Elsevier

Brain Research

Volume 957, Issue 1, 6 December 2002, Pages 183-191
Brain Research

Research report
Convergence of selected inputs from sensory afferents to trigeminal premotor neurons with possible projections to masseter motoneurons in the rabbit

https://doi.org/10.1016/S0006-8993(02)03662-4Get rights and content

Abstract

Peripheral input convergence on trigeminal premotor neurons in the vicinity of trigeminal motor nucleus has been investigated. Thirty neurons were identified by their antidromic responses to microstimulation of the masseteric subnucleus of trigeminal motor nucleus (NVmot-mass). Peripheral receptive fields were found in the buccal mucosae, periodontal ligaments, palate, tongue and vibrissae for 16 neurons located in the intertrigeminal area (NVint), supratrigeminal area (NVs), main sensory trigeminal nucleus (NVsnpr) and subnucleus Ī³ of the oral nucleus of the spinal trigeminal tract (NVspo-Ī³). Eleven neurons in the NVint, NVs and NVspo-Ī³ responded to passive jaw opening: nine neurons were activated and two were inhibited. None of the neurons responded to both the orofacial mechanical stimulation and passive jaw opening. Forty-six percent of neurons (13 out of 28 tested) received inputs from the inferior alveolar nerve (IAN) and 53% of neurons (8 out of 15 tested) received inputs from the infraorbital nerve (ION). Out of 15 neurons tested for inputs from the IAN and ION, 7 neurons in the NVsnpr and NVspo-Ī³ received input from both. Sixteen percent of neurons (4 out of 25) received inputs from the masseteric nerve (MassN). None of the neurons with inputs from IAN and/or ION also received inputs from the MassN. We suggest that trigeminal premotor interneurons with projections to the NVmot-mass fall into two broad categories, those with inputs from the IAN and/or ION and those with inputs from the MassN, possibly muscle spindle afferents, and no neuron receiving inputs from both.

Introduction

It is well known that a neural network for control of jaw movements is found in the brainstem. Electrophysiological studies have shown that a group of neurons responsible for generation of masticatory rhythm called masticatory central pattern generator (mCPG) is located in the medial bulbar reticular formation [33], [34]. However, it is obvious from recent studies that these circuits include more rostral nuclei surrounding the trigeminal motor nucleus (NVmot) in which the neural activity was shown to be modulated in fictive mastication [7], [15], [48]. On the other hand, it has been reported that interneurons in this area including the supratrigeminal area (NVs), intertrigeminal area (NVint), subnucleus Ī³ of the oral nucleus of the spinal trigeminal tract (NVspo-Ī³) and main sensory trigeminal nucleus (NVsnpr) project to the NVmot in electrophysiological [1], [2], [7], [36], [50] and anatomical [9], [17], [20], [21], [22], [30], [44], [52] studies. With regards to characteristics of peripheral input convergences to these neurons, most NVint, NVspo-Ī³ and NVsnpr neurons are found to have convergences from more than one peripheral afferent [35], [36], [50], [51]. Olsson and Westberg reported that input characteristics of NVspo-Ī³ premotor neurons differed from those of unselected NVspo-Ī³ neurons, in that unselected neuron groups had a wider convergence [36], [50]. They suggested that the activity of premotor neurons combined with the rhythmical drive from the mCPG might be a way to optimise the temporal ordering and the relative amplitude of the muscle activation pattern. This was also suggested by Kamogawa et al. who provided evidence that NVs neurons bilaterally projecting to the NVmot had peripheral input convergences from the inferior alveolar nerve (IAN) and infraorbital nerve (ION) [16], [17]. On these bases, it is of interest to investigate the convergence profile on and the projection of trigeminal premotor neurons to the NVmot.

The aim of this work is to identify trigeminal premotor neurons in the vicinity of the NVmot on the basis of input convergences from sensory afferents of intra-oral mechanoreceptors and jaw-closing muscle spindles. We also provide evidence in the present study that groups of interneurons located in the vicinity of the NVmot send their axons into the masseteric subnucleus of the trigeminal motor nucleus (NVmot-mass). Preliminary results have been reported in an abstract form [14].

