Neural activity in cortico-basal ganglia circuits of juvenile songbirds encodes performance during goal-directed learning

  1. Jennifer M Achiro
  2. John Shen
  3. Sarah Bottjer  Is a corresponding author
  1. University of Southern California, United States

Abstract

Cortico-basal ganglia circuits are thought to mediate goal-directed learning by a process of outcome evaluation to gradually select appropriate motor actions. We investigated spiking activity in core and shell subregions of the cortical nucleus LMAN during development as juvenile zebra finches are actively engaged in evaluating feedback of self-generated behavior in relation to their memorized tutor song (the goal). Spiking patterns of single neurons in both core and shell subregions during singing correlated with acoustic similarity to tutor syllables, suggesting a process of outcome evaluation. Both core and shell neurons encoded tutor similarity via either increases or decreases in firing rate, although only shell neurons showed a significant association at the population level. Tutor similarity predicted firing rates most strongly during early stages of learning, and shell but not core neurons showed decreases in response variability across development, suggesting that the activity of shell neurons reflects the progression of learning.

Article and author information

Author details

  1. Jennifer M Achiro

    Neuroscience Graduate Program, University of Southern California, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3978-1647
  2. John Shen

    Neuroscience Graduate Program, University of Southern California, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Sarah Bottjer

    Section of Neurobiology, University of Southern California, Los Angeles, United States
    For correspondence
    sarahbottjer@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4365-9166

Funding

NIH Office of the Director (Research grant NS087506)

  • Sarah Bottjer

NIH Office of the Director (Training grant DC009975)

  • Sarah Bottjer

NIH Office of the Director (Training fellowship NS 073323)

  • Jennifer M Achiro

NIH Office of the Director (Research grant 037547)

  • Sarah Bottjer

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

Reviewing Editor

  1. Ronald L Calabrese, Emory University, United States

Ethics

Animal experimentation: All procedures were performed in accordance with Protocol #9159 approved by the University of Southern California Animal Care and Use Committee and in accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health.

Version history

  1. Received: March 19, 2017
  2. Accepted: December 2, 2017
  3. Accepted Manuscript published: December 19, 2017 (version 1)
  4. Version of Record published: January 10, 2018 (version 2)

Copyright

© 2017, Achiro 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.

Metrics

  • 1,926
    views
  • 257
    downloads
  • 15
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Jennifer M Achiro
  2. John Shen
  3. Sarah Bottjer
(2017)
Neural activity in cortico-basal ganglia circuits of juvenile songbirds encodes performance during goal-directed learning
eLife 6:e26973.
https://doi.org/10.7554/eLife.26973

Share this article

https://doi.org/10.7554/eLife.26973

Further reading

    1. Neuroscience
    Annette Pisanski, Mitchell Prostebby ... Silvia Pagliardini
    Research Article

    The lateral parafacial area (pFL) is a crucial region involved in respiratory control, particularly in generating active expiration through an expiratory oscillatory network. Active expiration involves rhythmic abdominal (ABD) muscle contractions during late-expiration, increasing ventilation during elevated respiratory demands. The precise anatomical location of the expiratory oscillator within the ventral medulla’s rostro-caudal axis is debated. While some studies point to the caudal tip of the facial nucleus (VIIc) as the oscillator’s core, others suggest more rostral areas. Our study employed bicuculline (a γ-aminobutyric acid type A [GABA-A] receptor antagonist) injections at various pFL sites (–0.2 mm to +0.8 mm from VIIc) to investigate the impact of GABAergic disinhibition on respiration. These injections consistently elicited ABD recruitment, but the response strength varied along the rostro-caudal zone. Remarkably, the most robust and enduring changes in tidal volume, minute ventilation, and combined respiratory responses occurred at more rostral pFL locations (+0.6/+0.8 mm from VIIc). Multivariate analysis of the respiratory cycle further differentiated between locations, revealing the core site for active expiration generation with this experimental approach. Our study advances our understanding of neural mechanisms governing active expiration and emphasizes the significance of investigating the rostral pFL region.

    1. Neuroscience
    Max Schulz, Malte Wöstmann
    Insight

    Asymmetries in the size of structures deep below the cortex explain how alpha oscillations in the brain respond to shifts in attention.