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Changes in motor unit recruitment strategy during pain alters force direction
European Journal of Pain 14 (2010) 932–938
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European Journal of Pain journal homepage: www.EuropeanJournalPain.com
Changes in motor unit recruitment strategy during pain alters force direction Kylie J. Tucker *, Paul W. Hodges The University of Queensland, NHMRC Centre of Clinical Research Excellence in Spinal Pain, Injury and Health, School of Health and Rehabilitation Sciences, Australia
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Article history: Received 24 November 2009 Received in revised form 22 February 2010 Accepted 13 March 2010 Available online 7 April 2010 Keywords: Pain Motor unit Recruitment Force Adaptation
a b s t r a c t Motor unit (MU) recruitment is altered (decreased discharge rate and cessation of discharge in some units, and recruitment of new units) in force-matched contractions during pain compared to contractions performed before pain. As MU’s within a motoneurone pool have different force direction properties we hypothesised that altered MU recruitment during experimental knee pain would change the force vector (total force (FT): amplitude and angle) generated by the quadriceps. Force was produced at two levels during 1 60-s and 3 10-s isometric contractions of knee extensors, and recorded by two force transducers at right angles. This enabled calculation of both FE (extension force) and FT. MU recruitment was recorded from the medial and lateral vastii with four fine-wire electrodes. Pain was induced by hypertonic saline injection in the infra-patella fat pad. Nine subjects matched FE and six subjects also matched both medial and lateral forces (FT) before and during pain. Changes in MU discharge pattern (decreased discharge rate (P < 0.001), complete cessation of firing, and recruitment of new units) during pain were associated with a 5° change in absolute force angle. As force angle changed in both directions (left/right) for individual subjects with pain there was no change in average FT amplitude between conditions. When both medial and lateral forces were matched MU discharge rate decreased (P < 0.001) with pain, but, fewer units ceased firing or were newly recruited during pain. Change in motoneurone recruitment during pain alters direction of muscle force. This may be a strategy to avoid pain or protect the painful part. Ó 2010 European Federation of International Association for the Study of Pain Chapters. Published by Elsevier Ltd. All rights reserved.
1. Introduction The most commonly accepted theory to explain changes in muscle activity during pain; the ‘pain adaptation theory’ argues movement velocity and amplitude are reduced during pain by a combination of inhibition of agonist muscle and facilitation of antagonist muscles during voluntary movement (Lund et al., 1991). Although commonly referred to, the theory is not universally supported and much of the data is compromised by variable results (reviewed Murray and Peck, 2007). During experimental muscle pain, motoneurone discharge rate, which is a determinant of force (Burke, 1981; Stuart and Enoka, 1983), is decreased when force is maintained at pre-pain levels (Sohn et al., 2000; Farina et al., 2004; Hodges et al., 2008; Tucker et al., 2009; Tucker and Hodges, 2009). Until recently, reduced motoneurone discharge during pain was thought to support generalised inhibition of agonist muscles and therefore the ‘pain adaptation theory’; however there was little explanation how force was
* Correspondence to: K.J.Tucker, NHMRC Centre of Clinical Research Excellence in Spinal Pain, Injury and Health, School of Health and Rehabilitation Sciences, The University of Queensland, Brisbane, Qld 4072, Australia. Tel.: +61 7 3365 4589; fax: +61 7 3365 4567. E-mail address: [email protected] (K.J. Tucker).
maintained when motoneurone discharge rate was reduced. We have recently shown that in addition to decreased motoneurone discharge rate and derecruitment of units, other previously inactive motor units are recruited, presumably to help maintain force during pain (Tucker et al., 2009; Tucker and Hodges, 2009). These newly recruited units are not necessarily those expected given orderly recruitment of the motoneurone pool, and occur in both small non-synergistic (flexor pollicus longus) and large synergistic (quadriceps) muscles (Tucker et al., 2009; Tucker and Hodges, 2009). Reduced discharge of some units and increased discharge of others within a motoneurone pool during pain is inconsistent with generalised inhibition of the motoneurone pool. We conclude that the nervous system employs a different motor unit recruitment strategy to achieve the same force output, with an uneven distribution of synaptic input across the motoneurone pool during pain. The new theory predicts non-uniform changes within and between muscles during pain with some benefit to the system. Motor units within a motoneurone pool generate force in various directions (e.g. first dorsal interosseous (Suresh et al., 2008)), which may be associated with discrete functions of motor units within a muscle (e.g. (Thomas et al., 1978; ter Haar Romeny et al., 1982; Riek and Bawa, 1992)). We postulated that the new recruitment strategy during pain would result in an altered force
1090-3801/$36.00 Ó 2010 European Federation of International Association for the Study of Pain Chapters. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.ejpain.2010.03.006
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vector used to complete force-matched tasks (Tucker and Hodges, 2009). This may be beneficial in distributing load in a way that is less pain provocative or is protective of the painful area. We hypothesised that: (1) changes in motoneurone discharge during pain would alter the angle of whole muscle force produced during force-matched contractions; (2) given the change in angle of whole muscle force, total force required to complete the task during pain would be greater than during non-painful contractions; (3) by controlling both force amplitude and angle, subjects would override adaptations to motor unit recruitment during pain when force amplitude alone was matched; i.e. the pattern of motor unit recruitment during pain would be similar to that identified during amplitude and angle-matched contractions without pain. 2. Methods Nine volunteers with no history of significant knee/leg pain participated in this study (mean (SD) age; 28(8) years). The Institutional Medical Research Ethics Committee approved the study and all procedures conformed to the Declaration of Helsinki and the IASP’s guidelines for pain research in humans. 2.1. Electromyography Two pairs of intramuscular fine-wire electromyography (EMG) electrodes (two Teflon-coated 100 lm stainless steel wires with 0.5 mm insulation removed, threaded into a hypodermic needle (25 G 25 mm)) were inserted into both the medial (vastus medialis: VM) and lateral (vastus lateralis: VL) heads of the quadriceps. The needle was removed following insertion leaving the wires in place (Fig. 1A). EMG data were pre-amplified 2000– 10,000 times, band-pass filtered (30 Hz–2 kHz), notch filtered at 50 Hz, and sampled at 5 kHz using a Power1401 Data Acquisition System with Spike2 software (CED, UK). 2.2. Experimental design Subjects sat fully supported with their leg relaxed over the end of a plinth. Upper thighs were strapped firmly to the plinth to avoid changes in hip position during the knee extension tasks. Isometric knee extension force was measured with two force transducers (Futek, USA) that were secured to the plinth at right angles to each other. The force transducers were placed medially (FM) and laterally (FL) at 45° to the direction of extension force (FE) (Fig. 1B), then attached via a chain to a 5 cm wide thermoplastic band (1.6 mm UltraPerf, Sammons Preston, USA) that was moulded to the subject’s lower leg just above the ankle. Subjects were instructed to gently contract the test muscles before recording began in two separate trials until 2–6 (lower force), and 4–8 (higher force) single motor units (SMUs) were recorded consistently by any of the four fine-wire electrodes. These force levels were recorded for matching before and during experimental pain. During test contractions subjects increased force from rest to the displayed target level(s) over 6-s and then maintained this force for a 60-s reference contraction and 3 10-s contractions. After each contraction subjects reduced force to rest over 6-s, and rested for at least 10-s between contractions. This procedure was repeated during contractions when only extension force was provided as feedback and when feedback was provided from both the medial and lateral force transducers (explained in more detail below). To determine if the changes in SMU discharge that we have previously reported during pain (Tucker et al., 2009; Tucker and Hodges, 2009) were associated with a change in angle of force production, subjects were provided with feedback of, and asked
