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The Influence of Aging, Hearing, and Tinnitus on the Morphology of Cortical Gray Matter, Amygdala, and Hippocampus

. 2020 ; 12 () : 553461. [epub] 20201204

Status PubMed-not-MEDLINE Language English Country Switzerland Media electronic-ecollection

Document type Journal Article

Age related hearing loss (presbycusis) is a natural process represented by elevated auditory thresholds and decreased speech intelligibility, especially in noisy conditions. Tinnitus is a phantom sound that also potentially leads to cortical changes, with its highest occurrence coinciding with the clinical onset of presbycusis. The aim of our project was to identify age, hearing loss and tinnitus related structural changes, within the auditory system and associated structures. Groups of subjects with presbycusis and tinnitus (22 subjects), with only presbycusis (24 subjects), young tinnitus patients with normal hearing (10 subjects) and young controls (17 subjects), underwent an audiological examination to characterize hearing loss and tinnitus. In addition, MRI (3T MR system, analysis in Freesurfer software) scans were used to identify changes in the cortical and subcortical structures. The following areas of the brain were analyzed: Heschl gyrus (HG), planum temporale (PT), primary visual cortex (V1), gyrus parahippocampus (PH), anterior insula (Ins), amygdala (Amg), and hippocampus (HP). A statistical analysis was performed in R framework using linear mixed-effects models with explanatory variables: age, tinnitus, laterality and hearing. In all of the cortical structures, the gray matter thickness decreased significantly with aging without having an effect on laterality (differences between the left and right hemispheres). The decrease in the gray matter thickness was faster in the HG, PT and Ins in comparison with the PH and V1. Aging did not influence the surface of the cortical areas, however there were differences between the surface size of the reported regions in the left and right hemispheres. Hearing loss caused only a borderline decrease of the cortical surface in the HG. Tinnitus was accompanied by a borderline decrease of the Ins surface and led to an increase in the volume of Amy and HP. In summary, aging is accompanied by a decrease in the cortical gray matter thickness; hearing loss only has a limited effect on the structure of the investigated cortical areas and tinnitus causes structural changes which are predominantly within the limbic system and insula, with the structure of the auditory system only being minimally affected.

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Adjamian P., Hall D. A., Palmer A. R., Allan T. W., Langers D. R. M. (2014). Neuroanatomical abnormalities in chronic tinnitus in the human brain. Neurosci. Biobehav. Rev 45, 119–133. 10.1016/j.neubiorev.2014.05.013 PubMed DOI PMC

Adrian D., Refaie A. E. (2000). “The epidemiology of tinnitus,” in The Handbook of Tinnitus, 1–23.

Agrawal Y., Platz E. A., Niparko J. K. (2008). Prevalence of hearing loss and differences by demographic characteristics among US adults: data from the National Health and Nutrition Examination Survey, 1999–2004. Arch. Intern. Med. 168, 1522–1530. 10.1001/archinte.168.14.1522 PubMed DOI

Aldhafeeri F. M., Mackenzie I., Kay T., Alghamdi J., Sluming V. (2012). Neuroanatomical correlates of tinnitus revealed by cortical thickness analysis and diffusion tensor imaging. Neuroradiology 54, 883–892. 10.1007/s00234-012-1044-6 PubMed DOI

Allan T. W., Besle J., Langers D. R. M., Davies J., Hall D. A., Palmer A. R., et al. . (2016). Neuroanatomical alterations in tinnitus assessed with magnetic resonance imaging. Front. Aging Neurosci. 8:221. 10.3389/fnagi.2016.00221 PubMed DOI PMC

Allen J. S., Bruss J., Brown C. K., Damasio H. (2005). Normal neuroanatomical variation due to age: the major lobes and a parcellation of the temporal region. Neurobiol. Aging 26, 1279–1282. 10.1016/j.neurobiolaging.2005.05.023 PubMed DOI

Allen J. S., Emmorey K., Bruss J., Damasio H. (2008). Morphology of the Insula in relation to hearing status and sign language experience. J. Neurosci. 28, 11900–11905. 10.1523/JNEUROSCI.3141-08.2008 PubMed DOI PMC

