Smooth pursuit is a relatively recent eye movement which has developed in frontal-eyed species. The smooth pursuit system is involved during foveal smooth pursuit, the 'rapid' component of OKN slow phase and VOR suppression. The cortical areas controlling smooth pursuit (at the temporo-parieto-occipital junction and in the FEF) send ipsilateral projections onto the pontine nuclei, mainly the DLPN, passing through the anterior part of the midbrain. A midbrain or DLPN lesion results in ipsilateral smooth pursuit impairment (i.e. decreased gain) (Table 1). After the pontine nuclei, all smooth pursuit pathways pass through the cerebellum. They project onto the flocculus, mainly contralaterally (first decussation of the lateral smooth pursuit circuitry), and bilaterally onto the posterior vermis. Eye velocity is encoded in the activity of the floccular Purkinje cells, whereas target velocity is encoded in that of the vermal Purkinje cells. Unilateral floccular lesions and posterior vermal lesions (involving both sides of this structure) result in ipsilateral and bilateral smooth pursuit impairment, respectively. The flocculus sends an ipsilateral inhibitory projection onto the MVN, the y-group nucleus and the SVN, controlling contralateral, upward and perhaps downward smooth pursuit, respectively. Alternatively, the downward smooth pursuit pathway could pass through the dentate nuclei. The MVN sends a contralateral excitatory projection onto the abducens nucleus (second decussation of the lateral smooth pursuit circuitry). These anatomical and physiological characteristics of lateral smooth pursuit pathways, in addition to the results of lesion studies, suggest that, besides the floccular inhibitory Purkinje cell, there is another inhibitory neurone in the circuitry preceding this cell, perhaps within the flocculus itself. The posterior vermis projects onto the fastigial nuclei, which also control smooth pursuit. These nuclei could send efferents to those periabducens cells involved in ipsilateral smooth pursuit. The final part of the pathways involved in vertical smooth pursuit could pass mainly through the BC, originating in the y-group nucleus for upward movement and in the SVN or the dentate nuclei for downward movement. Alternatively, a ventral tegmental tract could transmit upward smooth pursuit signals between the y-group nucleus and the oculomotor nucleus. The MLF also belongs to this vestibulo-oculomotor circuitry, but does not appear to be crucial for vertical smooth pursuit since this eye movement is only partially impaired after MLF lesions. Lastly, parallel to the direct vestibulo-ocular motor nuclei pathways, there are other pathways passing through the brain stem integrators, converting eye velocity signals to eye position signals during all eye movements, including smooth pursuit.(ABSTRACT TRUNCATED AT 400 WORDS)