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to match extension force (FE: this is the amount of force produced in the extension direction, see Fig. 1B). By matching FE only (and not the angle of their force production) subjects were free to change the angle of their force production between trials (both in the control and pain trials) compared to the 60-s reference contraction. Extension force was determined from the forces recorded by the medial and lateral force transducers (FE = sin(45°) FM + sin(45°) FL; Fig. 1B and C). By using two force transducers to record force, we could measure changes in the angle of force production, and the total force used to match the extension force during each trial (force angle = a tan(FM/FL); total force (FT) amplitude = (F 2M þ F 2L ); Fig. 1B and C). Absolute force and angle change during each test contraction relative to the 60-s reference contraction was compared between trials with and without pain. The longer (60-s) contraction was used to account for variation over time, and allowed us to determine whether force characteristics deviated more (from reference) during pain than control. This was necessary as some degree of variation in angle of force production was expected even in the control conditions, and the variance could occur in both directions (more medially or laterally). To determine if changes in SMU discharge were associated with changes in the force vector (force angle and amount of total force produced at that angle) used to maintain extension force between conditions, SMU discharge characteristics were compared between the 3 10-s of data from each of the contractions with and without pain (for the low force contraction only). To determine if SMU recruitment was altered when subjects matched both force amplitude and direction (angle) of force production, subjects were provided with separate feedback from both force transducers (i.e. two feedback targets on the same feedback screen) during trials with and without pain. Subjects were instructed to modify the way (the angle) that they produced their extension force until both force targets were matched. Of the nine subjects, two subjects did not complete this task and another was unable to match their force with <5% error between conditions, and was therefore not used for this part of the study. For these FT (amplitude and angle) matched contractions, force vector characteristics were compared directly between the non-painful and painful contractions to ensure subjects had successfully matched the force and direction. For this analysis, force vector characteristics were determined from the 3 10-s contractions and from the best-matched 10-s period within the FT matched 60-s reference contraction. The three best-matched 10-s periods between the non-painful and painful trials were used for further analysis. SMU analysis was conducted on recordings from either the lower or higher force contractions, based on the contractions with least difference in FT (force amplitude and angle) between the non-painful and painful conditions. 2.3. Experimental pain Pain was induced by single bolus injection of hypertonic saline (0.25 mL, 5% NaCl) into the infra-patellar fat pad (Bennell et al., 2004; Tucker and Hodges, 2009). Experimental muscle pain was recorded throughout the pain trial using a custom-made electronic 10 cm visual analogue scale (VAS) whereby 0 = ‘no-pain’ and 10 = ‘worst pain imaginable’; or reported verbally using an 11 point (0–10) numerical rating scale (NRS) at 20-s intervals throughout the painful condition. In all trials the painful contractions commenced after the pain level reached 3/10. In all cases pain remained at P2/10 at the end of the painful contractions. The area of pain was recorded by subjects on a standardised figure (Fig. 1A) following the pain trial.
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(A) Electrode placement and pain location
VL
(B) Experimental set-up FE = 0°
VM
90°
Injection site
FL
FM VM
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(C) Calculating force vector characteristics FE FE = sin(45°)FM + sin(45°)FL FL FT
FT (maximum force produced at any angle) = (FM2+FL2) Angle of FT ( )=atan(FM/FL)
FM
Fig. 1. (A) The injection site; approximate area of reported pain for each subject (grey lines); and the location of fine-wire EMG electrodes in the lateral (VL) and medial (VM) heads of the quadriceps are shown. (B) Isometric knee extension force was measured from two force transducers (FM and FL) positioned at 90° to each other and attached to the subjects leg just above the ankle. (C) Extension force (FE), total force (FT), and angle of FT were calculated from FM and FL.
2.4. Data analysis SMUs were identified based on morphology using Spike2 software (CED, UK) from pairs of fine-wire electrodes that provided the recordings with clear discrimination between motor units throughout the trials. To ensure discrimination accuracy, motor unit inter-spike intervals were examined. Trials that contained abnormally short or long inter-spike intervals were re-analysed on a spike-by-spike basis to check for discrimination accuracy. Averages of SMU recordings were then triggered from the discharge of each discriminated unit over the three 10-s analysis periods to generate a profile template of the motor unit morphology (e.g. Fig. 2, bottom panel). These profiles were compared visually within subjects to determine if the same unit was present in each contraction. Motor units that discharged for more than half of at least two of the three 10-s contractions within a condition were considered reliable for that condition (Tucker and Hodges, 2009). The mean discharge rate of all reliable motor units was recorded for comparison between conditions. Motor units from the two regions of the quadriceps muscle (VM and VL) behaved similarly between conditions and were grouped for analysis (Tucker and Hodges, 2009). 2.5. Statistical analysis For the extension force match tasks, data was non-normally distributed. The Wilcoxon matched pairs sign rank test was therefore
used to compare the force vector characteristics (absolute change in FT, FE and angle of FT from the reference contraction) between the non-painful and painful contractions. The Wilcoxon matched pairs sign rank test was also used to compare the force vector characteristics directly between contractions with and without pain in the force amplitude and angle matched trial. Comparison of the discharge rate of motor units identified in both the trials with and without pain was made with paired t-tests (two-tails). An independent t-test (two-tails) was used to compare the discharge rate of the whole population of motor units recruited in either condition. Data are presented as mean (SD) throughout the text and figures. Significance was set at P < 0.05.
