The pain-adaptation model: a discussion of the relationship between chronic musculoskeletal pain and motor activity' JAMESP. L w b 2 AND REVERSDONGA Facult&cfe m&decine dentaire eb Centre de recherche en sciences neurologiques, Universite' ale Montr&al, C.Pe 6128, Succ. A , kfontre'al (Qukbec), Canada H3C 3J7

CHARLES G. WIDMER Dental Research Centre, Emory University, 1462 Cliflon Woad, Atlanta, GA 30322, U.S.A.

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AND

CHRISTIAN S. S ~ H L B R F~cultysf Dentistry, University of Michigan, Ann Arbor, MI 48109-1078, U.S.A. Received August 1, 1990 LUND,J. P., ~ N G A R.,, WIIDMER, C. G., and S'TBHLER, C. S. 1998 . The pain-adaptation model: a discussion s f the relationship between chronic musculoskeletal pain and motor activity. Can. J . Physiol . Pharmacol. 69: 683 - 694. Articles describing motor fennction in five chronic musculoskeletal pain conditions (temporomandibular disorders, muscle tension headache, fibromyalgia, chronic lower back pain, and postexercise muscle soreness) were reviewed. It was concluded that the data do not support the commonly held view that the pain of these conditions is maintained by some form of tonic muscular hyperactivity. Instead, it seems clear that in these conditions the activity of agonist muscles is often reduced by pain, even when this does not arise from the muscle itself. On the other hand, pain causes small increases in the level of activity of the antagonist. As a consequence of these changes, force production and the range and velocity of movement of the affected body part are often reduced. To explain how such changes in the behaviour come about, we propose a neurophysiological model based on the phasic modulation of excitatory and inhibitory interneurons supplied by high-threshold sensory afferents. We suggest that the "dysfunction" that is characteristic of several types of chronic rnusculoskeIeta1 pain is a normal protective adaptation and is not a cause of pain. Key words: pain, headache, temporomandibular disorders, fibromyalgia, chronic lower back pain, post-exercise muscle soreness.

LWND,J. Pa, BONGA,R., WIDMER,C. G., et STOHLER, C. S. 1991. The pain-adaptation model: a discussion of the relationship between chronic measculoskeletal pain and motor activity. Can. 9. Physiol. Pharmacol. 69 : 683 -694. On a revise des articles decrivant la fonction motrice dans cinq conditions de douleur musculo-squelettique chronique (desordres temporo-mandibulaires, cCphalCe par tension nerveuse, fibromyalgie, lombalgie chronique et courbature postexercice). On a conclu que les donnees ne supportent pas I'idCe habituelle que la douleur associee $ ces conditions est mainteneae par une forrne d'hyperactivite musculaire tonique. Au contraire, il semble clair que, dans ces conditions, l'activite des muscles agonistes est souvent ruuite par la douleur, meme lorsquqelHen'tname pas du muscle mCme. Par ailleurs, %adouleknr provoque de faibles augmentations des effets de type antagoniste. En consequence, la production de force, I'amplitude et Ha vitesse de mouvement de la partie corporelle affectke sont souvent rkduites. Pour expliqkner comment se prodanisent de telles variations de comportement, nous proposons un modkle neurophysiologique bas6 sur la modulation phasique d'interneurones inhibiteears et excitateurs pouwreas d'afferences sensitives h seuil ClevC. Nous suggerons que le "dysfonctionnement." qui est caracteristique de plusieurs types de douleur muscu%o-squelettique,est une adaptation protectrice normale et n'est pas une cause de douleur. Mots clds : douleur, cCphalCe, dksordres temporo-mandibulaires, fibromyalgie, lombalgie chronique, courbature postexercice. [Traduit par la redactisn]

Introduction In this article we will be proposing the hypothesis that the "dysfunction" that is characteristic of several types of chronic muscular pain is a normal protective adaptation and is not one of the causes of the pain. The alternative idea, that many of the common forms of chronic muscle pain are at least partly caused by abnormal muscle activity, is widespread and has had a long life. Beginning with the first EMG recordings of painful muscles that were made, several authors reported that the activity was highly abnormal, and indicative of cowtracture, 'This paper was presented at the XIIth International Symposium of the Centre de recherche en sciences neuro%ogiqanes,Universitd de MontrCal, called Chronic Musculoskeletal Pain, held in Montreal, QuC., May 24 -25, 1990, and has undergone the Journal's usual peer review. 2Aaathor for correspondence. Printed in Canada 1 Imprimc au Canada

spasm, or spastic contractions. However, it soon became clear that the large majority of patients with chronic muscle pain show few signs of neuropathology (Mills and Edwards 1983; Yemm 1985; McBrmm et aH. 1988; Zidar et al. 1998). Interest then moved towards models in which abnormal muscle activity at rest and (or) during function is supposed to cause or at least perpetuate the pain. Whether it is called fibromyalgia, myofascial pain, chronic lower back pain, tension headache, or postexercise muscle soreness, one of the most common explanations for the gain is that it is caused by muscle hyperactivity- This hyperactivity is thought to be due to a variety of causes, the most common being overwork or fatigue (Hough 1902; Asmussen 1956; de Vries 1966; Abraham 1977; Howell et al. 1985; Christensen 1986; Jones et al. 19871, structural abnormalities (Moss 1988), and stress (Schwartz 1959; L a k i n 1969; Yemm 1975: Yunus 1988). The transformation from an acute to a chronic condition was

