Many studies have documented the influence of the flocculus upon vestibulo-ocular reflex eye movements. Electrical stimulation of Purkinje cells in a central longitudinal zone evoked slow ipsilateral eye movements in the horizontal plane. Recently, the organization of neurons in the vestibulo-cerebellar pathways controlling single lateral rectus and medial rectus muscles was identified in rats using the transynaptic transport of pseudorabies virus. Overlapping distributions of neurons innervating single muscles were located predominantly in a central longitudinal zone of ventral paraflocculi/dorsal flocculi, and the rostral half of ventral flocculi. This study used two isogenic pseudorabies virus recombinants to determine whether individual cells in those brain regions have collateralized projections to motoneuron pools innervating the right lateral rectus and the left medial rectus muscles using different survival times and dual injection paradigms. The infected neurons were detected using dual-labeling immunofluorescence. Three populations of labeled neurons were observed: two populations replicated only one reporter while a third contained both viruses (i.e. dual-labeled). Most dual-labeled cells were located in a central longitudinal zone of the ventral paraflocculus, ipsilateral to the injection into the medial rectus, whereas very few were in the flocculus. This finding suggests that the flocculus and ventral paraflocculus may exert influence upon distinct vestibulo-cerebellar pathways. Most Purkinje cells in the ventral paraflocculus may influence the vestibulo-ocular reflex pathways through collateralization, whereas those in the flocculus may instead provide a monocular control of eye movements.