A Critical Role of the Insula in Sensorineural Hearing Loss

Abstract

Background: 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 neural hearing loss (SNHL). To address this issue, we used functional magnetic resonance imaging (fMRI) 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. Methods: Thirty-five SNHL subjects and 54 Controls enrolled in our study underwent auditory evaluation, neuropsychological assessments, functional and structure MRI, respectively. Thirty-three subjects underwent arterial spin labeling (ASL) 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). Findings: Compared to Controls, SNHL subjects demonstrated hyperperfusion in the insula and significantly decreased FC between some insula subdivisions and other brain regions, including thalamus, precuneus, middle frontal gyrus, mid-cingulate cortex, precentral gyrus and inferior parietal lobule. Anxiety status and cognitive impairments were correlated with FC values. Abnormal interactions among SN, DMN and CEN were observed in SNHL group. Interpretation: 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. Funding: This work was supported by the National Natural Science Foundation of China (81520108015), the Fundamental Research Funds for the Central Universities (2242018k30004) and Clinical Innovation Center of Medical Imaging and Interventional Radiology (YXZXA2016005). Declaration of Interest: The authors declare that they have no conflict of interest. Ethical Approval: The study was approved by the ethics committee of Zhongda Hospital, Southeast University, Nanjing, People’s Republic of China (2016ZDSYLL031.0). Written informed consent in accordance with the Declaration of Helsinki was obtained from all subjects.