Cortical Oscillatory Signatures Reveal the Prerequisites for Tinnitus Perception: A Comparison of Subjects With Sudden Sensorineural Hearing Loss With and Without Tinnitus.

Sang-Yeon Lee,Dirk De Ridder,Byung Yoon Choi,Ja-Won Koo,Jae-Jin Song

doi:10.3389/fnins.2020.596647

Sang-Yeon Lee, Dirk De Ridder + Show 3 more

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https://doi.org/10.3389/fnins.2020.596647

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Abstract

Just as the human brain works in a Bayesian manner to minimize uncertainty regarding external stimuli, a deafferented brain due to hearing loss attempts to obtain or “fill in” the missing auditory information, resulting in auditory phantom percepts (i.e., tinnitus). Among various types of hearing loss, sudden sensorineural hearing loss (SSNHL) has been extensively reported to be associated with tinnitus. However, the reason that tinnitus develops selectively in some patients with SSNHL remains elusive, which led us to hypothesize that patients with SSNHL with tinnitus (SSNHL-T) and those without tinnitus (SSNHL-NT) may exhibit different cortical activity patterns. In the current study, we compared resting-state quantitative electroencephalography findings between 13 SSNHL-T and 13 SSNHL-NT subjects strictly matched for demographic characteristics and hearing thresholds. By performing whole-brain source localization analysis complemented by functional connectivity analysis, we aimed to determine the as-yet-unidentified cortical oscillatory signatures that may reveal potential prerequisites for the perception of tinnitus in patients with SSNHL. Compared with the SSNHL-NT group, the SSNHL-T group showed significantly higher cortical activity in Bayesian inferential network areas such as the frontopolar cortex, orbitofrontal cortex (OFC), and pregenual anterior cingulate cortex (pgACC) for the beta 3 and gamma frequency bands. This suggests that tinnitus develops in a brain with sudden auditory deafferentation only if the Bayesian inferential network updates the missing auditory information and the pgACC-based top-down gatekeeper system is actively involved. Additionally, significantly increased connectivity between the OFC and precuneus for the gamma frequency band was observed in the SSNHL-T group, further suggesting that tinnitus derived from Bayesian inference may be linked to the default mode network so that tinnitus is regarded as normal. Taken together, our preliminary results suggest a possible mechanism for the selective development of tinnitus in patients with SSNHL. Also, these areas could serve as the potential targets of neuromodulatory approaches to preventing the development or prolonged perception of tinnitus in subjects with SSNHL.

Highlights

Non-pulsatile tinnitus is a common otologic symptom characterized by conscious auditory perception in the absence of an external stimulus
We investigated neural substrates accounting for the development of tinnitus exclusively in patients with SSNHL by comparing resting-state quantitative electroencephalography findings between SSNHL patients with and others without tinnitus (SSNHL-T and SSNHL-NT)
These findings suggest that auditory phantom percepts may develop when the brain experiences sudden decreased peripheral auditory input as the Bayesian inferential network updates the missing auditory information with the involvement of the pgACC-based top-down gatekeeper system

Summary

Introduction

Non-pulsatile tinnitus is a common otologic symptom characterized by conscious auditory perception in the absence of an external stimulus. This is often called a “phantom sound” because there is no corresponding genuine physical source of the sound (Vanneste et al, 2018b; Lee et al, 2019; Han et al, 2020). If the brain is deprived of auditory input, it attempts to “fill in” the missing auditory information from auditory memory, leading to the perception of auditory phantoms (i.e., tinnitus) (Friston et al, 2014; Eggermont and Kral, 2016; Lee et al, 2017, 2020a). According to the theoretical multiphase compensation model, the brain attempts to overcome missing auditory information input, generating predictions via increasing topographically restricted tones, widening receptive fields, rewiring dendrites and axons, and retrieving auditory memories, resulting in brain reorganization (De Ridder et al, 2014b)

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