Smooth pursuit (SP)-related neurons in the dorsal-medial part of medial superior temporal cortex (MSTd) carry extraretinal signals that may play a role in maintenance of SP once eye velocity matches target velocity. For example, it has not been determined whether the extraretinal signals reflect volitional SP commands or proprioception. The aim of this study was to test some potential sources of extraretinal signals in MSTd pursuit neurons. We tested 40 MSTd neurons during step-ramp SP with target blink conditions to show that they carried an extraretinal signal. To examine potential contributions from eye movements that might reflect proprioceptive feedback from eye muscles, we tested MSTd neurons during rotational vestibular ocular reflex in complete darkness (VORd). Vestibular stimulation was delivered in the earth horizontal plane to elicit reflex driven smooth eye movements that matched the speed and frequency of volitional SP. We also tested VOR in the light (VOR x 1) and cancellation of the VOR (VOR x 0). Our neurons were modulated during both SP and cancellation of the VOR. In contrast, MSTd smooth pursuit neurons with extraretinal signals were not significantly modulated during VORd (sensitivity < or = 0.10 spike/s/ degrees /s). This combination of properties is compatible with classifying these neurons as gaze-velocity related. Absence of modulation during VORd testing could be caused by cancellation of head and eye movement sensitivity or dependence of neuronal firing on volitional SP commands. Our results support the suggestion that modulation of SP-related MSTd neurons reflects volitional SP commands rather then eye movements generated by reflex pathways.