Association of hearing impairment with brain volume changes in older adults
Introduction
Two converging lines of evidence suggest that hearing impairment and alterations in peripheral auditory function could directly or indirectly lead to central effects on brain structure and function. Cross-sectional neuroimaging studies have demonstrated that peripheral hearing impairment is associated with reduced cortical volumes in the primary auditory cortex (Eckert et al., 2012, Husain et al., 2010, Peelle et al., 2011) and variation in the integrity of central auditory white matter tracks (Chang et al., 2004, Lin et al., 2008). The basis of these associations remains unknown but may be related to alterations in the degree of neural activation provided by an impoverished auditory signal with subsequent structural changes in cortical reorganization and brain morphometry (Peelle, Troiani et al., 2011). Interestingly, degradation in the fidelity of peripheral encoding of sound likely results in recruitment and activation of broader neural networks needed for auditory processing (Davis and Johnsrude, 2007, Peelle et al., 2010, Wingfield and Grossman, 2006), suggesting that peripheral hearing impairment may carry cascading consequences for other brain regions.
Broader functional implications of hearing impairment are suggested by epidemiologic studies investigating the association of hearing impairment with cognitive functioning. In these studies of older adults, peripheral hearing impairment was independently associated with poorer neurocognitive performance on both auditory and non-auditory tests (Gussekloo et al., 2005, Lin, 2011, Lin et al., 2011a, Lindenberger and Baltes, 1994, Tay et al., 2006), accelerated rates of cognitive decline (Lin, Yaffe et al., 2013), and increased risk of incident all-cause dementia (Gallacher et al., 2012, Lin et al., 2011b). Hypothesized mechanisms to explain these associations include a shared neuropathologic etiology, cognitive load from the reallocation of brain resources for auditory processing (Tun et al., 2009, Wingfield et al., 2005), and/or mediation through social isolation (Barnes et al., 2004, Bennett et al., 2006).
Whether peripheral hearing impairment is associated with regions outside the primary auditory cortex and with changes in brain volumes is unknown. A priori, we hypothesized that hearing impairment is associated with greater volume declines in regional brain volumes important for auditory and spoken language processing (superior, middle, and inferior temporal gyri) (Adank, 2012, Davis and Gaskell, 2009, Peelle, 2012). Understanding the association of hearing impairment with structural brain volumes may provide insights into mechanistic pathways through which peripheral impairments in sensory function could contribute to brain aging.
Section snippets
Study participants
Participants were followed in the neuroimaging substudy (Resnick, Goldszal et al., 2000) of the BLSA, an ongoing prospective study of the effects of aging that was initiated in 1958 and is conducted by the National Institute on Aging (Shock, Greulich et al., 1984). The present investigation is based on a longitudinal cohort of participants (n = 126, ages 56–86 at baseline) who were enrolled beginning in 1994 in the neuroimaging substudy of the BLSA and had audiometric assessments. Baseline was
Results
Individuals with hearing impairment (n = 51) were more likely to be men, older, white, and smokers than individuals with normal hearing (n = 75) (Table 1). Mean audiograms for individuals with normal hearing vs. hearing impairment are presented in Fig. 1. The majority of individuals with hearing impairment had impairments in the mild range (n = 40, 78%) rather than in the moderate (n = 9, 18%) or severe range (n = 2, 4%). Among participants with hearing impairment, 13 individuals (25.5%) reported hearing
Discussion
In this study, hearing impairment in older adults was independently associated with accelerated rates of decline in regional brain volumes in the right temporal lobe (STG, MTG, ITG) critical for spoken language processing as well as whole brain volume over a mean follow-up period of 6.4 years. These results were robust to adjustment for multiple potential confounders, and the observation of specific vulnerability of the temporal lobe, particularly on the right side, was consistent in both
Acknowledgments
Funding/support
This study was supported by the intramural research program of the National Institute on Aging. Dr. Lin was supported by NIH K23DC011279, a Triological Society/American College of Surgeons Clinician Scientist Award, and the Eleanor Schwartz Charitable Foundation.
Conflict of interest
Dr. Lin reports being a consultant to Cochear Limited, on the scientific advisory board of Pfizer and Autifony, and a speaker for Med El and Amplifon.
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