Direct translation of climbing fiber burst-mediated sensory coding into post-synaptic Purkinje cell dendritic calcium

  1. Seung-Eon Roh
  2. Seung Ha Kim
  3. Changhyeon Ryu
  4. Chang-Eop Kim
  5. Yong Gyu Kim
  6. Paul F Worley
  7. Sun Kwang Kim
  8. Sang Jeong Kim  Is a corresponding author
  1. Johns Hopkins University School of Medicine, United States
  2. Seoul National University College of Medicine, Korea (South), Republic of
  3. Gachon University College of Korean Medicine, Republic of Korea
  4. Kyoung Hee University College of Korean Medicine, Republic of Korea
  5. Seoul National University College of Medicine, Republic of Korea

Abstract

Climbing fibers (CFs) generate complex spikes (CS) and Ca2+ transients in cerebellar Purkinje cells (PCs), serving as instructive signals. The so-called 'all-or-none' character of CSs has been questioned since the CF burst was described. Although recent studies have indicated a sensory-driven enhancement of PC Ca2+ signals, how CF responds to sensory events and contributes to PC dendritic Ca2+ and CS remains unexplored. Here, single or simultaneous Ca2+ imaging of CFs and PCs in awake mice revealed the presynaptic CF Ca2+ amplitude encoded the sensory input's strength and directly influenced post-synaptic PC dendritic Ca2+ amplitude. The sensory-driven variability in CF Ca2+ amplitude depended on the number of spikes in the CF burst. Finally, the spike number of the CF burst determined the PC Ca2+ influx and CS properties. These results reveal the direct translation of sensory information-coding CF inputs into PC Ca2+, suggesting the sophisticated role of CFs as error signals.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for Figures 1 through 5. Code has been made available via GitHub at https://github.com/NeuRoh1/Calcium_signal_processing .

Article and author information

Author details

  1. Seung-Eon Roh

    Neuroscience, Johns Hopkins University School of Medicine, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Seung Ha Kim

    Biomedical Sciences, Seoul National University College of Medicine, Seoul, Korea (South), Republic of
    Competing interests
    The authors declare that no competing interests exist.
  3. Changhyeon Ryu

    Physiology, Seoul National University College of Medicine, Seoul, Korea (South), Republic of
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5207-9142
  4. Chang-Eop Kim

    Physiology, Gachon University College of Korean Medicine, Seongnam, Republic of Korea
    Competing interests
    The authors declare that no competing interests exist.
  5. Yong Gyu Kim

    Department of Physiology, Seoul National University College of Medicine, Seoul, Korea (South), Republic of
    Competing interests
    The authors declare that no competing interests exist.
  6. Paul F Worley

    Neuroscience, Johns Hopkins University School of Medicine, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5086-614X
  7. Sun Kwang Kim

    Physiology, Kyoung Hee University College of Korean Medicine, Seoul, Republic of Korea
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2649-6652
  8. Sang Jeong Kim

    Physiology, Seoul National University College of Medicine, Seoul, Republic of Korea
    For correspondence
    sangjkim@snu.ac.kr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8931-3713

Funding

National Research Foundation of Korea (2018R1A5A2025964)

  • Sang Jeong Kim

National Research Foundation of Korea (2017M3C7A1029611)

  • Sang Jeong Kim

National Research Foundation of Korea (2016R1D1A1A02937329)

  • Sun Kwang Kim

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

Ethics

Animal experimentation: This study was performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All of the animals were handled according to approved institutional animal care and use committee (IACUC) protocols (#SNU-111214-6-3) of the Seoul National University. The protocol was approved by the Committee on the Ethics of Animal Experiments of the Seoul National Universtiy. All surgery was performed under intraperitoneal injections of Zoletil/Rompun mixture (30 mg / 10 mg/kg), and every effort was made to minimize suffering.

Reviewing Editor

  1. Megan R Carey, Champalimaud Foundation, Portugal

Publication history

  1. Received: July 30, 2020
  2. Accepted: September 17, 2020
  3. Accepted Manuscript published: September 28, 2020 (version 1)
  4. Version of Record published: October 22, 2020 (version 2)

Copyright

© 2020, Roh 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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  1. Seung-Eon Roh
  2. Seung Ha Kim
  3. Changhyeon Ryu
  4. Chang-Eop Kim
  5. Yong Gyu Kim
  6. Paul F Worley
  7. Sun Kwang Kim
  8. Sang Jeong Kim
(2020)
Direct translation of climbing fiber burst-mediated sensory coding into post-synaptic Purkinje cell dendritic calcium
eLife 9:e61593.
https://doi.org/10.7554/eLife.61593

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