Association of hearing impairment with brain volume changes in older adults

F R Lin, L Ferrucci, Y An, J O Goh, Jimit Doshi, E J Metter, C Davatzikos, M A Kraut, S M Resnick, F R Lin, L Ferrucci, Y An, J O Goh, Jimit Doshi, E J Metter, C Davatzikos, M A Kraut, S M Resnick

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.

Keywords: Aging; Brain volume; Hearing impairment; Hearing loss; MRI.

Conflict of interest statement

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.

Copyright © 2014 Elsevier Inc. All rights reserved.

Figures

Figure 1. Mean audiograms of individuals with…
Figure 1. Mean audiograms of individuals with normal hearing (n = 75) and hearing impairment (n = 51)
Error bars denote 95% confidence intervals of the mean.
Figure 2
Figure 2
Axial slices displaying lobar volumes and temporal lobe ROIs used in this study
Figure 3. Difference in average slopes of…
Figure 3. Difference in average slopes of RAVENS gray matter maps between those with hearing impairment versus normal hearing
Blue/green are regions in which individuals with hearing impairment compared to those with normal hearing had a higher rate of gray matter decrease. Color bars denote regression coefficient t-values (regression coefficient/standard error).

References

    1. Adank P. Design choices in imaging speech comprehension: an Activation Likelihood Estimation (ALE) meta-analysis. Neuroimage. 2012;63(3):1601–1613.
    1. Barnes LL, Mendes de Leon CF, et al. Social resources and cognitive decline in a population of older African Americans and whites. Neurology. 2004;63(12):2322–2326.
    1. Bennett DA, Schneider JA, et al. The effect of social networks on the relation between Alzheimer’s disease pathology and level of cognitive function in old people: a longitudinal cohort study. Lancet Neurol. 2006;5(5):406–412.
    1. Chang Y, Lee SH, et al. Auditory neural pathway evaluation on sensorineural hearing loss using diffusion tensor imaging. Neuroreport. 2004;15(11):1699–1703.
    1. Chetelat G, Landeau B, et al. Using voxel-based morphometry to map the structural changes associated with rapid conversion in MCI: a longitudinal MRI study. Neuroimage. 2005;27(4):934–946.
    1. Cheung SW, Bonham BH, et al. Realignment of interaural cortical maps in asymmetric hearing loss. J Neurosci. 2009;29(21):7065–7078.
    1. Cole SW, Hawkley LC, 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;108(7):3080–3085.
    1. Cole SW, Hawkley LC, et al. Social regulation of gene expression in human leukocytes. Genome Biol. 2007;8(9):R189.
    1. Davatzikos C, Genc A, et al. Voxel-based morphometry using the RAVENS maps: methods and validation using simulated longitudinal atrophy. Neuroimage. 2001;14(6):1361–1369.
    1. Davis MH, Gaskell MG. A complementary systems account of word learning: neural and behavioural evidence. Philos Trans R Soc Lond B Biol Sci. 2009;364(1536):3773–3800.
    1. Davis MH, I, Johnsrude S. Hearing speech sounds: top-down influences on the interface between audition and speech perception. Hear Res. 2007;229(1–2):132–147.
    1. Driscoll I, Davatzikos C, et al. Longitudinal pattern of regional brain volume change differentiates normal aging from MCI. Neurology. 2009;72(22):1906–1913.
    1. Eckert MA, Cute SL, et al. Auditory cortex signs of age-related hearing loss. J Assoc Res Otolaryngol. 2012;13(5):703–713.
    1. Friston KJ, Worsley KJ, et al. Assessing the significance of focal activations using their spatial extent. Human Brain Mapping. 1993;1(3):210–220.
    1. Gallacher J, Ilubaera V, et al. Auditory threshold, phonologic demand, and incident dementia. Neurology. 2012;79(15):1583–1590.
    1. Goldszal AF, Davatzikos C, et al. An image-processing system for qualitative and quantitative volumetric analysis of brain images. J Comput Assist Tomogr. 1998;22(5):827–837.
    1. Groschel M, Gotze R, 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;27(8):1499–1507.
    1. Gussekloo J, de Craen AJ, et al. Sensory impairment and cognitive functioning in oldest-old subjects: the Leiden 85+ Study. Am J Geriatr Psychiatry. 2005;13(9):781–786.
    1. Husain FT, Medina RE, et al. Neuroanatomical changes due to hearing loss and chronic tinnitus: a combined VBM and DTI study. Brain Res. 2010;1369:74–88.
    1. Kakigi A, Hirakawa H, et al. Tonotopic mapping in auditory cortex of the adult chinchilla with amikacin-induced cochlear lesions. Audiology. 2000;39(3):153–160.
