A neural circuit mechanism for regulating vocal variability during song learning in zebra finches

  1. Jonathan Garst-Orozco
  2. Baktash Babadi
  3. Bence P Ölveczky  Is a corresponding author
  1. Harvard University, United States

Abstract

Motor skill learning is characterized by improved performance and reduced motor variability. The neural mechanisms that couple skill level and variability, however, are not known. The zebra finch, a songbird, presents a unique opportunity to address this question because production of learned song and induction of vocal variability are instantiated in separate circuits that converge on a motor cortex analogue controlling vocal output. To probe the interplay between learning and variability, we made intracellular recordings from neurons in this area, characterizing how their inputs from the functionally distinct pathways change throughout song development. We found that inputs that drive stereotyped song-patterns are strengthened and pruned, while inputs that induce variability remain unchanged. A simple network model showed that strengthening and pruning of action-specific connections reduces the sensitivity of motor control circuits to variable input and neural 'noise'. This identifies a simple and general mechanism for learning-related regulation of motor variability.

Article and author information

Author details

  1. Jonathan Garst-Orozco

    Center for Brain Science, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Baktash Babadi

    Center for Brain Science, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Bence P Ölveczky

    Center for Brain Science, Harvard University, Cambridge, United States
    For correspondence
    olveczky@fas.harvard.edu
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Ronald L Calabrese, Emory University, United States

Ethics

Animal experimentation: The 124 male zebra finches (Taeniopygia guttata) used for this study were obtained from our breeding colony. The care and experimental manipulation of the animals were carried out in accordance with guidelines of the National Institutes of Health and were reviewed and approved by the Harvard Institutional Animal Care and Use Committee (Protocol #: 10-09).

Version history

  1. Received: June 15, 2014
  2. Accepted: December 13, 2014
  3. Accepted Manuscript published: December 15, 2014 (version 1)
  4. Version of Record published: January 14, 2015 (version 2)

Copyright

© 2014, Garst-Orozco 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

  • 3,130
    views
  • 434
    downloads
  • 37
    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. Jonathan Garst-Orozco
  2. Baktash Babadi
  3. Bence P Ölveczky
(2014)
A neural circuit mechanism for regulating vocal variability during song learning in zebra finches
eLife 3:e03697.
https://doi.org/10.7554/eLife.03697

Share this article

https://doi.org/10.7554/eLife.03697

Further reading

    1. Genetics and Genomics
    2. Neuroscience
    Bohan Zhu, Richard I Ainsworth ... Javier González-Maeso
    Research Article

    Genome-wide association studies have revealed >270 loci associated with schizophrenia risk, yet these genetic factors do not seem to be sufficient to fully explain the molecular determinants behind this psychiatric condition. Epigenetic marks such as post-translational histone modifications remain largely plastic during development and adulthood, allowing a dynamic impact of environmental factors, including antipsychotic medications, on access to genes and regulatory elements. However, few studies so far have profiled cell-specific genome-wide histone modifications in postmortem brain samples from schizophrenia subjects, or the effect of antipsychotic treatment on such epigenetic marks. Here, we conducted ChIP-seq analyses focusing on histone marks indicative of active enhancers (H3K27ac) and active promoters (H3K4me3), alongside RNA-seq, using frontal cortex samples from antipsychotic-free (AF) and antipsychotic-treated (AT) individuals with schizophrenia, as well as individually matched controls (n=58). Schizophrenia subjects exhibited thousands of neuronal and non-neuronal epigenetic differences at regions that included several susceptibility genetic loci, such as NRG1, DISC1, and DRD3. By analyzing the AF and AT cohorts separately, we identified schizophrenia-associated alterations in specific transcription factors, their regulatees, and epigenomic and transcriptomic features that were reversed by antipsychotic treatment; as well as those that represented a consequence of antipsychotic medication rather than a hallmark of schizophrenia in postmortem human brain samples. Notably, we also found that the effect of age on epigenomic landscapes was more pronounced in frontal cortex of AT-schizophrenics, as compared to AF-schizophrenics and controls. Together, these data provide important evidence of epigenetic alterations in the frontal cortex of individuals with schizophrenia, and remark for the first time on the impact of age and antipsychotic treatment on chromatin organization.

    1. Neuroscience
    Katharina Eichler, Stefanie Hampel ... Andrew M Seeds
    Research Advance

    Mechanosensory neurons located across the body surface respond to tactile stimuli and elicit diverse behavioral responses, from relatively simple stimulus location-aimed movements to complex movement sequences. How mechanosensory neurons and their postsynaptic circuits influence such diverse behaviors remains unclear. We previously discovered that Drosophila perform a body location-prioritized grooming sequence when mechanosensory neurons at different locations on the head and body are simultaneously stimulated by dust (Hampel et al., 2017; Seeds et al., 2014). Here, we identify nearly all mechanosensory neurons on the Drosophila head that individually elicit aimed grooming of specific head locations, while collectively eliciting a whole head grooming sequence. Different tracing methods were used to reconstruct the projections of these neurons from different locations on the head to their distinct arborizations in the brain. This provides the first synaptic resolution somatotopic map of a head, and defines the parallel-projecting mechanosensory pathways that elicit head grooming.