Excitatory actions of experimental muscle pain on early and late components of human jaw stretch reflexes
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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2011, PainCitation Excerpt :This includes presynaptic inhibition of the 1a afferent terminal [73], amongst other problems. The stretch reflex, which depends on various factors including motoneuron excitability, spindle sensitivity, gamma motoneuron drive to the intrafusal muscle fibres, and presynaptic effects on the Ia afferent synapse, increases [87,100,101] or decreases [4,88] in pain. The response of a muscle to electrical stimulation of the descending corticospinal axons at the cervicomedullary junction has been studied [21,55].
Effect of experimental pain on EMG-activity in human jaw-closing muscles in different jaw positions
2009, Archives of Oral BiologyCitation Excerpt :It is also likely that stretch of the jaw-closers during jaw-opening would activate muscle spindle afferents. We have provided evidence that experimental muscle pain has an excitatory effect on the jaw-stretch reflex28,47–50 and this could contribute to the observed increase in EMG activity in the jaw-closing muscles during half-maximal jaw-opening. When the subjects kept their jaw in the maximal opening position, there was less EMG activity in the jaw-closing muscles during infusion of HS than before and after the infusion (Fig. 2C).
Effects of noxious stimulation of orofacial tissues on rat licking behaviour
2008, Archives of Oral BiologyCitation Excerpt :Only limited information is available on the effects of pain on motor output, despite the fact that musculoskeletal structures represent the most common site of pain in humans.1–3 Deep craniofacial structures such as the masseter muscle and temporomandibular joint (TMJ) represent very common sites for acute and chronic pain,4–6 and clinical and experimental observations suggest that jaw motor output can be impaired in humans and animals experiencing orofacial muscle pain (e.g.7–12). For example, orofacial pain can have significant effects on masseter motor behaviour in awake rats, since injection of Complete Freund's Adjuvant (CFA) into the masseter muscle produces a significant reduction in peak force of biting,9 findings that are supported by clinical studies documenting a decrease in bite force in patients with TMJ or jaw muscle pain.7,10,13,14
Effect of pinching-evoked pain on jaw-stretch reflexes and exteroceptive suppression periods in healthy subjects
2007, Clinical NeurophysiologyCitation Excerpt :The rationale for such studies has been that experimental pain might provide a better insight into the interpretation of observations in patients with different craniofacial pain conditions. Studies on the modulation of the jaw-stretch reflex induced by experimental jaw-muscle pain have consistently reported a facilitation of the reflex responses (Wang et al., 2000, 2001, 2002, 2004a; Svensson et al., 2000, 2001; Peddireddy et al., 2005). A facilitation of the stretch reflex has also been observed in other muscles, e.g., the anterior tibialis muscle (Matre et al., 1998, 1999), suggesting that the net effect of deep nociceptive inputs is an increase in sensitivity of the fusimotor system.
Influence of jaw gape on EMG of jaw muscles and jaw-stretch reflexes
2007, Archives of Oral Biology