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Links from complex spikes to local plasticity and motor learning in the cerebellum of awake-behaving monkeys

Nature Neuroscience volume 11, pages 1185–1192 (2008)Cite this article

A Corrigendum to this article was published on 01 June 2009

This article has been updated

Abstract

The hypothesis of cerebellar learning proposes that complex spikes in Purkinje cells engage mechanisms of plasticity in the cerebellar cortex; in turn, changes in the cerebellum depress the simple-spike response of Purkinje cells to a given stimulus and cause the adaptive modification of a motor behavior. Many elements of this hypothesis have been supported by prior experiments, and correlations have been found between complex spikes, simple-spike plasticity and behavior during the learning process. We carried out a trial-by-trial analysis of Purkinje cell responses in awake-behaving monkeys and found evidence for a causal role for complex spikes in the induction of cerebellar plasticity during a simple motor learning task. We found that the presence of a complex spike on one learning trial was linked to a substantial depression of simple-spike responses on the subsequent trial, at a time when behavioral learning was expressed.

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Figure 1: Example trials showing the target motions used to instruct and probe directional learning in pursuit eye movements.
Figure 2: Effects of learning on responses of one Purkinje cell.
Figure 3: Relationship between complex-spike probability in learning trials and learned simple-spike response in probe trials for group 1 and group 2 Purkinje cells.
Figure 4: Quantitative relationship between complex-spike probability in learning trials and learned changes in simple-spike activity in probe trials.
Figure 5: Time courses of complex spike–related instructive signals and learned changes in eye velocity and simple-spike responses.
Figure 6: Neural and behavioral learning after single complex spikes emitted during off-direction learning trials.
Figure 7: Neural and behavioral learning after single complex spikes were emitted at the offset of target motion in on-direction learning trials.

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Change history

  • 15 January 2009

    In the version of this article initially published, two citations were inadvertently omitted. To correct this, the following two sentences were added to the second paragraph of the introduction, following the sixth sentence. "One line of work has supported the theory by demonstrating that arm movement errors evoke complex spikes51,52 and that subsequent learned changes in motor behavior are associated with suitable changes in simple spike responses51. This work demonstrates a strong correlation, but stops short of showing cause-and-effect links between individual complex spikes, changes in simple spikes and behavioral learning." Two references were also added to the reference list as follows: “51. Gilbert, P.F. & Thach W.T. Purkinje cell activity during motor learning. Brain Res. 128, 309–328 (1977). 52. Ojakangas C.L & Ebner T.J. Purkinje cell complex and simple spike changes during a voluntary arm movement learning task in the monkey. J. Neurophysiol. 68, 2222–2236 (1992)." The error has been corrected in the HTML and PDF versions of the article.

  • 30 April 2009

    The second sentence of the abstract should read “Many elements of this hypothesis have been supported by prior experiments, and correlations have been found between complex spikes, simple-spike plasticity and behavior during the learning process."

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Acknowledgements

This work was supported by the Howard Hughes Medical Institute and by US National Institutes of Health grant P50 MH77970.

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Authors and Affiliations

  1. Department of Psychology, University of Pennsylvania, 3720 Walnut Street, Philadelphia, 19104, Pennsylvania, USA

    Javier F Medina

  2. and Department of Physiology, Howard Hughes Medical Institute, W. M. Keck Foundation Center for Integrative Neuroscience, University of California San Francisco, 513 Parnassus Avenue, San Francisco, 94143, California, USA

    Stephen G Lisberger

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  1. Javier F Medina
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Contributions

J.F.M. conducted recordings from the floccular complex and analyzed data. J.F.M. and S.G.L. wrote the manuscript. S.G.L. provided advice, guidance and suggestions throughout.

Corresponding author

Correspondence to Stephen G Lisberger.

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Medina, J., Lisberger, S. Links from complex spikes to local plasticity and motor learning in the cerebellum of awake-behaving monkeys. Nat Neurosci 11, 1185–1192 (2008). https://doi.org/10.1038/nn.2197

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