Ultrastructural degeneration studies were carried out on the cat trochlear nucleus following lesion of the vestibulo-trochlear pathway in order to characterize the location and type of presynaptic endings involved in this pathway. Four types of boutons are found in the normal trochlear nucleus. Types I and II are large and demonstrate typical en passant profiles with small diameter synaptic vesicles (35 and 40 nm). These terminals are characterized by the absence of neurofilaments in the Type II endings. Types III and IV are smaller boutons, located more axondendritically, and contain larger diameter synaptic vesicles (45 nm). Type V terminals contain large, granulated vesicles and occur only rarely. Following the interruption of the ascending projection from the ipsilateral superior and medial vestibular nuclei by parasagittal medullary lesions, degeneration of Type II boutons was commonly encountered in the ipsilateral trochlear nucleus. Predominantly Type HI degeneration was found in the contralateral trochlear nucleus. Electrical stimulation of the vestibular nerve showed that these lesions resulted in (1) a complete loss of inhibition in the ipsilateral trochlear nucleus and (2) a significant (75.90%) reduction in the contralateral excitatory pathway to the trochlear nucleus. Midline sagittal lesions in the floor of the fourth ventricle interupting the decussating fiber projection from the bilateral medial vestibular nuclei resulted in selective degeneration of only Type III boutons in both trochlear nuclei. We conclude that inhibitory vestibular neurons eminating from the superior vestibular nucleus terminate on trochlear motoneurons with Type II boutons and excitatory vestibular neurons from the contralateral medial vestibular nucleus end on trochlear motoneurons with Type III boutons.