Inefficient Involvement of Insula in Sensorineural Hearing Loss.

Xiao-Min Xu,Jian Zhang,Gao-Jun Teng,Richard Salvi,Yun Jiao,Tian-Yu Tang

doi:10.3389/fnins.2019.00133

Xiao-Min Xu, Jian Zhang + Show 4 more

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https://doi.org/10.3389/fnins.2019.00133

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Abstract

The insular cortex plays an important role in multimodal sensory processing, audio-visual integration and emotion; however, little is known about how the insula is affected by auditory deprivation due to sensorineural hearing loss (SNHL). To address this issue, we used structural and functional magnetic resonance imaging to determine if the neural activity within the insula and its interregional functional connectivity (FC) was disrupted by SNHL and if these alterations were correlated clinical measures of emotion and cognition. Thirty-five SNHL subjects and 54 Controls enrolled in our study underwent auditory evaluation, neuropsychological assessments, functional and structure MRI, respectively. Twenty five patients and 20 Controls underwent arterial spin labeling scanning. FC of six insula subdivisions were assessed and the FC results were compared to the neuropsychological tests. Interregional connections were also compared among insula-associated networks, including salience network (SN), default mode network (DMN), and central executive network (CEN). Compared to Controls, SNHL subjects demonstrated hyperperfusion in the insula and significantly decreased FC between some insula subdivisions and other brain regions, including thalamus, putamen, precentral gyrus, postcentral gyrus, mid-cingulate cortex, dorsolateral prefrontal cortex, rolandic operculum. Anxiety, depression and cognitive impairments were correlated with FC values. Abnormal interactions among SN, DMN, and CEN were observed in SNHL group. Our result provides support for the “inefficient high-order control” theory of the insula in which the auditory deprivation caused by SNHL contributes to impaired sensory integration and central deficits in emotional and cognitive processing.

Highlights

Sensorineural hearing loss (SNHL), primarily resulting from damage to the sensory hair cells and spiral ganglion neurons, arising from various etiologies, including neurodegenerative disease, noise, and ototoxic drugs (Cox et al, 2014; Wang et al, 2016; Crowson et al, 2017), is the most common sensory disorder affecting roughly one-eighth of the population (Edmiston and Mitchell, 2013; Cunningham and Tucci, 2017)
We examined the interactions among the salience network (SN), default mode network (DMN), and central executive network (CEN), due to the fact that the insula is a major component of SN, which plays an important role in switching CEN and DMN
Because of known regional differences (Deen et al, 2011), our analysis focused on six regions, the left and right ventral anterior insula, dorsal AI, and posterior insula (PI)

Summary

Introduction

Sensorineural hearing loss (SNHL), primarily resulting from damage to the sensory hair cells and spiral ganglion neurons, arising from various etiologies, including neurodegenerative disease, noise, and ototoxic drugs (Cox et al, 2014; Wang et al, 2016; Crowson et al, 2017), is the most common sensory disorder affecting roughly one-eighth of the population (Edmiston and Mitchell, 2013; Cunningham and Tucci, 2017). The insula has numerous connections with frontal cortex, cingulate cortex and amygdala which contribute to emotional, cognitive and other high level processes (Pandya et al, 1971; Hoistad and Barbas, 2008; Baur et al, 2013; Nomi et al, 2016), as well as neuropsychiatric disorders (Namkung et al, 2017), including depression, anxiety, and bipolar disorder (Stein et al, 2007; Liu et al, 2010; Hulvershorn et al, 2012) These preceding results suggest that the insula is a key structure of modulating acoustic information and could contribute to SNHL-associated psychiatric symptoms

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