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CAN. J. PHYSIOL. PHARMACOL. VOL. 69, 1991

explained by Trave119shypothesis that pain and dysfunction are reciprocally linked: dysfunction causing pain which then reinforces dysfunction, setting up the "vicious cycle" that maintains the condition (Travel1 et al. 1942). This idea has been widely accepted (Cobb et al. 1975; Okeson 1985; Michler et al. 1987; Blasberg and Chalmers 1989; Parker 1990), and muscle hyperactivity has even been included as a possible etiological factor in some of the newer models of fibromyalgia (Yunus 1988; Bengtsson and Bengtsson 1988). However, the Back of convincing evidence to support the belief in hyperactivity as an etiological factor has been pointed out in recent reviews of several chronic muscle pain conditions (Nouwen and Bush 1984; Chapman 1986; Ahern et al. 1988; Lund and Widmer 1989; Hendriksson and Bengtsson 1991). The demise of the hyperactivity -causality models does not mean that motor performance is unaltered in the presence of pain. We will present evidence that, although pain causes little change in postural activity, it does modify performance by reducing the output of agonist muscles and increasing the level of antagonist co-contraction. We believe that these changes occur in several chronic pain conditions, that they are protective adaptations, and that they can be explained by the action of pain on segmental interneurons. Some of the topics to be discussed have been covered in more detail by Eund and Widmer (1989), Lund et al. (1989), and Widmer et al. (1990).

Changes in muscle function in chronic pain syndromes Resting and postural activity Ternporomrrdibular disorders The jaw-closing muscles of the large majority of temporomandibular disorder (TMD) patients are tender to palpation, and approximately 40% report pain on chewing (Dworkin et al. 1990). There are several reports that support the hypothesis that these symptoms are caused by higher than normal postural electromyographic (EMG) activity. One of the first quantitative studies on patients and control subjects was carried out by Eous et al. (1970). They reported that there were significant differences in EMG activity in the masseter and temporalis muscles, with the patient group having the higher levels. Unfortunately this and most of the other studies suffered from problems of experimental design, the most serious being the choice of inappropriate control subjects. The patients were mostly females over 30, while the controls were younger males, and it is known that both sex and age have significant effects on the level of resting EMG activity (Carlson et al. 1964; Visser and Be Rijke 1974). However, support for the hypothesis can be found in two other studies that did use age- and sex-matched controls (Dahlstrom et al. 4985; Rugh and Montgomery 198'7). On the other hand, no differences in resting EMG activity were found in a third study (Majewski and Gale 1984). It now seems likely that the higher postural levels in patients found by Dahlstrom et al. (1985) and Rugh and Montgomery (1987) were due to another uncontrolled variable, bruxism (nonfunctional clenching and grinding of teeth), which is more prevalent in TMB patients than in the general population (Trenouth 1979; Easkin 1969). Sherman (1985) found that people who brux, and therefore exercise their jaw muscles more than normal, have significantly higher resting EMG levels than controls. In the same study, there were no differences in resting activity of nonbruxing controls and TMD patients, nor between TMB bruxers and bruxers free from

pain. These problems with uncontrolled variables can be eliminated when sub$ects act as their own controls, as can be done when the pain is unilateral. If muscle pain is due to local postural hyperactivity, then the muscles on the painful side should have higher resting EMG activity than those on the contralateral side, but they do not (Majewski and Gale 1984; Dahlstrom et al. 1985; Dolan and Keefe 1988). Muscle tension headache The very name of this stress-related disorder emphasizes the traditional view that muscle tension headache (MTH) pain is caused by tonically elevated activity in the muscles of the head and neck (Tunis and Wolff 1954; Bakal and Kaganov 1977; Beaty and Waynes 1979). This belief prompted the development of EM@ biofeedback therapy to monitor and reduce facial, masticatory, and cervical muscle activity to "acceptable" levels to control the headache pain (Budsynski et al. 1973; Wickramasekera 1974; Cox et al. 1975). Before we accept that there is a close association of muscle, headache, and stress, it needs to be shown that EMG levels of facial, masticatory, neck, or shoulder muscles are higher in the headache patients than in control subjects. Again, many studies did not include properly selected control subjects, and this probably explains why there is no consensus among them. Three of these studies supported the concept that resting frontalis EM@ levels are higher in MTH than in a nonheadache group (Vaughn et al. 1977; Van Boxtel and van der Ven 1978; Hursey et al. 1985), but six did not (Bakal and Kaganov 1977; Anderson and Franks 1981; Feuerstein et al. 1982; Van Boxtel et al. 1983; Hudzinski and Lawrence 1988; Pritchard 1989). However, the situation has been clarified by studies in which patient and control groups were matched for age and sex. These revealed no evidence of elevated EMG levels in frontalis (Martin and Mathews 1978; Sutton and Belar 1982), neck (Martin and Mathews 1978), or temporalis (Majewski and Gale 1984) muscles in MTH. A corollary of the muscle tension hypothesis is that EMG levels should be higher in the headache patient during or just prior to the pain episode than at other times. Although most reports of studies of MTH patients did not include the current pain status of the patients being monitored electromyographically, those that did found no correlation between pain intensity and mean EMG levels (Bakal and Kaganov 1977; Martin and Mathews 1978; Hudzinski and Lawrence 1988; Pritchard 1989) or, surprisingly, a negative correlation (Anderson and Franks 1981). Since stress seems to be a predisposing factor, one should also expect the craniocervicd muscles of MTH patients to be more reactive to stress than controls. Experimental stressors have been applied to headache patients and unmatched controls in the laboratory after establishing a pre-stress EMG baseline. Two papers reported that stressors caused an increase in EMG activity (Hursey et al. 1985; Pritchard 1989), but on the other hand, most authors found no change (Vaughn et al. 1977; Van Boxtel and van der Ven 1978; Anderson and Franks 1981; Feuerstein et al. 1982). Stressors had similar effects on both patient and control groups in two wellcontrolled studies (Martin and Mathews 1978; Sutton and Belar 1982). It could be argued that lack of response is due to the artificial laboratory setting, but a recent within-subject study of MTH sufferers in their natural environment found that there was no statistically significant correlation between self-reported stress,