3. Results The average pain rating reported during the contractions with pain was 4.1(2.1)/10. Pain was generally localised to the medial aspect of the patella around the location of the saline injection (Fig. 1A). The average knee extension force (FE) used during the 60-s lower and higher reference contractions was 9.8(6.7) N (range 3.7– 25.6 N) and 16.6(13.2) N (range 5.3–50.6 N), respectively. The average total force (FT) used to complete the lower and higher force reference contractions was 10.6(6.8) N (range 3.7–26.1 N) and 17.5(13.5) N (range 5.3–51.9 N), respectively. As FE represents the
K.J. Tucker, P.W. Hodges / European Journal of Pain 14 (2010) 932–938
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Fig. 2. Force profile during ramp hold contractions during extension force (FE) and total force (i.e. feedback from FM and FL) feedback trials are shown in the top three traces. The 10-s period used for analysis from each of these contractions is highlighted by the grey box. When FE feedback is provided the angle of force production is altered during pain. This is demonstrated by a change in the relative contribution of FM and FL in the top left traces during pain compared to the No-pain condition. When feedback was provided from both FM and FL (in the two right panels) both force and angle of force production are matched between the no-pain and pain contractions. Each discharge of all discriminated motor units (A–F) from two fine-wire EMG channels is shown in the middle section of this figure. The mean discharge rates of these motor units during the 10-s analysis period are also shown. The fine-wire EMG data and discharge of motor units from 1-s during each of the contractions is expanded in the bottom panel. The profile of each single motor unit action potential that discharged during these contractions is also shown. When FE is matched (no attempt to maintain same angle during pain) some motor units (e.g. D and E) were recruited in each condition. These units decreased in discharge rate during Pain. Other units were no longer recruited during pain (e.g. C) and a third population of units were newly recruited during pain (e.g. A, B and F). When feedback was provided from both force transducers (right panels), so that both extension force and angle was matched, the change in recruitment of units are less profound. In this example all of the motor units were recruited in both the no-pain and pain trials, and all decreased in discharge rate during pain.
part of FT that is produced in the extension direction (Fig. 1B and C), it is expected that FE will be less than or equal to FT. The angle of FT produced during the 60-s lower and higher reference contractions was 20.8(12.1)° (range 3.1–34.11°) and 17.9(8.3)° (range 3.0° to 25.11°), respectively. When subjects were provided with feedback of the FE alone, the absolute change in both FE and FT amplitude, compared to the reference condition, were similar in the non-painful and painful
contractions at both force levels (Fig. 3A and B; all P > 0.1). Although there was no significant change in force amplitude between conditions, the angle of FT was changed with pain. The absolute deviation in angle of FT compared to the reference contraction was 5° greater during pain than during the brief non-painful contractions (Fig. 3C: P < 0.01 during lower force and Fig. 3D: P = 0.01 during higher force contractions). This change in angle occurred with similar frequency to the left and right (medially and laterally)
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Fig. 3. Absolute amplitude and angle change (mean (SD)) during the non-painful and painful contractions relative to the 60-s reference contraction, during both lower and higher force contractions are shown. The extension force (FE) and total force (FT) used to complete the test contractions were not different between conditions (A and B). However, the absolute change in angle during the painful contractions was 5° greater than that during the contractions without pain during both the lower (C) and higher (D) force contractions.
to that in the reference contraction. In two subjects the direction of angle change during pain was opposite during the lower and higher force contractions. The change in angle of FT during pain (Fig. 2, top left; Figs. 3C and D) was associated with altered motor unit recruitment
(Fig. 2, FE feedback; and Fig. 4B and C). A total of 55 single motor units were discriminated from the lower force contraction data. Of these units, 24 discharged in both the contractions with and without pain. An additional 13 units were only identified during contractions without pain (i.e. they were derecruited during pain), and 18 units that were not identified during the condition without pain were identified during pain (i.e. recruitment of new units during pain) (Fig. 4B). This means that of the units identified during these contractions 55% differed between conditions. The discharge rate of the units identified in both conditions and of the total population of units identified in either condition decreased with pain (Fig. 4C: both P < 0.001). Although the group data showed a decrease in discharge rate during pain, n = 1 of the units recruited in both conditions increased its discharge rate during pain (from 10.3(0.2) to 10.5(0.3) Hz). When subjects were required to match both the medial and lateral forces (to match FT amplitude and angle), changes in motor unit recruitment strategy during pain were less evident (Fig. 2, right panel, Fig. 4E and F). Within the six subjects used for this analysis the largest variability between conditions was 3% amplitude (for both FT and FE) and 2° angle of FT. For the non-painful and painful contractions respectively: FE: 10.1(7.6) and 10.0(7.5) N; FT 10.9(8.0) and 10.9(8.0) N; both P > 0.5; angle of FT: 18.9(10.7) and 18.9(10.9)°; P > 0.9 (Fig. 4D). A total of 32 motor units were discriminated from the test contractions. Of these, 25 were present in both the contractions with and without pain. This means that of the units identified during these contractions 78% discharged in both the contractions with and without pain. Of the six subjects, three recruited the same units in both conditions, one subject recruited 4 units during the no-pain condition that were not recruited during pain and two other subjects recruited 1–2 motor units during pain that were not recorded in the non-painful contraction (Fig. 4E). Despite the relatively consistent active population of units, the discharge rate of the units identified in both
Fig. 4. The range of angles and changes in motor unit recruitment used by all subjects to match force during the contractions with and without pain are shown. Data from contractions when feedback of extension force (FE) alone (top row) and both medial (FM) and lateral force (FL) (bottom row) are shown. The angle change observed during painful contractions when feedback of extension force was provided (A) is associated with considerable changes in motor unit discharge patterns (B and C). In contrast, when feedback was provided from both FM and FL, the angle used remained the same between conditions (D) and some changes in motor unit discharge pattern are less prevalent (E and F).
