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.

Reviewing Editor

  1. Ronald L Calabrese, Emory University, United States

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.

Version history

  1. Received: December 27, 2013
  2. Accepted: June 12, 2014
  3. Accepted Manuscript published: June 16, 2014 (version 1)
  4. Version of Record published: July 29, 2014 (version 2)

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

  • 4,001
    views
  • 450
    downloads
  • 80
    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
    Ivan Tomić, Paul M Bays
    Research Article

    Probing memory of a complex visual image within a few hundred milliseconds after its disappearance reveals significantly greater fidelity of recall than if the probe is delayed by as little as a second. Classically interpreted, the former taps into a detailed but rapidly decaying visual sensory or ‘iconic’ memory (IM), while the latter relies on capacity-limited but comparatively stable visual working memory (VWM). While iconic decay and VWM capacity have been extensively studied independently, currently no single framework quantitatively accounts for the dynamics of memory fidelity over these time scales. Here, we extend a stationary neural population model of VWM with a temporal dimension, incorporating rapid sensory-driven accumulation of activity encoding each visual feature in memory, and a slower accumulation of internal error that causes memorized features to randomly drift over time. Instead of facilitating read-out from an independent sensory store, an early cue benefits recall by lifting the effective limit on VWM signal strength imposed when multiple items compete for representation, allowing memory for the cued item to be supplemented with information from the decaying sensory trace. Empirical measurements of human recall dynamics validate these predictions while excluding alternative model architectures. A key conclusion is that differences in capacity classically thought to distinguish IM and VWM are in fact contingent upon a single resource-limited WM store.