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LUND ET AL.

EMG levels, and pain (Wugh et al. 1998). Finally, if "muscle tension" is pathognomonic of MTH, cranial EMG levels should be higher in this patient population than in other headache groups. Frontalis EMG levels of different headache groups such as migraine, tension, or mixed headaches have been compared, and in the majority of studies no differences were found between groups (Anderson and Franks 1981; Feuerstein et al. 1982; Van Boxtel et a1. 1983; Pritchard 1989). There is one report that higher frontalis EMG is associated with one headache category, but this was migraine rather than MTM (Bakal and Kaganov 1977). In another study, occipital muscle activity was significantly higher in the tension headache group, while reduced in the migraine headache category (Pritchard 1989). None of the above studies used ageand sex-matched groups. Therefore, there is little evidence in the literature in favour of the association of stress, elevated EMG activity of facial, masticatory, or cervical muscles, and pain in headache patients. Similar conclusions have been reached by the authors of other reviews (Haynes et al. 1982; Philips 1980; Chapman 1986). Even if it is eventually proved that some groups of headache patients do have small increases in EMG levels in the muscles of the head and neck, this may not be sufficient evidence that "hyperactivity" is causing the pain. It is more probable that it is part of a general response of the patient to pain that includes a change in facial expression or head posture. Evidence is accumulating that chronic pain patients can be distinguished by their body posture, gestures, and their facial expressions (Collins et al. 1982; LeResche and Dworkin 1988; Prkachin and Mercer 1989; Keefe et al. 1998). For instance, subjects with chronic lower back pain (CLBP) show significantly higher levels of "pain behaviours" during walking than controls, and two of the five behaviours that were scored (grimacing and sighing) involve the orofacial muscles (Keefe and Hill 1985). More specifically, Collins et al. (198%)have shown that frontalis EMG activity was significantly higher in a group with CLBP than in age-matched-controls at rest and during movement.

685

Nouwen and Bush concluded that the evidence for higher resting activity in CLBP was minimal. In addition, Nouwen and Bush (1984) found three reports indicating that paraspinal activity of CLBP subjects was higher than normal during prolonged standing, and three stating that it was not. Another positive relationship between CLBP and paraspinal activity during standing was reported by Arena et al. (1989), but there were no significant differences in the two studies in which care was taken to match CLBP patients and controls for age, sex, and other factors (Collins et al. 1982; Ahern et al. 1988). Postexercise muscle soreness The pain associated with conditions like bruxism or restless leg syndrome (Lavigne et al. 1991) are perhaps types of postexercise muscle soreness (PEMS). The chronic nature of these pains could be due to the periodic repetition of trauma, because the pain and stiffness that occur a day or two after a single bout of unaccustomed exercise rarely lasts for more than a few days. Although it has long been proposed that the source of the pain and stiffness of PEMS was physical damage to muscle fibers or connective tissue (Hough 190%;Asmussen 1956), there were others who believed that it was caused by muscle spasm (de Vries 1966). As in the case sf the other conditions we have discussed, there is now evidence that the hyperactivity-causality model of PEMS is incorrect (Abraham 1977; McGlynn et al. 1979a, 1979b). The strongest negative evidence comes from two investigations of the relationship between EMG activity of biceps brachii and the pain that follows eccentric exercise (Howell et al. 1985; Jones et al. 1987). After exercise, the elbows of most subjects in these studies developed a flexed posture before pain developed. This posture was maintained for several days, while pain and tenderness in the biceps rose and then diminished. However, the changes were not accompanied by increased resting EMG activity. The authors suggested that the increased flexion was caused by the shortening of noncontractile elements in the muscle tissues or by edema. Coasclusions The findings of the studies that used age- and sex-matched controls are summarized in Table 1. These and the other data that we reviewed lead to the conclusion that the level of resting or postural muscle activity is no higher than normal in the five musculoskeletal pain conditions that we have described, with the occasional exception of the facial muscles. However, it is likely that this exception is unrelated to the source of pain and is simply a reflection of the changes in facial expression that pain often causes.

