Oculomotor function in the rhesus monkey after deafferentation of the extraocular muscles

Abstract.

The function of extraocular muscle proprioception in the control of eye movements remains uncertain. In this study, we examined the effect of bilateral proprioceptive deafferentation of the extraocular muscles on eye movements in two rhesus monkeys. Before and after deafferentation, we analyzed baseline ocular alignment, saccades, pursuit, and vestibular eye movements. We also examined visually mediated adaptation of ocular alignment, saccades, and pursuit. Deafferentation of the eye muscles did not affect baseline ocular motor control, either acutely or over a 5-week period of study. Furthermore, visually mediated adaptation of the eye movement subtypes was also unaffected by deafferentation. These results suggest that ocular proprioception in primates is not used in the immediate, on-line control of eye movements and does not interact with visual cues in the adaptive modification of ocular motor function. We conclude that the efferent command (efference copy) provides sufficient information about eye kinematics to the brain for accurate eye movement control in normal monkeys, and that this information is modified by visual feedback independently of proprioception. We hypothesize that proprioception may be used to calibrate the efference copy during development and in response to perturbations by signaling potential mismatches between eye movement information derived from the efferent command and the actual motion of the eye transduced by the proprioceptive organs.