provided between injections. Following the hypertonic saline injection, the rest period commenced when pain was no longer reported.
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2.3. Procedure In both experimental sessions subjects were comfortably seated in a chair with their back supported, knees in 90° of flexion and feet flat on the ground. The subjects were asked to hold both arms in 90° of abduction for 60 s, with elbows fully extended and forearms pronated with palms facing toward the ground. Two flexible bars positioned on a board behind the subject extended horizontally over the subjects shoulders to provide tactile position feedback. The bars also allowed the investigator to monitor the subjects shoulder position during the 60 s contraction to ensure that the subject did not move their arms in the transverse or coronal planes. Guides were also placed behind and on the side of the subject which were used by the investigator to ensure the same position of the neck and head in all contractions. The sustained contraction was performed before, and immediately following the injection of hypertonic and isotonic saline into the right (dominant side) upper trapezius muscle. 2.4. Sensory assessment Participants were asked to verbally rate their level of perceived pain intensity on an 11 point numerical rating scale (NRS) with ‘‘no pain” equal to 0 and ‘‘the worst possible pain imaginable” equal to 10. Pain intensity ratings were obtained immediately following the injection and every 30 s until pain was no longer reported. Peak pain intensity and duration of pain were extracted. Participants documented the area of pain on a body chart. Pain drawings were subsequently digitized (ACECAD D9000 + Taiwan) and pain areas were measured. 2.5. Multi-channel surface EMG Prior to electrode placement, the main innervation zone location of the upper trapezius along the seventh cervical vertebra (C7)–acromion line was identified with an array of eight electrodes (silver bars, 5-mm long, 1-mm diameter, 5-mm interelectrode distance), as previously described (Farina et al., 2002). During the experimental measures, surface EMG signals were detected with a semi-disposable adhesive grid of electrodes (LISiN-OT Bioelettronica, Torino, Italy). The grid consists of 10 rows and 5 columns of electrodes (1-mm diameter, 8-mm interelectrode distance in both directions) with one electrode absent from the upper right corner. The position corresponding to the absent electrode was used as the origin of the coordinate system to define the electrode location. The subject’s skin was prepared by gentle local abrasion using abrasive paste (Medic-Every, Parma, Italy) and cleaned with water. The electrode grid was placed with the fourth row along the C7–acromion line and with the most lateral electrode column 10-mm distant from the innervation zone location. Thus the injections were performed lateral to the electrode grid (10 mm) and corresponded to the second and ninth row for the cranial and caudal locations, respectively (Fig. 2). 30 ll of conductive gel was inserted into each cavity of the grid to provide electrode-skin contact. A reference electrode was placed around the right wrist. 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 by a 12-bit analog-to-digital converter. 2.6. Signal analysis Surface EMG signals were off-line band-pass filtered (second order Butterworth filter; 3 dB bandwidth, 10–400 Hz). 39 bipolar EMG signals along the direction of the muscle fibers were obtained
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Fig. 1. Schematic representation of the experimental sessions. Participants attend two experimental sessions separated by a minimum of 48 and maximum of 72 h. The locations of the injections are defined in Fig. 2.
from the grid (10 4 bipolar recordings with one absent electrode). Root mean square (RMS) values were computed from each bipolar recording from adjacent, non-overlapping signal epochs of 1-s duration, as described previously (Merletti et al., 1990). For graphical representation, the 39 values were interpolated by a factor of 8 but only the original values were used for data processing and statistical analysis. To characterize the spatial distribution of muscle activity, the following variables were extracted from the
39 bipolar signals: RMS averaged over the 39 signals and the two coordinates of the centroid of the root mean square map (x- and y-axis coordinates for the medial-lateral and cranial-caudal direction, respectively) (Farina et al., 2008). Consecutive values over time of RMS, x- and y-axis coordinates of the centroid were averaged to obtain mean values corresponding to 5-s intervals of the sustained contraction. In addition, the difference in the position of the y-axis coordinate of the centroid
Fig. 2. Surface EMG signals were detected using a semi-disposable adhesive grid of electrodes over the right upper trapezius muscle. The grid consists of 10 rows and 5 columns of electrodes with one electrode absent at the upper right corner. The electrode grid was placed with the fourth row along the C7–acromion line. Injections were performed lateral to the electrode grid (10 mm) and corresponded to the second row of the grid for the cranial location and ninth row for the caudal location. For the simultaneous injection condition, injections were performed in the cranial and caudal locations simultaneously.
