Elsevier

Brain Research

Volume 960, Issues 1–2, 17 January 2003, Pages 81-89
Brain Research

Research report
Mesencephalic trigeminal neurons are innervated by nitric oxide synthase-containing fibers and respond to nitric oxide

https://doi.org/10.1016/S0006-8993(02)03776-9Get rights and content

Abstract

In the present study we found that mesencephalic trigeminal (Mes-V) neurons of the rat are innervated by nitrergic fibers and that nitric oxide (NO) modifies the electrophysiological properties of these cells. Mes-V neurons were surrounded by a network of fibers that contained neuronal nitric oxide synthase (nNOS); these fibers gave rise to terminal-, bouton-like structures which ended in Mes-V cells bodies. These cells, which did not display nNOS-like immunoreactivity were immunoreactive to a cGMP antibody. By performing intracellular recordings in the adult rat brain slice preparation, the effects of diethylenetriamine/NO adduct (DETA/NO) applications were examined. DETA/NO induced a depolarization that averaged 2.2 mV (range: 1–6 mV) in nine of 22 neurons. In 15 of 22 neurons (68% of the cells), there was a decrease in current threshold from 0.74 to 0.60 nA (19%; P<0.001). The excitatory effects of DETA/NO were abolished by ODQ, a blocker of soluble guanylate cyclase. Input resistance (Rin) decreased in 80% of the cells from a mean of 24.8 to 20.6 MΩ (17%; P<0.001) and the membrane time constant (τm) decreased from 7.5 to 5.6 ms (25%; P<0.05). The ‘sag’ seen in the membrane response of these cells to current pulses was augmented during DETA/NO application. These findings indicate that there is a nitrergic innervation of Mes-V neurons and that these sensory cells are target for NO that may act on them as an excitatory neuromodulator promoting the synthesis of intracellular cGMP.

Introduction

The cell bodies of primary afferent trigeminal mesencephalic (Mes-V) neurons are located within the brain stem and are contacted by numerous synapses containing different neurotransmitters and neuromodulators [8], [20]. These cells are large pseudo-unipolar neurons; the peripheral branch of their axons innervate jaw closer muscle spindles or periodontal receptors [6], [10]. The central branches of Mes-V axons innervate trigeminal motoneurons, the trigeminal sensory complex, the parvocellular reticular formation and the supratrigeminal nucleus where information from peripheral propioceptive receptors is processed [22], [30]. The central location of these neurons and the fact that they are innervated have been a curiosity among neurophysiologists. Other than that these neurons function as interneurons in the organization of jaw movements [31], there are no obvious reasons to account for their location or for the synaptic contacts that they display on their surface. In the present study, we found that these neurons are innervated by fibers that contained nNOS-like immunoreactivity; we also established that NO increases the excitability and modifies other electrophysiological properties of these cells.

Section snippets

Material and methods

Seventeen adult Wistar rats (150–230 g) were used. Four were employed in anatomical studies and 13 were used in electrophysiological experiments.

Histological results

Large pseudo-unipolar Mes-V neurons were identified by their morphology and location. In the middle to caudal portion of the Mes-V nucleus, where the electrophysiological recordings were performed, Mes-V neurons were retrogradely labeled by CTb-HRP (Fig. 1). Numerous nNOS-like immunoreactive fibers were observed both surrounding and in close apposition to Mes-V somas. These fibers gave rise to bouton-like structures ending on the cell bodies of Mes-V cells. Similar results were obtained when

Discussion

In the present study we demonstrate that Mes-V neurons are innervated by fibers capable of producing NO and that NO modifies the electrophysiological properties of these cells. Mes-V neurons also displayed cGMP-like immunoreactivity whereas nitregic fibers impinging upon them did not. Based on these findings we postulate that, under physiological conditions, NO may be produced in the network of fibers that surrounds Mes-V neurons and modulate the activity of these cells. The evidence, we

Acknowledgements

This work was supported by the following grants from the US Public Health Service: NS 23426, NS09999; from the CSIC, Universidad de la República, and CONICYT–Fondo Clemente Estable N1082 to I.E. Pose. We are grateful to J.K. Engelhardt for his critical revision of this manuscript.

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