Elsevier

NeuroImage

Volume 90, 15 April 2014, Pages 84-92
NeuroImage

Association of hearing impairment with brain volume changes in older adults

https://doi.org/10.1016/j.neuroimage.2013.12.059Get rights and content

Abstract

Hearing impairment in older adults is independently associated in longitudinal studies with accelerated cognitive decline and incident dementia, and in cross-sectional studies, with reduced volumes in the auditory cortex. Whether peripheral hearing impairment is associated with accelerated rates of brain atrophy is unclear. We analyzed brain volume measurements from magnetic resonance brain scans of individuals with normal hearing versus hearing impairment (speech-frequency pure tone average > 25 dB) followed in the neuroimaging substudy of the Baltimore Longitudinal Study of Aging for a mean of 6.4 years after the baseline scan (n = 126, age 56–86 years). Brain volume measurements were performed with semi-automated region-of-interest (ROI) algorithms, and brain volume trajectories were analyzed with mixed-effect regression models adjusted for demographic and cardiovascular factors. We found that individuals with hearing impairment (n = 51) compared to those with normal hearing (n = 75) had accelerated volume declines in whole brain and regional volumes in the right temporal lobe (superior, middle, and inferior temporal gyri, parahippocampus, p < .05). These results were robust to adjustment for multiple confounders and were consistent with voxel-based analyses, which also implicated right greater than left temporal regions. These findings demonstrate that peripheral hearing impairment is independently associated with accelerated brain atrophy in whole brain and regional volumes concentrated in the right temporal lobe. Further studies investigating the mechanistic basis of the observed associations are needed.

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.

References (50)

  • D. Tranel et al.

    A neural basis for the retrieval of conceptual knowledge

    Neuropsychologia

    (1997)
  • American National Standards Institute

    (1989)
  • L.L. Barnes et al.

    Social resources and cognitive decline in a population of older African Americans and whites

    Neurology

    (2004)
  • Y. Chang et al.

    Auditory neural pathway evaluation on sensorineural hearing loss using diffusion tensor imaging

    Neuroreport

    (2004)
  • S.W. Cheung et al.

    Realignment of interaural cortical maps in asymmetric hearing loss

    J. Neurosci.

    (2009)
  • S.W. Cole et al.

    Social regulation of gene expression in human leukocytes

    Genome Biol.

    (2007)
  • S.W. Cole et al.

    Transcript origin analysis identifies antigen-presenting cells as primary targets of socially regulated gene expression in leukocytes

    Proc. Natl. Acad. Sci. U. S. A.

    (2010)
  • M.H. Davis et al.

    A complementary systems account of word learning: neural and behavioural evidence

    Philos. Trans. R. Soc. Lond. B Biol. Sci.

    (2009)
  • I. Driscoll et al.

    Longitudinal pattern of regional brain volume change differentiates normal aging from MCI

    Neurology

    (2009)
  • M.A. Eckert et al.

    Auditory cortex signs of age-related hearing loss

    J. Assoc. Res. Otolaryngol.

    (2012)
  • K.J. Friston et al.

    Assessing the significance of focal activations using their spatial extent

    Hum. Brain Mapp.

    (1993)
  • J. Gallacher et al.

    Auditory threshold, phonologic demand, and incident dementia

    Neurology

    (2012)
  • A.F. Goldszal et al.

    An image-processing system for qualitative and quantitative volumetric analysis of brain images

    J. Comput. Assist. Tomogr.

    (1998)
  • M. Groschel et al.

    Differential impact of temporary and permanent noise-induced hearing loss on neuronal cell density in the mouse central auditory pathway

    J. Neurotrauma

    (2010)
  • F.T. Husain et al.

    Neuroanatomical changes due to hearing loss and chronic tinnitus: a combined VBM and DTI study

    Brain Res.

    (2010)
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