Section snippets

Surgical procedures

The experiments were carried out on 9 adult male New Zealand white rabbits weighing between 2.0 and 4.1 kg. The animals were pre-medicated with ketamine (50 mg/kg, im). After half an hour, they were anesthetized with a mixture of urethane (0.5 g/kg) and Ī±-chloralose (50 mg/kg) administered intravenously through the marginal ear vein, supplemented with Ī±-chloralose (10 mg/kg/h, iv). Physiological saline was administered by intravenous infusion (10 ml/kg/h). Tracheal cannulation was performed and

Identification

This paper is based on recordings made from 30 neurons which were identified as trigeminal premotor neurons. Six neurons were found to project to the NVmot-mass ipsilaterally, 12 neurons contralaterally, and 6 neurons bilaterally. Although the remaining 6 neurons were identified to project contralaterally, their ipsilateral projection was not tested. Histological location of interneurons recorded in this study is summarized in Fig. 1. Eight neurons were found in the NVint, 7 in the NVs, 6 in

Discussion

Our present results provide a functional profile of premotor neurons which are located in the vicinity of the NVmot and project to the NVmot-mass. Interneurons which received inputs from the IAN and/or ION were found mainly in the NVint, NVsnpr and NVspo-Ī³ and most neurons tested received inputs from both of these nerves. Furthermore, interneurons which received input from the MassN and/or responded to passive jaw opening were found in the NVint, NVs and NVspo-Ī³. Our results indicate that those

Acknowledgements

We thank Dr. H. Crick and Dr. S. Ariyasinghe for their helpful comments on this manuscript.

References (53)

  • N. Mizuno et al.

    Commissural interneurons for masticatory motoneurons: a light and electron microscope study using the horseradish peroxidase tracer technique

    Exp. Neurol.

    (1978)
  • S. Nomura et al.

    Differential distribution of cell bodies and central axons of mesencephalic trigeminal nucleus neurons supplying the jaw-closing muscles and periodontal tissue: a transganglionic tracer study in the cat

    Brain Res.

    (1985)
  • B.J. Sessle et al.

    Jaw movement-related activity and reflexly induced changes in the lateral pterygoid muscle of the monkey Macaca fascicularis

    Arch. Oral. Biol.

    (1982)
  • Y. Shigenaga et al.

    Two types of jaw-muscle spindle afferents in the cat as demonstrated by intra-axonal staining with HRP

    Brain Res.

    (1990)
  • Y. Shigenaga et al.

    Morphology of single mesencephalic trigeminal neurons innervating masseter muscle of the cat

    Brain Res.

    (1988)
  • Y. Shigenaga et al.

    Morphology of single mesencephalic trigeminal neurons innervating periodontal ligament of the cat

    Brain Res.

    (1988)
  • Y. Shigenaga et al.

    Morphological and functional properties of trigeminal nucleus oralis neurons projecting to the trigeminal motor nucleus of the cat

    Brain Res.

    (1988)
  • M. Takata et al.

    The properties of excitatory postsynaptic potentials evoked in trigeminal motoneurons by trigeminal nerve stimulation

    Brain Res.

    (1982)
  • A. Woda et al.

    The properties of cells in the cat trigeminal main sensory and spinal subnuclei activated by mechanical stimulation of the periodontium

    Arch. Oral. Biol.

    (1983)
  • K. Appenteng et al.

    The monosynaptic excitatory connections of single to the V motor nucleus of the rat

    J. Physiol.

    (1989)
  • K. Appenteng et al.

    Morphological and electrophysiological determination of the projections of jaw-elevator muscle spindle afferents in rats

    J. Physiol.

    (1985)
  • M.J. Bourque et al.

    Properties and interconnections of trigeminal interneurons of the lateral pontine reticular formation in the rat

    J. Neurophysiol.

    (2001)
  • K.B. Corbin

    Observations on the peripheral distribution of fibers arising in the mesencephalic nucleus of the fifth cranial nerve

    J. Comp. Neurol.

    (1942)
  • D. Dessem et al.

    Primary- and secondary-like jaw-muscle spindle afferents have characteristic topographic distributions

    J. Neurophysiol.

    (1997)
  • D. Dessem et al.

    Morphology of jaw-muscle spindle afferents in the rat

    J. Comp. Neurol.

    (1989)
  • R. Donga et al.

    Discharge patterns of trigeminal commissural last-order interneurons during fictive mastication in the rabbit

    J. Neurophysiol.

    (1991)
  • Cited by (0)

    View full text