Role of the vestibular nuclear complex in facilitating the jaw-opening reflex following stimulation of the red nucleus

doi:10.1016/j.neures.2016.02.008

Neuroscience Research

Volume 110, September 2016, Pages 29-36

https://doi.org/10.1016/j.neures.2016.02.008 Get rights and content

Highlights

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Stimulation of the red nucleus (RN) facilitated the jaw-opening reflex (JOR).
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Vestibular nuclear complex (VN) lesion reduced or increased RN-induced facilitation.
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Muscimol injection into the VN also reduced or increased RN-induced facilitation.
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RN-induced facilitation of the JOR is mediated partly by a relay in the VN.

Abstract

According to our previous studies, stimulation of the red nucleus (RN) facilitates the low-threshold afferent-evoked jaw-opening reflex (L-JOR). It has been reported that the RN projects to the superior (SVN), lateral (LVN) and inferior vestibular (IVN) nuclei. The SVN and the LVN have reciprocal intrinsic connections with the medial vestibular nucleus (MVN). Our previous study demonstrated that stimulation of the vestibular nuclear complex (VN) modulates the L-JOR. These facts suggest that RN-induced facilitation of the L-JOR is mediated via the VN. In the present work we investigated whether electrically induced lesions of the VN, or microinjection of muscimol into the VN, affects RN-induced facilitation of the L-JOR. The L-JOR was evoked by electrical stimulation of the inferior alveolar nerve. The stimulus intensity was 1.2 times the evocation threshold. Lesions of the MVN or the LVN or the SVN, and the muscimol injection into the MVN or the LVN or the SVN, reduced the RN-induced facilitation of the L-JOR. Conversely, lesions of the IVN, and the muscimol injection into the IVN, increased the RN-induced facilitation of the L-JOR. These results suggest that the RN-induced facilitation of the L-JOR is mediated by a relay in the VN.

Introduction

The jaw-opening reflex is evoked by innocuous and by noxious stimulation of the orofacial region, via one or more interneurons (Kidokoro et al., 1968, Sumino, 1971, Thexton, 1973). The jaw-opening reflex can be evoked by electrical stimulation of either the low- or high-threshold afferents of the trigeminal nerve. The low-threshold afferent-evoked jaw-opening reflex (L-JOR) is believed to be evoked by innocuous stimulation, and the high-threshold afferent-evoked jaw-opening reflex by noxious stimulation (Lund and Olsson, 1983, Lund et al., 1984).

In our previous papers we reported that stimulation of the red nucleus (RN) facilitates the L-JOR (Satoh et al., 2003, Satoh et al., 2013). The effect is probably mediated by an indirect pathway, since there is little evidence for direct projections from the RN to the ventromedial division of the trigeminal motor nucleus (jaw-opening motoneuron pool) (Edwards, 1972, Godefroy et al., 1988, Travers and Norgen, 1983, Yasui et al., 2001). It is possible that an interneuronal link in this pathway is located within the vestibular nuclear complex (VN). The VN consists of four major nuclei: the medial (MVN), lateral (LVN), superior (SVN) and inferior vestibular (IVN) nuclei. Cytoarchitecturally, the MVN is divided into two parts: the parvicellular part (MVNPC) and the magnocellular part (MVNMC) (Paxinos and Watson, 2007). The hypothesis has been made that the RN projects to the bilateral LVN, to the contralateral SVN (Godefroy et al., 1988) and to the contralateral IVN (Edwards, 1972). The SVN has strong reciprocal intrinsic connections with the MVN and the IVN. The LVN is reciprocally related to the MVN and receives inputs from the IVN. These intrinsic connections between individual nuclei suggest an integrative function within the VN (Rubertone et al., 1983). Our previous study demonstrated that stimulation of the LVN, the SVN, the MVNPC and the MVNMC facilitates the L-JOR, and that stimulation of the IVN suppresses the L-JOR (Satoh et al., 2009). Furthermore, antidromic action potentials in the LVN neurons were evoked by electrical stimulation of the RN (Sarkisian and Fanardijian, 1992). Guided by these observations, we test herein our hypothesis that RN-induced facilitation of the L-JOR is mediated via the VN, by examining whether: (1) RN-induced facilitation of the L-JOR is affected by electrically created lesions in the bilateral VN and (2) whether RN-induced facilitation of the L-JOR is affected by microinjection of muscimol into the same areas. The present study aims to determine whether the facilitatory effects of RN stimulation on the L-JOR are mediated by the VN.

Section snippets

Materials and methods

Our experiments were performed on 62 male Sprague-Dawley rats, weighing 290–416 g. All animal procedures were carried out in accordance with the National Institute of Health Guide for the Care and Use of Laboratory Animals, and were approved by the Laboratory Animal Committee of The Nippon Dental University School of Life Dentistry at Niigata (approval number 146).

The rats were initially anesthetized with urethane and α-chloralose (500 mg/kg and 50 mg/kg, respectively; i.p.). Supplemental doses of

Results

The threshold intensity for eliciting the L-JOR by stimulating the IAN was 21–200 μA (77.1 ± 42.6 μA, mean ± SD, n = 62). Conditioning electrical stimulation of the RN facilitated the L-JOR to an extent that was statistically significant (Wilcoxon t-test, P < 0.05); see Fig. 1A. The facilitated L-JOR was 233.4 ± 13.0% (mean ± SE, n = 62) of the control level. Latency of the control L-JOR evoked by the IAN on the side contralateral to RN stimulation (6.5 ± 0.1 ms, mean ± SE, n = 62) decreased significantly when

Discussion

We found that RN-induced facilitation of the L-JOR was reduced following the creation of lesions in the LVN, the SVN, the MVNPC and the MVNMC. In contrast, electrically induced lesions in the IVN increased the RN-induced facilitation of the L-JOR. Muscimol injection into the VN gave same results as electric lesions in the VN. Muscimol is known to be an agonist for GABA_A receptors (Andrews and Johnston, 1979). It also has the same physiological effects as GABA, increasing the conductance of