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The Journal of Neuroscience, July 19, 2006, 26(29):7741-7755; doi:10.1523/JNEUROSCI.4658-05.2006

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Behavioral/Systems/Cognitive
Complex Spike Activity of Purkinje Cells in the Oculomotor Vermis during Behavioral Adaptation of Monkey Saccades

Robijanto Soetedjo^2,3 and Albert F. Fuchs^1,3

Departments of ¹Physiology and Biophysics, ²Biological Structure, and ³Washington Regional Primate Research Center, University of Washington, Seattle, Washington 98195-7330

Correspondence should be addressed to Dr. Albert F. Fuchs, 1959 NE Pacific Street, HSB I421, Washington Regional Primate Research Center, Box 357330, University of Washington, Seattle, WA 98195-7330. Email: fuchs{at}u.washington.edu

Throughout life, the oculomotor system can correct itself when saccadic eye movements become inaccurate. This adaptation mechanism can be engaged in the laboratory by displacing the target when the saccade toward it is in flight. Forward and backward target displacements cause gradual increases and decreases in saccade amplitude, respectively. Equipped with this paradigm, we asked whether Purkinje cells (P-cells) in the vermis of the oculomotor cerebellum, lobules VIc and VII, changed their complex spike (CS) discharge during the behavioral adaptation of horizontal saccades. We tested the hypothesis that CS activity would change only when a targeting saccade caused an error in eye position relative to the target, i.e., during the error interval between the primary and corrective saccades. We examined only those P-cells whose simple spike activity exhibited either a burst or pause with saccades in several directions. Approximately 80% of such P-cells exhibited an increase in CS activity during the error interval when the adaptation paradigm imposed horizontal eye-position errors in one direction and a decrease in activity for errors in the other. As adaptation progressed and errors were reduced, there was no consistent change in the CS activity. These data suggest that the CS activity of P-cells in the oculomotor vermis signals the direction but not the magnitude of eye-position error during saccade adaptation. Our results are consistent with cerebellar learning models that have been proposed to explain adaptation of the vestibulo-ocular reflex so similar mechanisms may also underlie plasticity of this precision voluntary oculomotor behavior.

Key words: saccades; cerebellum; complex spikes; adaptation; motor learning; climbing fiber

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Received Oct. 31, 2005; revised June 13, 2006; accepted June 14, 2006.

Correspondence should be addressed to Dr. Albert F. Fuchs, 1959 NE Pacific Street, HSB I421, Washington Regional Primate Research Center, Box 357330, University of Washington, Seattle, WA 98195-7330. Email: fuchs{at}u.washington.edu

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