The Accessory Optic System Contributes to the Spatio-Temporal Tuning of Motion-Sensitive Pretectal Neurons

Abstract

The nucleus of the basal optic root (nBOR) of the accessory optic system (AOS) and the pretectal nucleus lentiformis mesencephali (LM) are involved in the analysis of optic flow that results from self-motion and are important for oculomotor control. These neurons have large receptive fields and exhibit direction selectivity to large moving stimuli. In response to drifting sine wave gratings, LM and nBOR neurons are tuned to either low spatial/high temporal frequencies (SF, TF) or high SF/low TF stimuli. Given that velocity = TF/SF, these are referred to as "fast" and "slow" neurons, respectively. There is a heavy projection from the AOS to the pretectum, although its function is unknown. We recorded the directional and spatio-temporal tuning of LM units in pigeons before and after nBOR was inactivated by tetrodotoxin injection. After nBOR inactivation, changes in direction preference were observed for only one of 18 LM units. In contrast, the spatio-temporal tuning of LM units was dramatically altered by nBOR inactivation. Two major effects were observed. First, in response to motion in the preferred direction, most (82%) neurons showed a substantially reduced (mu = -67%) excitation to low SF/high TF gratings. Second, in response to motion in the anti-preferred direction, most (63%) neurons showed a dramatically reduced (mu = -78%) inhibition to high SF/low TF gratings. Thus the projection from the nBOR contributes to the spatio-temporal tuning rather than the directional tuning of LM neurons. We propose a descriptive model whereby LM receives inhibitory and excitatory input from "slow" and "fast" nBOR neurons, respectively.