Fibromyalgia Although resting hyperactivity has been implicated in the etiology of fibromyalgia, we could only find one attempt to test the hypothesis. This study was done by Zidar et al. (1998), who carried out EMG recordings from biceps brachii, trapezius, and tibialis anterior of female fibromyalgia patients and age-matched controls. Patients reported pain in all three muscles before and after intramuscular EMG recording, while the control subjects did not, and these differences were highly significant. On the other hand, there was no difference in the level of resting EMG activity; in fact no motor units were active at rest in any of the controls nor in 86% of the patients. The authors concluded that factors other than continuous muscle tension maintain the pain of fibromyalgia.

Activity during static and dy?zarnic contractions In this section we will be able to deal with only three of the five disorders discussed in the section on Resting and postural activity, because of a lack of relevant studies in two categories. First, we will describe the situation when inuscles act as agonists.

Chronic lower back pain Nouwen and Bush (1984) tested several predictions of the hyperactivity-causality models of CLBP. The first of these was that resting activity should be higher in the paraspinal muscles of low back pain patients. They reviewed four studies, only one of which reported significantly higher levels in the patient group. Since that particular experiment used an uninterpretable technique (counting pulses exceeding 10 pV),

Changes in output of agonists (a) Temporomndibular disorders Some of the supporters of the hyperactivity -causality models have concluded that the jaw-closing muscles of TMB patients are hyperactive when they act as agonists during the jawclosing phases of mastication (MBller et al. 1984; Magberg 1987); but to arrive at this conclusion, they had to express activity as a "relative" score. This was done by dividing the

CAN.

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VOL. 69, 1991

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TABLE 1. Westing and postural activity studies with age- and sex-matched controls References

Activity

TMB Dalstrom et al. 1985 Rugh and Montgomery 1987 Majewski and Gale 1984 Sherman 1985 (matched for bmxism) Headache Martin and Mathews 1978 Sutton and Belar 1982 Majewski and Gale 1984 Fibromyalgia Zidar 1998 CLBP Moyt et al. 1981 Collins et al. 1982 Ahern et al. I988 PEMS Newham et al. 1983 Howell et al. 1985 Jones et al. 1987

Resting jaw-closer EMG > control

+ +

-

Facial muscle EMG > control -

Limb muscle EMG > control

-

Paraspinal activity > control -

Postexercise > pre-exercise -

NOTE:CLBP, chronic lower back pain; $EMS, postexercise muscle soreness; TMD, temporomandibulardisorder.

TABLE 2. Summary of studies in which the amplitudes or areas of agonist muscle E M 6 bursts from subjects suffering with chronic musculeaskeletal pain were compared with control data Agonist action

References - - -

--

-

-

-

TMD Molin 1972 (matched 9) CLBP Alston et al. 1966 (unmatched 0 and Q ) Thorstensson and Amidson 1982 (matched 0) Suzuki a d Endo 1983 (matched 0 ) Triano and Schulta 1987 (unmatched 0 and Q ) Fibromyalgia Jacobsen and Danneskiold-SamsOe 1987 Backman et al. 1988

-

-

Control MVC > TMD

+ +

Control trunk strength > CLBP +/f

+

Control MVC > control -k

+

NOTE:CEBP, chronic lower back pain; MVC, maximum voluntary contraction; TMD, ternpromandibular disorder.

EMG value calculated during mastication by the activity $enerated during a maximum voluntary contraction 2 (MVC). The danger with this manipulation is that any factor that affects the MVC, like age and sex, changes the relative activity. This is particularly important when groups are unmatched, as shown by the fact that the absolute level of EMG activity in the study by Moiler et al. (1984) was actually higher in most of the muscles of control subjects than in patients when the two groups chewed apple. This result is more in line with the common impression that pain makes muscles difficult to use and less powerful (Mills and Edwards 1983). There is now evidence that the latter is the true situation in TMD. Molin (1972) has clearly shown that the MVC of the jaw-closing muscles is much lower in female TMD patients than in female controls. Other workers came to the same or to the opposite conclusion, but they were not using groups that were age- or sex-matched (Naeije and Hansson 1986; Sheikholeslam et al. 1980; Hagberg 198%).Another reason to link the fall in MVC to pain is that bite force increases as the symptoms disappear (Helkimo et al. 1975). It is interesting that the effect of pain is not restricted to the muscle in which-it arises, for there are no differences in unilateral biting force between painhl and nonpainfbal sides (Molin 1972; Helkimo et al.

1975). Furthermore, pain has this effect even when it does not originate in the muscle or in the joint around which the muscles act. When High et al. (1988) measured subjective pain levels and maximum biting force of patients before and after third molar extraction they found that the MVC of almost all subjects was much less after surgery, and that there was a weak negative correlation between the two measurements.

