Eye saccades align optic flow with retinal specializations during object pursuit in freely moving ferrets.

Abstract

During prey pursuit, how eye rotations, such as saccades, enable continuous tracking of erratically moving targets while enabling an animal to navigate through the environment is unknown. To better understand this, we measured head and eye rotations in freely running ferrets during pursuit behavior. By also tracking the target and all environmental features, we reconstructed the animal's visual fields and their relationship to retinal structures. In the reconstructed visual fields, the target position clustered on and around the high-acuity retinal area location, the area centralis, and surprisingly, this cluster was not significantly shifted by digital removal of either eye saccades, exclusively elicited when the ferrets made turns, or head rotations that were tightly synchronized with the saccades. Here, we show that, while the saccades did not fixate the moving target with the area centralis, they instead aligned the area centralis with the intended direction of travel. This also aligned the area centralis with features of the optic flow pattern, such as flow direction and focus of expansion, used for navigation by many species. While saccades initially rotated the eyes in the same direction as the head turn, saccades were followed by eye rotations countering the ongoing head rotation, which reduced image blur and limited information loss across the visual field during head turns. As we measured the same head and eye rotational relationship in freely moving tree shrews, rats, and mice, we suggest that these saccades and counter-rotations are a generalized mechanism enabling mammals to navigate complex environments during pursuit.