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

Abstract

SummaryCentral disinhibition works like an amplifier, boosting neural sensitivity to progressively weaker peripheral inputs arising from degenerating sensory organs. The Excess Central Gain model posits that central disinhibition also gives rise to cardinal features of sensory disorders including sensory overload and phantom percepts. Here, we tested predictions of this model with neural, autonomic, and behavioral approaches in participants with sound sensitivity and tinnitus (phantom ringing). We confirmed enhanced auditory neural gain but found no association with their sound aversion and anxiety. Instead, we hypothesized that symptom severity was linked to affective sound encoding. In neurotypical controls, emotionally evocative sounds elicited pupil dilations, electrodermal responses and facial reactions that scaled with valence. Participants with disordered hearing exhibited disrupted pupil and facial reactivity that accurately predicted their self-reported tinnitus and hyperacusis severity. These findings highlight auditory-limbic dysregulation in tinnitus and sound sensitivity disorders and introduce approaches for their objective measurement.