(b) Fibromyalgia The MVC of fibromyalgia patients also seems to be diminished. Backman et d.(8988) found that the maximum handgrip strength of female fibromyalgia patients was significantly less than that of matched controls, while Jacobsen and DanneskioldSamsoe (1987) obtained similar results when they measured the strength of knee extensor muscles. In addition, when Backman et al. (1988) used direct electrical stimulation to investigate the capacity of the adductor pollicis muscle to develop force, they found no diminution in the patient group. This led them to suggest that the lower MVC of this group was due to central, rather than peripheral, factors.

(4 Chronic lower back pain The studies published prior to 1984 summarized by Nouwen and Bush (1984) present a confusing picture: one study sug-

LUND ET AL.

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TABLE3. Summary sf studies in which the amplitudes or areas of antagonist muscle EMG activity from subjects suffering with chronic musculoskeleta~pain, measured during the burst of the agsnist muscle, were compared with control data References

Antagonist action

TMB Miiller et al. 1984 (unmatched Q° and Q) Stokler et al. 1985 (unmatched CY and Q) Stohler et al. 1988 (within subject, painful vs. nonpainful cycles) CEBP Floyd and Silver 1955 (unmatched 0 and Q) Triano and Schultz 1987 (unmatched Q° and Q ) Ahern et al. I988 (matched Q° and 9 )

TMB closer EMG > control -?-

+ -?-

CEBP paraspinal EMG > control -!-?-

+

NOTE:CLBP, chronic lower back p i n ; TMD, temporomandibular disorder.

POSTUWAL MUSCLE ACTIVITY

gested that paraspinal activity was higher than normal in CLBP during some movements, the other reported that it was less, and a third that it was unchanged. Part of the problem is that again the groups were not age- and sex-matched in most studies, and that statistical analyses were not done in others. However, we believe that the most important factor was that some of the movements required the dorsal paraspinal muscles to act as agonists, while in others they were working as antagonists. Most measurements of the force output of the lower back flexor and extensor muscles when they act as agonists indicate that the MVC of CLBP patients is less than that of matched controls (Alston et al. 1966; McNeil et al. 1980; Thorsteinssen and Amidson 1982; Suzuki and Endo 1983). All of the above were cross-sectional studies, and therefore do not help one to distinguish between cause and effect. The question "Do weak muscles predispose to CLBP or is the fall in MVC a secondary effect?" can only be answered by prospective studies, suck as that by Eeino et al. (1987). They carried out a survey, medical examination, and physical testing of several hundred employees in the metal industry and repeated their measurements after a 10-year interval. They found no association between the initial level of muscle function and the subsequent development of CLBP, leading to the conclusion that reduced trunk muscle hnction seems to be a consequence rather than a cause of CEBP.

FIG. 1. Myoelectric activity recorded over the left masseter muscle at rest (baseline BL), during experimental pain (P), during sham p i n (SP), and after pain (AP). During sham pain, subjects were requested to re-experience an earlier p i n (if the sham trial came before pain induction), or the previous experimental p i n . Data represent rootmean-square (RMS)muscle activities in microvolts of at least 30 epochs of 2 s of artifact-free recording.

Changes in outjFPut of antagonists (a) TemporomncBibuIar disorders Dworlcin et al. (1990) carried out an epidemiological study that compared the clinical signs and symptoms of TMD patients with those of randomly selected members of the same cornunity . They reported that the average unassisted vertical jaw opening, both with and without pain, was less in patients and in members of the community who reported TMD pain, than in the community controls. This study of a large population confirms several other reports that masticatory muscle pain alters voluntary jaw opening (Helkimo 1974; Stohler et al. 1988; Clark and Lynn 1986). It is usudly assumed that the decrease in amplitude and velocity of jaw opening is caused by muscle spasm, trismus, or by splinting (Clark 1985; Yemm 19851, but only a few scientists have examined muscle khaviour underlying restricted movements. In the first of these, Greenfield and Moore (1969) compared surface EMG activity before and after oral surgery, but no statistical tests were done. The authors were convinced that there was a considerable reduction in the amplitude of voluntary jaw opening, and that this occurred because the

patients stopped to avoid pain. If the patients could be persuaded to open further, Greenfield and Moore reported that there was a sudden and substantial increase in EMG activity in the rnasseter and tempralis muscles on both sides. There is now numerical data that support this observation. Stohler et d. (1985) found that when TMD patients opened their mouths voluntarily, EMG levels in jaw closing muscles were significantly higher than in controls. Similarly, jaw-closer EMG activity has been reported to be higher in TMD patients during the opening phase of mastication (M811er et al. 1984). Unfortunately, the groups in these studies were not age- and sex-matched. Finally Stohler et al. (1988) showed that there was significantly greater EMG activity in jaw-closing muscles of TMD patients during the opening phase of painful masticatory cycles than in the pain-free cycles. (b) Chronic lower back pain Many authors have reported that CLBP patients show limitations of movement, and in particular are unable or unwilling to flex the spine to a normal degree (Floyd and Silver 1955; Nouwen and Bush 1984; Triano and Schultz 1987; Ahern

Left Masseter

SUBJECT 1

SUBJECT 2

SUBJECT 3

CAN. J. PHYSIBPL. PHARMACOL. VBPL. 69, 1991

k MASS PdP

. . . .. .. .. .. . . . . . . . . . . . ............................... ........................... .................... *

'

*

S

R MASS NP

. . . . . . . . . . . . . .. .. .. .. ..

