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Signals That Modulate Gain Control for Smooth Pursuit Eye Movements in Monkeys

² Howard Hughes Medical Institute, Department of Physiology, W. M. Keck Foundation Center for Integrative Neuroscience, and Neuroscience Graduate Program, University of California, San Francisco, California 94143-0444 ¹ Department of Physiology, W. M. Keck Foundation Center for Integrative Neuroscience, and Neuroscience Graduate Program, University of California, San Francisco, California 94143-0444

Submitted 30 May 2003; accepted in final form 10 October 2003

The generation of primate smooth pursuit eye movements involves two processes. One process transforms the direction and speed of target motion into a motor command and the other regulates the strength, or "gain," of the visual-motor transformation. We have conducted a behavioral analysis to identify the signals that modulate the internal gain of pursuit. To test whether the modulatory signals are related to eye velocity in the orbit or in the world (gaze velocity), we used brief perturbations of target motion to probe the gain of pursuit during tracking conditions that used head rotation to dissociate eye and gaze velocity. We found that the responses to perturbations varied primarily as a function of gaze velocity. To further understand the gaze velocity signals that control internal pursuit gain, we used adaptive modification of the gain of the vestibulo-ocular reflex (VOR) to dissociate physical gaze velocity from the component of gaze velocity that is driven by visual inputs. After VOR adaptation, perturbation responses were altered; the smallest perturbation responses now occurred during tracking conditions that required nonzero physical gaze velocity. However, perturbation responses during tracking conditions that mimicked the modified VOR were still enhanced relative to those obtained during fixation. We conclude that the signals that modulate the internal gain of pursuit are modified by VOR adaptation so that they are rendered intermediate between physical and visually driven gaze velocity. Similar changes in the gaze velocity signal have been reported in the cerebellar floccular complex following adaptive modification of the VOR and could be present in other brain areas that carry putative gaze velocity signals.

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