Motor context dominates output from Purkinje cell functional regions during reflexive visuomotor behaviours

  1. Laura D Knogler
  2. Andreas M Kist
  3. Ruben Portugues  Is a corresponding author
  1. Max Planck Institute of Neurobiology, Germany

Abstract

The cerebellum integrates sensory stimuli and motor actions to enable smooth coordination and motor learning. Here we harness the innate behavioral repertoire of the larval zebrafish to characterize the spatiotemporal dynamics of feature coding across the entire Purkinje cell population during visual stimuli and the reflexive behaviors that they elicit. Population imaging reveals three spatially-clustered regions of Purkinje cell activity along the rostrocaudal axis. Complementary single-cell electrophysiological recordings assign these Purkinje cells to one of three functional phenotypes that encode a specific visual, and not motor, signal via complex spikes. In contrast, simple spike output of most Purkinje cells is strongly driven by motor-related tail and eye signals. Interactions between complex and simple spikes show heterogeneous modulation patterns across different Purkinje cells, which become temporally restricted during swimming episodes. Our findings reveal how sensorimotor information is encoded by individual Purkinje cells and organized into behavioral modules across the entire cerebellum.

Data availability

Example electrophysiological datasets are available at https://zenodo.org/record/1494071. An example imaging dataset is available at https://zenodo.org/record/1638807. MATLAB code for electrophysiological analysis available via GitHub (https://github.com/portugueslab/Knogler_etal_2019_eLife

Article and author information

Author details

  1. Laura D Knogler

    Research Group of Sensorimotor Control, Max Planck Institute of Neurobiology, Martinsried, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Andreas M Kist

    Research Group of Sensorimotor Control, Max Planck Institute of Neurobiology, Martinsried, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Ruben Portugues

    Research Group of Sensorimotor Control, Max Planck Institute of Neurobiology, Martinsried, Germany
    For correspondence
    rportugues@neuro.mpg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1495-9314

Funding

Alexander von Humboldt-Stiftung

  • Laura D Knogler

Carl von Siemens Foundation

  • Laura D Knogler

Fonds de Recherche du Québec - Santé

  • Laura D Knogler

Max Planck Gesellschaft (Open-access funding)

  • Laura D Knogler
  • Andreas M Kist
  • Ruben Portugues

International Max Planck Research School for Life Sciences

  • Andreas M Kist

Joachim Herz Stiftung

  • Andreas M Kist

Deutsche Forschungsgemeinschaft (PO 2105/2-1)

  • Laura D Knogler
  • Andreas M Kist
  • Ruben Portugues

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

Reviewing Editor

  1. Indira M Raman, Northwestern University, United States

Ethics

Animal experimentation: All procedures involving animals were in accordance with the Max Planck Society guidelines and approved by the Regierung von Oberbayern (TVA# 55-2-1-54-2532-82-2016)

Version history

  1. Received: September 18, 2018
  2. Accepted: December 26, 2018
  3. Accepted Manuscript published: January 25, 2019 (version 1)
  4. Version of Record published: February 13, 2019 (version 2)

Copyright

© 2019, Knogler 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. Laura D Knogler
  2. Andreas M Kist
  3. Ruben Portugues
(2019)
Motor context dominates output from Purkinje cell functional regions during reflexive visuomotor behaviours
eLife 8:e42138.
https://doi.org/10.7554/eLife.42138

Share this article

https://doi.org/10.7554/eLife.42138

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