Accelerated redevelopment of vocal skills is preceded by lasting reorganization of the song motor circuitry

  1. Michiel Vellema  Is a corresponding author
  2. Mariana Diales Rocha
  3. Sabrina Bascones
  4. Sándor Zsebők
  5. Jes Dreier
  6. Stefan Leitner
  7. Annemie Van der Linden
  8. Jonathan Brewer
  9. Manfred Gahr
  1. Max Planck Institute for Ornithology, Germany
  2. Institut Hospital del Mar d'Investigacions Mèdiques (IMIM), Spain
  3. Eötvös Loránd University, Hungary
  4. University of Southern Denmark, Denmark
  5. University of Antwerp, Belgium

Abstract

Complex motor skills take considerable time and practice to learn. Without continued practice the level of skill performance quickly degrades, posing a problem for the timely utilization of skilled motor behaviors. Here we quantified the recurring development of vocal motor skills and the accompanying changes in synaptic connectivity in the brain of a songbird, while manipulating skill performance by consecutively administrating and withdrawing testosterone. We demonstrate that a songbird with prior singing experience can significantly accelerate the re-acquisition of vocal performance. We further demonstrate that an increase in vocal performance is accompanied by a pronounced synaptic pruning in the forebrain vocal motor area HVC, a reduction that is not reversed when birds stop singing. These results provide evidence that lasting synaptic changes in the motor circuitry are associated with the savings of motor skills, enabling a rapid recovery of motor performance under environmental time constraints.

Data availability

SQL data of extracted song features for each individual have been deposited in Dryad.Further source data files have been provided for Figure 2, Figure 2 -figure supplement 1, Figure 3, Figure 3 -figure supplement 1, Figure 4, Figure 4 -figure supplement 1, Figure 4 -figure supplement 2, Figure 5.

The following data sets were generated

Article and author information

Author details

  1. Michiel Vellema

    Department of Behavioural Neurobiology, Max Planck Institute for Ornithology, Seewiesen, Germany
    For correspondence
    vellema@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7172-4776
  2. Mariana Diales Rocha

    Department of Behavioural Neurobiology, Max Planck Institute for Ornithology, Seewiesen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Sabrina Bascones

    Program for Inflammatory and Cardiovascular Disorders, Institut Hospital del Mar d'Investigacions Mèdiques (IMIM), Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  4. Sándor Zsebők

    Department of Systematic Zoology and Ecology, Eötvös Loránd University, Budapest, Hungary
    Competing interests
    The authors declare that no competing interests exist.
  5. Jes Dreier

    Department of Biochemistry and Molecular Biology, University of Southern Denmark, Odense, Denmark
    Competing interests
    The authors declare that no competing interests exist.
  6. Stefan Leitner

    Department of Behavioural Neurobiology, Max Planck Institute for Ornithology, Seewiesen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9482-0362
  7. Annemie Van der Linden

    Bio Imaging Lab, University of Antwerp, Antwerp, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  8. Jonathan Brewer

    Department of Biochemistry and Molecular Biology, University of Southern Denmark, Odense, Denmark
    Competing interests
    The authors declare that no competing interests exist.
  9. Manfred Gahr

    Department of Behavioural Neurobiology, Max Planck Institute for Ornithology, Seewiesen, Germany
    Competing interests
    The authors declare that no competing interests exist.

Funding

Horizon 2020 Framework Programme (701660)

  • Michiel Vellema

National Research, Development and Innovation Office Hungary (K-115970)

  • Sándor Zsebők

Interuniversity Attraction Poles (IUAP-NIMI-P6/38)

  • Annemie Van der Linden

Max-Planck-Gesellschaft

  • Manfred Gahr

National Research, Development and Innovation Office Hungary (K-129215)

  • Sándor Zsebők

National Research, Development and Innovation Office Hungary (PD-115730)

  • Sándor Zsebők

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

Ethics

Animal experimentation: Experimental procedures were conducted according to the guidelines of the Federation of European Animal Science Associations (FELASA) and approved by the Ethical Committee on animal experiments of the University of Antwerp (protocol number: 2007-14) .

Reviewing Editor

  1. Richard B Ivry, University of California, Berkeley, United States

Publication history

  1. Received: October 29, 2018
  2. Accepted: May 16, 2019
  3. Accepted Manuscript published: May 17, 2019 (version 1)
  4. Version of Record published: June 14, 2019 (version 2)

Copyright

© 2019, Vellema 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. Michiel Vellema
  2. Mariana Diales Rocha
  3. Sabrina Bascones
  4. Sándor Zsebők
  5. Jes Dreier
  6. Stefan Leitner
  7. Annemie Van der Linden
  8. Jonathan Brewer
  9. Manfred Gahr
(2019)
Accelerated redevelopment of vocal skills is preceded by lasting reorganization of the song motor circuitry
eLife 8:e43194.
https://doi.org/10.7554/eLife.43194
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