Abstract

ObjectiveTinnitus is a prevalent hearing disorder, which could have a devastating impact on a patient’s life. Functional studies have revealed connectivity pattern changes in the tinnitus brains that suggested a change of network dynamics as well as topological organization. However, no studies have yet provided evidence for the topological network changes in the gray matter. In this research, we aim to use the graph-theoretical approach to investigate the changes of topology in the tinnitus brain using structural MRI data, which could provide insights into the underlying anatomical basis for the neural mechanism in generating phantom sounds.MethodsWe collected 3D MRI images on 46 bilateral tinnitus patients and 46 age and gender-matched healthy controls. Brain networks were constructed with correlation matrices of the cortical thickness and subcortical volumes of 80 cortical/subcortical regions of interests. Global network properties were analyzed using local and global efficiency, clustering coefficient, and small-world coefficient, and regional network properties were evaluated using the betweenness coefficient for hub connectivity, and interregional correlations for edge properties. Between-group differences in cortical thickness and subcortical volumes were assessed using independent sample t-tests, and local efficiency, global efficiency, clustering coefficient, sigma, and interregional correlation were compared using non-parametric permutation tests.ResultsTinnitus was found to have increased global efficiency, local efficiency, and cluster coefficient, indicating generally heightened connectivity of the network. The small-world coefficient remained normal for tinnitus, indicating intact small-worldness. Betweenness centrality analysis showed that hubs in the amygdala and parahippocampus were only found for tinnitus but not controls. In contrast, hubs in the auditory cortex, insula, and thalamus were only found for controls but not tinnitus. Interregional correlation analysis further found in tinnitus enhanced connectivity between the auditory cortex and prefrontal lobe, and decreased connectivity of the insula with anterior cingulate gyrus and parahippocampus.ConclusionThese findings provided the first morphological evidence of altered topological organization of the brain networks in tinnitus. These alterations suggest that heightened efficiency of the brain network and altered auditory-limbic connection for tinnitus, which could be developed in compensation for the auditory deafferentation, leading to overcompensation and, ultimately, an emotional and cognitive burden.

Highlights

  • IntroductionSubjective tinnitus ( referred to as tinnitus), known as “ringing in the ears,” refers to the perception of sound in the absence of corresponding external source

  • Subjective tinnitus, known as “ringing in the ears,” refers to the perception of sound in the absence of corresponding external source

  • A proposed model further suggested that the tinnitus sensation might be perceived only when aberrant neuronal activity in the primary auditory cortex is transmitted to a global workplace involving frontal, parietal, and limbic regions (De Ridder et al, 2011)

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Summary

Introduction

Subjective tinnitus ( referred to as tinnitus), known as “ringing in the ears,” refers to the perception of sound in the absence of corresponding external source. When the limbic regions become dysfunctional, noise-cancelation breaks down and the tinnitus signal pervades to the conscious perception (Rauschecker et al, 2010; Leaver et al, 2011) This model has been supported by empirical evidence from functional and structural imaging studies. The compromised auditory representation could be compensated with enhanced auditory memory retrieval through parahippocampal regions, sustaining the memory of the phantom sounds (Yoo et al, 2016b) These regions could constitute a complex network in maintaining and enhancing the symptoms, which is involved in auditory representation and attention, memory, and emotion (Weisz et al, 2007; Leaver et al, 2011; Auerbach et al, 2014)

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