K.J. Tucker, P.W. Hodges / European Journal of Pain 14 (2010) 932–938
conditions, and the total population of units identified in either condition, decreased with pain (Fig. 4F: both P < 0.001). Although the group data showed a decrease in discharge rate during pain, n = 3 (12%) of the units recruited in both conditions increased their discharge rate during the painful FT matched task (from 7.7(0.9) to 7.9(1.1) Hz).
4. Discussion These data show that changes in motor unit discharge during pain are associated with changes in force direction during matched force tasks. Our findings support the theory that rather than uniform inhibition or facilitation of the motoneurone pool, there is a reorganisation of motor unit recruitment during pain, and that this reorganisation is associated with altered force angle during pain (Murray and Peck, 2007). Motor units within the same motor unit pool can produce force in variable directions (Burke, 1991; Suresh et al., 2008) and therefore changes in whole muscle output and force orientation may result from non-uniform changes in recruitment of units within a muscle’s motoneurone pool (Thomas et al., 1978; ter Haar Romeny et al., 1982; Riek and Bawa, 1992; Yang et al., 1998; Butler et al., 1999). When subjects were asked to contract their vastii muscles during the non-painful reference contraction in the current investigation, force was produced on average 21° laterally. This is likely to be a result of the configuration of the knee joint and superior mechanical pull of the lateral quadriceps compared to their synergist muscles (Lieb and Perry, 1968). When force amplitude (but not direction) was matched, the 5° difference in angle between conditions was associated with a change in the population of motor units recruited. Approximately 55% of the identified units were only recruited in either the contractions with or without pain (and not in both conditions). The change in motor unit recruitment during pain is supported by other work from our laboratory (Tucker et al., 2009; Tucker and Hodges, 2009). In muscle groups with large mechanical redundancy (i.e. multiple possible strategies to produce similar movements; e.g. the jaw (Van Eijden et al., 1990) and trunk (van Dieen et al., 2003) muscles); and regions within muscles with differences in mechanical efficacy (e.g. respiratory system (De Troyer et al., 2003; Gandevia et al., 2006), limbs (Thomas et al., 1978; ter Haar Romeny et al., 1982; Riek and Bawa, 1992; Yang et al., 1998; Butler et al., 1999)) the recruitment of motor units has been argued to be organised to achieve the best mechanical advantage at the lowest metabolic cost. It is commonly assumed that the most stable and efficient strategy of muscle recruitment is selected to complete a task, and if the strategy was to change during pain, the new strategy may be less efficient (Murray and Peck, 2007). This assumption is consistent with the hypothesis that the changes in muscle activity in people with chronic low-back pain are aimed at avoiding noxious stresses in injured structures, thereby avoiding or minimizing pain (Hodges et al., 2003; van Dieen et al., 2003) rather than completing the task in the most efficient manner. In the current investigation we hypothesised that a change in angle of force production would result in greater total force (FT) being required to match the force generated in the extension direction (FE). However, this did not occur as force changed in the medial and lateral direction with no net change in total force. However, our data show that initially the force was generated at 21° from the extension direction and thus the required force was greater than the target extension force, i.e. not the minimum force. This suggests that some parameter other than minimum force was being controlled to extend the knee, and this may be related to the complex mechanics of the knee extensor mechanism. As the reference condition was
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not performed with the least force there was the potential for the contractions during pain to be performed with both more or less force, and this was the case. Thus our hypothesis of decreased force was not supported, but this does not exclude the possibility that the ‘‘new” task was less efficient. One possible advantage of the altered motor unit recruitment during pain may be to alter the direction of force production to minimize the provocation of pain while still completing the task. Although this conclusion could be argued to be compromised by the data that show changes in force direction both towards and away from the location of pain reported subjectively at the end of the trials, it cannot be assumed that a change in either direction will be less pain provocative for an individual subject. This is because it is impossible to predict which changes would alter load on the fat pad in a manner to reduce pain provocation. It is also possible that the change in angle is a consequence of the adaptation in motor unit discharge and not the goal of the change in motor unit recruitment during pain. It is possible that the aim of the altered recruitment may be to selectively recruit units with different force production capacity, i.e. larger units that can match force at a lower discharge rate, or produce a faster change in force, rather than to selectively recruit units with a different force direction profile. However, our findings that the change in recruitment of units was less prevalent when force amplitude and angle are both matched lend support to the change in direction being the goal. In the current investigation when contractions were matched for both force amplitude and angle, 78% of the units were recruited in both the contractions with and without pain. Interestingly, there was a greater prevalence of units with increased discharge rate in this condition than during the amplitude-matched task (from n = 1/24 to 3/25). The alternative force production strategy of increasing the discharge rate of individual units during pain (Tucker et al., 2009) may be needed to compensate for the decreased discharge rate of some units when the ability to change direction was restricted. From the findings of this and our previous investigations (Tucker et al., 2009; Tucker and Hodges, 2009), we argue that during force match contractions with pain, motor unit recruitment strategies are altered in a complex manner that cannot be explained by generalised inhibition to the motoneurone pool. This change in recruitment strategy involves the reduction in discharge rate and complete cessation of discharge of some units, the increase of discharge rate in some units and the recruitment of new units during pain. The change in motor unit recruitment is related to a change in force direction, and when both force direction and amplitude are matched a different motor unit recruitment strategy is required to maintain force. The data provide further evidence of non-uniform input to the motoneurone pool during pain. Given the assumption that the optimal recruitment strategy is likely during non-painful contractions (De Troyer et al., 2003; Gandevia et al., 2006), and that the nervous system may attend to the combined goals of task completion and pain minimization during painful contraction (Hodges et al., 2008; Tucker and Hodges, 2009), the altered motor unit recruitment and angle of total force may indicate a less efficient mechanical system during pain. 5. Conflict of interest statement There was no conflict of interest. Acknowledgements Financial support was provided by the National Health and Medical Research Council of Australia, and the University of Queensland Early Research Career Grant.
