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

• Published in: bioRxiv
• Main Authors: Smith, Samuel S, Jahn, Kelly N, Sugai, Jenna A, Hancock, Ken E, Polley, Daniel B
• Format: Journal Article Paper
• Language: English
• Published: United States Cold Spring Harbor Laboratory Press 18.01.2024
• Subjects: Autonomic nervous system; Aversion; Hearing; Sense organs; Sound; Tinnitus
• ISSN: 2692-8205; 2692-8205
• DOI: 10.1101/2023.12.22.571929

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.