Abstract

In all vertebrates the eyes are moved by six pairs of extraocular muscles enabling horizontal, vertical and rotatory movements. Recent work showed that each extraocular muscle is controlled by two motoneuronal groups: (1) Motoneurons of singly-innervated muscle fibers (SIF) that lie within the boundaries of motonuclei mediating a fast muscle contraction; and (2) motoneurons of multiply-innervated muscle fibers (MIF) in the periphery of motonuclei mediating a tonic muscle contraction. Currently only limited data about the transmitter inputs to the SIF and MIF motoneurons are available. Here we performed a quantitative study on the transmitter inputs to SIF and MIF motoneurons of individual muscles in the oculomotor and trochlear nucleus in monkey. Pre-labeled motoneurons were immunostained for GABA, glutamate decarboxylase, GABA-A receptor, glycine transporter 2, glycine receptor 1, and vesicular glutamate transporters 1 and 2. The main findings were: (1) the inhibitory control of SIF motoneurons for horizontal and vertical eye movements differs. Unlike in previous primate studies a considerable GABAergic input was found to all SIF motoneuronal groups, whereas a glycinergic input was confined to motoneurons of the medial rectus (MR) muscle mediating horizontal eye movements and to those of the levator palpebrae (LP) muscle elevating the upper eyelid. Whereas SIF and MIF motoneurons of individual eye muscles do not differ numerically in their GABAergic, glycinergic and vGlut2 input, vGlut1 containing terminals densely covered the supraoculomotor area (SOA) targeting MR MIF motoneurons. It is reasonable to assume that the vGlut1 input affects the near response system in the SOA, which houses the preganglionic neurons mediating pupillary constriction and accommodation and the MR MIF motoneurones involved in vergence.

Highlights

  • The vertebrate eye is rotated by six extraocular muscles: four recti and two oblique muscles

  • In the present study we investigated the presence of glycinergic, GABAergic and glutamatergic inputs to singly-innervated muscles fibers (SIF) and multiply-innervated muscles fibers (MIF) motoneurons of oculomotor nucleus (nIII) and trochlear nucleus (nIV) in monkey

  • Since glutamate decarboxylase (GAD) immunoreactivity was strongly expressed in nerve endings (Ottersen and Storm-Mathisen, 1984), thin paraffin sections stained for GAD were used for the quantitative analysis of GABAergic input to motoneurons (Figure 3)

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Summary

Introduction

The vertebrate eye is rotated by six extraocular muscles: four recti (superior, inferior, medial and lateral recti muscles) and two oblique muscles (superior and inferior oblique). Motoneurons of the oculomotor nucleus (nIII) innervate the ipsilateral medial rectus (MR), inferior rectus (IR), inferior oblique (IO) and contralateral superior rectus (SR) muscles. Motoneurons of the trochlear nucleus (nIV) control the contralateral superior oblique muscle (SO), and motoneurons of the abducens nucleus (nVI) activate the ipsilateral lateral rectus (LR) muscle (Büttner-Ennever, 2006). There are fast contracting (twitch) muscle fibers innervated by one single ‘‘en plaque’’ ending in the middle third of the muscle fiber (singly-innervated fibers, SIF; Chiarandini and Stefani, 1979; Lynch et al, 1994; for review: Spencer and Porter, 2006). Thereby, in monkey the MIF motoneurons of the MR and IR are situated together in the C-group at the dorsomedial border of nIII Those of IO and SR are located midline within the S-group sandwiched between the two oculomotor nuclei. Recent studies in monkey revealed that neurons within these peripheral cell groups give rise to the palisade endings located at the myotendinous junctions of MIFs (Lienbacher et al, 2011; Zimmermann et al, 2011)

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