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Research ArticleResearch Article: New Research, Cognition and Behavior

Fast Periodic Auditory Stimulation Reveals a Robust Categorical Response to Voices in the Human Brain

Francesca M. Barbero, Roberta P. Calce, Siddharth Talwar, Bruno Rossion and Olivier Collignon
eNeuro 20 May 2021, 8 (3) ENEURO.0471-20.2021; DOI: https://doi.org/10.1523/ENEURO.0471-20.2021
Francesca M. Barbero
1Institute of Research in Psychology and Institute of Neuroscience, Louvain Bionics Center, University of Louvain, Louvain-la-Neuve 1348, Belgium
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Roberta P. Calce
1Institute of Research in Psychology and Institute of Neuroscience, Louvain Bionics Center, University of Louvain, Louvain-la-Neuve 1348, Belgium
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Siddharth Talwar
1Institute of Research in Psychology and Institute of Neuroscience, Louvain Bionics Center, University of Louvain, Louvain-la-Neuve 1348, Belgium
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Bruno Rossion
1Institute of Research in Psychology and Institute of Neuroscience, Louvain Bionics Center, University of Louvain, Louvain-la-Neuve 1348, Belgium
2Université de Lorraine, Centre National de la Recherche Scientifique, Centre de Recherche en Automatique de Nancy, Nancy F-54000, France
3Université de Lorraine, Service de Neurologie, Centre Hospitalier Régional et Universitaire-Nancy F-54000, France
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Olivier Collignon
1Institute of Research in Psychology and Institute of Neuroscience, Louvain Bionics Center, University of Louvain, Louvain-la-Neuve 1348, Belgium
4Center for Mind/Brain Sciences, University of Trento, Rovereto 38068, Italy
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Abstract

Voices are arguably among the most relevant sounds in humans’ everyday life, and several studies have suggested the existence of voice-selective regions in the human brain. Despite two decades of research, defining the human brain regions supporting voice recognition remains challenging. Moreover, whether neural selectivity to voices is merely driven by acoustic properties specific to human voices (e.g., spectrogram, harmonicity), or whether it also reflects a higher-level categorization response is still under debate. Here, we objectively measured rapid automatic categorization responses to human voices with fast periodic auditory stimulation (FPAS) combined with electroencephalography (EEG). Participants were tested with stimulation sequences containing heterogeneous non-vocal sounds from different categories presented at 4 Hz (i.e., four stimuli/s), with vocal sounds appearing every three stimuli (1.333 Hz). A few minutes of stimulation are sufficient to elicit robust 1.333 Hz voice-selective focal brain responses over superior temporal regions of individual participants. This response is virtually absent for sequences using frequency-scrambled sounds, but is clearly observed when voices are presented among sounds from musical instruments matched for pitch and harmonicity-to-noise ratio (HNR). Overall, our FPAS paradigm demonstrates that the human brain seamlessly categorizes human voices when compared with other sounds including musical instruments’ sounds matched for low level acoustic features and that voice-selective responses are at least partially independent from low-level acoustic features, making it a powerful and versatile tool to understand human auditory categorization in general.

  • auditory cortex
  • electroencephalography
  • frequency tagging
  • voice

Footnotes

  • The authors declare no competing financial interests.

  • This work was supported in part by the European Research Council Grant Mapping the Deprived Visual System (MADVIS): Cracking function for Prediction (Project: 337573, ERC-20130StG; to O.C.), the Belgian Excellence of Science (EOS) Program (Project: 30991544; partly to O.C. and B.R.), and by the Fonds de la Recherche Scientifique-FNRS Mandate d’Impulsion Scientifique (to O.C.). F.M.B. is a Research Fellow of the Fonds de la Recherche Scientifique - FNRS, R.P.C. is a FRIA grantee of the Fonds de la Recherche Scientifique-FNRS, S.T. is a PhD student supported by a Louvain Cooperation Grant, and O.C. is a Research Associate of the Fonds de la Recherche Scientifique-FNRS.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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Fast Periodic Auditory Stimulation Reveals a Robust Categorical Response to Voices in the Human Brain
Francesca M. Barbero, Roberta P. Calce, Siddharth Talwar, Bruno Rossion, Olivier Collignon
eNeuro 20 May 2021, 8 (3) ENEURO.0471-20.2021; DOI: 10.1523/ENEURO.0471-20.2021

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Fast Periodic Auditory Stimulation Reveals a Robust Categorical Response to Voices in the Human Brain
Francesca M. Barbero, Roberta P. Calce, Siddharth Talwar, Bruno Rossion, Olivier Collignon
eNeuro 20 May 2021, 8 (3) ENEURO.0471-20.2021; DOI: 10.1523/ENEURO.0471-20.2021
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Keywords

  • auditory cortex
  • electroencephalography
  • frequency tagging
  • voice

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