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.

#

.

.

a

.

s

.

.

.

.

.

.

I

.

.

0

L MASS P

R MASS P

FIG.2. Root-mean-squarevoltage traces of surface EMG records s f the left (L mass) and right (W mass) masseter and suprahysid musculature obtained during slow, time-controlled empty mandibular open-close movements in the presence (P) and absence (NP) s f experimental pain. During this task, peak agonistic activities represent approximately 30-40% of the maximum myselectric output produced by these muscles in the absence of pain. Note the altered bursts s f the jaw closers in the presence of pain.

et al. 1988). At Beast part of the restriction in motion appears to be due to an abnormal persistence of activity in the paraspinal muscles in CLBP patients. In control subjects, the extensors of the spine are active during the first half of flexion, but inactive at the more acute angles. In the patients, the paraspinal muscles do not relax (Floyd and Silver 1955; Triano and Schultz 1987; Ahern et al, 1988). Triano and Schultz also reported that antagonist muscles are abnormally active during rotation of the trunk in CLBP. They made the important observation that the persistence of paraspinal EMG activity in the patient group is not due to an inability to flex past the angle at which relaxation normally occurs. (c) Postexercise muscle pain One of the effects of eccentric exercise reported by Jones et d.(1987) was that bursts of activity occurred in the painful biceps during extension. On the other hand, Howell et al. (1985) reported that mean biceps activity was less in active movement of extension during PEMS than in the control condition. Although this may be true, in these experiments the velocity was uncontrolled and the extension range was defined relative to the postural position, but this changes in PEMS (see section on Postexercise muscle soreness). This makes the data difficult to interpret. (4 Conchsiopl~ We conclude that, in general? chronic pain reduces the output of muscles when they act as agonists and increases the output when they became antagonists. Summaries of the data are given in Tables 2 and 3.

Experimental pain Our conclusions on the interrelationship of movement, EMG activity, and muscle pain have been tested in an experimental model by one of us (C.S.S.) and his csllaborators. Motor function at rest and during open-close movements of

the mandible at a controlled rate was studied in normal subjects before, during, and after pain. In addition, resting EMG activity was recorded while the subjects remembered a previous painful experience (sham pain). Experimental muscle pain was induced by the injection of 5% saline into the M y of the left masseter muscle through an implanted catheter (Stohler and Ashton-Miller 1989). Following the first injection of 0.1 mL, the intensity of the pain rose-to an average-of 5.5 on a visual-analog scale with endpoints labeled "no pain" and "pain as bad as it could be." Repeated injections of very small amounts of hypertonic saline were then begun so as to mainbin a constant pain level. Myoelectric activity was mapped with surface electrodes placed over the masseter, temporalis, and facial muscles on both sides of the head, and needle electrodes were inserted in some subjects near the site of infusion. The protocol was approved by an institutional ethics committee. Subjects were told to expect pain and informed that they could stop the experiment at any time. The preliminary data support the following conclusions. (a) Muscle pain was not a direct cause of increased postural activity of the jaw-closing muscles. Mean surface EMG activity was not significantly increased during pain in most subjects. In a few others, similar increases occurred during pain and during sham pain (Fig, 1). (b) Surface EMG activity recorded over the frondis region sometimes increased during pain and sham pain, but this was coincident with a change in facial expression. (c) The velocity and amplitude of the repetitive opening movements decreased during pain. ( d ) The area of the right and left masseter bursts was reduced during jaw closure in the presence of pain (Fig. 2). (e) Some masseter motor units that were silent during jaw opening in the control periods became active during pain, while others increased their firing rate. This result is illustrated in Fig. 3, in which the subject opened maximdally.

EUND ET AL.

ANTAGONISTIC CO-CONTRACTION PRESENT PAIN INTENSIV: 5

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1 st second of keeping jaw open rneximaily

TlME (2000 dotopoints = 1 s )

ANTAGONISTIC CO-CONTRACTION *

PAIN INTENSITY: 5 MIN AFTER I s t second sf keeping jaw open maximally

8

SURFACE-WMS

6 4

2 0

NEEDLE E M 6

2 4

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TlME (2000 datapoints = 1 s) FIG. 3. Recordings s f vertical jaw displacement, surface) and concentric needle EMG of the masseter during the task sf keeping the muth open maximally in the. presence (Fig. 3A) and absence (Fig. 3B) of pain. N ~ t ethe reduction of mouth opening associated with the increased firing pattern of motor units in the presence of pain. RMS, root-mean-square myoelwtric activity.

