Effect of eye position on the three-dimensional kinematics of saccadic and vestibular-evoked eye movements

Abstract

Saccadic and vestibular-evoked eye movements are similar in that their three-dimensional kinematic properties show eye position-dependence. When the line of sight is directed towards an eccentric target, the eye velocity axis tilts in a manner that depends on the instantaneous position of the eye in the head, with the magnitude of tilt also depending on whether the eye movement is saccadic or vestibular-evoked. The mechanism responsible for producing eye velocity axis tilting phenomena is not well understood. Some authorities have suggested that muscle pulleys in the orbit are critical for implementing eye velocity axis tilting, while others have suggested that the cerebellum plays an important role. In the current study, three-dimensional eye and head rotation data were acquired, using the magnetic search coil technique, to confirm the presence of eye position-dependent eye velocity axis tilting during saccadic eye movements. Both normal humans and humans with cerebellar atrophy were studied. While the humans with cerebellar atrophy were noted to have abnormalities in the two-dimensional metrics and consistency of their saccadic eye movements, the eye position-dependent eye velocity axis tilts were similar to those observed in the normal subjects. A mathematical model of the human saccadic and vestibular systems was utilized to investigate the means by which these eye position-dependent properties may arise for both types of eye movement. The predictions of the saccadic model were compared with the saccadic data obtained in the current study, while the predictions of the vestibular model were compared with vestibular-evoked eye movement data obtained in a previous study. The results from the model simulations suggest that the muscle pulleys are responsible for bringing about eye position-dependent eye velocity axis tilting for both saccadic and vestibular-evoked eye movements, and that these phenomena are not centrally programmed.