Motor cortex analogue neurons in songbirds utilize Kv3 subunits to generate ultranarrow spikes

  1. Benjamin M Zemel
  2. Alexander A Nevue
  3. Leonardo ES Tavares
  4. Andre Dagostin
  5. Peter V Lovell
  6. Dezhe Z Jin
  7. Claudio V Mello  Is a corresponding author
  8. Henrique von Gersdorff  Is a corresponding author
  1. Oregon Health and Science University, United States
  2. Pennsylvania State University, United States

Abstract

Complex motor skills in vertebrates require specialized upper motor neurons with precise action potential (AP) firing. To examine how diverse populations of upper motor neurons subserve distinct functions and the specific repertoire of ion channels involved, we conducted a thorough study of the excitability of upper motor neurons controlling somatic motor function in the zebra finch. We found that robustus arcopallialis projection neurons (RAPNs), key command neurons for song production, exhibit ultranarrow spikes and higher firing rates compared to neurons controlling non-vocal somatic motor functions (AId neurons). Pharmacological and molecular data indicate that this striking difference is associated with the higher expression in RAPNs of a high threshold, fast-activating voltage-gated K+ channel, Kv3.1 (KCNC1). The spike waveform and Kv3.1 expression in RAPNs mirror properties of Betz cells, specialized upper motor neurons involved in fine digit control in humans and other primates but absent in rodents. Our study thus provides evidence that songbirds and primates have convergently evolved the use of Kv3.1 to ensure precise, rapid AP firing in upper motor neurons controlling fast and complex motor skills.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting file; Source Data files have been provided for all Figures.

Article and author information

Author details

  1. Benjamin M Zemel

    Vollum Institute, Oregon Health and Science University, Portland, United States
    Competing interests
    No competing interests declared.
  2. Alexander A Nevue

    Department of Behavioral Neuroscience, Oregon Health and Science University, Portland, United States
    Competing interests
    No competing interests declared.
  3. Leonardo ES Tavares

    Department of Physics, Pennsylvania State University, University Park, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8642-5186
  4. Andre Dagostin

    Vollum Institute, Oregon Health and Science University, Portland, United States
    Competing interests
    No competing interests declared.
  5. Peter V Lovell

    Department of Behavioral Neuroscience, Oregon Health and Science University, Portland, United States
    Competing interests
    No competing interests declared.
  6. Dezhe Z Jin

    Department of Physics, Pennsylvania State University, University Park, United States
    Competing interests
    No competing interests declared.
  7. Claudio V Mello

    Department of Behavioral Neuroscience, Oregon Health and Science University, Portland, United States
    For correspondence
    melloc@ohsu.edu
    Competing interests
    No competing interests declared.
  8. Henrique von Gersdorff

    Vollum Institute, Oregon Health and Science University, Portland, United States
    For correspondence
    vongersd@ohsu.edu
    Competing interests
    Henrique von Gersdorff, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4404-3307

Funding

National Science Foundation (NSF1456302)

  • Claudio V Mello

National Science Foundation (NSF1645199)

  • Claudio V Mello

National Institutes of Health (GM120464)

  • Claudio V Mello

National Institutes of Health (DC004274)

  • Henrique von Gersdorff

National Institutes of Health (DC012938)

  • Henrique von Gersdorff

National Institutes of Health (AG055378)

  • Benjamin M Zemel

National Science Foundation (NSF2154646)

  • Claudio V Mello
  • Henrique von Gersdorff

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 of the OHSU (IACUC # IP0000146).

Reviewing Editor

  1. John R Huguenard, Stanford University School of Medicine, United States

Publication history

  1. Received: July 19, 2022
  2. Accepted: May 8, 2023
  3. Accepted Manuscript published: May 9, 2023 (version 1)

Copyright

© 2023, Zemel 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. Benjamin M Zemel
  2. Alexander A Nevue
  3. Leonardo ES Tavares
  4. Andre Dagostin
  5. Peter V Lovell
  6. Dezhe Z Jin
  7. Claudio V Mello
  8. Henrique von Gersdorff
(2023)
Motor cortex analogue neurons in songbirds utilize Kv3 subunits to generate ultranarrow spikes
eLife 12:e81992.
https://doi.org/10.7554/eLife.81992

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