Effects of chemical stimulation of masseter muscle nociceptors on trigeminal motoneuron and interneuron activities during fictive mastication in the rabbit

Abstract

An electrophysiological study was carried out in sixteen decerebrate and paralyzed New Zealand rabbits to determine how a bolus injection of a nociceptor stimulant (hypertonic saline, 5%) into the masseter muscle influences the activity of the trigeminal motor circuitry during fictive jaw movements. Hypodermic needles connected to a syringe held in a computer-controlled infusion pump were inserted into the anterior deep layer of either the right or the left masseter. Twenty-three infusions of 50, 70 or 80 microl saline were made in fourteen animals at constant rates over 1 min. Eight control infusions of normal saline (0.9%) were made in a subpopulation of five animals in an identical manner. Fictive jaw movements were evoked before and after the infusions by repetitive electrical stimulation of the corticobulbar tract. Effects were assessed by extracellular microelectrode recordings made from the digastric motoneuron pool and from putative last-order interneurons in the oral subnucleus of the spinal trigeminal tract and adjacent structures. In comparison with pre-infusion control cycles, nociceptor stimulation caused significant slowing of the rhythm and a reduction of the area of the digastric motoneuron bursts in the majority of the animals (12/14). The decrease in cycle frequency was due almost entirely to a lengthening of the time between the digastric bursts. Changes usually began 1-2 min after the infusion and returned to pre-infusion values within 10-15 min. No significant effects were seen when isotonic saline was applied. Recordings were obtained from nine interneurons, eight of which had low threshold mechanosensitive receptive fields. One neuron was, in addition, excited by pinch. Eight were not active in the absence of motor activity and this did not change when hypertonic saline was applied. However, once fictive movements began, all started to fire rhythmic bursts of spikes. In five cases, there was a significant post-infusion increase in spike frequency, and three showed decreases. Seven showed significant post-infusion changes in mean phase and/or concentration of their firing within the movement cycle. Changes in the preferred phase of interneuronal firing were significantly correlated to changes in the phase of offset of the digastric burst. The present results provide evidence that the stimulation of nociceptors in a muscle slows the frequency of rhythmical movements in the absence of sensory feedback. They confirm that infusions into one muscle affect the output of its antagonist. The results also suggest that neurons in the oral subnucleus of the spinal trigeminal tract and adjacent reticular formation appear to participate in programming these changes in motor output.

Craniofacial Pain and Motor Function: Pathogenesis, Clinical Correlates, and Implications

“…In decerebrate rabbits, heavy pressure on the periosteum of the zygoma reduces the frequency, amplitude, and mandibular velocities in mastication evoked by the electrical stimulation of the corticobulbar tract . A similar response was observed with the same experimental paradigm used during the infusion of hypertonic saline into the masseter muscle at rates that have been shown to cause pain in humans (Westberg et al, 1997). For noxious input arising in parts other than the craniofacial complex, the corresponding mechanisms are assumed to occur at the level of the spinal cord.…”

“…Because the frequency of fictive masticatory movements in the decerebrate rabbit is reduced during noxious stimulation Westberg et al, 1997), projection of nociceptive input on neurons located in the midline of the reticular formation is assumed, since this area has been shown to be critical to the generation of the masticatory rhythm (Nozaki et al, 1986). Neurons in the rostral trigeminal nuclei and adjacent reticular formation that integrate the rhythmic command, sensory input, and input from higher centers shape the bursts of the motoneuron.…”

“…Neurons in the rostral trigeminal nuclei and adjacent reticular formation that integrate the rhythmic command, sensory input, and input from higher centers shape the bursts of the motoneuron. Some of these neurons change their firing pattern when hypertonic saline is infused into the masseter muscle (Westberg et al, 1995b(Westberg et al, , 1997.…”

The influence of experimental muscle pain on motor unit activity during low-level contraction

“…Furthermore, during the abovementioned studies the mechanical conditions varied, and were actually a dependent variable. Although it has been documented in animal studies that the pain-induced inhibition most likely occurs at the segmental level (Westberg et al 1997), studies in humans cannot rule out that modulation of muscle activity is due to``pain behavior'', governed from supraspinal levels.…”

Input–output organization of jaw movement‐related areas in monkey frontal cortex

“…It has been reported that the medial parabrachial nucleus and the nucleus of Kölliker-Fuse are involved in nociceptive as well as visceral (or gustatory) functions (Beckstead et al, 1980;Feil and Herbert, 1995;Pritchard et al, 2000). Thus, CMaAd-induced RJMs may be modified by activation of peripheral nociceptors, as Schwartz and Lund (1995) and Westberg et al (1997) have demonstrated that tonic stimulation of nociceptors in the periosteum of the zygoma or the masseter muscle decreases the frequency, velocity, and amplitude of jaw movements induced by repetitive cortical stimulation. It should also be mentioned here that the medial parabrachial nucleus and the nucleus of Kölliker-Fuse receive somatosensory information via the principal sensory trigeminal nucleus and the oral subnucleus of the spinal trigeminal nucleus (Yoshida et al, 1994(Yoshida et al, , 2001Feil and Herbert, 1995), while the supraV receives inputs from jaw muscle spindle afferents or periodontal ligament afferents with cell bodies in the mesencephalic trigeminal nucleus (Shigenaga et al, 1989(Shigenaga et al, , 1990Kishimoto et al, 1998;Yoshida et al, 1999;Luo et al, 2001).…”