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European Journal of Pain journal homepage: www.EuropeanJournalPain.com
Changes in motor unit recruitment strategy during pain alters force direction Kylie J. Tucker *, Paul W. Hodges The University of Queensland, NHMRC Centre of Clinical Research Excellence in Spinal Pain, Injury and Health, School of Health and Rehabilitation Sciences, Australia
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Article history: Received 24 November 2009 Received in revised form 22 February 2010 Accepted 13 March 2010 Available online 7 April 2010 Keywords: Pain Motor unit Recruitment Force Adaptation
a b s t r a c t Motor unit (MU) recruitment is altered (decreased discharge rate and cessation of discharge in some units, and recruitment of new units) in force-matched contractions during pain compared to contractions performed before pain. As MU’s within a motoneurone pool have different force direction properties we hypothesised that altered MU recruitment during experimental knee pain would change the force vector (total force (FT): amplitude and angle) generated by the quadriceps. Force was produced at two levels during 1 60-s and 3 10-s isometric contractions of knee extensors, and recorded by two force transducers at right angles. This enabled calculation of both FE (extension force) and FT. MU recruitment was recorded from the medial and lateral vastii with four fine-wire electrodes. Pain was induced by hypertonic saline injection in the infra-patella fat pad. Nine subjects matched FE and six subjects also matched both medial and lateral forces (FT) before and during pain. Changes in MU discharge pattern (decreased discharge rate (P < 0.001), complete cessation of firing, and recruitment of new units) during pain were associated with a 5° change in absolute force angle. As force angle changed in both directions (left/right) for individual subjects with pain there was no change in average FT amplitude between conditions. When both medial and lateral forces were matched MU discharge rate decreased (P < 0.001) with pain, but, fewer units ceased firing or were newly recruited during pain. Change in motoneurone recruitment during pain alters direction of muscle force. This may be a strategy to avoid pain or protect the painful part. Ó 2010 European Federation of International Association for the Study of Pain Chapters. Published by Elsevier Ltd. All rights reserved.
1. Introduction The most commonly accepted theory to explain changes in muscle activity during pain; the ‘pain adaptation theory’ argues movement velocity and amplitude are reduced during pain by a combination of inhibition of agonist muscle and facilitation of antagonist muscles during voluntary movement (Lund et al., 1991). Although commonly referred to, the theory is not universally supported and much of the data is compromised by variable results (reviewed Murray and Peck, 2007). During experimental muscle pain, motoneurone discharge rate, which is a determinant of force (Burke, 1981; Stuart and Enoka, 1983), is decreased when force is maintained at pre-pain levels (Sohn et al., 2000; Farina et al., 2004; Hodges et al., 2008; Tucker et al., 2009; Tucker and Hodges, 2009). Until recently, reduced motoneurone discharge during pain was thought to support generalised inhibition of agonist muscles and therefore the ‘pain adaptation theory’; however there was little explanation how force was
* Correspondence to: K.J.Tucker, NHMRC Centre of Clinical Research Excellence in Spinal Pain, Injury and Health, School of Health and Rehabilitation Sciences, The University of Queensland, Brisbane, Qld 4072, Australia. Tel.: +61 7 3365 4589; fax: +61 7 3365 4567. E-mail address: [email protected] (K.J. Tucker).
maintained when motoneurone discharge rate was reduced. We have recently shown that in addition to decreased motoneurone discharge rate and derecruitment of units, other previously inactive motor units are recruited, presumably to help maintain force during pain (Tucker et al., 2009; Tucker and Hodges, 2009). These newly recruited units are not necessarily those expected given orderly recruitment of the motoneurone pool, and occur in both small non-synergistic (flexor pollicus longus) and large synergistic (quadriceps) muscles (Tucker et al., 2009; Tucker and Hodges, 2009). Reduced discharge of some units and increased discharge of others within a motoneurone pool during pain is inconsistent with generalised inhibition of the motoneurone pool. We conclude that the nervous system employs a different motor unit recruitment strategy to achieve the same force output, with an uneven distribution of synaptic input across the motoneurone pool during pain. The new theory predicts non-uniform changes within and between muscles during pain with some benefit to the system. Motor units within a motoneurone pool generate force in various directions (e.g. first dorsal interosseous (Suresh et al., 2008)), which may be associated with discrete functions of motor units within a muscle (e.g. (Thomas et al., 1978; ter Haar Romeny et al., 1982; Riek and Bawa, 1992)). We postulated that the new recruitment strategy during pain would result in an altered force
1090-3801/$36.00 Ó 2010 European Federation of International Association for the Study of Pain Chapters. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.ejpain.2010.03.006
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vector used to complete force-matched tasks (Tucker and Hodges, 2009). This may be beneficial in distributing load in a way that is less pain provocative or is protective of the painful area. We hypothesised that: (1) changes in motoneurone discharge during pain would alter the angle of whole muscle force produced during force-matched contractions; (2) given the change in angle of whole muscle force, total force required to complete the task during pain would be greater than during non-painful contractions; (3) by controlling both force amplitude and angle, subjects would override adaptations to motor unit recruitment during pain when force amplitude alone was matched; i.e. the pattern of motor unit recruitment during pain would be similar to that identified during amplitude and angle-matched contractions without pain. 2. Methods Nine volunteers with no history of significant knee/leg pain participated in this study (mean (SD) age; 28(8) years). The Institutional Medical Research Ethics Committee approved the study and all procedures conformed to the Declaration of Helsinki and the IASP’s guidelines for pain research in humans. 2.1. Electromyography Two pairs of intramuscular fine-wire electromyography (EMG) electrodes (two Teflon-coated 100 lm stainless steel wires with 0.5 mm insulation removed, threaded into a hypodermic needle (25 G 25 mm)) were inserted into both the medial (vastus medialis: VM) and lateral (vastus lateralis: VL) heads of the quadriceps. The needle was removed following insertion leaving the wires in place (Fig. 1A). EMG data were pre-amplified 2000– 10,000 times, band-pass filtered (30 Hz–2 kHz), notch filtered at 50 Hz, and sampled at 5 kHz using a Power1401 Data Acquisition System with Spike2 software (CED, UK). 2.2. Experimental design Subjects sat fully supported with their leg relaxed over the end of a plinth. Upper thighs were strapped firmly to the plinth to avoid changes in hip position during the knee extension tasks. Isometric knee extension force was measured with two force transducers (Futek, USA) that were secured to the plinth at right angles to each other. The force transducers were placed medially (FM) and laterally (FL) at 45° to the direction of extension force (FE) (Fig. 1B), then attached via a chain to a 5 cm wide thermoplastic band (1.6 mm UltraPerf, Sammons Preston, USA) that was moulded to the subject’s lower leg just above the ankle. Subjects were instructed to gently contract the test muscles before recording began in two separate trials until 2–6 (lower force), and 4–8 (higher force) single motor units (SMUs) were recorded consistently by any of the four fine-wire electrodes. These force levels were recorded for matching before and during experimental pain. During test contractions subjects increased force from rest to the displayed target level(s) over 6-s and then maintained this force for a 60-s reference contraction and 3 10-s contractions. After each contraction subjects reduced force to rest over 6-s, and rested for at least 10-s between contractions. This procedure was repeated during contractions when only extension force was provided as feedback and when feedback was provided from both the medial and lateral force transducers (explained in more detail below). To determine if the changes in SMU discharge that we have previously reported during pain (Tucker et al., 2009; Tucker and Hodges, 2009) were associated with a change in angle of force production, subjects were provided with feedback of, and asked
