Elsevier

Brain Research Bulletin

Volume 47, Issue 1, 1 September 1998, Pages 49-56
Brain Research Bulletin

Original Articles
Suppressive 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

https://doi.org/10.1016/S0361-9230(98)00059-8Get rights and content

Abstract

The purpose of the present study is to test the hypothesis that via the endogenous pain control system, vagal afferent input modulates the activity of the trigeminal spinal nucleus oralis (TSNO) related to the tooth pulp (TP)-evoked jaw-opening reflex (JOR). Extracellular single-unit recordings were made from 36 TSNO units responding to TP electrical stimulation with a constant temporal relationship to a digastric electromyogram (dEMG) signal in 26 pentobarbital-anesthetized rats. The activity of 36 TSNO neurons and the amplitude of the dEMG increased proportionally during 1.0–3.5 times the threshold for JOR. Some of these neurons (4 out of 5) were also excited by chemical stimulation (bradykinin, 1–2 μl, 1 mM) of TP. In 31 out of 36 TSNO neurons (86%), their activities during tooth pulp stimulation were suppressed by conditioning stimulation of the right vagus nerve. The suppressive effect of vagal afferent stimulation occurred at conditioning-test intervals of 20–150 ms after the onset of the stimulation, and its maximal suppressive effect occurred at approximately 50 ms. The mean time course of this suppressive effect paralleled that of the dEMG. After administration of naloxone (0.5 and 1.0 mg/kg, i.v.), an opiate receptor blocker, the suppressive effect on the activity of TSNO neurons (6 out of 8) was significantly attenuated at the conditioning-test interval of 50 ms compared to the control (p < 0.01). These results suggested that vagal afferent input inhibits nociceptive transmission in the TSNO related to TP-evoked JOR and this inhibitory effect may occur via the endogenous opioid system in rats.

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).

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