    1. Kantarci K, Jack CR., Jr Quantitative magnetic resonance techniques as surrogate markers of Alzheimer’s disease. NeuroRx. 2004;1(2):196–205.
    1. Knecht S, Drager B, et al. Handedness and hemispheric language dominance in healthy humans. Brain. 2000;123(Pt 12):2512–2518.
    1. Lin FR. Hearing loss and cognition among older adults in the United States. J Gerontol A Biol Sci Med Sci. 2011;66(10):1131–1136.
    1. Lin FR, Ferrucci L, et al. Hearing loss and cognition in the Baltimore Longitudinal Study of Aging. Neuropsychology. 2011;25(6):763–770.
    1. Lin FR, Metter EJ, et al. Hearing loss and incident dementia. Arch Neurol. 2011;68(2):214–220.
    1. Lin FR, Thorpe R, et al. Hearing loss prevalence and risk factors among older adults in the United States. J Gerontol A Biol Sci Med Sci. 2011;66(5):582–590.
    1. Lin FR, Yaffe K, et al. Hearing loss and cognitive decline among older adults. JAMA Intern Med. 2013 Epublished January 21, 2013.
    1. Lin Y, Wang J, et al. Diffusion tensor imaging of the auditory pathway in sensorineural hearing loss: changes in radial diffusivity and diffusion anisotropy. J Magn Reson Imaging. 2008;28(3):598–603.
    1. Lindenberger U, Baltes PB. Sensory functioning and intelligence in old age: a strong connection. Psychol Aging. 1994;9(3):339–355.
    1. McEwen BS. Central effects of stress hormones in health and disease: Understanding the protective and damaging effects of stress and stress mediators. Eur J Pharmacol. 2008;583(2–3):174–185.
    1. Mesulam MM. From sensation to cognition. Brain. 1998;121(Pt 6):1013–1052.
    1. Peelle JE. “The hemispheric lateralization of speech processing depends on what speech” is: a hierarchical perspective. Front Hum Neurosci. 2012;6:309.
    1. Peelle JE, I, Johnsrude S, et al. Hierarchical processing for speech in human auditory cortex and beyond. Front Hum Neurosci. 2010;4:51.
    1. Peelle JE, Troiani V, et al. Hearing loss in older adults affects neural systems supporting speech comprehension. J Neurosci. 2011;31(35):12638–12643.
    1. Pickles JO. An introduction to the physiology of hearing. Bingley, UK: Emerald Group Publishing; 2008.
    1. Radley JJ, Morrison JH. Repeated stress and structural plasticity in the brain. Ageing Res Rev. 2005;4(2):271–287.
    1. Resnick SM, Goldszal AF, et al. One-year age changes in MRI brain volumes in older adults. Cereb Cortex. 2000;10(5):464–472.
    1. Resnick SM, Pham DL, et al. Longitudinal magnetic resonance imaging studies of older adults: a shrinking brain. J Neurosci. 2003;23(8):3295–3301.
    1. Sapolsky RM. Glucocorticoids, stress, and their adverse neurological effects: relevance to aging. Exp Gerontol. 1999;34(6):721–732.
    1. Schwaber MK, Garraghty PE, et al. Neuroplasticity of the adult primate auditory cortex following cochlear hearing loss. Am J Otol. 1993;14(3):252–258.
    1. Shen D, Davatzikos C. HAMMER: hierarchical attribute matching mechanism for elastic registration. IEEE Trans Med Imaging. 2002;21(11):1421–1439.
    1. Shock NW, Greulich RC, et al. Normal Human Aging: the Baltimore Longitudinal Study of Aging. Wasington, D.C: National Institutes of Health; 1984.
    1. Spitzer RL, Williams JB. Diagnostic and statistical manual of mental disorders DSM III-R. 3. Washington, DC: American Psychiatric Press; 1987.
    1. Tay T, Wang JJ, et al. Sensory and cognitive association in older persons: findings from an older Australian population. Gerontology. 2006;52(6):386–394.
    1. Tranel D, Damasio H, et al. A neural basis for the retrieval of conceptual knowledge. Neuropsychologia. 1997;35(10):1319–1327.
    1. Tun PA, McCoy S, et al. Aging, hearing acuity, and the attentional costs of effortful listening. Psychol Aging. 2009;24(3):761–766.
    1. Uhlmann RF, Larson EB, et al. Relationship of hearing impairment to dementia and cognitive dysfunction in older adults. JAMA. 1989;261(13):1916–1919.
    1. WHO World Health Organization Prevention of Blindness and Deafness (PBD) Program. Prevention of Deafness and Hearing Impaired Grades of Hearing Impairment. < >.
    1. Wingfield A, Grossman M. Language and the aging brain: patterns of neural compensation revealed by functional brain imaging. J Neurophysiol. 2006;96(6):2830–2839.
    1. Wingfield A, Tun PA, et al. Hearing loss in older adulthood - What it is and how it interacts with cognitive performance. Current directions in psychological science. 2005;14(3):144–148.

Source: PubMed

3
Abonner