Inefficient Involvement of Insula in Sensorineural Hearing Loss

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.

Insula and Amygdala Atrophy Are Associated With Functional Impairment in Subjects With Presbycusis

“…After the whole-brain analysis, we selected regions of interest that have been consistently implicated in previous neuroimaging studies relating audition, cognition, and dementia (Li et al, 2017;Ren et al, 2018;Xu X.-M. et al, 2019). To define ROI's, we used the Desikan-Killiany atlas, a gyrus-based atlas (Desikan et al, 2006) that has been commonly employed to explore cortical morphometry (Fornito et al, 2013;Jalbrzikowski et al, 2013).…”

“…Considering that our study explores audition, cognition, NPS and functional impairment, we looked for the main cortical and subcortical brain areas responsible for the following functions in the literature: (i) temporal cortex (e.g., superior, middle, and inferior gyri) was atrophied in a longitudinal hearing impairment study (Lin et al, 2011); (ii) cingulate cortex has been previously related with presbycusis (Husain, 2016;Belkhiria et al, 2019); (iii) amygdala atrophy has been related with neuropsychiatric symptoms in early AD (Poulin et al, 2011); and (iv) structural and functional changes of the insula have been reported in hearing loss patients (Yang et al, 2014;Li et al, 2017;Ren et al, 2018;Xu X.-M. et al, 2019). Other regions such as the hippocampus, thalamus and accumbens areas were included because of their early affection in AD (ten Kate et al, 2018).…”

“…Some of these areas, such as the cingulate cortex and the insula, have been shown to be activated during speech understanding of acoustically degraded situations. During these conditions, subjects need to increase their listening effort to comprehend the acoustic information (Sharma and Glick, 2016;Xu X.-M. et al, 2019). The listening effort might increase the cognitive load, deteriorating cognitive processing of non-auditory stimuli in patients with presbycusis (Cardin, 2016;Husain, 2016).…”

“…The listening effort might increase the cognitive load, deteriorating cognitive processing of non-auditory stimuli in patients with presbycusis (Cardin, 2016;Husain, 2016). Accordingly, a recent study evaluating functional and structural MRI in hearing impaired patients (Xu X.-M. et al, 2019) showed that the functional connections between insula and other brain regions were significantly decreased and associated with emotional and cognitive dysregulation in these patients. In addition, a study in patients with presbycusis and structural MRI showed evidence that a thicker right insula was associated with better speech perception (Ren et al, 2018).…”

Silence, Solitude, and Serotonin: Neural Mechanisms Linking Hearing Loss and Social Isolation

“…Other imaging studies in human subjects have shown that sensorineural hearing loss is associated with a widespread decrease in connectivity in multiple functional brain networks involved in decoding or assessing the meaning of the acoustic environment. These networks include auditory cortical regions and the insula, amygdala, and different cerebellar subregions that combine multimodal sensory information with information on internal state [ 171 , 172 , 173 , 174 ]. For some networks, the lack of connectivity further correlates with measures of speech comprehension, as well as general measures of cognitive performance or affective state.…”