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to match extension force (FE: this is the amount of force produced in the extension direction, see Fig. 1B). By matching FE only (and not the angle of their force production) subjects were free to change the angle of their force production between trials (both in the control and pain trials) compared to the 60-s reference contraction. Extension force was determined from the forces recorded by the medial and lateral force transducers (FE = sin(45°) FM + sin(45°) FL; Fig. 1B and C). By using two force transducers to record force, we could measure changes in the angle of force production, and the total force used to match the extension force during each trial (force angle = a tan(FM/FL); total force (FT) amplitude = (F 2M þ F 2L ); Fig. 1B and C). Absolute force and angle change during each test contraction relative to the 60-s reference contraction was compared between trials with and without pain. The longer (60-s) contraction was used to account for variation over time, and allowed us to determine whether force characteristics deviated more (from reference) during pain than control. This was necessary as some degree of variation in angle of force production was expected even in the control conditions, and the variance could occur in both directions (more medially or laterally). To determine if changes in SMU discharge were associated with changes in the force vector (force angle and amount of total force produced at that angle) used to maintain extension force between conditions, SMU discharge characteristics were compared between the 3 10-s of data from each of the contractions with and without pain (for the low force contraction only). To determine if SMU recruitment was altered when subjects matched both force amplitude and direction (angle) of force production, subjects were provided with separate feedback from both force transducers (i.e. two feedback targets on the same feedback screen) during trials with and without pain. Subjects were instructed to modify the way (the angle) that they produced their extension force until both force targets were matched. Of the nine subjects, two subjects did not complete this task and another was unable to match their force with <5% error between conditions, and was therefore not used for this part of the study. For these FT (amplitude and angle) matched contractions, force vector characteristics were compared directly between the non-painful and painful contractions to ensure subjects had successfully matched the force and direction. For this analysis, force vector characteristics were determined from the 3 10-s contractions and from the best-matched 10-s period within the FT matched 60-s reference contraction. The three best-matched 10-s periods between the non-painful and painful trials were used for further analysis. SMU analysis was conducted on recordings from either the lower or higher force contractions, based on the contractions with least difference in FT (force amplitude and angle) between the non-painful and painful conditions. 2.3. Experimental pain Pain was induced by single bolus injection of hypertonic saline (0.25 mL, 5% NaCl) into the infra-patellar fat pad (Bennell et al., 2004; Tucker and Hodges, 2009). Experimental muscle pain was recorded throughout the pain trial using a custom-made electronic 10 cm visual analogue scale (VAS) whereby 0 = ‘no-pain’ and 10 = ‘worst pain imaginable’; or reported verbally using an 11 point (0–10) numerical rating scale (NRS) at 20-s intervals throughout the painful condition. In all trials the painful contractions commenced after the pain level reached 3/10. In all cases pain remained at P2/10 at the end of the painful contractions. The area of pain was recorded by subjects on a standardised figure (Fig. 1A) following the pain trial.
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(A) Electrode placement and pain location
VL
(B) Experimental set-up FE = 0°
VM
90°
Injection site
FL
FM VM
VL
(C) Calculating force vector characteristics FE FE = sin(45°)FM + sin(45°)FL FL FT
FT (maximum force produced at any angle) = (FM2+FL2) Angle of FT ( )=atan(FM/FL)
FM
Fig. 1. (A) The injection site; approximate area of reported pain for each subject (grey lines); and the location of fine-wire EMG electrodes in the lateral (VL) and medial (VM) heads of the quadriceps are shown. (B) Isometric knee extension force was measured from two force transducers (FM and FL) positioned at 90° to each other and attached to the subjects leg just above the ankle. (C) Extension force (FE), total force (FT), and angle of FT were calculated from FM and FL.
2.4. Data analysis SMUs were identified based on morphology using Spike2 software (CED, UK) from pairs of fine-wire electrodes that provided the recordings with clear discrimination between motor units throughout the trials. To ensure discrimination accuracy, motor unit inter-spike intervals were examined. Trials that contained abnormally short or long inter-spike intervals were re-analysed on a spike-by-spike basis to check for discrimination accuracy. Averages of SMU recordings were then triggered from the discharge of each discriminated unit over the three 10-s analysis periods to generate a profile template of the motor unit morphology (e.g. Fig. 2, bottom panel). These profiles were compared visually within subjects to determine if the same unit was present in each contraction. Motor units that discharged for more than half of at least two of the three 10-s contractions within a condition were considered reliable for that condition (Tucker and Hodges, 2009). The mean discharge rate of all reliable motor units was recorded for comparison between conditions. Motor units from the two regions of the quadriceps muscle (VM and VL) behaved similarly between conditions and were grouped for analysis (Tucker and Hodges, 2009). 2.5. Statistical analysis For the extension force match tasks, data was non-normally distributed. The Wilcoxon matched pairs sign rank test was therefore
used to compare the force vector characteristics (absolute change in FT, FE and angle of FT from the reference contraction) between the non-painful and painful contractions. The Wilcoxon matched pairs sign rank test was also used to compare the force vector characteristics directly between contractions with and without pain in the force amplitude and angle matched trial. Comparison of the discharge rate of motor units identified in both the trials with and without pain was made with paired t-tests (two-tails). An independent t-test (two-tails) was used to compare the discharge rate of the whole population of motor units recruited in either condition. Data are presented as mean (SD) throughout the text and figures. Significance was set at P < 0.05.
