Spatiotemporal Tuning of Optic Flow Inputs to the Vestibulocerebellum in Pigeons: Differences Between Mossy and Climbing Fiber Pathways

Abstract

The pretectum, accessory optic system (AOS), and vestibulocerebellum (VbC) have been implicated in the analysis of optic flow and generation of the optokinetic response. Recently, using drifting sine-wave gratings as stimuli, it has been shown that pretectal and AOS neurons exhibit spatiotemporal tuning. In this respect, there are two groups: fast neurons, which prefer low spatial frequency (SF) and high temporal frequency (TF) gratings, and slow neurons, which prefer high SF–low TF gratings. In pigeons, there are two pathways from the pretectum and AOS to the VbC: a climbing fiber (CF) pathway to Purkinje cells (P cells) via the inferior olive and a direct mossy fiber (MF) pathway to the granular layer (GL). In the present study, we assessed spatiotemporal tuning in the VbC of ketamine-anesthetized pigeons using standard extracellular techniques. Recordings were made from 17 optic-flow-sensitive units in the GL, presumably granule cells or MF rosettes, and the complex spike activity (CSA) of 39 P-cells, which reflects CF input. Based on spatiotemporal tuning to gratings moving in the preferred direction, eight GL units were classified as fast units, with a primary response to low SF–high TF gratings (mean = 0.13 cpd/8.24 Hz), whereas nine were slow units preferring high SF–low TF gratings (mean = 0.68 cpd/0.30 Hz). CSA was almost exclusively tuned to slow gratings (mean = 0.67 cpd/0.35 Hz). We conclude that MF input to the VbC is from both fast and slow cells in the AOS and pretectum, whereas the CF input is primarily tuned to slow gratings.