1. Neuroscience

Purkinje cell neurotransmission patterns cerebellar basket cells into zonal modules defined by distinct pinceau sizes

  1. Joy Zhou
  2. Amanda M Brown
  3. Elizabeth P Lackey
  4. Marife Arancillo
  5. Tao Lin
  6. Roy V Sillitoe  Is a corresponding author
  1. Baylor College of Medicine, United States
  2. Texas Children's Hospital, United States
https://doi.org/10.7554/eLife.55569
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Cite this article
  1. Joy Zhou
  2. Amanda M Brown
  3. Elizabeth P Lackey
  4. Marife Arancillo
  5. Tao Lin
  6. Roy V Sillitoe
(2020)
Purkinje cell neurotransmission patterns cerebellar basket cells into zonal modules defined by distinct pinceau sizes
eLife 9:e55569.
https://doi.org/10.7554/eLife.55569
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Abstract

Ramón y Cajal proclaimed the neuron doctrine based on circuit features he exemplified using cerebellar basket cell projections. Basket cells form dense inhibitory plexuses that wrap Purkinje cell somata and terminate as pinceaux at the initial segment of axons. Here, we demonstrate that HCN1, Kv1.1, PSD95 and GAD67 unexpectedly mark patterns of basket cell pinceaux that map onto Purkinje cell functional zones. Using cell-specific genetic tracing with an Ascl1CreERT2 mouse conditional allele, we reveal that basket cell zones comprise different sizes of pinceaux. We tested whether Purkinje cells instruct the assembly of inhibitory projections into zones, as they do for excitatory afferents. Genetically silencing Purkinje cell neurotransmission blocks the formation of sharp Purkinje cell zones and disrupts excitatory axon patterning. The distribution of pinceaux into size-specific zones is eliminated without Purkinje cell GABAergic output. Our data uncover the cellular and molecular diversity of a foundational synapse that revolutionized neuroscience.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files. Source data files have been provided for Figures 2, 4, 6, 7, and 8.

Article and author information

Author details

  1. Joy Zhou

    Pathology and Immunology, Neuroscience, Baylor College of Medicine, Houston, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1731-8800

  2. Amanda M Brown

    Department of Neuroscience, Baylor College of Medicine, Houston, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1484-8972

  3. Elizabeth P Lackey

    Pathology and Immunology, Neuroscience, Baylor College of Medicine, Houston, United States
    Competing interests
    The authors declare that no competing interests exist.

  4. Marife Arancillo

    Pathology and Immunology, Baylor College of Medicine, Houston, United States
    Competing interests
    The authors declare that no competing interests exist.

  5. Tao Lin

    Jan and Dan Duncan Neurological Research Institute, Texas Children's Hospital, Houston, United States
    Competing interests
    The authors declare that no competing interests exist.

  6. Roy V Sillitoe

    Department of Pathology, Department of Neuroscience, Program in Development Disease Models and Therapeutics, Baylor College of Medicine, Houston, United States
    For correspondence
    sillitoe@bcm.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6177-6190

Funding

Baylor College of Medicine

  • Joy Zhou
  • Amanda M Brown
  • Elizabeth P Lackey
  • Marife Arancillo
  • Tao Lin
  • Roy V Sillitoe

Texas Children's Hospital

  • Joy Zhou
  • Amanda M Brown
  • Elizabeth P Lackey
  • Marife Arancillo
  • Tao Lin
  • Roy V Sillitoe

Bachmann-Strauss Dystonia and Parkinson Foundation

  • Roy V Sillitoe

National Center for Research Resources (C06RR029965)

  • Roy V Sillitoe

National Institute of Neurological Disorders and Stroke (R01NS089664,R01NS100874)

  • Roy V Sillitoe

National Ataxia Foundation (Postdoctoral Award)

  • Marife Arancillo

National Institutes of Health (F31NS101891)

  • Amanda M Brown

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

Reviewing Editor

  1. Harry T Orr, University of Minnesota, United States

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 animals were housed in an AALAS-certified facility on a 14hr light cycle. Husbandry, housing, euthanasia, and experimental guidelines were reviewed and approved by the Institutional Animal Care and Use Committee (IACUC) of Baylor College of Medicine (protocol number: AN-5996).

Version history

  1. Received: January 29, 2020
  2. Accepted: September 29, 2020
  3. Accepted Manuscript published: September 29, 2020 (version 1)
  4. Version of Record published: October 15, 2020 (version 2)

Copyright

© 2020, Zhou 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. Joy Zhou
  2. Amanda M Brown
  3. Elizabeth P Lackey
  4. Marife Arancillo
  5. Tao Lin
  6. Roy V Sillitoe
(2020)
Purkinje cell neurotransmission patterns cerebellar basket cells into zonal modules defined by distinct pinceau sizes
eLife 9:e55569.
https://doi.org/10.7554/eLife.55569

Share this article

https://doi.org/10.7554/eLife.55569

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