A role for descending auditory cortical projections in songbird vocal learning

  1. Yael Mandelblat-Cerf  Is a corresponding author
  2. Liora Las
  3. Natalia Denisenko
  4. Michale Fee
  1. McGovern Institute for Brain Research, Massachusetts Institute of Technology, United States

Abstract

Many learned motor behaviors are acquired by comparing ongoing behavior with an internal representation of correct performance, rather than using an explicit external reward. For example, juvenile songbirds learn to sing by comparing their song with the memory of a tutor song. At present, the brain regions subserving song evaluation are not known. Here we report several findings suggesting that song evaluation involves an avian 'cortical' area previously shown to project to the dopaminergic midbrain and other downstream targets. We find that this ventral portion of the intermediate arcopallium (AIV) receives inputs from auditory cortical areas, and that lesions of AIV result in significant deficits in vocal learning. Additionally, AIV neurons exhibit fast responses to disruptive auditory feedback presented during singing, but not during nonsinging periods. Our findings suggest that auditory cortical areas may guide learning by transmitting song evaluation signals to the dopaminergic midbrain and/or other subcortical targets.

Article and author information

Author details

  1. Yael Mandelblat-Cerf

    McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, United States
    For correspondence
    ycerf@bidmc.harvard.edu
    Competing interests
    The authors declare that no competing interests exist.
  2. Liora Las

    McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Natalia Denisenko

    McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Michale Fee

    McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.

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, were reviewed and approved by the Massachusetts Institute of Technology Committee on Animal Care (IACUC). Permit Number: 0712-071-15. Every effort was made to minimize suffering.

Copyright

© 2014, Mandelblat-Cerf 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

  • 4,054
    views
  • 470
    downloads
  • 87
    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. Yael Mandelblat-Cerf
  2. Liora Las
  3. Natalia Denisenko
  4. Michale Fee
(2014)
A role for descending auditory cortical projections in songbird vocal learning
eLife 3:e02152.
https://doi.org/10.7554/eLife.02152

Share this article

https://doi.org/10.7554/eLife.02152

Further reading

    1. Neuroscience
    Gáspár Oláh, Rajmund Lákovics ... Gábor Tamás
    Research Article

    Human-specific cognitive abilities depend on information processing in the cerebral cortex, where the neurons are significantly larger and their processes longer and sparser compared to rodents. We found that, in synaptically connected layer 2/3 pyramidal cells (L2/3 PCs), the delay in signal propagation from soma to soma is similar in humans and rodents. To compensate for the longer processes of neurons, membrane potential changes in human axons and/or dendrites must propagate faster. Axonal and dendritic recordings show that the propagation speed of action potentials (APs) is similar in human and rat axons, but the forward propagation of excitatory postsynaptic potentials (EPSPs) and the backward propagation of APs are 26 and 47% faster in human dendrites, respectively. Experimentally-based detailed biophysical models have shown that the key factor responsible for the accelerated EPSP propagation in human cortical dendrites is the large conductance load imposed at the soma by the large basal dendritic tree. Additionally, larger dendritic diameters and differences in cable and ion channel properties in humans contribute to enhanced signal propagation. Our integrative experimental and modeling study provides new insights into the scaling rules that help maintain information processing speed albeit the large and sparse neurons in the human cortex.