Elsevier

Brain Research

Volume 813, Issue 2, 7 December 1998, Pages 359-366
Brain Research

Research report
Inhibitory effects of electrical stimulation of ventrolateral orbital cortex on the rat jaw-opening reflex

https://doi.org/10.1016/S0006-8993(98)01050-6Get rights and content

Abstract

In previous studies, we have shown that electrically or chemically evoked activation of the ventrolateral orbital cortex (VLO) depresses the rat tail-flick (TF) reflex, and this antinociceptive effect is mediated by the periaqueductal gray (PAG). The aim of the present study was to examine whether electrical stimulation of the VLO could inhibit the rat jaw-opening reflex (JOR), and to determine whether electrolytic lesions of the PAG could attenuate this VLO-evoked inhibition. Unilateral electrical stimulation of the VLO significantly depressed the JOR elicited by tooth pulp or facial skin stimuli, with a mean threshold of 30.5±2.3 μA (n=22). Increasing stimulation intensities from 30 to 80 μA resulted in greater reduction of the dEMG amplitude from 22.9±5.0% to 69.7±3.7% of the baseline value (P<0.01, n=22). The inhibitory effect appeared 50 ms after the beginning of VLO stimulation and lasted about 150 ms, as determined by varying the conditioning-test (C-T) time interval. Unilateral lateral or ventrolateral lesions of the PAG produced only a small attenuation of the VLO-evoked inhibition of the JOR, but bilateral lesions eliminated this inhibition. These findings suggest that the VLO plays an important role in modulation of orofacial nociceptive inputs, and provide further support for the hypothesis that the antinociceptive effect of VLO is mediated by PAG leading to activation of a brainstem descending inhibitory system and depression of nociceptive inputs at the trigeminal level. The role played by VLO in pain modulation is discussed in association with the proposed endogenous analgesic system consisting of medullary cord–Sm–VLO–PAG–medullary cord.

Introduction

Anatomical studies have established that in the rat and the cat the ventrolateral orbital cortex (VLO) receives major projections from the thalamic nucleus submedius (Sm) 8, 11, 29, 40and projects to the somatosensory cortex 10, 11. The Sm receives direct projections from the trigeminal subnucleus caudalis and the spinal cord dorsal horn 3, 10, 13, 29, 39. Electrophysiological studies 1, 17, 35have demonstrated that in rats most of the neurons in VLO respond to peripheral noxious stimuli and have very large and bilateral receptive fields. The VLO neurons activated by peripheral noxious stimulation also are frequently activated by electrical stimulation of the Sm. Since the Sm has been demonstrated to be involved in nociception 12, 15, 27, 31, 36, 37, the VLO may also be involved in nociception and related more closely to the affective-motivational aspects of pain. This hypothesis is supported by some studies on the prefrontal cortex in animals and human beings 16, 20, 33.

However, it is interesting that in the rat and cat the VLO projects bilaterally to the lateral or ventrolateral parts of the periaqueductal gray matter (PAG) 11, 21, 22, a region that has been implicated repeatedly in descending modulation of nociception 2, 19, 34. One study demonstrated that bilateral anesthetization of the ventrolateral parts of the prefrontal cortex lowered the threshold of the jump response elicited by footshock [9]. In one of our recent studies [42], it was found that electrolytic lesions of the VLO or PAG resulted in abolition of the inhibitory effects elicited by stimulation of the Sm on the rat tail-flick (TF) reflex, suggesting that the antinociception produced by Sm stimulation is mediated through a loop via VLO toward PAG, leading to activation of a brainstem descending inhibitory system and depression of the nociceptive inputs at the spinal level. Therefore, it is reasonable to suppose that the VLO may also be involved in nociceptive modulation. This suggestion has been supported by recent experiments in our laboratory that electrically or chemically evoked activation of the VLO significantly suppresses the rat tail-flick (TF) reflex, and this antinociceptive effect is blocked by electrolytic lesions of the PAG [45]or microinjection of GABA into PAG [41]. The aim of this study is to examine whether electrical stimulation of VLO could depress the rat jaw-opening reflex (JOR) elicited by tooth pulp or facial skin stimulation, and to determine whether this inhibitory effect could be eliminated or reduced by electrolytic lesions of the PAG in order to establish whether the VLO is involved in descending modulation of orofacial nociceptive inputs.

Section snippets

Animal preparation

Experiments were conducted on 33 adult Sprague–Dawley rats weighing between 220 and 370 g of either sex. Each rat was initially anesthetized with sodium pentobarbital (50 mg kg−1, i.p.) for surgery. After cannulation of the trachea and left jugular vein, a pair of Teflon-coated stainless wires (diameter 0.1 mm, exposed tip 2 mm) were inserted into the right anterior digastric muscle for recording the digastric electromyogram (dEMG) response. The right mandibular incisor was cut off to expose

Features of the JOR

The features of the JOR associated with the dEMG which was elicited by stimulation of the tooth pulp or the facial skin have been described in detail in another report (Zhang et al., unpublished). In brief, the mean thresholds (T) and the response latencies for eliciting the dEMG by incisor tooth pulp and face skin stimuli were 0.6±0.1 and 0.9±0.1 mA, and 7.8±0.2 and 6.5±0.7 ms, respectively. The dEMG increased linearly in amplitude with increasing intensities of test stimulation delivered to

VLO modulation of orofacial nociceptive input

Results of the present study demonstrated that unilateral VLO electrical stimulation in rats under light pentobarbital anesthesia significantly inhibits the JOR elicited by tooth pulp or facial skin stimulations, and this inhibitory effect had a time-course of about 150 ms. The results of the present study are consistent with those reported recently by our research group in which electrically or chemically evoked-activation of the VLO inhibited the radiant-heat-evoked rat tail-flick (TF) reflex

Acknowledgements

The authors wish to thank Professor J.O. Dostrovsky for his help in reviewing an earlier version of this manuscript. The project was supported by the National Natural Science Foundation of China, No. 39470870.

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