Baguley D., McFerran D., Hall D. (2013). Tinnitus. Lancet 382, 1600–1607. 10.1016/S0140-6736(13)60142-7 PubMed DOI

Barbey A. K., Colom R., Grafman J. (2013). Dorsolateral prefrontal contributions to human intelligence. Neuropsychologia 51, 1361–1369. 10.1016/j.neuropsychologia.2012.05.017 PubMed DOI PMC

Bhatt J. M., Lin H. W., Bhattacharyya N. (2016). Prevalence, severity, exposures, and treatment patterns of tinnitus in the United States. JAMA Otolaryngol. Head Neck Surg. 142, 959–965. 10.1001/jamaoto.2016.1700 PubMed DOI PMC

Bora E., Fornito A., Pantelis C., Yücel M. (2012). Gray matter abnormalities in major depressive disorder: a meta-analysis of voxel based morphometry studies. J. Affect. Disord. 138, 9–18. 10.1016/j.jad.2011.03.049 PubMed DOI

Boyen K., Langers D. R. M., de Kleine E., van Dijk P. (2013). Gray matter in the brain: differences associated with tinnitus and hearing loss. Hear. Res. 295, 67–78. 10.1016/j.heares.2012.02.010 PubMed DOI

Buckner R. L., Head D., Parker J., Fotenos A. F., Marcus D., Morris J. C., et al. . (2004). A unified approach for morphometric and functional data analysis in young, old, and demented adults using automated atlas-based head size normalization: reliability and validation against manual measurement of total intracranial volume. Neuroimage 23, 724–738. 10.1016/j.neuroimage.2004.06.018 PubMed DOI

Bureš Z., Profant O., Svobodová V., Tóthová D., Vencovský V., Syka J. (2019). Speech comprehension and its relation to other auditory parameters in elderly patients with tinnitus. Front. Aging Neurosci. 11:219. 10.3389/fnagi.2019.00219 PubMed DOI PMC

Carpenter-Thompson J. R., Akrofi K., Schmidt S. A., Dolcos F., Husain F. T. (2014). Alterations of the emotional processing system may underlie preserved rapid reaction time in tinnitus. Brain Res. 1567, 28–41. 10.1016/j.brainres.2014.04.024 PubMed DOI

Chen Q., Beaty R. E., Cui Z., Sun J., He H., Zhuang K., et al. . (2019). Brain hemispheric involvement in visuospatial and verbal divergent thinking. Neuroimage 202:116065. 10.1016/j.neuroimage.2019.116065 PubMed DOI

Chen Y.-C., Xia W., Chen H., Feng Y., Xu J.-J., Gu J.-P., et al. . (2017). Tinnitus distress is linked to enhanced resting-state functional connectivity from the limbic system to the auditory cortex. Hum. Brain Mapp. 38, 2384–2397. 10.1002/hbm.23525 PubMed DOI PMC

Chiarello C., Vazquez D., Felton A., Leonard C. M. (2013). Structural asymmetry of anterior insula: behavioral correlates and individual differences. Brain Lang. 126, 109–122. 10.1016/j.bandl.2013.03.005 PubMed DOI PMC

Chiarello C., Vazquez D., Felton A., McDowell A. (2016). Structural asymmetry of the human cerebral cortex: regional and between-subject variability of surface area, cortical thickness, and local gyrification. Neuropsychologia 93, 365–379. 10.1016/j.neuropsychologia.2016.01.012 PubMed DOI PMC

Dale A. M., Fischl B., Sereno M. I. (1999). Cortical surface-based analysis. I. segmentation and surface reconstruction. Neuroimage 9, 179–194. 10.1006/nimg.1998.0395 PubMed DOI

Dale A. M., Sereno M. I. (1993). Improved localizadon of cortical activity by combining EEG and MEG with MRI cortical surface reconstruction: a linear approach. J. Cogn. Neurosci. 5, 162–176. 10.1162/jocn.1993.5.2.162 PubMed DOI

Dalgaard P. (2010). R Development Core Team. (2010). R: A Language and Environment for Statistical Computing. Available online at: https://research.cbs.dk/en/publications/r-development-core-team-2010-r-a-language-and-environment-for-sta (accessed December 13, 2019).

