Original ArticlesSuppressive effect of vagal afferents on the activity of the trigeminal spinal neurons related to the jaw-opening reflex in rats: involvement of the endogenous opioid system
Introduction
The trigeminal spinal nucleus is an important relay station in the transmission of orofacial sensory information [51]. This nucleus is functionally and anatomically subdivided into three nuclei from rostral to caudal: oralis, interpolaris, and caudalis [13]. Among them, the nucleus oralis conveys information for nociceptive reflexes (e.g., the jaw-opening reflex) from the orofacial region, including tooth pulp 23, 46, 47.
The jaw-opening reflex (JOR) is a masticatory reflex [24], and the tooth pulp (TP)-evoked JOR as a nociceptive reflex is known to be suppressed by antinociceptive pathways mediated by the periaqueductal gray matter, the nucleus raphe magnus, or both 36, 48 as well as by analgesic drugs [12]. The TP-evoked JOR has been considered a valid model of pain if it is evoked by adequate TP stimulation (e.g., with 3–5 times the threshold of the JOR, as this threshold is very close to the sensory threshold in humans) [29]. The majority of sensory neurons in the JOR arc are located in the trigeminal spinal nucleus oralis (TSNO) [14] which projects to the trigeminal motor nucleus of the digastric muscles 31, 47.
Several lines of evidence suggest that vagal afferents play a role not only in the control of autonomic function, such as circulation and respiration, but also in the modification of nociception 38, 39. For example, electrical stimulation of vagal afferents suppresses the JOR evoked by noxious tooth-pulp stimulation at certain conditioning-test (C-T) intervals and this suppressive effect is independent of cardiovascular changes caused by vagal afferent stimulation 8, 27. Similar results of vagal modulation of the JOR in C-T manipulation have been reported 10, 11. Behavioral studies, based on a reflex effect alone have a disadvantage, however; they cannot distinguish inhibition of the sensory events from the motor response to noxious stimulus. Recently, Bossut and Maixner [9] have shown that electrical stimulation of vagal afferents inhibits the response of trigeminal neurons to noxious orofacial stimulation. To date, no studies have evaluated whether vagal afferent stimulation modifies the activities of trigeminal spinal neurons associated with TP-evoked JOR. Moreover, a study by Bossut and Maixner [9] has not investigated whether vagal afferent stimulation attenuates noxious transmission through the endogenous pain control system.
The present study was designed therefore, to test the hypothesis that via the endogenous opioid system, vagal afferent input modifies the activity of spinal trigeminal neurons related to JOR.
Section snippets
Animal preparation
The experiments were performed on 26 adult male rats (310–450 g). All experimental protocols used in this study were approved by the Animal Use and Care Committee at the Nippon Dental University. Each animal was initially anesthetized with sodium pentobarbital (45 mg/kg, i.p.) and maintained with additional doses of 2–3 mg/kg/h as required, through a cannula in the jugular vein. The trachea was cannulated. The rectal temperature was maintained at 37 ± 0.5°C with a radiant heater. Arterial blood
Changes of dEMG and TSNO neuronal activities in response to TP stimulation
Electrical stimulation of the TP-induced reflex responses in the ipsilateral anterior belly of the digastric muscle at a latency of 5.38 ± 0.44 ms (n = 26). The mean threshold intensity was 0.61 ± 0.09 mA (n = 26). As shown in Fig. 1, most of the units were located in the dorsal oralis. Thirteen units (36%, 13/36) showed spontaneous discharges at a rate of 0.2–11.0 spikes per s. During TP stimulation, they revealed a short latency (2.8–8.0 ms; mean values 4.2 ± 0.48 ms, n = 36). At a threshold
Discussion
The present series of experiments provided evidence that vagal afferent input inhibited nociceptive transmission in the TP-evoked TSNO neuronal activity related to dEMG, and that this effect could appear via the endogenous opioid system in the rat. The present findings support the idea that the neuronal network formed by the cardiovascular system and the pain-regulating system may participate in the elaboration of adaptive responses to physical and psychological stressors 9, 38, 39, 43.
In this
Acknowledgements
This study was supported by a grant-in-aid from the Ministry of Education, Science and Culture of Japan (05771529).
References (52)
- et al.
Responses of medullary raphe magnus to peripheral stimulation and to systemic opiates
Brain Res.
(1977) - et al.
Parametric analysis of the effects of cardiopulmonary vagal electrostimulation on the digastric reflex in cats
Brain Res.
(1992) - et al.
Effects of cardiac vagal afferent electrostimulation on the responses of trigeminal and trigeminothalamic neurons to noxious orofacial stimulation
Pain
(1996) - et al.
Afferent vagal modulation of brainstem somatic reflex activity
Exp. Neurol.
(1970) - et al.
The influence of vagal afferent fiber activity on the masticatory reflexes
Exp. Neurol.
(1970) - et al.
Is selective stimulation of the rat incisor tooth pulp possible?
Pain
(1983) Can endogenous systems produce pain?
Am. Physiol. Soc. J.
(1992)- et al.
Stimulus-response relation of tooth pulp unit in rat trigeminal nucleus
Brain Res. Bull.
(1985) - et al.
Evaluation of vagal afferent modulation of the digastric reflex in cats
Brain Res.
(1991) - et al.
Opioid-receptor mRNA expression in the rat CNSAnatomical and functional implications
Trends Neurosci.
(1995)