Longitudinal Changes in Resting-State Functional Connectivity and Gray Matter Volume Are Associated with Conversion to Hearing Impairment in Older Adults

Abstract

Background: Hearing loss was recently identified as a modifiable risk factor for dementia although the potential mechanisms explaining this relationship are unknown.

Objective: The current study examined longitudinal change in resting-state fMRI functional connectivity and gray matter volume in individuals who developed a hearing impairment compared to those whose hearing remained normal.

Methods: This study included 440 participants from the UK Biobank: 163 who had normal hearing at baseline and impaired hearing at follow-up (i.e., converters, mean age = 63.11±6.33, 53% female) and 277 who had normal hearing at baseline and maintained normal hearing at follow-up (i.e., non-converters, age = 63.31±5.50, 50% female). Functional connectivity was computed between a priori selected auditory seed regions (left and right Heschl's gyrus and cytoarchitectonic subregions Te1.0, Te1.1, and Te1.2) and select higher-order cognitive brain networks. Gray matter volume within these same regions was also obtained.

Results: Converters had increased connectivity from left Heschl's gyrus to left anterior insula and from right Heschl's gyrus to right anterior insula, and decreased connectivity between right Heschl's gyrus and right hippocampus, compared to non-converters. Converters also had reduced gray matter volume in left hippocampus and left lateral visual cortex compared to non-converters.

Conclusion: These findings suggest that conversion to a hearing impairment is associated with altered brain functional connectivity and gray matter volume in the attention, memory, and visual processing regions that were examined in this study.

Keywords: Alzheimer’s disease risk factor; functional neuroimaging; hearing impairment; hearing loss.

Figure 1.

Increased functional connectivity over time between auditory cortex and regions of the cingulo-opercular network in converters, and decreased connectivity over time in non-converters. Functional connectivity was measured between left and right auditory cortex (Heschl’s gyrus and two of its subregions, Te1.0 and Te1.2) and the left and right anterior insula/frontal operculum of the cingulo-opercular network. Converters (green) were those that converted from good to impaired hearing from baseline to follow-up, whereas non-converters (orange) were those that maintained normal hearing. L = Left, R = Right, HG = Heschl’s Gyrus, Ant. Ins. = Anterior Insula. Error bars show 95% confidence intervals.

Figure 2.

Decreased functional connectivity over time between auditory cortex and the hippocampus in converters. Functional connectivity was measured between right auditory cortex (the Te1.1 subregion of Heschl’s gyrus) and the right hippocampus. Converters (green) were those that converted from good to impaired hearing from baseline to follow-up, whereas non-converters (orange) were those that maintained normal hearing. R = Right, Hipp. = Hippocampus. Error bars show 95% confidence intervals.

Figure 3.

Gray matter volume in the left hippocampus and left lateral superior occipital region showed a significant group-by-time interaction, in which converters had lower gray matter volume at follow-up compared to non-converters, relative to baseline. L = Left. Error bars show 95% confidence intervals.