Nature of optokinetic response and zonal organization of climbing fiber afferents in the vestibulocerebellum of the pigmented rabbit. I. The flocculus.

In pigmented rabbits anesthetized with N2O (70%) and halothane (2-4%), Purkinje cells were extracellularly recorded in the flocculus. A large central visual field (60 degrees x 60 degrees) was used to optokinetically stimulate either the ipsi- or contralateral eye, and the direction and velocity selectivities of complex spike responses were examined. For optokinetic stimulation (OKS) delivered to the ipsilateral eye (n = 129), the preferred direction was forward (F, n = 57) or upward (U, n = 37), while the remaining cells (n = 35) showed no response (N). For OKS delivered to the contralateral eye (n = 107), the preferred direction was backward (B, n = 11), downward (D, n = 42) or upward (U, n = 2), and the rest (n = 52) showed N. Cells tested with both eyes (n = 89) fell into five categories based on the preferred direction to ipsi- and contralateral OKS: (1) ipsi-F and contra-B (F/B type, n = 9), (2) ipsi-F but contra-N (F/N type, n = 28), (3) ipsi-U and contra-D (U/D type, n = 13), (4) ipsi-U but contra-N (U/N type, n = 17), and (5) ipsi-N but contra-D (N/D type, n = 22). The optimum velocity was within 0.1-2.0 degrees/s for all cells. On the average, the best response was obtained at 0.2-0.5 degrees/s stimulation. All ipsi-F cells responded to electrical stimulation of the optic tract (OT), while most cells preferring ipsi-U, contra-B and contra-D directions did not respond. No characteristic feature was found in cells innervated with collateralized climbing fiber branches to the nodulus. In the flocculus, cells preferring horizontal orientation (H cells, preferring ipsi-F and/or contra-B directions) were localized in a narrow dorsoventral zone (less than 1.0 mm) along the caudal border of the rostral one third, while those preferring the vertical orientation (V cells, preferring ipsi-U and/or contra-D directions) were in two distinct narrow zones located rostral and caudal to the H cell zone. H and V cells were intermingled in the central portion of the ventral flocculus. These four zones are in good agreement with previously defined H, anterior V, posterior V and R zones, respectively. The results indicate that the subdivision of the flocculus which controls horizontal (vertical) eye movements receives information regarding movements of the visual surround in the horizontal (vertical) orientation through visual climbing fiber afferents, thus being organized in olivo-cortico-nuclear functional units for control of eye movements.