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between the painful conditions and baseline conditions was obtained for each epoch. The shift of the centroid over time was defined as the modulus of the centroid displacement in the medial-lateral and cranial-caudal direction with respect to the position at the beginning of the contraction. 2.7. Statistical analysis One-way ANOVA were applied to parameters of pain intensity, duration and area with injection (hypertonic cranial, hypertonic caudal, hypertonic combined, isotonic individual and isotonic combined) as repeated measures. Two-way ANOVA were applied to values of RMS, and x- and y-axis coordinates for the combined injection condition with factors, condition (baseline, isotonic, hypertonic) and time (12 time intervals of 5 s) as repeated measures. Moreover, two-way ANOVA were applied to values of RMS, and x- and y-axis coordinates for the individual injection condition with factors, condition (baseline, isotonic, hypertonic cranial, hypertonic caudal) and time (12 time intervals of 5 s) as repeated measures. Differences in the position of the y-axis coordinate between the baseline and painful condition were compared using a two-way ANOVA with condition (hypertonic cranial, hypertonic caudal, hypertonic combined) and time (12 time intervals of 5 s) as repeated measures. A two-way ANOVA was utilized to compare the shift of the centroid of the RMS map across the sustained contraction for both the individual and simultaneous injection conditions with factors, condition and time (11 time instants) as repeated measures. Significant differences revealed by ANOVA were followed by post-hoc Student–Newman–Keuls (SNK) pair-wise comparisons. Results are reported as mean and standard deviation (SD) in the text and standard error (SE) in the figures. Statistical significance was set at P < 0.05. 3. Results 3.1. Sensory characteristics Peak pain intensity was greater following the injection of hypertonic (simultaneous injections: 4.6 ± 1.7, caudal: 4.1 ± 1.7, cranial: 4.2 ± 0.9) compared to isotonic saline in all conditions (F = 32.4, P < 0.00001; Fig. 1). No differences in peak pain intensity were identified between the hypertonic saline injections given at
3.2. EMG amplitude RMS values averaged over all locations of the grid were reduced across the entire duration of the 60 s shoulder abduction contraction following the simultaneous hypertonic saline injections compared to both baseline and isotonic saline conditions (ANOVA: F = 5.1, P < 0.05, SNK both P < 0.05; Fig. 5A). Moreover, individual injections of hypertonic saline in the cranial or caudal region of the upper trapezius resulted in lower RMS values compared to baseline and isotonic conditions (ANOVA: F = 9.2, P < 0.001; SNK: all P < 0.01; Fig. 5A). The average RMS remained constant across the duration of the contraction for the baseline and isotonic conditions. However, a condition by time interaction revealed that the average RMS increased over time following injection of hypertonic saline in either the caudal or cranial region of upper trapezius or following the injections performed simultaneously (ANOVA: F = 2.4, P < 0.0001; SNK: P < 0.05). 3.3. Changes in the root mean square map The x-axis coordinate of the RMS map was not dependent on time or condition (Fig. 6A). In both experimental sessions the ycoordinate of the RMS map reduced across the duration of the contraction (simultaneous and individual injection experimental sessions: F = 12.8, P < 0.00001 and F = 14.96, P < 0.00001, respectively; Fig. 6B) indicating a shift of activity towards the cranial region of the muscle. Following the injection of hypertonic saline, higher estimates of the y-axis coordinate of the RMS map were observed compared to both baseline and isotonic injection conditions indicating a shift of activity towards the caudal region (simultaneous and individual injection experimental sessions: F = 15.6, P < 0.0001 and F = 16.9, P < 0.00001, respectively; Figs. 6B and 7). Differences in the position of the y-axis coordinate 6
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single sites or when injected at both sites simultaneously (SNK: P > 0.41). Pain duration and area were not dependent on the location of the hypertonic saline injection (P = 0.83 and P = 0.76, respectively; Figs. 3 and 4). Total mapped pain areas were 5.3 ± 3.5, 4.5 ± 4.8 and 4.2 ± 3.8 (arbitrary units) for the simultaneous, caudal and cranial hypertonic saline injections, respectively. Both isotonic saline injections (simultaneous and individual) produced lower scores on all measured pain parameters compared to the hypertonic saline injections (P < 0.05).