3. Results The average pain rating reported during the contractions with pain was 4.1(2.1)/10. Pain was generally localised to the medial aspect of the patella around the location of the saline injection (Fig. 1A). The average knee extension force (FE) used during the 60-s lower and higher reference contractions was 9.8(6.7) N (range 3.7– 25.6 N) and 16.6(13.2) N (range 5.3–50.6 N), respectively. The average total force (FT) used to complete the lower and higher force reference contractions was 10.6(6.8) N (range 3.7–26.1 N) and 17.5(13.5) N (range 5.3–51.9 N), respectively. As FE represents the
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Fig. 2. Force profile during ramp hold contractions during extension force (FE) and total force (i.e. feedback from FM and FL) feedback trials are shown in the top three traces. The 10-s period used for analysis from each of these contractions is highlighted by the grey box. When FE feedback is provided the angle of force production is altered during pain. This is demonstrated by a change in the relative contribution of FM and FL in the top left traces during pain compared to the No-pain condition. When feedback was provided from both FM and FL (in the two right panels) both force and angle of force production are matched between the no-pain and pain contractions. Each discharge of all discriminated motor units (A–F) from two fine-wire EMG channels is shown in the middle section of this figure. The mean discharge rates of these motor units during the 10-s analysis period are also shown. The fine-wire EMG data and discharge of motor units from 1-s during each of the contractions is expanded in the bottom panel. The profile of each single motor unit action potential that discharged during these contractions is also shown. When FE is matched (no attempt to maintain same angle during pain) some motor units (e.g. D and E) were recruited in each condition. These units decreased in discharge rate during Pain. Other units were no longer recruited during pain (e.g. C) and a third population of units were newly recruited during pain (e.g. A, B and F). When feedback was provided from both force transducers (right panels), so that both extension force and angle was matched, the change in recruitment of units are less profound. In this example all of the motor units were recruited in both the no-pain and pain trials, and all decreased in discharge rate during pain.
part of FT that is produced in the extension direction (Fig. 1B and C), it is expected that FE will be less than or equal to FT. The angle of FT produced during the 60-s lower and higher reference contractions was 20.8(12.1)° (range 3.1–34.11°) and 17.9(8.3)° (range 3.0° to 25.11°), respectively. When subjects were provided with feedback of the FE alone, the absolute change in both FE and FT amplitude, compared to the reference condition, were similar in the non-painful and painful
contractions at both force levels (Fig. 3A and B; all P > 0.1). Although there was no significant change in force amplitude between conditions, the angle of FT was changed with pain. The absolute deviation in angle of FT compared to the reference contraction was 5° greater during pain than during the brief non-painful contractions (Fig. 3C: P < 0.01 during lower force and Fig. 3D: P = 0.01 during higher force contractions). This change in angle occurred with similar frequency to the left and right (medially and laterally)
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Fig. 3. Absolute amplitude and angle change (mean (SD)) during the non-painful and painful contractions relative to the 60-s reference contraction, during both lower and higher force contractions are shown. The extension force (FE) and total force (FT) used to complete the test contractions were not different between conditions (A and B). However, the absolute change in angle during the painful contractions was 5° greater than that during the contractions without pain during both the lower (C) and higher (D) force contractions.
to that in the reference contraction. In two subjects the direction of angle change during pain was opposite during the lower and higher force contractions. The change in angle of FT during pain (Fig. 2, top left; Figs. 3C and D) was associated with altered motor unit recruitment
(Fig. 2, FE feedback; and Fig. 4B and C). A total of 55 single motor units were discriminated from the lower force contraction data. Of these units, 24 discharged in both the contractions with and without pain. An additional 13 units were only identified during contractions without pain (i.e. they were derecruited during pain), and 18 units that were not identified during the condition without pain were identified during pain (i.e. recruitment of new units during pain) (Fig. 4B). This means that of the units identified during these contractions 55% differed between conditions. The discharge rate of the units identified in both conditions and of the total population of units identified in either condition decreased with pain (Fig. 4C: both P < 0.001). Although the group data showed a decrease in discharge rate during pain, n = 1 of the units recruited in both conditions increased its discharge rate during pain (from 10.3(0.2) to 10.5(0.3) Hz). When subjects were required to match both the medial and lateral forces (to match FT amplitude and angle), changes in motor unit recruitment strategy during pain were less evident (Fig. 2, right panel, Fig. 4E and F). Within the six subjects used for this analysis the largest variability between conditions was 3% amplitude (for both FT and FE) and 2° angle of FT. For the non-painful and painful contractions respectively: FE: 10.1(7.6) and 10.0(7.5) N; FT 10.9(8.0) and 10.9(8.0) N; both P > 0.5; angle of FT: 18.9(10.7) and 18.9(10.9)°; P > 0.9 (Fig. 4D). A total of 32 motor units were discriminated from the test contractions. Of these, 25 were present in both the contractions with and without pain. This means that of the units identified during these contractions 78% discharged in both the contractions with and without pain. Of the six subjects, three recruited the same units in both conditions, one subject recruited 4 units during the no-pain condition that were not recruited during pain and two other subjects recruited 1–2 motor units during pain that were not recorded in the non-painful contraction (Fig. 4E). Despite the relatively consistent active population of units, the discharge rate of the units identified in both
Fig. 4. The range of angles and changes in motor unit recruitment used by all subjects to match force during the contractions with and without pain are shown. Data from contractions when feedback of extension force (FE) alone (top row) and both medial (FM) and lateral force (FL) (bottom row) are shown. The angle change observed during painful contractions when feedback of extension force was provided (A) is associated with considerable changes in motor unit discharge patterns (B and C). In contrast, when feedback was provided from both FM and FL, the angle used remained the same between conditions (D) and some changes in motor unit discharge pattern are less prevalent (E and F).
