Encoding of global visual motion in the avian pretectum shifts from a bias for temporal-to-nasal selectivity to omnidirectional excitation across speeds

Abstract

The pretectum of vertebrates contains neurons responsive to global visual motion. These signals are sent to the cerebellum, forming a subcortical pathway for processing optic flow. Global motion neurons exhibit selectivity for both direction and speed, but this is usually assessed by first determining direction preference at intermediate velocity (16-32 deg/sec), and then assessing speed tuning at the preferred direction. A consequence of this approach is that it is unknown if and how direction preference changes with speed. We measured directional selectivity in 114 pretectal neurons from 44 zebra finches (Taeniopygia guttata) across spatial and temporal frequencies, corresponding to a speed range of 0.062 to 1024°/s. Pretectal neurons were most responsive at 32-64°/s with lower activity as speed increased or decreased. At each speed, we determined if cells were directionally-selective, bidirectionally-selective, omnidirectionally responsive, or unmodulated. Notably, at 32°/s, 60% of the cells were directionally selective and 28% were omnidirectionally responsive. In contrast, at 1024°/s, 20% of the cells were directionally selective and nearly half of the population was omnidirectionally responsive. Only 15% of the cells were omnidirectionally excited across most speeds. The remaining 85% of the cells had direction tuning that changed with speed. Collectively, these results indicate a shift from a bias for directional tuning at intermediate speeds of global visual motion to a bias for omnidirectional responses at faster speeds. These results suggest a potential role for the pretectum during flight by detecting unexpected drift or potentials collisions, depending on the speed of the optic flow signal.

Significance Statement During locomotion, images of edges and surfaces in the environment move across the retina, a signal of global visual motion called optic flow. Retinal recipient areas in the accessory optic system and the pretectum are the earliest sites to encode this signal, and the neurons are selective for direction and speed. Previous work suggested that directional selectivity may change across speeds but this has never been systematically studied. We measured direction preferences from 0.062 to 1024°/s in the avian pretectum. We found that pretectal global motion neurons are biased for temporal-to-nasal motion at intermediate speeds but biased for omnidirectional responses at faster speeds. These results suggest the pretectum could function to detect both unexpected drift and potential collisions during locomotion.