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

During prey pursuit, how eye-rotations, such as saccades, enable
continuous tracking of erratically moving targets while simultaneously
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 which
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.