EXCITATORY AND INHIBITORY VESTIBULAR PATHWAYS TO THE EXTRAOCULAR MOTOR NUCLEI IN GOLDFISH. Werner Graf, Robert Spencer, Harriet Baker and Robert Baker. Laboratoire de Physiologie de la Perception et de l'Action, CNRS, 15 rue de l'Ecole de Medecine, 75270 Paris Cedex 06, France, Department of Anatomy, Medical College of Virginia, 1101 East Marshall Street, Richmond, VA, 23298, Department of Neurology, Burke Rehabilition Center, 785 Mamaroneck Avenue, White Plains, NY 10605, Department of Physiology and Neuroscience, New York University Medical Center, 550 First Avenue, New York, NY 10016.
APStracts 4:0054N, 1997.
ABSTRACT
Electrophysiological, ultrastructural and immunohistochemical techniques were utilized to describe the excitatory and inhibitory vestibular innervation of extraocular motor nuclei in the goldfish. In antidromically activated oculomotor motoneurons, electrical stimulation of the intact contralateral vestibular nerve produced short latency, variable amplitude electrotonic EPSPs at 0.5-0.7 ms followed by chemical EPSPs at 1.0-1.3 ms. Stimulation of the ipsilateral vestibular nerve produced small amplitude membrane hyperpolarizations at a latency of 1.3 -1.7 ms in which equilibrium potentials were slightly more negative than resting potentials. The IPSPs reversed with large amplitudes after the injection of chloride ions suggesting a proximal soma-dendritic location of terminals exhibiting high efficacy inhibitory synaptic conductances. In antidromically identified abducens motoneurons and putative internuclear neurons, electrical stimulation of the contralateral vestibular nerve produced large amplitude, short latency electrotonic EPSPs at 0.5 ms followed by chemical depolarizations at 1.2-1.3 ms. Stimulation of the ipsilateral vestibular nerve evoked IPSPs at 1.4 ms that were reversed following injection of current and/or chloride ions. GABA antibodies labeled inhibitory neurons in vestibular subdivisions with axons projecting into the ipsilateral MLF. Putative GABAergic terminals surrounded oculomotor, but not abducens, motoneurons retrogradely labeled with HRP. Hence, the spatial distribution of GABAergic neurons and terminals appears highly similar in the vestibulo-ocular system of goldfish and mammals. Electron microscopy of motoneurons in the oculomotor and abducens nucleus showed axosomatic and axodendritic synaptic endings containing spheroidal synaptic vesicles establishing chemical, presumed excitatory, synaptic contacts with asymmetrical pre-/postsynaptic membrane specializations. The majority of contacts with spheroidal vesicles displayed gap junctions in which the chemical and electrotonic synapses were either en face to dissimilar or adjacent to one another on the same soma/dendritic profiles. Another separate set of axosomatic synaptic endings, presumed to be inhibitory, contained pleiomorphic synaptic vesicles with symmetrical pre-/postsynaptic membrane specializations that never included gap junctions. Excitatory and inhibitory synaptic contacts appeared equal in number, but were more sparsely distributed along the soma-dendritic profiles of oculomotor as compared to abducens motoneurons. Collectively these data provide evidence for both disynaptic vestibular inhibition and excitation in all subdivisions of the extraocular motor nuclei suggesting the basic vestibulo-oculomotor blueprint to be conserved among vertebrates. We propose that unique vestibular neurons, transmitters, pathways and synaptic arborizations are homologous structural traits that have been essentially preserved throughout vertebrate phylogeny by a shared developmental plan. 

Received 5 September 1996; accepted in final form 21 January 1997.
APS Manuscript Number J711-6.
Article publication pending J. Neurophysiol.
ISSN 1080-4757 Copyright 1997 The American Physiological Society.
Published in APStracts on 20 February 1997