Encoding of Global Visual Motion in the Avian Pretectum Shifts from a Bias for Temporal-to-Nasal Selectivity to Omnidirectional Excitation across Speeds

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°/s) 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 (<i>Taeniopygia guttata</i>) across spatial and temporal frequencies, corresponding to a speed range of 0.062-1,024°/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 1,024°/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 potential collisions, depending on the speed of the optic flow signal.