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The pain-adaptation model On the basis of the preceding analysis of the clinical literature and the new data from the chronic muscle pain model, we conclude that chronic pain seems t s be associated with a general alteration in behaviour, one manifestation of which can be a change in facial expression. In addition, muscle activity in md around the site of the pain is altered during issmetric contractions or movements, but there is no systematic increase in p s t u r d activity or during movement, as predicted by the vicious cycle model. The data suggest that there is a decrease in motoneuron output when the muscle is acting as an agonist and an increase in output when it acts as an antagonist. This leads to a reduction in MVC, and in the range and velocity of movement. We have already argued that these adaptations are designed to protect the injured part, and that they can be explained by a simple model based on smalldiameter muscle afferents, interneurons, and a-motoneurons (Lund et d. 1989). The reasons for excluding other neurond elements are given in the original paper. Sensory agerents Like dmost d l tissues, muscles are innervated by large numbers of small myelinated (group 111 or A6) and unmyelinated (group IV or group C) sensory afferent fibers (Stacey 1969). From the time of the first reports of the physiological properties of their receptors, both groups have been linked to muscle pain because they are excited by heavy pressure, hypertonic saline injections, and by muscle contraction during ischemia (Paintd 1968; Iggo 1961; Bessou and Laporte 1961; Mense 1991). Many of these afferents respond when endogenous dgesic chemicals are injected into the muscle or into its blood supply (see Mense 1991). Kinins and other products of inflammation sensitize some of the receptors, which causes them to begin to fire during muscle contraction (Berberich et al. 1985; Mense a d Meyer 1985, 1988; Mense 1991). Fine articular receptors also respond to the injections of kinins (Kanaka et al. 1985; Sessle and Hu 1991), and like muscle afferents, their mechanosensitivity increases after injury (Schaible and Schmidt 1985; Guilbaud 1991; Sessle and Hu 1991). a-Motoneurons Electrical stimulation of fine afferents from joints, sagin and muscles of the limbs usually causes a flexion reflex (Lloyd 1943; Brock et d. 1951; Hunt 1954). In line with this, most flexor mtoneurons are depolarized and most extensor motoneurons are hyperpolarized by electrical stimulation of smalldiameter muscle afferents, dthough some extensor motoneurons give a mixed response (Kniffki et al 1981) . Inhsion of bradykinin into the gastrocnemius has a similar effect: most extensor motoneurons are inhibited and most flexors are excited. However, some show the reverse pattern, while others appear to receive both excitatory and inhibitory inputs (KniffE et al. 1979, 1981). Inflammation of the knee joint in anesthetized spin& cats appears to increase the responsiveness of some flexor motoneurons to manual movement of the limb, but again a small number seem to be inhibited (He et al. 1988). In the t r i g e ~ n dsystem, jaw-closing muscles like the masseters are the physiological extensors because they maintain the posture of the mandible and resist gravity. These muscles are inhibited during the jaw-opening reflex, the equivalent of the flexion reflex. As would be expected, electrical stimulation of high threshold muscle afferents is usually inhibitory to masseter motsneurons on both sides, and excitatory to jaw-opening motoneurons (Nakamura et al. 1973). However, injections of

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INHIBITK~~

flinG

AGONlST

FIG. 4. Hypothetical model to explain the changes in muscle activity caused by chronic pain. As explained in the text, fine afferents converge on cells in the spinal cord and brain stern, such as the group 11 interneurons shown. We hypothesize that the motor cornmand includes (1) facilitation of the inhibitory pathway to agonist motoneurons and excitatory pathway to the antagonist motoneurons, and (2) inhibition s f the antagonist subgroups of interneursns. The result is a reduction of the agonist motoneuron output and an increase in antagonist firing during movement.

dgesic chemicals into the tempromandibular joint have some excitatory effects on both jaw-opening and jaw-closing motoneurons @roton and Sessle 1988), but the effects on closer motoneurons appear to be weak (Sessle and Hu 1991). The evidence that we have briefly reviewed shows that although the predominant effect of stimulation of muscle nociceptors is a decrease in extensor and an increase in flexor activity, an alternative pathway exists that has opposite effects, Since none of these afferents makes monosynaptic connections with motoneurons, this implies that each motoneuron pool is supplied by both excitatory and inhibitory nociceptive interneurons.

Imtemeurons To explain the changes in motor activity that occur in the chronic pain conditions we have reviewed, we suggest that motor programs control the premotor nociceptive interneurons to agonist and antagonist motoneurons in a reciprocal way. To account for the lowering of agonist output in the presence of pain, the motor command includes excitation (or facilitation) of the inhibitory group and the inhibition (or disfacilitation) of the excitatory group supplying agonist motoneurons. The increase of antagonist muscle EMG activity is explained by facilitation of the excitatory pathway and reduction of transmission through the inhibitory interneurons (Fig. 4).

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FIG.5. An example of the firing pattern of two interneurons recorded in nucleus trigeminalis oralis 7 of the anesthetized and paralysed rabbit at the point indicated by the asterisk. There neurons were shown to project to the contralateral trigeminal motor nucleus by aratidrornic stimulation. It can be seen om the left that both the neurons (upper trace, large and small action potentials) fired rhythmically during repetitive stimulatisn (40 Hz) of the masticatory area of the sensorimotor cortex (indicated by the artifacts in the lower trace). Their rhythmical activity began during the last half of the burst of firing of the right hypoglossal nerve (W XII). When the left inferior alveolar nerve was stimulatedt the threshold of the spikes was 2.3 (small) and 5 . 4 (large) times that of the incoming volley (R. k n g a and J. P. Eund, unpublished observations). Abbreviations from Meessen and Olsaewski (1949).

