Age-related auditory nerve deficits propagate central gain throughout the auditory system: Associations with cortical microstructure and speech recognition

Abstract

There is growing evidence that many perceptual difficulties associated with age-related hearing loss are not solely due to cochlear damage and are exacerbated by changes within the central nervous system. We examined electrophysiological (EEG) responses to clicks and diffusion kurtosis imaging (DKI) in 49 older (29 female) and 26 younger (20 female) adults to determine the extent to which auditory nerve (AN) deficits in older adults contributed to functional and structural changes throughout the auditory system. Older adults exhibited smaller AN responses, similar brainstem responses, and larger auditory cortex (AC) responses, demonstrating progressive "central gain". Audiometric thresholds were not predictive of EEG measures. Reduced AN function predicted deficits in cortical microstructure (lower AC fractional anisotropy, FA) in older adults, consistent with myelin degeneration. These lower FA values in the AC of older adults also predicted larger AC responses and more central gain. Older adults exhibited significantly lower AC FA and higher mean diffusivity (MD) than younger adults, and AC FA and MD were significant predictors of speech-in-noise (SIN) recognition in older adults. The results suggest that reduced afferent input in older adults not only results in functional changes throughout the auditory system consistent with progressive gain, but also contributes to deficits in AC structure beyond those explained by age alone, contributing to SIN deficits. Understanding the complex effects of age, reduced AN input, central gain, and AC structure on SIN recognition may provide potential therapeutic targets for intervention. SignificanceAge-related hearing loss is the most common sensory deficit with aging, but little is known about how the auditory cortex adapts to the chronic loss of afferent auditory input. We measured auditory nerve, brainstem, and cortical responses in younger and older adults. In older adults, deficits in afferent input predicted progressive hyperexcitability, or "central gain", at the brainstem and cortex. Smaller auditory nerve responses predicted poorer white matter structure in auditory cortex. Poorer white matter structure predicted smaller auditory cortex responses, more auditory cortical gain, and worse speech-in-noise recognition in older adults. This is the first study to show that reduced afferent input leads to both amplified cortical responses and reduced cortical integrity in older adults, contributing to speech-in-noise deficits.