Inhibitory synaptic inputs to the oculomotor nucleus from vestibulo-ocular-reflex-related nuclei in the rabbit

Studies of the pathways involved in the vestibulo-ocular reflex have suggested that the projection from the superior vestibular nucleus to the ipsilateral oculomotor nucleus is inhibitory, whereas the medial vestibular nucleus, the abducens nucleus and the contralateral superior vestibular nucleus most likely exert excitatory effects on oculomotor neurons. In order to determine directly the termination pattern and the neurotransmitter of these afferents, we studied their input to the oculomotor nucleus in the rabbit at the light microscopic level with the use of anterograde tracing of Phaseolus vulgaris-leucoagglutinin combined with retrograde tracing of horseradish peroxidase from the extraocular muscles, and at the ultrastructural level with the use of anterograde tracing of wheatgerm-agglutinated horseradish peroxidase combined with GABA and glycine postembedding immunocytochemistry. The general ultrastructural characteristics of the neuropil and the types of boutons observed in the rabbit oculomotor nuclei are in general agreement with the descriptions for the oculomotor complex of other mammals. The superior vestibular nucleus projected bilaterally to the superior rectus and inferior oblique subdivisions, and ipsilaterally to the inferior rectus and medial rectus subdivision; the medial vestibular nucleus projected bilaterally to the medial rectus, inferior oblique, inferior rectus and superior rectus subdivisions with a strong contralateral predominance. The abducens nucleus projected contralaterally to the medial rectus subdivision. More than 90% of all the anterogradely labeled terminals from the ipsilateral superior vestibular nucleus were GABAergic. These terminals were characterized by flattened vesicles and symmetric synapses, and they contacted somata, as well as proximal and distal dendrites of motoneurons. All terminals derived from the medial vestibular nucleus the abducens nucleus and the contralateral superior vestibular nucleus were non-GABAergic. These non-GABAergic terminals showed spherical vesicles and asymmetric synapses, and they contacted predominantly distal dendrites. None of the anterogradely labeled terminals from the studied vestibular nuclei or abducens nucleus were glycinergic. The present study provides the first direct anatomical evidence that most, if not all, of the synaptic input from the superior vestibular nucleus to the ipsilateral oculomotor nucleus is GABAergic, and that the medial rectus subdivision is included in the termination area. Furthermore, it confirms that the projections from the medial vestibular nucleus, the abducens nucleus and the contralateral superior vestibular nucleus are exclusively non-GABAergic.