Abstract

Neurons in the trigeminal mesencephalic nucleus (Vme) have axons that branch peripherally to innervate the orofacial region and project centrally to several motor nuclei in brainstem. The dorsal motor nucleus of vagus nerve (DMV) resides in the brainstem and takes a role in visceral motor function such as pancreatic exocrine secretion. The present study aimed to demonstrate the presence of Vme–DMV circuit, activation of which would elicit a trigeminal neuroendocrine response. A masticatory dysfunctional animal model termed unilateral anterior crossbite (UAC) model created by disturbing the dental occlusion was used. Cholera toxin B subunit (CTb) was injected into the inferior alveolar nerve of rats to help identify the central axon terminals of Vme neurons around the choline acetyltransferase (ChAT) positive motor neurons in the DMV. The level of vesicular glutamate transporter 1 (VGLUT1) expressed in DMV, the level of acetylcholinesterase (AChE) expressed in pancreas, the level of glucagon and insulin expression in islets and serum, and the blood glucose level were detected and compared between UAC and the age matched sham-operation control mice. Data indicated that compared with the controls, there were more CTb/VGLUT1 double labeled axon endings around the ChAT positive neurons in the DMV of UAC groups. Mice in UAC group expressed a higher VGLUT1 protein level in DMV, AChE protein level in pancreas, glucagon and insulin level in islet and serum, and higher postprandial blood glucose level, but lower fasting blood glucose level. All these were reversed at 15-weeks when UAC cessation was performed from 11-weeks (all, P < 0.05). Our findings demonstrated Vme–DMV circuit via which the aberrant occlusion elicited a trigeminal neuroendocrine response such as alteration in the postprandial blood glucose level. Dental occlusion is proposed as a potential therapeutic target for reversing the increased postprandial glucose level.

Highlights

  • The periodontal biomechanical message is mediated by trigeminal mesencephalic nucleus (Vme) which resides in the brainstem

  • As we indicated in the introduction section, the sign of Cholera toxin B subunit (CTb) positivity in neurons of the Vme in animals accepted CTb injection into the alveolar nerve was taken as an indication of the afferent message from the mandibular periodontal region where the proprioceptive receptors are located at (Liu et al, 2017)

  • By using these reported methods, presently, we demonstrated that the CTb labeled vesicular glutamate transporter 1 (VGLUT1) positive axon terminals of Vme were distributed surrounding neurons in dorsal motor nucleus of vagus nerve (DMV)

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Summary

Introduction

The periodontal biomechanical message is mediated by trigeminal mesencephalic nucleus (Vme) which resides in the brainstem. The cell bodies of the neurons in Vme form a mediolaterally narrow band of neurons located across the entire rostro-caudal axis of the midbrain (Lazarov, 1996) This anatomic feature makes it possible for the projections of neurons in the Vme to target many other neurons in the brainstem. The neurons of Vme are pseudo-monopolar neurons, the peripheral processes of which extend to the periodontal ligament through the inferior alveolar nerve, and the central processes extend to many motor neurons such as motor neurons of trigeminal motor nucleus, facial nucleus, hypoglossal nucleus, and spinal nucleus of the accessory nerve. X. et al, 2018) combined with the detection of the protein expression level of acetylcholinesterase (AChE) in masseters, stapedius, lingualis, and sternocleidomastoid muscles, the excitatory impact of UAC on trigeminal motor nucleus, facial nucleus, hypoglossal nucleus, and spinal nucleus of the accessory nerve were demonstrated (Liu et al, 2017, 2018)

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