In the spinal cord, the most obvious candidates for inclusion in the model are group HI intemeurons, dthsugh the participation of other dorsal horn neurons that receive similar inputs (see Mense 1991; Guilbaud 1991; SessHe and Hu 199%)is probable. Group H I interneurons are excited by many of the inputs that evoke the flexion reflex, including group III fibers from muscle (Fedina and Hultbrn 1972; Kniffki et d. 1981 ; Lundberg et d. 198'7). In the brain stem, neurons that receive a similar mix of inputs have been implicated in the control of trigeminal motoneurons. Some of the neurons in parts of the rostra1 trigemlnd nuclei and adjacent reticular areas that project to the Vth motor nucleus are excited by small cutaneous, joint, and muscle afferents (Kidokoro et al. 1968; Nakamura et al. 1973; Eandgren and Olsson 1976; Olsson et d. 1986 and Eandgren et d - 1986; Appenteng et al. 1990; Donga et al. 1998 Sessle and Hu 199%). Litde is known about the effect of movement on the behaviour of spinal interneurons with high-threshold inputs, apart from the fact that some group I1 interneurons are inhibited during "fictive" locomotion (rhythmic activity of limb motoneurons in paralysed animals) evoked by systemic injections of L-DOPA (Edgley et d. 1988). There Is more information concerning the modulation of high-threshold trigeminal interneurons. First of d l , Olsson et al. (1986) reported that %he excitability of a group of neurons with high-threshold inputs recorded close to the Vth motor nucleus was strongly modulated in phase with the masticatory cycle. Most of them were excitable during the jaw-closer muscle burst, but some others were least active at this time. More recently, the properties of last-order intemeurons that project to the contralateral Vth motor nucleus have been described (Donga et al. 1990; Donga and Lund 1990). The finding of most relevance to this review is that the firing of many of these interneurons changes during fictive mastication. Although most of the interneurons had low threshold mechanoreceptive fields, a smdB number could only be excited by heavy pressure or by electrical stimulation of

afferent nerves at intensities well a b v e that of the lowest threshold afferents. The discharge patterns of two interneurons that projected to contralateral closer motoneuron pools are shown in Fig. 5. Both (one with the large and one with the smdl action potential) discharge at the end of the bursts In the XIIth nerve. No mechanoreceptive field was found for either neuron, but both were excited by stimulation of the inferior alveolar nerve at 2.3 (small) and 5.4 (large) times the threshold of the incoming volley. The Batter was classified as receiving a high threshold (probably group HIE) input. This suggests that noxious inputs from the teeth or lower lip would enhance the activity of these neurons. However, we do not know yet if interneurons like these receive convergent joint and muscle afferents.

Conclusions Our review of the descriptions of the changes in motor output that take place in chronic muscle pain conditions has convinced us that the "vicious cycle" model and other similar models based on the principle of pain and hyperactivity reinforcing one another are incorrect. There is evidence that pain does not cause muscles to become tonically hyperactive; the ability to contract them forcefully is reduced, not increased by pain. The only situation in which EMG activity appears to be higher than normal in the presence of chronic pain occurs when a muscle acts as an antagonist. Although the proponents of hyperactivity as the cause of pain could take this finding as evidence for the vicious cycle hypothesis, we argue that this reflex adaptation that limits the range and velocity is a asxf%nl of motion and that probably reduces further injury and pain. The model that we propose explains why pain arising from joints, teeth, and other nonmusculaa tissues can sometimes cause the same signs of dyshnction as muscle pain, because the interneurons receive convergent excitatory inputs from different tissues.

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For at least 40 years, it has been thought h a t many forms of chronic musculoskeletal pain were due to abnormal patterns of muscular activity, and research was usually limited to attempts to confirm various reiterations of the hyperactivity causality model. We believe that this approach will not lead to

investigations on the afferent fibres from muscle nerves. Proc. R. Soc. London B, 138: 453 -475. B R ~ NJ. ,G., and sass^^, B. J. 1988. Reflex excitation of masticatory muscles induced by algesic chemicals applied to the temporomandibular joint of the cat. Arch Oral. Biol. 33: 741 -747. B ~ S Y N S KT* I , H., S ~ Y V A J. ,M., ADLER,C. S., and MULLANEY, an understanding of the etiology of these conditions, nor even D J. 1973. EM43 biofeedback and tension headache: a controlled to descriptions of the pathology that causes the pain. New outcome study. Semin. Psychiatry, 5: 397 -4 10. approaches, such as those used by some of the other contribuCARISON,K. E., AUTDN, W., and FIELDMAN, J. 1964. Electrotors to this symposium (see papers by Basbaurn and leevine rnyographic study of aging in skeletal muscle. Am. J. Phys. Med. 1991; Hendriksson and Bengtsson 1991) must be tried before 43: 141-145. CHAPMAN, S. L. 1986. 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