Across-species differences in pitch perception are consistent with differences in cochlear filtering

  1. Kerry M M Walker  Is a corresponding author
  2. Ray Gonzalez
  3. Joe Zhengyu Kang
  4. Josh H McDermott
  5. Andrew J King
  1. University of Oxford, United Kingdom
  2. Massachusetts Institute of Technology, United States

Abstract

Pitch perception is critical for recognizing speech, music and animal vocalizations, but its neurobiological basis remains unsettled, in part because of divergent results across species. We investigated whether species-specific differences exist in the cues used to perceive pitch and whether these can be accounted for by differences in the auditory periphery. Ferrets accurately generalized pitch discriminations to untrained stimuli whenever temporal envelope cues were robust in the probe sounds, but not when resolved harmonics were the main available cue. By contrast, human listeners exhibited the opposite pattern of results on an analogous task, consistent with previous studies. Simulated cochlear responses in the two species suggest that differences in the relative salience of the two pitch cues can be attributed to differences in cochlear filter bandwidths. The results support the view that cross-species variation in pitch perception reflects the constraints of estimating a sound’s fundamental frequency given species-specific cochlear tuning.

Data availability

All psychophysical data and stimuli for this study have been uploaded to Dryad doi:10.5061/dryad.95j80kv).

The following data sets were generated

Article and author information

Author details

  1. 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
  2. Ray Gonzalez

    Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    No competing interests declared.
  3. Joe Zhengyu Kang

    Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford, United Kingdom
    Competing interests
    No competing interests declared.
  4. Josh H McDermott

    Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    No competing interests declared.
  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

Funding

Wellcome (Principal Research Fellowship WT076508AIA)

  • Andrew J King

Wellcome (Enhancement Award)

  • Josh H McDermott
  • Andrew J King

James S McDonnell Foundation (Scholar Award)

  • Josh H McDermott

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

  • Kerry M M Walker

University Of Oxford (DPAG Early Career Fellowship)

  • Kerry M M Walker

Wellcome (Principal Research Fellowship WT108369/Z/2015/Z)

  • Andrew J King

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

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.

Human subjects: Informed consent was obtained from human participants. Consent to publish was not required, as there is no identifying information present in the manuscript. All experimental procedures on humans were approved by the Committee on the Use of Humans as Experimental Subjects at MIT (Protocol 1208005210).

Reviewing Editor

  1. Catherine Emily Carr, University of Maryland, United States

Publication history

  1. Received: September 1, 2018
  2. Accepted: March 14, 2019
  3. Accepted Manuscript published: March 15, 2019 (version 1)
  4. Version of Record published: March 26, 2019 (version 2)

Copyright

© 2019, Walker 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. Kerry M M Walker
  2. Ray Gonzalez
  3. Joe Zhengyu Kang
  4. Josh H McDermott
  5. Andrew J King
(2019)
Across-species differences in pitch perception are consistent with differences in cochlear filtering
eLife 8:e41626.
https://doi.org/10.7554/eLife.41626

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