De Ridder D., Vanneste S., Weisz N., Londero A., Schlee W., Elgoyhen A. B., et al. . (2014). An integrative model of auditory phantom perception: tinnitus as a unified percept of interacting separable subnetworks. Neurosci. Biobehav. Rev. 44, 16–32. 10.1016/j.neubiorev.2013.03.021 PubMed DOI

Destrieux C., Fischl B., Dale A., Halgren E. (2010). Automatic parcellation of human cortical gyri and sulci using standard anatomical nomenclature. Neuroimage 53, 1–15. 10.1016/j.neuroimage.2010.06.010 PubMed DOI PMC

Dotson V. M., Szymkowicz S. M., Sozda C. N., Kirton J. W., Green M. L., O'Shea A., et al. . (2016). Age differences in prefrontal surface area and thickness in middle aged to older adults. Front. Aging Neurosci. 7:250. 10.3389/fnagi.2015.00250 PubMed DOI PMC

Eggermont J. J. (2006). Cortical tonotopic map reorganization and its implications for treatment of tinnitus. Acta Otolaryngol. 126, 9–12. 10.1080/03655230600895259 PubMed DOI

Eggermont J. J., Roberts L. E. (2015). Tinnitus: animal models and findings in humans. Cell Tissue Res. 361, 311–336. 10.1007/s00441-014-1992-8 PubMed DOI PMC

Emmett S. D., Francis H. W. (2015). The socioeconomic impact of hearing loss in us adults. Otol. Neurotol. 36, 545–550. 10.1097/MAO.0000000000000562 PubMed DOI PMC

Fischl B., Dale A. M. (2000). Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc. Natl. Acad. Sci. U.S.A. 97, 11050–11055. 10.1073/pnas.200033797 PubMed DOI PMC

Fischl B., Liu A., Dale A. M. (2001). Automated manifold surgery: constructing geometrically accurate and topologically correct models of the human cerebral cortex. IEEE Trans. Med. Imaging 20, 70–80. 10.1109/42.906426 PubMed DOI

Fischl B., Rajendran N., Busa E., Augustinack J., Hinds O., Yeo B. T. T., et al. . (2008). Cortical folding patterns and predicting cytoarchitecture. Cereb. Cortex 18, 1973–1980. 10.1093/cercor/bhm225 PubMed DOI PMC

Fischl B., Salat D. H., Busa E., Albert M., Dieterich M., Haselgrove C., et al. . (2002). Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33, 341–355. 10.1016/S0896-6273(02)00569-X PubMed DOI

Fischl B., Sereno M. I., Dale A. M. (1999a). Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system. Neuroimage 9, 195–207. 10.1006/nimg.1998.0396 PubMed DOI

Fischl B., Sereno M. I., Tootell R. B., Dale A. M. (1999b). High-resolution intersubject averaging and a coordinate system for the cortical surface. Hum. Brain Mapp. 8, 272–284. 10.1002/(SICI)1097-0193(1999)8:4<272::AID-HBM10>3.0.CO;2-4 PubMed DOI PMC

Fischl B., van der Kouwe A., Destrieux C., Halgren E., Ségonne F., Salat D. H., et al. . (2004). Automatically parcellating the human cerebral cortex. Cereb. Cortex 14, 11–22. 10.1093/cercor/bhg087 PubMed DOI

Fjell A. M., McEvoy L., Holland D., Dale A. M., Walhovd K. B., Alzheimer's Disease Neuroimaging Initiative (2014). What is normal in normal aging? effects of aging, amyloid and Alzheimer's disease on the cerebral cortex and the hippocampus. Prog. Neurobiol. 117, 20–40. 10.1016/j.pneurobio.2014.02.004 PubMed DOI PMC

Gates G. A., Cooper J. C. (1991). Incidence of hearing decline in the elderly. Acta Otolaryngol. 111, 240–248. 10.3109/00016489109137382 PubMed DOI

Glasser M. F., Sotiropoulos S. N., Wilson J. A., Coalson T. S., Fischl B., Andersson J. L., et al. . (2013). The minimal preprocessing pipelines for the human connectome project. Neuroimage 80, 105–124. 10.1016/j.neuroimage.2013.04.127 PubMed DOI PMC

