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The Journal of Neurophysiology Vol. 80 No. 5 November 1998,
pp. 2405-2416
Copyright ©1998 The American Physiological Society
1 Department of Biology, City College, City University of New York, New York 10031; and 2 Regional Primate Research Center and Department of Physiology and Biophysics, University of Washington, Seattle, Washington 98195
Wallman, Josh and Albert F. Fuchs. Saccadic gain modification: visual error drives motor adaptation. J. Neurophysiol. 80: 2405-2416, 1998. The brain maintains the accuracy of saccadic eye movements by adjusting saccadic amplitude relative to the target distance (i.e., saccade gain) on the basis of the performance of recent saccades. If an experimenter surreptitiously moves the target backward during each saccade, thereby causing the eyes to land beyond their targets, saccades undergo a gradual gain reduction. The error signal driving this conventional saccadic gain adaptation could be either visual (the postsaccadic distance of the target from the fovea) or motoric (the direction and size of the corrective saccade that brings the eye onto the back-stepped target). Similarly, the adaptation itself might be a motor adjustment (change in the size of saccade for a given perceived target distance) or a visual remapping (change in the perceived target distance). We studied these possibilities in experiments both with rhesus macaques and with humans. To test whether the error signal is motoric, we used a paradigm devised by Heiner Deubel. The Deubel paradigm differed from the conventional adaptation paradigm in that the backward step that occurred during the saccade was brief, and the target then returned to its original displaced location. This ploy replaced most of the usual backward corrective saccades with forward ones. Nevertheless, saccadic gain gradually decreased over hundreds of trials. Therefore, we conclude that the direction of saccadic gain adaptation is not determined by the direction of corrective saccades. To test whether gain adaptation is a manifestation of a static visual remapping, we decreased the gain of 10° horizontal saccades by conventional adaptation and then tested the gain to targets appearing at retinal locations unused during adaptation. To make the target appear in such "virgin territory," we had it jump first vertically and then 10° horizontally; both jumps were completed and the target spot extinguished before saccades were made sequentially to the remembered target locations. Conventional adaptation decreased the gain of the second, horizontal saccade even though the target was in a nonadapted retinal location. In contrast, the horizontal component of oblique saccades made directly to the same virgin location showed much less gain decrease, suggesting that the adaptation is specific to saccade direction rather than to target location. Thus visual remapping cannot account for the entire reduction of saccadic gain. We conclude that saccadic gain adaptation involves an error signal that is primarily visual, not motor, but that the adaptation itself is primarily motor, not visual.
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