Transitioning between preparatory and precisely sequenced neuronal activity in production of a skilled behavior

  1. Vamsi K Daliparthi
  2. Ryosuke O Tachibana
  3. Brenton G Cooper
  4. Richard HR Hahnloser
  5. Satoshi Kojima
  6. Samuel J Sober
  7. Todd F Roberts  Is a corresponding author
  1. UT Southwestern Medical Center, United States
  2. University of Tokyo, Japan
  3. Texas Christian Unversity, United States
  4. University of Zurich/ETH Zurich, Switzerland
  5. Korea Brain Research Institute, Korea (South), Republic of
  6. Emory University, United States

Abstract

Precise neural sequences are associated with the production of well-learned skilled behaviors. Yet, how neural sequences arise in the brain remains unclear. In songbirds, premotor projection neurons in the cortical song nucleus HVC are necessary for producing learned song and exhibit precise sequential activity during singing. Using cell-type specific calcium imaging we identify populations of HVC premotor neurons associated with the beginning and ending of singing-related neural sequences. We characterize neurons that bookend singing-related sequences and neuronal populations that transition from sparse preparatory activity prior to song to precise neural sequences during singing. Recordings from downstream premotor neurons or the respiratory system suggest that pre-song activity may be involved in motor preparation to sing. These findings reveal population mechanisms associated with moving from non-vocal to vocal behavioral states and suggest that precise neural sequences begin and end as part of orchestrated activity across functionally diverse populations of cortical premotor neurons.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been included for the following main figures: 1F; 2B; 2D; 3G; 3H; 3I; 3J; 4G; 5D; 6B-E. All the data has been compiled into a single excel file, with the corresponding data represented in different sheet tabs. Matlab files used for calcium imaging analysis, specifically for selecting ROIs and filtering calcium traces, have also been included.

Article and author information

Author details

  1. Vamsi K Daliparthi

    Department of Neuroscience, UT Southwestern Medical Center, Dallas, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Ryosuke O Tachibana

    Department of Life Sciences, University of Tokyo, Tokyo, Japan
    Competing interests
    The authors declare that no competing interests exist.
  3. Brenton G Cooper

    Department of Psychology, Texas Christian Unversity, Fort Worth, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Richard HR Hahnloser

    Institute of Neuroinformatics, University of Zurich/ETH Zurich, Zurich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4039-7773
  5. Satoshi Kojima

    Department of Structure and Function of Neural Network, Korea Brain Research Institute, Daegu, Korea (South), Republic of
    Competing interests
    The authors declare that no competing interests exist.
  6. Samuel J Sober

    Department of Biology, Emory University, Atlanta, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1140-7469
  7. Todd F Roberts

    Neuroscience, UT Southwestern Medical Center, Dallas, United States
    For correspondence
    todd.roberts@utsouthwestern.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0967-6598

Funding

National Institute of Neurological Disorders and Stroke (R01NS108424)

  • Todd F Roberts

National Institute on Deafness and Other Communication Disorders (R01DC014364)

  • Todd F Roberts

National Science Foundation (IOS-1457206)

  • Todd F Roberts

Swiss National Science Foundation (31003A_127024)

  • Richard HR Hahnloser

Swiss National Science Foundation (31003A_156976)

  • Richard HR Hahnloser

National Institute of Neurological Disorders and Stroke (R01NS108424)

  • Brenton G Cooper
  • Richard HR Hahnloser
  • Todd F Roberts

National Institute of Neurological Disorders and Stroke (R01NS084844)

  • Samuel J Sober

National Institute of Neurological Disorders and Stroke (R01NS099375)

  • Samuel J Sober

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

Ethics

Animal experimentation: Experiments described in this study were conducted using adult male zebra finches and Bengalese finches ( >90 days post hatch). During experiments, birds were housed individually in sound-attenuating chambers on a 12/12 h day/night schedule and were given ad libitum access to food and water. All procedures were performed in accordance with established protocols approved by Animal Care and Use Committee's at UT Southwestern Medical Centers (2016-101562), Texas Christian University, Emory University, and the Korea Brain Research Institute. Research conducted by our colleagues in Korea was under IACUC-15-00028 and research at Emory was under 2003538.

Reviewing Editor

  1. Erich D Jarvis, The Rockefeller University, United States

Publication history

  1. Received: November 17, 2018
  2. Accepted: June 10, 2019
  3. Accepted Manuscript published: June 11, 2019 (version 1)
  4. Version of Record published: June 25, 2019 (version 2)

Copyright

© 2019, Daliparthi 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. Vamsi K Daliparthi
  2. Ryosuke O Tachibana
  3. Brenton G Cooper
  4. Richard HR Hahnloser
  5. Satoshi Kojima
  6. Samuel J Sober
  7. Todd F Roberts
(2019)
Transitioning between preparatory and precisely sequenced neuronal activity in production of a skilled behavior
eLife 8:e43732.
https://doi.org/10.7554/eLife.43732

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