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The Journal of Neuroscience, October 13, 2004, 24(41):9035-9048; doi:10.1523/JNEUROSCI.0337-04.2004

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Behavioral/Systems/Cognitive
A Population Decoding Framework for Motion Aftereffects on Smooth Pursuit Eye Movements

Justin L. Gardner, Stefanie N. Tokiyama, and Stephen G. Lisberger

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

Both perceptual and motor systems must decode visual information from the distributed activity of large populations of cortical neurons. We have sought a common framework for understanding decoding strategies for visually guided movement and perception by asking whether the strong motion aftereffects seen in the perceptual domain lead to similar expressions in motor output. We found that motion adaptation indeed has strong sequelae in the direction and speed of smooth pursuit eye movements. After adaptation with a stimulus that moves in a given direction for 7 sec, the direction of pursuit is repelled from the direction of pursuit targets that move within 90° of the adapting direction. The speed of pursuit decreases for targets that move at the direction and speed of the adapting stimulus and is repelled from the adapting speed in the sense that the decrease either becomes greater or smaller (eventually turning to an increase) when tracking targets move slower or faster than the adapting speed. The effects of adaptation are spatially specific and fixed to the retinal location of the adapting stimulus. The magnitude of adaptation of pursuit speed and direction is uncorrelated, suggesting that the two parameters are decoded independently. Computer simulation of motion adaptation in the middle temporal visual area (MT) shows that vector-averaging decoding of the population response in MT can account for the effects of adaptation on the direction of pursuit. Our results suggest a unified framework for thinking, in terms of population decoding, about motion adaptation for both perception and action.

Key words: adaptation; MT; visual motion processing; waterfall illusion; distributed representations; vector averaging

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Received Jan 30, 2004; revised September 2, 2004; accepted September 3, 2004.

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