Complex spike activity of floccular Purkinje cells responds to patterns of rotational optic flow about the vertical axis (rVA neurons) or a horizontal axis 45° to the midline (rH45 neurons). The pigeon flocculus is organized into four parasagittal zones: two rVA zones (zones 0 and 2) interdigitated with two rH45 zones (zones 1 and 3). Climbing fiber input to the rVA and rH45 zones arises in the caudal and rostral regions of the medial column of the inferior olive (mcIO), respectively. To determine whether the two rVA zones and the two rH45 zones receive input from different areas of the caudal and rostral mcIO and whether individual neurons project to both zones of the same rotational preference, different colors of fluorescent retrograde tracer were injected into the two rVA or two rH45 zones. For the rVA injections, retrogradely labeled cells from the two zones were intermingled in the caudal mcIO, but the distribution of cells labeled from zone 0 was slightly caudal to that from zone 2. On average, 18% of neurons were double labeled. For the rH45 injections, cells retrogradely labeled from the two zones were intermingled in the rostral mcIO, but the distribution of cells labeled from zone 1 was slightly rostral to that from zone 3. On average, 22% of neurons were double labeled. In sum, each of the two rVA zones and the two rH45 zones receives input from slightly different regions of the mcIO, and about 20% of the neurons project to both zones. J. Comp. Neurol. 486:159–168, 2005. © 2005 Wiley-Liss, Inc.