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The human pupil and face encode sound affect and provide objective signatures of tinnitus and auditory hypersensitivity disorders

View ORCID ProfileSamuel S. Smith, View ORCID ProfileKelly N. Jahn, View ORCID ProfileJenna A. Sugai, Ken E. Hancock, View ORCID ProfileDaniel B. Polley
doi: https://doi.org/10.1101/2023.12.22.571929
Samuel S. Smith
1Eaton-Peabody Laboratories, Massachusetts Eye and Ear, Boston MA, 02114 USA
2Department of Otolaryngology – Head and Neck Surgery, Harvard Medical School, Boston MA 02114 USA
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  • ORCID record for Samuel S. Smith
Kelly N. Jahn
1Eaton-Peabody Laboratories, Massachusetts Eye and Ear, Boston MA, 02114 USA
2Department of Otolaryngology – Head and Neck Surgery, Harvard Medical School, Boston MA 02114 USA
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Jenna A. Sugai
1Eaton-Peabody Laboratories, Massachusetts Eye and Ear, Boston MA, 02114 USA
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Ken E. Hancock
1Eaton-Peabody Laboratories, Massachusetts Eye and Ear, Boston MA, 02114 USA
2Department of Otolaryngology – Head and Neck Surgery, Harvard Medical School, Boston MA 02114 USA
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Daniel B. Polley
1Eaton-Peabody Laboratories, Massachusetts Eye and Ear, Boston MA, 02114 USA
2Department of Otolaryngology – Head and Neck Surgery, Harvard Medical School, Boston MA 02114 USA
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Summary

Sound is jointly processed along acoustic and emotional dimensions. These dimensions can become distorted and entangled in persons with sensory disorders, producing a spectrum of loudness hypersensitivity, phantom percepts, and – in some cases – debilitating sound aversion. Here, we looked for objective signatures of disordered hearing (DH) in the human face. Pupil dilations and micro facial movement amplitudes scaled with sound valence in neurotypical listeners but not DH participants with chronic tinnitus (phantom ringing) and sound sensitivity. In DH participants, emotionally evocative sounds elicited abnormally large pupil dilations but blunted and invariant facial reactions that jointly provided an accurate prediction of individual tinnitus and hyperacusis questionnaire handicap scores. By contrast, EEG measures of central auditory gain identified steeper neural response growth functions but no association with symptom severity. These findings highlight dysregulated affective sound processing in persons with bothersome tinnitus and sound sensitivity disorders and introduce approaches for their objective measurement.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

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  • Revised abstract. Additional references.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted January 18, 2024.
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The human pupil and face encode sound affect and provide objective signatures of tinnitus and auditory hypersensitivity disorders
Samuel S. Smith, Kelly N. Jahn, Jenna A. Sugai, Ken E. Hancock, Daniel B. Polley
bioRxiv 2023.12.22.571929; doi: https://doi.org/10.1101/2023.12.22.571929
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The human pupil and face encode sound affect and provide objective signatures of tinnitus and auditory hypersensitivity disorders
Samuel S. Smith, Kelly N. Jahn, Jenna A. Sugai, Ken E. Hancock, Daniel B. Polley
bioRxiv 2023.12.22.571929; doi: https://doi.org/10.1101/2023.12.22.571929

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