Eye velocity responsiveness of floccular Purkinje cells was studied in alert, pigmented rabbits. Conjugate horizontal eye nystagmus was elicited by application of electric pulse trains (10-50 microA, 30 c/s) to the optic tract through chronically implanted electrodes. Purkinje cells were sampled with an extracellular microelectrode from the flocculus, and their involvement in different oculomotor functions was specified by electrical stimulation at their recording sites. At those sites where abduction of the ipsilateral eye was elicited, the discharge frequency of simple spikes usually increased during slow eye movement to the ipsilateral side and decreased during eye movement to the contralateral side in nystagmus and after-nystagmus. Within a limited range, the discharge frequency increased linearly with eye velocity, at an average rate of 1.6 impulse s-1/degree s-1. An opposite directional specificity (decrease in ipsilateral and increase in contralateral eye movement) and directional non-specificity were common at other floccular sites where local stimulation elicited downward or no eye movement. Retrobulbar anesthesia of proprioceptive afferents from one eye reduced the eye velocity responsiveness of Purkinje cells in the ipsilateral flocculus by 31%, but did not affect their responsiveness in the contralateral flocculus. These observations indicate that eye velocity input to the rabbit flocculus arises partly from peripheral receptors but mainly from the central oculomotor system, and that responsiveness of Purkinje cells to the input is organized specifically according to their functional involvement.