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Fig. 4. Area of pain reported following individual injections of 0.4 ml of hypertonic saline into the cranial and caudal region of the upper trapezius and following injections of 0.2 ml of hypertonic saline in the caudal and cranial region simultaneously (total 0.4 ml). Area of pain is also shown following injection of 0.4 ml isotonic saline into either the cranial or caudal region of the muscle.
between the baseline and painful condition were not dependent on the location of the injection or time. The centroid of the EMG amplitude map moved in the cranial direction across the duration of the sustained contraction (simultaneous and individual injection experimental sessions: F = 8.8, P < 0.000001 and F = 7.8, P < 0.00001, respectively; Fig. 8) and was not influenced by intramuscular injection of hypertonic saline.
previous reports of hypertonic saline-induced upper trapezius muscle pain (Ge et al., 2005; Komiyama et al., 2005; Falla et al., 2007a). Previously it has been shown that four simultaneous but spatially separated injections of 0.1 ml hypertonic saline into the tibialis anterior muscle induce a greater pain intensity, distributed over a larger area compared to a single injection of 0.1 ml hypertonic saline (Graven-Nielsen et al., 1997a), consistent with an increased perceived pain intensity due to spatial summation (Price et al., 1989). However, it was also shown that the intensity of pain induced by infusion of 0.4 ml hypertonic saline at spatially separated sites or injection of 0.4 ml at a single site was comparable (Graven-Nielsen et al., 1997a), which is consistent with the observations in the present study.
4. Discussion Intramuscular injection of hypertonic saline into the upper trapezius muscle induced a relatively larger reduction of upper trapezius EMG amplitude in the cranial compared to caudal regions of the muscle independent of the location of noxious stimulation. This finding indicates that muscle regions with a higher threshold of activation are the most inhibited in the presence of pain.
4.2. Spatial distribution of EMG amplitude During the sustained contraction the cranial region became progressively more active than the caudal region consistent with observations from previous surface EMG studies (Madeleine et al., 2006; Falla and Farina, 2007; Farina et al., 2008).
4.1. Sensory responses Injection of hypertonic saline in the upper trapezius muscle resulted in muscle pain of moderate intensity, consistent with
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Fig. 5. Mean (±SE) of the average root mean square (RMS) estimated at 5-s intervals throughout sustained shoulder abduction before and following individual injections of 0.4 ml isotonic and hypertonic saline into the cranial and caudal region of the upper trapezius and following injections of 0.2 ml of isotonic and hypertonic saline in the caudal and cranial region simultaneously (total 0.4 ml). Significant difference of hypertonic saline conditions compared to baseline and isotonic condition: *P < 0.05.
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Fig. 6. Mean (±SE) of the x-axis coordinate (A) and y-axis coordinate (B) of the centroid of the RMS map, estimated at 5-s intervals throughout sustained shoulder abduction before and following individual injections of 0.4 ml isotonic and hypertonic saline into the cranial and caudal region of the upper trapezius and following injections of 0.2 ml of isotonic and hypertonic saline in the caudal and cranial region simultaneously (total 0.4 ml). Significant difference of hypertonic saline condition compared to baseline and isotonic condition: *P < 0.0001.
