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J Neurophysiol 87: 2936-2945, 2002;
0022-3077/02 $5.00
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The Journal of Neurophysiology Vol. 87 No. 6 June 2002, pp. 2936-2945
Copyright ©2002 by the American Physiological Society

Gain Control in Human Smooth-Pursuit Eye Movements

Anne K. Churchland and Stephen G. Lisberger

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

Churchland, Anne K. and Stephen G. Lisberger. Gain Control in Human Smooth-Pursuit Eye Movements. J. Neurophysiol. 87: 2936-2945, 2002. In previous experiments, on-line modulation of the gain of visual-motor transmission for pursuit eye movements was demonstrated in monkeys by showing that the response to a brief perturbation of target motion was strongly enhanced during pursuit relative to during fixation. The present paper elaborates the properties of on-line gain control by recording the smooth-pursuit eye movements of human subjects during tracking of a spot target. When perturbations consisted of one cycle of a 5-Hz sine wave, responses were significantly larger during pursuit than during fixation. Furthermore, responses grew as a function of eye/target velocity at the time of the perturbation and of perturbation amplitude. Thus human pursuit, like monkey pursuit, is modulated by on-line gain control. For larger perturbations consisting of a single sine wave at 2.8 Hz, ±19°/s, the degree of enhancement depended strongly on the phase of the perturbation. Enhancement was present when "peak-first" perturbations caused the target speed to increase first and was attenuated when "peak-last" perturbations caused target speed to decrease first. This effect was most profound when the perturbation was 2.8 Hz, ±19°/s but was also present when the amplitude of the peak-last perturbation was ±5o/s. For peak-last perturbations, the eye velocity evoked by the later peak of the perturbation was inversely related to that evoked by the preceding trough of the perturbation. We interpret these effects of perturbation phase as evidence that peak-last perturbations cause a decrease in the on-line gain of visual-motor transmission for pursuit. We conclude that gain control is modulated dynamically as behavioral conditions change. Finally, when perturbations were presented as a sequence of three large, peak-last sine waves starting at the onset of target motion at 10°/s, repeating the conditions used in prior studies on humans, we were able to replicate the prior finding that the response to the perturbations was equal during pursuit and fixation. We conclude that on-line gain control modulates human pursuit and that it can be probed most reliably with small, brief perturbations that do not affect the on-line gain themselves.




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