Adaptive response to ocular muscle weakness in human pursuit and saccadic eye movements

Abstract

Eye movement deficits caused by ocular muscle weakness vary according to the position of the eye in the orbit and the direction of eye movement. We studied the ability of both the saccadic and pursuit eye-movement systems to compensate for these anisotropic deficits in four patients with ocular muscle weakness. The eye-position dependence of each patient's motor deficit was characterized by plotting the position of the weak eye against that of the normal eye (in various orbital positions) when fusion was prevented, thus giving a static eye-position curve from which relative muscle strength could be inferred. Movements of the weak eye were smaller and slower than those made by the normal eye, so that the weak eye required more time to acquire a visual target. When patients were forced to view monocularly with their weak eye for several days, both the saccadic and pursuit systems showed changes in the movements of the normal eye consistent with an increased central innervation designed to decrease the time it takes to bring the target's image onto the fovea of the weak eye and to keep it there. These adaptive changes varied with eye position and movement direction and compensated for the weak muscle in both its agonistic and antagonistic actions. Saccadic adaptation consisted of a change in the relationship between saccadic amplitude and retinal error (distance between the target's image and the fovea) to compensate for hypometria (undershoot) and a readjustment of the ratio of the phasic (pulse) and tonic (step) components of the saccadic innervation to suppress postsaccadic ocular drift. Pursuit adaptation consisted of an increase in the relationship between eye acceleration and the rate of motion of the image of the target on the retina during the initial phase of tracking as well as an increase in the velocity during tracking of a target moving at a constant velocity. These changes reflect an increase in pursuit innervation that would cause the weak eye's velocity to approach target velocity sooner. The average acceleration of the normal eye during the initial period of tracking (130 ms) increased by as much as threefold. The corresponding maximum smooth eye velocity increased so that, for example, the pursuit response to a 15 degree/s target movement could be over 50 degree/s in the normal eye.