Recordings were made from secondary vestibular axons in the medial longitudinal fasciculus (MLF) of barbiturate-anesthetized squirrel monkeys. Antidromic stimulation techniques were used to identify the axons as belonging to one of three classes of neurons: vestibulo-oculo-collic (VOC) neurons project both to the extraocular motor nuclei and to the spinal cord; vestibulo-ocular (VO) neurons do not have a spinal projection; and vestibulocollic (VC) neurons do not have an oculomotor projection. Galvanic stimulation was used to show that axons of all three classes received excitatory inputs from one labyrinth and inhibitory inputs from the other. VOC axons were confined to the MLF contralateral to the labyrinth from which they were excited. They made up more than half of the vestibular axons descending in the contralateral medial vestibulospinal tract (MVST), but less than one-quarter of those ascending in the contralateral MLF to the level of the oculomotor nucleus. Spinal projections were restricted to cervical segments with about half of the axons reaching segment C6. Conduction velocities, measured for Co-projecting axons, were similar for VOC and VC axons and were typically 25–50 m/s. Unlike the situation in the rabbit (Akaike et al. 1973) and cat (Akaike 1983), none of the MVST axons had conduction velocities > 75 m/s. The morphology of VOC neurons was studied by injection of horseradish peroxidase (HRP) into 60 physiologically identified axons in the MLF. Since individual axons were only stained for short distances, it was not possible to ascertain their complete branching patterns. Labeled fibers could be traced to an origin in and around the ventral lateral vestibular nucleus. This localization was confirmed by comparing the distributions within the vestibular nuclei of neurons retrogradely labeled from the upper cervical spinal cord (this study) and from the oculomotor nucleus (McCrea et al. 1987a; Highstein and McCrea 1988). VOC axons reached the contralateral MLF at the level of the abducens nucleus and immediately divided into an ascending and a descending, usually thicker, branch. Seven VOC axons could be traced to the extraocular motor nuclei; three terminated in the medial aspect of the oculomotor nucleus bilaterally and four terminated in the medial aspect of the contralateral abducens nucleus. The former axons may be part of a crossed, excitatory anterior-canal pathway; the latter, part of a similar horizontal-canal pathway. There were no terminations in the trochlear nucleus even though 12 labeled fibers passed close to it. VOC axons projected to several brainstem nuclei, including the contralateral interstitial nucleus of Cajal, cell groups in the region of the medial longitudinal fasciculus rostral to the abducens nucleus, the nucleus prepositus, the nucleus raphe obscuris, Roller's nucleus, and the paramedian medullary reticular formation. Virtually all of the above connections, except for the bilateral projection to the oculomotor nucleus, were contralateral to the cells of origin. The results in the squirrel monkey are compared with previous studies of VOC neurons in the cat (Isu and Yokota 1983; Uchino and Hirai 1984; Isu et al. 1988). In both species, VOC neurons make up a large proportion of contralaterally projecting MVST fibers. On the other hand, such dual-projecting neurons may provide a considerably smaller fraction of the secondary vestibular axons reaching the oculomotor nucleus in the monkey than they do in the cat.