1. Neuroscience
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Inhibition gates supralinear Ca2+ signaling in Purkinje cell dendrites during practiced movements

  1. Michael A Gaffield
  2. Matthew J M Rowan
  3. Samantha B Amat
  4. Hirokazu Hirai
  5. Jason Christie  Is a corresponding author
  1. Max Planck Florida Institute for Neuroscience, United States
  2. Gunma University, Japan
Research Article
  • Cited 13
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Cite this article as: eLife 2018;7:e36246 doi: 10.7554/eLife.36246

Abstract

Motor learning involves neural circuit modifications in the cerebellar cortex, likely through re-weighting of parallel fiber inputs onto Purkinje cells (PCs). Climbing fibers instruct these synaptic modifications when they excite PCs in conjunction with parallel fiber activity, a pairing that enhances climbing fiber-evoked Ca2+ signaling in PC dendrites. In vivo, climbing fibers spike continuously, including during movements when parallel fibers are simultaneously conveying sensorimotor information to PCs. Whether parallel fiber activity enhances climbing fiber Ca2+ signaling during motor behaviors is unknown. In mice, we found that inhibitory molecular layer interneurons (MLIs), activated by parallel fibers during practiced movements, suppressed parallel fiber enhancement of climbing fiber Ca2+ signaling in PCs. Similar results were obtained in acute slices for brief parallel fiber stimuli. Interestingly, more prolonged parallel fiber excitation revealed latent supralinear Ca2+ signaling. Therefore, the balance of parallel fiber and MLI input onto PCs regulates concomitant climbing fiber Ca2+ signaling.

Data availability

All data are included in the manuscript or the source data files.

Article and author information

Author details

  1. Michael A Gaffield

    Max Planck Florida Institute for Neuroscience, Jupiter, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Matthew J M Rowan

    Max Planck Florida Institute for Neuroscience, Jupiter, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Samantha B Amat

    Max Planck Florida Institute for Neuroscience, Jupiter, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Hirokazu Hirai

    Graduate School of Medicine, Gunma University, Maebashi, Japan
    Competing interests
    The authors declare that no competing interests exist.
  5. Jason Christie

    Max Planck Florida Institute for Neuroscience, Jupiter, United States
    For correspondence
    jason.christie@mpfi.org
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0276-2554

Funding

National Institutes of Health (NS083894)

  • Jason Christie

Max Planck Society

  • Jason Christie

Max Planck Florida Institute for Neuroscience

  • Jason Christie

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: Animal procedures were conducted using protocol 15-205 approved by the Institutional Animal Care and Use Committee (IACUC) at Max Planck Florida Institute for Neuroscience.

Reviewing Editor

  1. Jennifer L Raymond, Stanford School of Medicine, United States

Publication history

  1. Received: February 26, 2018
  2. Accepted: August 16, 2018
  3. Accepted Manuscript published: August 17, 2018 (version 1)
  4. Version of Record published: September 3, 2018 (version 2)

Copyright

© 2018, Gaffield et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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