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conditions, and the total population of units identified in either condition, decreased with pain (Fig. 4F: both P < 0.001). Although the group data showed a decrease in discharge rate during pain, n = 3 (12%) of the units recruited in both conditions increased their discharge rate during the painful FT matched task (from 7.7(0.9) to 7.9(1.1) Hz).
4. Discussion These data show that changes in motor unit discharge during pain are associated with changes in force direction during matched force tasks. Our findings support the theory that rather than uniform inhibition or facilitation of the motoneurone pool, there is a reorganisation of motor unit recruitment during pain, and that this reorganisation is associated with altered force angle during pain (Murray and Peck, 2007). Motor units within the same motor unit pool can produce force in variable directions (Burke, 1991; Suresh et al., 2008) and therefore changes in whole muscle output and force orientation may result from non-uniform changes in recruitment of units within a muscle’s motoneurone pool (Thomas et al., 1978; ter Haar Romeny et al., 1982; Riek and Bawa, 1992; Yang et al., 1998; Butler et al., 1999). When subjects were asked to contract their vastii muscles during the non-painful reference contraction in the current investigation, force was produced on average 21° laterally. This is likely to be a result of the configuration of the knee joint and superior mechanical pull of the lateral quadriceps compared to their synergist muscles (Lieb and Perry, 1968). When force amplitude (but not direction) was matched, the 5° difference in angle between conditions was associated with a change in the population of motor units recruited. Approximately 55% of the identified units were only recruited in either the contractions with or without pain (and not in both conditions). The change in motor unit recruitment during pain is supported by other work from our laboratory (Tucker et al., 2009; Tucker and Hodges, 2009). In muscle groups with large mechanical redundancy (i.e. multiple possible strategies to produce similar movements; e.g. the jaw (Van Eijden et al., 1990) and trunk (van Dieen et al., 2003) muscles); and regions within muscles with differences in mechanical efficacy (e.g. respiratory system (De Troyer et al., 2003; Gandevia et al., 2006), limbs (Thomas et al., 1978; ter Haar Romeny et al., 1982; Riek and Bawa, 1992; Yang et al., 1998; Butler et al., 1999)) the recruitment of motor units has been argued to be organised to achieve the best mechanical advantage at the lowest metabolic cost. It is commonly assumed that the most stable and efficient strategy of muscle recruitment is selected to complete a task, and if the strategy was to change during pain, the new strategy may be less efficient (Murray and Peck, 2007). This assumption is consistent with the hypothesis that the changes in muscle activity in people with chronic low-back pain are aimed at avoiding noxious stresses in injured structures, thereby avoiding or minimizing pain (Hodges et al., 2003; van Dieen et al., 2003) rather than completing the task in the most efficient manner. In the current investigation we hypothesised that a change in angle of force production would result in greater total force (FT) being required to match the force generated in the extension direction (FE). However, this did not occur as force changed in the medial and lateral direction with no net change in total force. However, our data show that initially the force was generated at 21° from the extension direction and thus the required force was greater than the target extension force, i.e. not the minimum force. This suggests that some parameter other than minimum force was being controlled to extend the knee, and this may be related to the complex mechanics of the knee extensor mechanism. As the reference condition was
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not performed with the least force there was the potential for the contractions during pain to be performed with both more or less force, and this was the case. Thus our hypothesis of decreased force was not supported, but this does not exclude the possibility that the ‘‘new” task was less efficient. One possible advantage of the altered motor unit recruitment during pain may be to alter the direction of force production to minimize the provocation of pain while still completing the task. Although this conclusion could be argued to be compromised by the data that show changes in force direction both towards and away from the location of pain reported subjectively at the end of the trials, it cannot be assumed that a change in either direction will be less pain provocative for an individual subject. This is because it is impossible to predict which changes would alter load on the fat pad in a manner to reduce pain provocation. It is also possible that the change in angle is a consequence of the adaptation in motor unit discharge and not the goal of the change in motor unit recruitment during pain. It is possible that the aim of the altered recruitment may be to selectively recruit units with different force production capacity, i.e. larger units that can match force at a lower discharge rate, or produce a faster change in force, rather than to selectively recruit units with a different force direction profile. However, our findings that the change in recruitment of units was less prevalent when force amplitude and angle are both matched lend support to the change in direction being the goal. In the current investigation when contractions were matched for both force amplitude and angle, 78% of the units were recruited in both the contractions with and without pain. Interestingly, there was a greater prevalence of units with increased discharge rate in this condition than during the amplitude-matched task (from n = 1/24 to 3/25). The alternative force production strategy of increasing the discharge rate of individual units during pain (Tucker et al., 2009) may be needed to compensate for the decreased discharge rate of some units when the ability to change direction was restricted. From the findings of this and our previous investigations (Tucker et al., 2009; Tucker and Hodges, 2009), we argue that during force match contractions with pain, motor unit recruitment strategies are altered in a complex manner that cannot be explained by generalised inhibition to the motoneurone pool. This change in recruitment strategy involves the reduction in discharge rate and complete cessation of discharge of some units, the increase of discharge rate in some units and the recruitment of new units during pain. The change in motor unit recruitment is related to a change in force direction, and when both force direction and amplitude are matched a different motor unit recruitment strategy is required to maintain force. The data provide further evidence of non-uniform input to the motoneurone pool during pain. Given the assumption that the optimal recruitment strategy is likely during non-painful contractions (De Troyer et al., 2003; Gandevia et al., 2006), and that the nervous system may attend to the combined goals of task completion and pain minimization during painful contraction (Hodges et al., 2008; Tucker and Hodges, 2009), the altered motor unit recruitment and angle of total force may indicate a less efficient mechanical system during pain. 5. Conflict of interest statement There was no conflict of interest. Acknowledgements Financial support was provided by the National Health and Medical Research Council of Australia, and the University of Queensland Early Research Career Grant.
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