Development of frequency tuning shaped by spatial cue reliability in the barn owl's auditory midbrain

  1. Keanu Shadron  Is a corresponding author
  2. José Luis Peña
  1. Albert Einstein College of Medicine, United States

Abstract

Sensory systems preferentially strengthen responses to stimuli based on their reliability at conveying accurate information. While previous reports demonstrate that the brain reweighs cues based on dynamic changes in reliability, how the brain may learn and maintain neural responses to sensory statistics expected to be stable over time is unknown. The barn owl's midbrain features a map of auditory space where neurons compute horizontal sound location from the interaural time difference (ITD). Frequency tuning of midbrain map neurons correlates with the most reliable frequencies for the neurons' preferred ITD. Removal of the facial ruff led to a specific decrease in the reliability of high frequencies from frontal space. To directly test if permanent changes in ITD reliability drive frequency tuning, midbrain map neurons were recorded from adult owls, with the facial ruff removed during development, and juvenile owls, before facial ruff development. In both groups, frontally-tuned neurons were tuned to frequencies lower than in normal adult owls, consistent with the change in ITD reliability. In addition, juvenile owls exhibited more heterogeneous frequency tuning, suggesting normal developmental processes refine tuning to match ITD reliability. These results indicate causality of long-term statistics of spatial cues in the development of midbrain frequency tuning properties, implementing probabilistic coding for sound localization.

Data availability

All data and original code used in this paper is publicly available at https://doi.org/10.12751/g-node.p52i4s.Shadron K, Peña JL (2022) Shadron_Pena_2022. G-Node. https://gin.g-node.org/penalab/Shadron_Pena_2022.

Article and author information

Author details

  1. Keanu Shadron

    Dominick P Purpura Department of Neuroscience, Albert Einstein College of Medicine, Bronx, United States
    For correspondence
    keanu.shadron@einsteinmed.org
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5217-9282
  2. José Luis Peña

    Dominick P Purpura Department of Neuroscience, Albert Einstein College of Medicine, Bronx, United States
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Institute on Deafness and Other Communication Disorders (F31DC019303)

  • Keanu Shadron

National Institute on Deafness and Other Communication Disorders (R01DC007690)

  • José Luis Peña

National Institute of Neurological Disorders and Stroke (R01NS104911)

  • José Luis Peña

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

Ethics

Animal experimentation: All procedures complied with the National Institute of Health guidelines and were approved by the institutional animal care and use committee of the Albert Einstein College of Medicine (00001189). All surgeries were performed under ketamine/xylazine to minimize suffering. The trimming of facial ruff feathers were painless and did not require anesthetics. No experiments were terminal.

Reviewing Editor

  1. Andrew J King, University of Oxford, United Kingdom

Publication history

  1. Received: November 8, 2022
  2. Accepted: May 10, 2023
  3. Accepted Manuscript published: May 11, 2023 (version 1)

Copyright

© 2023, Shadron & Peña

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. Keanu Shadron
  2. José Luis Peña
(2023)
Development of frequency tuning shaped by spatial cue reliability in the barn owl's auditory midbrain
eLife 12:e84760.
https://doi.org/10.7554/eLife.84760

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