VESTIBULAR PROJECTIONS TO MEDIAL RECTUS SUBDIVISION OF OCULOMOTOR NUCLEUS

Extra- and intracellular records were obtained from the medial rectus subdivision of the oculomotor complex in anesthetized cats following electrical stimulation of the vestibular nerve, nuclei, pontine tegmentum, and medial longitudinal fasciculi (MLF). Stimulation of the ipsilateral vestibular nerve produced large-amplitude disynaptic EPSPs in medial rectus motoneurons with a latency of 1.3 ms. The second-order excitatory vestibular neurons were localized to the rostral ventral part of the lateral vestibular nucleus. Axons from these cells reached medial rectus motoneurons by curving under the superior vestibular nucleus before ascending in the pontine tegmentum lateral to the lateral wing of the MLF. The origin and course of this pathway was confirmed by acute and chronic lesions in the cat brain stem. Electrical stimulation of the contralateral vestibular nerve produced small-amplitude disynaptic EPSPs in a majority of medial rectus motoneurons with a latency of 1.4 ms. Disynaptic IPSPs were not observed. The latter finding was established as not being due to a difference in threshold for the vestibular stimulus by recording sequentially from ipsi- and contralateral medial rectus motoneurons. Suprathreshold electrical stimulation of the contralateral vestibular nerve produced the aforementioned short-latency EPSP followed either by an EPSP and/or IPSP with a minimum latency of 2.8 ms in the latter case. The EPSP-IPSP sequence was of small amplitude and the latter component could only be visualized after intracellular injection of chloride. Following suprathreshold stimulation of the medial longitudinal fasciculus and pontine tegmentum, only monosynaptic EPSPs were observed in medial rectus motoneurons. Simultaneous reversal of EPSPs elicited from the vestibular nerve (ipsi- and contralateral) by intracellular injections of depolarizing current demonstrated that the excitatory synaptic terminations on the somadendritic membrane from contralateral vestibular neurons were more distally placed on the dendritic tree. The complete EPSP reversal confirms the chemical as opposed to electrotonic mode of synaptic transmission for all vestibular excitatory pathways terminating on the medial rectus subdivision in the mammal. The absence of a disynaptic, reciprocal, semicircular canal-evoked excitation-inhibition in the medial rectus subgroup is strikingly different than the synaptic organization found for any other vertical or horizontal extraocular motoneuron. Superimposition of the vergence and version function in the horizontal oculomotor system is discussed in light of the absence of a direct inhibitory vestibular neuron and the presumed medullary site for the immediate supranuclear organization of horizontal conjugate gaze.