The activity of 62 antidromically identified prepositus hypoglossi neurons was recorded in 10 alert cats during spontaneous, vestibular or visually induced eye movements. Neurons were antidromically activated from stimulating electrodes implanted in the ipsilateral medial longitudinal fasciculus (n = 24), the ipsilateral interstitial nucleus of Cajal (n = 6), the ipsilateral parabigeminal nucleus (n = 2), the contralateral superior colliculus (n = 6) and the contralateral cerebellar posterior peduncle (n = 24). Neurons were identified as eye-movement-related when their rate-position and/or rate-velocity plots showed correlation coefficients greater than or equal to 0.6. They were further classified as "position", "position-velocity" and "velocity-position" according to their relative eye position and velocity coefficients. However, they seemed to be distributed as a continuum in which a progressive decrease of eye velocity sensitivity was accompanied by a proportional increase in eye position sensitivity. "Position-velocity" neurons (n = 9) were mainly horizontal type II neurons projecting to the vicinity of the oculomotor complex; two of these neurons with vertical sensitivity were also activated from the interstitial nucleus of Cajal. Mean position and velocity sensitivity of these neurons were 5.2 spikes/s per degree and 0.62 spikes/s per degree per second, respectively. Pure "position" neurons (n = 7) also showed activation during ipsilateral eye fixations; their mean position gain was 7.3 spikes/s per degree and they projected to the ipsilateral oculomotor and Cajal nuclei, and to the contralateral superior colliculus. "Velocity-position" neurons (n = 18) were type I or II neurons with rather irregular tonic firing rates and a mean velocity gain of 0.75 spikes/s per degree per second. Type II "velocity-position" neurons projected mainly to the oculomotor area, while type I neurons projected preferentially to the cerebellum. A special type of "pause" neuron (n = 5), with very low firing rate and pausing mainly for contralateral saccades, was activated exclusively from the contralateral posterior peduncle. Many neurons with weak eye movement sensitivity (n = 22) were activated mainly (73%) from the cerebellum. It can be concluded that the prepositus hyperglossi nucleus distributes specific eye movement related signals to motor and premotor brainstem and cerebellar structures. The variability of interspike intervals of representative prepositus hypoglossi neurons of each class was compared to the discharge variability of identified abducens motoneurons.(ABSTRACT TRUNCATED AT 400 WORDS)