Topographical organization of inferior olive cells projecting to translation and rotation zones in the vestibulocerebellum of pigeons

Previous electrophysiological studies in pigeons have shown that the vestibulocerebellum can be divided into two parasagittal zones based on responses to optic flow stimuli. The medial zone responds best to optic flow resulting from self-translation, whereas the lateral zone responds best to optic flow resulting from self-rotation. This information arrives from the retina via a projection from the accessory optic system to the medial column of the inferior olive. In this study we investigated inferior olive projections to translational and rotational zones of the vestibulocerebellum using the retrograde tracer cholera toxin subunit B. Extracellular recordings of Purkinje cell activity (complex spikes) in response to large-field visual stimuli were used to identify the injection sites. We found a distinct segregation of inferior olive cells projecting to translational and rotational zones of the vestibulocerebellum. Translation zone injections resulted in retrogradely labeled cells in the ventrolateral area of the medial column, whereas rotation zone injections resulted in retrogradely labeled cells in the dorsomedial region of the medial column. Motion of any object through space, including self-motion of organisms, can be described with reference to translation and rotation in three-dimensional space. Our results show that, in pigeons, the brainstem visual systems responsible for detecting optic flow are segregated into channels responsible for the analysis of translational and rotational optic flow in the inferior olive, which is only two synapses from the retina.