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Elimination of climbing fiber instructive signals during motor learning

Nature Neuroscience volume 12, pages 1171–1179 (2009)Cite this article

Abstract

The climbing fiber input to the cerebellum from the inferior olive is thought to act as a teacher whose activity controls the induction of motor learning. We designed training conditions that did not elicit instructive signals in the climbing fibers, but nevertheless induced robust and consistent motor learning in the vestibulo-ocular reflex of rhesus monkeys. Our results indicate that instructive signals in the climbing fibers are not necessary for cerebellum-dependent learning. Instead, instructive signals carried by either the climbing fibers or Purkinje cell simple spikes may be sufficient to induce motor learning, with additive effects occurring when both instructive signals are present during training.

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Figure 1: VOR circuit and Marr-Albus-Ito hypothesis for VOR learning.
Figure 2: Climbing fiber responses to standard and novel training stimuli.
Figure 3: Purkinje cell simple spike responses during training.
Figure 4: In the absence of instructive signals in the climbing fibers, learning was correlated with simple spike responses during training.
Figure 5: Purkinje cell simple spike and climbing fiber signals together predict learned behavioral changes.

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Acknowledgements

We thank P. Louderback and R. Levine for technical assistance, and E. Knudsen, D. Angelaki, M. Goldman, D. Fisher, I. Witten, E. Mukamel, A. Katoh, R. Kimpo, B. Nguyen-Vu and S.-L. Shin for their comments on the manuscript. This work was supported by the US National Institutes of Health (grants R01 DC004154 to J.L.R. and F31 DC008078 to M.C.K.), a Howard Hughes Medical Institute fellowship for Medical Students and the Stanford Medical Scientist Training Program to M.C.K. and a Stanford Graduate Fellowship to C.C.G.

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Author notes

  1. Michael C Ke and Cong C Guo: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Neurobiology, Stanford University School of Medicine, Stanford, California, USA

    Michael C Ke, Cong C Guo & Jennifer L Raymond

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  1. Michael C Ke
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  2. Cong C Guo
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Contributions

M.C.K. and C.C.G. performed the experiments and analyzed data. M.C.K., C.C.G. and J.L.R. wrote the manuscript. J.L.R. provided guidance throughout the project.

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Correspondence to Jennifer L Raymond.

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Supplementary Figures 1–7 and Supplementary Table 1 (PDF 1177 kb)

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Ke, M., Guo, C. & Raymond, J. Elimination of climbing fiber instructive signals during motor learning. Nat Neurosci 12, 1171–1179 (2009). https://doi.org/10.1038/nn.2366

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