It has been shown that excitation of nociceptors in the cranial region of the upper trapezius muscle results in a relatively larger reduction in EMG amplitude in cranial compared to caudal regions which was revealed by a shift of the EMG amplitude distribution towards the caudal fibers of the upper trapezius muscle (Madeleine et al., 2006). A novel finding of the current study is that the same change in activation occurred following excitation of nociceptive afferent fibers in the caudal region of the upper trapezius or in both the caudal and cranial locations simultaneously. Thus, the pattern of inhibition was the same regardless of the site of nociceptive stimulation. Several studies have shown a reduction in interference EMG amplitude when a localized noxious stimulus is applied to a muscle (e.g. Graven-Nielsen et al., 1997b; Svensson et al., 1998). The results of this study also show a global reduction in upper trapezius EMG amplitude following injection of hypertonic saline. However, assessment of the EMG amplitude distribution across the upper trapezius muscle revealed that the greatest reduction in EMG amplitude was not always local to the site of noxious stimulation. Thus, a shift of the distribution of muscle activity towards the painful region was observed when hypertonic saline was injected into the caudal region of the upper trapezius muscle.
The task performed in this study corresponded to 15–20% of the maximum voluntary contraction of the trapezius muscle (Mathiassen et al., 1995). At this contraction intensity it is likely that only type I motor units were active (Stephens and Usherwood, 1977). Across these motor units, those in the caudal region of the upper trapezius have been observed to discharge at higher rates for a given force (Falla and Farina, 2008a) and to be recruited at lower forces than motor units in the cranial region (Holtermann and Roeleveld, 2006). Thus, the results of this study suggest that nociceptive input reduces the net excitatory input to the population of motor neurons, resulting in reduced activation and derecruitment, with derecruitment following the reverse order of recruitment. Reduced excitatory input may be due to decreased descending drive to the painful muscle or to pure spinal mechanisms, or more likely, a combination of both. In the present study the electrode was positioned in order to be within the region of the upper trapezius and achieve coverage of a large proportion of the upper trapezius in the longitudinal direction. It may be argued that in some cases (e.g. smaller subjects) the caudal region of the electrode grid covered a portion of the middle division of trapezius. However, this possibility would not affect the main result of this study; that muscle regions with a
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Fig. 7. Representative topographical maps (interpolation by a factor 8) of the EMG root mean square value recorded for one subject for the first 5 s of the sustained shoulder abduction contraction performed at baseline and following individual injections of 0.4 ml of hypertonic saline into the cranial and caudal region of the upper trapezius (session A). Topographical maps are also displayed for the same subject from a separate experimental session (session B) for the sustained contraction performed at baseline and following injections of 0.2 ml of hypertonic saline in the caudal and cranial region simultaneously (total 0.4 ml). Colors are scaled between the minimum and maximum RMS values. Areas of dark blue correspond to areas of low EMG amplitude and dark red to areas of high EMG amplitude. Note the greatest reduction in EMG amplitude is consistently for the cranial location. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this paper.)
higher threshold of activation are the most inhibited in the presence of pain.
This finding offers some support to the hypothesis that low-threshold motor units are continuously active even in the presence of pain (Cinderella Hypothesis) (Hägg, 1991) and may have implications for the development of chronic neck and shoulder pain. Although the cranial region of the upper trapezius showed the greatest pain-induced reduction in activity for the task of shoulder abduction, other regions of the muscle may show a greater inhibition in different tasks with different biomechanical demands.
4.3. Implications Injection of hypertonic saline into the caudal region of the upper trapezius muscle resulted in a greater inhibition of activity at a site distant to the location of the injection compared to the actual site of noxious stimulation. This observation indicates that the painful region of a muscle is not always the most ‘‘protected”. The consistent change in the motor strategy which was observed suggests that regions of the muscle with a higher threshold for activation are the first to be inhibited. As a consequence the region of the upper trapezius muscle which is first to be activated during shoulder abduction remains continuously active in the presence of pain.
5. Conclusion Muscle pain induces a decrease in the net excitatory input to the motor neuron pool innervating the painful muscle, which causes reduced muscle activity. Motor neurons with a higher threshold for activation and lower discharge rate at a given force
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Fig. 8. Mean (±SE) of the displacement of the centroid estimated from the surface EMG signals during 60 s sustained shoulder abduction before and following individual injections of 0.4 ml isotonic and hypertonic saline into the cranial and caudal region of the upper trapezius and following injections of 0.2 ml of isotonic and hypertonic saline in the caudal and cranial region simultaneously (total 0.4 ml).
D. Falla et al. / Clinical Neurophysiology 120 (2009) 150–157
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