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.

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.

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. 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

Share this article

https://doi.org/10.7554/eLife.84760

Further reading

    1. Neuroscience
    2. Physics of Living Systems
    Moritz Schloetter, Georg U Maret, Christoph J Kleineidam
    Research Article

    Neurons generate and propagate electrical pulses called action potentials which annihilate on arrival at the axon terminal. We measure the extracellular electric field generated by propagating and annihilating action potentials and find that on annihilation, action potentials expel a local discharge. The discharge at the axon terminal generates an inhomogeneous electric field that immediately influences target neurons and thus provokes ephaptic coupling. Our measurements are quantitatively verified by a powerful analytical model which reveals excitation and inhibition in target neurons, depending on position and morphology of the source-target arrangement. Our model is in full agreement with experimental findings on ephaptic coupling at the well-studied Basket cell-Purkinje cell synapse. It is able to predict ephaptic coupling for any other synaptic geometry as illustrated by a few examples.

    1. Neuroscience
    Sven Ohl, Martin Rolfs
    Research Article

    Detecting causal relations structures our perception of events in the world. Here, we determined for visual interactions whether generalized (i.e. feature-invariant) or specialized (i.e. feature-selective) visual routines underlie the perception of causality. To this end, we applied a visual adaptation protocol to assess the adaptability of specific features in classical launching events of simple geometric shapes. We asked observers to report whether they observed a launch or a pass in ambiguous test events (i.e. the overlap between two discs varied from trial to trial). After prolonged exposure to causal launch events (the adaptor) defined by a particular set of features (i.e. a particular motion direction, motion speed, or feature conjunction), observers were less likely to see causal launches in subsequent ambiguous test events than before adaptation. Crucially, adaptation was contingent on the causal impression in launches as demonstrated by a lack of adaptation in non-causal control events. We assessed whether this negative aftereffect transfers to test events with a new set of feature values that were not presented during adaptation. Processing in specialized (as opposed to generalized) visual routines predicts that the transfer of visual adaptation depends on the feature similarity of the adaptor and the test event. We show that the negative aftereffects do not transfer to unadapted launch directions but do transfer to launch events of different speeds. Finally, we used colored discs to assign distinct feature-based identities to the launching and the launched stimulus. We found that the adaptation transferred across colors if the test event had the same motion direction as the adaptor. In summary, visual adaptation allowed us to carve out a visual feature space underlying the perception of causality and revealed specialized visual routines that are tuned to a launch’s motion direction.