The preceding study in the alert cat has shown that many secondary vestibular axons that ascend in the medial longitudinal fasciculus (MLF) increase their firing rate in proportion to downward eye position. In the present study, projection and termination of these downward-position-vestibular (DPV) neurons within extraocular motoneuron pools were studied electrophysiologically by spike-triggered averaging techniques and morphologically be reconstructing their axonal trajectory after intra-axonal injection of horseradish peroxidase (HRP). Extracellular field potentials recorded within the trochlear nucleus and/or the inferior rectus subdivision of the oculomotor nucleus were averaged by the use of spike potentials of single DPV neurons as triggers. All the crossed-DPV axons tested induced negative unitary field potentials in the trochlear nucleus (n = 9) and in the inferior rectus subdivision of the oculomotor nucleus (n = 5), suggesting that they made monosynaptic excitatory connection with motoneurons in these nuclei. The four crossed-DPV axons tested in the two motoneuron pools induced unitary field potentials in both. The majority of crossed-DPV axons terminated in these nuclei were directly activated from the caudal MLF, indicating that they had descending collaterals projecting to the spinal cord as well. The uncrossed-DPV axons did not induce such unitary field potentials either in the trochlear nucleus (n = 4) or in the inferior rectus subdivision (n = 3). All the uncrossed-DPV axons examined (n = 14) induced positive unitary field potentials in the superior rectus subdivision of the oculomotor nucleus, suggesting that they made monosynaptic inhibitory connections with motoneurons innervating the superior rectus muscle. These uncrossed-DPV axons displayed regular firing patterns and were not activated from the caudal MLF. None of the crossed-DPV axons tested (n = 4) induced unitary field potentials in the superior rectus subdivision. Five crossed-DPV axons were injected with HRP. All these axons ascended in the MLF contralateral to their soma, gave off many collaterals to the trochlear nucleus, and projected more rostrally. For three well-stained axons, numerous terminal branches were also found in the rostroventral part of the contralateral oculomotor nucleus, the area corresponding to the inferior rectus subdivision. Some collaterals in the oculomotor nucleus recrossed the midline to terminate in the medial part of the ipsilateral oculomotor nucleus. Other terminations were observed in the interstitial nucleus of Cajal and in the periaquaductal gray adjacent to the oculomotor nucleus. The crossed axons injected included both regular and irregular types, and three of the four examined were activated from the caudal MLF. Five uncrossed-DPV axons were satisfactorily stained with HRP. All these axons ascended in the ipsilateral MLF and terminated in the caudal part of the oculomotor nucleus but not in the trochlear nucleus or in the rostroventral part of the oculomotor nucleus. Numerous terminals found to be in contact with retrogradely labeled superior rectus motoneurons. Collaterals of uncrossed axons also terminated in the interstitial nucleus of Cajal. Four axons had regular discharge patterns. The remaining one was irregular and directly activated from the caudal MLF. It was concluded that DPV neurons projected to the motor nuclei of extraocular muscles involved in vertical eye movements. Crossed-DPV axons made monosynaptic excitatory connections with motoneurons innervating the superior oblique and inferior rectus muscles, whereas uncrossed-DPV axons made monosynaptic inhibitory connection with motoneurons innervating the superior rectus and inferior oblique muscles. Because the firing rate of DPV neurons is closely related to vertical eye position, their excitatory and inhibitory actions contribute to the control of the tonic activity in their target motoneurons during fixations.