Corticostriatal functional connectivity of bothersome tinnitus in single-sided deafness

Jennifer Henderson-Sabes,Danielle Mizuiri,Srikantan S Nagarajan,Anne M Findlay,Philip L Perez,Seth E Pross,Jolie L Chang,Steven W Cheung,Yingying Shang,Leighton B Hinkley

doi:10.1038/s41598-019-56127-1

Abstract

Subjective tinnitus is an auditory phantom perceptual disorder without an objective biomarker. Bothersome tinnitus in single-sided deafness (SSD) is particularly challenging to treat because the deaf ear can no longer be stimulated by acoustic means. We contrasted an SSD cohort with bothersome tinnitus (TIN; N = 15) against an SSD cohort with no or non-bothersome tinnitus (NO TIN; N = 15) using resting-state functional magnetic resonance imaging (fMRI). All study participants had normal hearing in one ear and severe or profound hearing loss in the other. We evaluated corticostriatal functional connectivity differences by placing seeds in the caudate nucleus and Heschl’s Gyrus (HG) of both hemispheres. The TIN cohort showed increased functional connectivity between the left caudate and left HG, and left and right HG and the left caudate. Within the TIN cohort, functional connectivity between the right caudate and cuneus was correlated with the Tinnitus Functional Index (TFI) relaxation subscale. And, functional connectivity between the right caudate and superior lateral occipital cortex, and the right caudate and anterior supramarginal gyrus were correlated with the TFI control subscale. These findings support a striatal gating model of tinnitus and suggest tinnitus biomarkers to monitor treatment response and to target specific brain areas for innovative neuromodulation therapies.

Highlights

Subjective tinnitus is an auditory phantom perceptual disorder without an objective biomarker
We report on connectivity differences between TIN and non-bothersome tinnitus (NO TIN) cohorts, and voxelwise connectivity strength correlations with subscale scores of the validated Tinnitus Functional Index (TFI)[37] within the TIN cohort
The key finding of this study is increased connectivity between the caudate nucleus and auditory cortex in the single-sided deafness (SSD) cohort with chronic, bothersome tinnitus

Summary

Introduction

Subjective tinnitus is an auditory phantom perceptual disorder without an objective biomarker. Functional connectivity between the right caudate and superior lateral occipital cortex, and the right caudate and anterior supramarginal gyrus were correlated with the TFI control subscale These findings support a striatal gating model of tinnitus and suggest tinnitus biomarkers to monitor treatment response and to target specific brain areas for innovative neuromodulation therapies. Human physiological studies[14,15], case reports[16,17], and an early clinical trial[18] focused on the caudate nucleus of the basal ganglia support a striatal gating model[15] of tinnitus awareness This model delineates modulators of tinnitus persistence and tinnitus severity, where corticostriatal connections between the striatum and auditory cortex act to gate auditory phantom representations to reach perceptual awareness and connections between the striatum and limbic structures act to modulate auditory phantom distress. This intervention requires surgical implantation of hardware to the skull and complicates future head magnetic resonance imaging (MRI) examinations

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