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

ABSTRACT: Central 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.

SUBMITTER: Smith SS

PROVIDER: S-EPMC10769427 | biostudies-literature | 2023 Dec

REPOSITORIES: biostudies-literature

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

Smith Samuel S SS Jahn Kelly N KN Sugai Jenna A JA Hancock Ken E KE Polley Daniel B DB

bioRxiv : the preprint server for biology 20240118

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 chro ...[more]

PMID: 38187580

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Project description:The ability to process and act upon incoming sounds during locomotion is critical for survival and adaptive behavior. Despite the established role that the auditory cortex (AC) plays in behavior- and context-dependent sound processing, previous studies have found that auditory cortical activity is on average suppressed during locomotion as compared to immobility. While suppression of auditory cortical responses to self-generated sounds results from corollary discharge, which weakens responses to predictable sounds, the functional role of weaker responses to unpredictable external sounds during locomotion remains unclear. In particular, whether suppression of external sound-evoked responses during locomotion reflects reduced involvement of the AC in sound processing or whether it results from masking by an alternative neural computation in this state remains unresolved. Here, we tested the hypothesis that rather than simple inhibition, reduced sound-evoked responses during locomotion reflect a tradeoff with the emergence of explicit and reliable coding of locomotion velocity. To test this hypothesis, we first used neural inactivation in behaving mice and found that the AC plays a critical role in sound-guided behavior during locomotion. To investigate the nature of this processing, we used two-photon calcium imaging of local excitatory auditory cortical neural populations in awake mice. We found that locomotion had diverse influences on activity of different neurons, with a net suppression of baseline-subtracted sound-evoked responses and neural stimulus detection, consistent with previous studies. Importantly, we found that the net inhibitory effect of locomotion on baseline-subtracted sound-evoked responses was strongly shaped by elevated ongoing activity that compressed the response dynamic range, and that rather than reflecting enhanced "noise," this ongoing activity reliably encoded the animal's locomotion speed. Decoding analyses revealed that locomotion speed and sound are robustly co-encoded by auditory cortical ensemble activity. Finally, we found consistent patterns of joint coding of sound and locomotion speed in electrophysiologically recorded activity in freely moving rats. Together, our data suggest that rather than being suppressed by locomotion, auditory cortical ensembles explicitly encode it alongside sound information to support sound perception during locomotion.

Project description:To determine the neural mechanism underlying the effects of sound therapy on tinnitus, we hypothesize that sound therapy may be effective by modulating both local neural activity and functional connectivity that is associated with auditory perception, auditory information storage or emotional processing. In this prospective observational study, 30 tinnitus patients underwent resting-state functional magnetic resonance imaging scans at baseline and after 12 weeks of sound therapy. Thirty-two age- and gender-matched healthy controls also underwent two scans over a 12-week interval; 30 of these healthy controls were enrolled for data analysis. The amplitude of low-frequency fluctuation was analysed, and seed-based functional connectivity measures were shown to significantly alter spontaneous local brain activity and its connections to other brain regions. Interaction effects between the two groups and the two scans in local neural activity as assessed by the amplitude of low-frequency fluctuation were observed in the left parahippocampal gyrus and the right Heschl's gyrus. Importantly, local functional activity in the left parahippocampal gyrus in the patient group was significantly higher than that in the healthy controls at baseline and was reduced to relatively normal levels after treatment. Conversely, activity in the right Heschl's gyrus was significantly increased and extended beyond a relatively normal range after sound therapy. These changes were found to be positively correlated with tinnitus relief. The functional connectivity between the left parahippocampal gyrus and the cingulate cortex was higher in tinnitus patients after treatment. The alterations of local activity and functional connectivity in the left parahippocampal gyrus and right Heschl's gyrus were associated with tinnitus relief. Resting-state functional magnetic resonance imaging can provide functional information to explain and 'visualize' the mechanism underlying the effect of sound therapy on the brain.

Dataset Information

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

Publications

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

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