Eyeball translations affect saccadic eye movements beyond brainstem control.

Abstract

Vision requires that we rotate our eyes frequently to look at informative structures in the scene. Eye movements are planned by the brain but their execution depends on the mechanical properties of the oculomotor plant, that is, the arrangement of eyeball position, muscle insertions, and pulley locations. Therefore, the biomechanics of rotations is sensitive to eyeball translation because it changes muscle levers. Eyeball translations are little researched as they are difficult to measure with conventional techniques. Here, we investigated the effects of eyeball translation on the coordination of eyeball rotation by high-speed MRI recordings of saccadic eye movements during blinks, which are known to produce strong translations. We found that saccades during blinks massively overshoot their targets and that these overshoots occur in a transient fashion such that the gaze is back on target at the time the blink ends. These dynamic overshoots were tightly coupled to the eyeball translation, both in time and in size. Saccades made without blinks were also accompanied by small amounts of transient eyeball retraction, the size of which scaled with saccade amplitude. These findings demonstrate a complex combination of rotation and translation of the eye. The mechanical consequences of eyeball translation on oculomotor control should be considered along with the neural implementation in the brainstem to understand the generation of eye movements and their disorders.NEW & NOTEWORTHY We found that saccades during blinks can massively overshoot their target when the eyeball is retracted. Our data imply that the overshoots are not part of the saccade plan prepared in the brainstem, but instead a consequence of the altered biomechanics resulting from concurrent eyeball translation and rotation. To our best knowledge, this is the first direct observation of dynamic properties of the oculomotor plant altering the execution of rotational eye movements.