Excitatory actions of experimental muscle pain on early and late components of human jaw stretch reflexes

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Abstract

It has recently been shown that a slow stretch evokes a short-latency (probably monosynaptic) and a long-latency (polysynaptic) reflex response in human jaw-closing muscles. The effect of nociceptive muscle input on the fusimotor system has not been investigated in detail. In order to investigate the effect of sustained muscle pain on the jaw stretch reflex, two main experiments were performed. Stretch reflex responses were evoked in the masseter and temporalis muscles by slow stretches (1-mm displacement, 40-ms ramp time) before, during and 15 min after a period of experimentally induced muscle pain. In experiment I, a dose of 1.0 M hypertonic or 154 mM isotonic (control) saline was infused in random order into the left masseter for up to 15 min (n=12). The level of excitation of the left masseter at 15% maximal voluntary contraction was controlled by visual feedback of the surface EMG (sEMG). In experiment II, a dose of 1.0 M saline was infused into the left masseter but with feedback from the sEMG of the right masseter (n=12). In a control experiment, both sEMG and intramuscular EMG (imEMG) were recorded from the left and right masseters; the feedback was from imEMG of the left masseter (n=12). The early (onset: 9–10 ms) and late (duration from 25 to 40 ms) reflex components were recorded and analysed in all experiments. Infusion of 1.0 M saline caused moderate pain (mean score on a Visual Analogue Pain Scale: 4.9–5.0 cm). The peak-to-peak amplitude of the early reflex component in the painful masseter normalized to the pre-stimulus EMG activity was significantly higher during the pain than the pre- and post-infusion conditions in all experiments. The normalized area of the late reflex component in the painful masseter was significantly larger than in the pre-infusion condition in all experiments. Isotonic saline had no significant effect on the jaw stretch reflexes. These results indicate that experimental jaw-muscle pain in humans facilitates the early as well as the late component of the jaw stretch reflex response as revealed by both sEMG and imEMG. This effect appears to be independent of the level of excitation of the muscle and not related to volume effects of the injected saline. A change in the sensitivity of the fusimotor system during muscle pain is suggested as an explanation.

Introduction

Jaw stretch reflexes are thought to work as postural reflexes, helping to maintain a stable position of the mandible (Cooker et al., 1980). They may also play an important part in the integration and coordination of jaw movement during chewing, breaking down and swallowing food, and in avoiding tissue damage (Miles et al., 1995). Recently, in contrast to earlier studies claiming that the jaw-closing muscles lack a long-latency stretch reflex response, Poliakov and Miles (1994) showed that slow stretches (15 mm/s) of the mandible can elicit both short-latency (early component), probably monosynaptic, excitatory responses and long-latency (late component), polysynaptic excitatory responses in the masseter surface EMG. The majority of tonically active masseter motor units were excited in both the short- and long-latency phases of the reflex responses evoked by a slow stretch (63 mm/s) (Miles et al., 1995, Miles, 1999). The late component of the stretch reflex is generally believed to have greater functional significance in the coordinated response to a muscle stretch (Gielen et al., 1988). The neural circuit of the short-latency jaw stretch reflex has been described (for reviews, see Dubner et al., 1978, Ongerboer de Visser, 1983), but the pathway of the long-latency response in the masseter is still unclear (Miles et al., 1995).

The functional influence of pain on the jaw stretch reflex remains unclear (De Laat et al., 1998). Some studies have described significant asymmetries in its latency and amplitude in patients with temporomandibular disorders (Murray and Klineberg, 1984, Buchner et al., 1989, Cruccu et al., 1997); others have revealed no differences between patients with temporomandibular joint disorders and controls (Lobbezoo et al., 1993a, Lobbezoo et al., 1996). This discrepancy could partly be due to differences in the techniques used to evoke a reflex response as well as differences in the clinical populations of patients with these joint disorders.

There is also conflicting evidence from animal studies. Some suggest that activation of group III and IV muscle afferents by electrical or chemical stimulation leads to increased fusimotor firing and increased sensitivity of the Ia muscle spindle afferents to stretching (Appelberg et al., 1983, Johansson et al., 1993, Pedersen et al., 1997, Hellström et al., 1999). In contrast, Mense and Skeppar (1991) demonstrated significant inhibition of extensor γ-motoneurones by inflammatory muscle pain. Again, differences in method and in muscle function make it difficult to interpret the effects of nociceptive inputs on the stretch reflex.

Human experimental pain studies on the stretch reflexes have provided equivocal results. Matre et al., 1998, Matre et al., 1999 demonstrated a facilitated stretch reflex in the soleus and tibialis muscles when hypertonic saline was infused into them. Zedka et al. (1999) report that infusion of hypertonic saline into the erector spinae muscles inhibited their voluntary activation but left the mono- and polysynaptic stretch reflex unchanged. Recently, Wang et al. (2000) found that sustained pain in jaw muscles facilitated the short-latency jaw stretch reflex evoked by fast stretching (10-ms ramp time) as revealed by both intramuscular and surface EMG. As it is difficult to show the late component of the reflex by a fast stretch, the slow stretch was suggested as a way of investigating the late component (Poliakov and Miles, 1994). No studies have so far examined the influence of pain on the late component of the jaw stretch reflexes.

Thus, our aim now was to investigate the effects of experimental muscle pain on both the early and late component of the human reflex responses evoked by a slow jaw stretch under standardized conditions.

Section snippets

Participants

The volunteers for this study were all healthy and unmedicated, without signs or symptoms of temporomandibular joint disorder (Dworkin and LeResche, 1992). Eleven men and one woman (mean age±SEM: 25.9±0.8 years) participated in experiment I, ten men and two women (25.8±0.7 years) in experiment II, and 11 men and one woman (25.4±1.2 years) in the control experiment. Seven individuals participated in more than one experiment and one participated in all the experiments. The three experiments were

Experimental muscle pain

In experiment I, an average of 2.04±0.04 ml hypertonic saline was infused into the left masseter over 15 min. The mean pain score during the EMG recordings was 4.9±0.3 cm. All participants reported no pain (Visual Analogue Scale=0) 5–10 min after stopping the infusion, but slight soreness usually persisted during the post-infusion recordings. Infusion of a similar amount of isotonic saline caused no or very little pain; the mean score on the Visual Analogue Scale was 0.3±0.1 cm.

In experiment

Discussion

The main finding was the facilitation of the early and late component of the jaw stretch reflex during sustained experimental muscle pain when the excitation level of the muscle was taken into account. The muscle pain had significant effects on the pre-stimulus EMG activity in uncontrolled muscles, depending on the specific clenching tasks.

Acknowledgements

This study was supported by the Danish National Research Foundation and the Danish Dental Association. The participation of the volunteers is greatly appreciated.

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