Complexity of frequency receptive fields predicts tonotopic variability across species

Abstract

Primary cortical areas contain maps of sensory features, including sound frequency in primary auditory cortex (A1). Two-photon calcium imaging in mice has confirmed the presence of these global tonotopic maps, while uncovering an unexpected local variability in the stimulus preferences of individual neurons in A1 and other primary regions. Here we show that local heterogeneity of frequency preferences is not unique to rodents. Using two-photon calcium imaging in layers 2/3, we found that local variance in frequency preferences is equivalent in ferrets and mice. Neurons with multipeaked frequency tuning are less spatially organized than those tuned to a single frequency in both species. Furthermore, we show that microelectrode recordings may describe a smoother tonotopic arrangement due to a sampling bias towards neurons with simple frequency tuning. These results help explain previous inconsistencies in cortical topography across species and recording techniques.

Data availability

We have provided our data and Matlab scripts for generating our figures on Dryad: https://doi.org/10.5061/dryad.9ghx3ffd9.

The following data sets were generated

Article and author information

Author details

  1. Quentin Gaucher

    Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford, United Kingdom
    Competing interests
    No competing interests declared.
  2. Mariangela Panniello

    Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford, United Kingdom
    Competing interests
    No competing interests declared.
  3. Aleksandar Z Ivanov

    Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford, United Kingdom
    Competing interests
    No competing interests declared.
  4. Johannes C Dahmen

    Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford, United Kingdom
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9889-8303
  5. Andrew J King

    Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford, United Kingdom
    Competing interests
    Andrew J King, Senior editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5180-7179
  6. Kerry M M Walker

    Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford, United Kingdom
    For correspondence
    kerry.walker@dpag.ox.ac.uk
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1043-5302

Funding

Biotechnology and Biological Sciences Research Council (BB/M010929/1)

  • Kerry M M Walker

University Of Oxford (DPAG Early Career Fellowship)

  • Kerry M M Walker

Wellcome (WT076508AIA)

  • Andrew J King

Wellcome (WT108369/Z/2015/Z)

  • Andrew J King

University Of Oxford (Christopher Welch Scholarship)

  • Aleksandar Z Ivanov

University Of Oxford (Newton-Abraham Scholarship)

  • Mariangela Panniello

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

Reviewing Editor

  1. Brice Bathellier, CNRS, France

Ethics

Animal experimentation: The animal procedures were approved by the University of Oxford Committee on Animal Care and Ethical Review and were carried out under license from the UK Home Office, in accordance with the Animals (Scientific Procedures) Act 1986 and in line with the 3Rs. Project licence PPL 30/3181 and PIL l23DD2122.

Version history

  1. Received: November 8, 2019
  2. Accepted: May 18, 2020
  3. Accepted Manuscript published: May 18, 2020 (version 1)
  4. Version of Record published: June 3, 2020 (version 2)

Copyright

© 2020, Gaucher 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.

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  1. Quentin Gaucher
  2. Mariangela Panniello
  3. Aleksandar Z Ivanov
  4. Johannes C Dahmen
  5. Andrew J King
  6. Kerry M M Walker
(2020)
Complexity of frequency receptive fields predicts tonotopic variability across species
eLife 9:e53462.
https://doi.org/10.7554/eLife.53462

Share this article

https://doi.org/10.7554/eLife.53462

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