Han X., Jovicich J., Salat D., van der Kouwe A., Quinn B., Czanner S., et al. . (2006). Reliability of MRI-derived measurements of human cerebral cortical thickness: the effects of field strength, scanner upgrade and manufacturer. Neuroimage 32, 180–194. 10.1016/j.neuroimage.2006.02.051 PubMed DOI

Helzner E. P., Cauley J. A., Pratt S. R., Wisniewski S. R., Zmuda J. M., Talbott E. O., et al. . (2005). Race and sex differences in age-related hearing loss: the health, aging and body composition study. J. Am. Geriatr. Soc. 53, 2119–2127. 10.1111/j.1532-5415.2005.00525.x PubMed DOI

Holm S. (1979). a simple sequentially rejective multiple test procedure. Scand. J. Stat. 6, 65–70.

Horikawa C., Kodama S., Tanaka S., Fujihara K., Hirasawa R., Yachi Y., et al. . (2013). Diabetes and risk of hearing impairment in adults: a meta-analysis. J. Clin. Endocrinol. Metab. 98, 51–58. 10.1210/jc.2012-2119 PubMed DOI

Husain F. T. (2016). Neural networks of tinnitus in humans: Elucidating severity and habituation. Hear. Res. 334, 37–48. 10.1016/j.heares.2015.09.010 PubMed DOI

Husain F. T., Medina R. E., Davis C. W., Szymko-Bennett Y., Simonyan K., Pajor N. M., et al. . (2011). Neuroanatomical changes due to hearing loss and chronic tinnitus: a combined VBM and DTI study. Brain Res. 1369, 74–88. 10.1016/j.brainres.2010.10.095 PubMed DOI PMC

Husain F. T., Schmidt S. A. (2014). Using resting state functional connectivity to unravel networks of tinnitus. Hear. Res. 307, 153–162. 10.1016/j.heares.2013.07.010 PubMed DOI

Iglesias J. E., Augustinack J. C., Nguyen K., Player C. M., Player A., Wright M., et al. . (2015). A computational atlas of the hippocampal formation using ex vivo, ultra-high resolution MRI: application to adaptive segmentation of in vivo MRI. Neuroimage 115, 117–137. 10.1016/j.neuroimage.2015.04.042 PubMed DOI PMC

Irimia A., Goh S. Y., Torgerson C. M., Vespa P., Van Horn J. D. (2014). Structural and connectomic neuroimaging for the personalized study of longitudinal alterations in cortical shape, thickness and connectivity after traumatic brain injury. J. Neurosurg. Sci. 58, 129–144. PubMed PMC

Jacobs B., Scheibel A. B. (1993). A quantitative dendritic analysis of Wernicke's area in humans. I. Lifespan changes. J. Comp. Neurol. 327, 83–96. 10.1002/cne.903270107 PubMed DOI

Jakab A., Molnár P. P., Bogner P., Béres M., Berényi E. L. (2012). Connectivity-based parcellation reveals interhemispheric differences in the insula. Brain Topogr. 25, 264–271. 10.1007/s10548-011-0205-y PubMed DOI

Jilek M., Šuta D., Syka J. (2014). Reference hearing thresholds in an extended frequency range as a function of age. J. Acoust. Soc. Am. 136, 1821–1830. 10.1121/1.4894719 PubMed DOI

Jovicich J., Czanner S., Greve D., Haley E., van der Kouwe A., Gollub R., et al. . (2006). Reliability in multi-site structural MRI studies: effects of gradient non-linearity correction on phantom and human data. Neuroimage 30, 436–443. 10.1016/j.neuroimage.2005.09.046 PubMed DOI

Kann S., Zhang S., Manza P., Leung H.-C., Li C.-S. R. (2016). Hemispheric Lateralization of resting-state functional connectivity of the anterior insula: association with age, gender, and a novelty-seeking trait. Brain Connect. 6, 724–734. 10.1089/brain.2016.0443 PubMed DOI PMC

Kong X.-Z., Mathias S. R., Guadalupe T., ENIGMA Laterality Working Group. Glahn D. C., Franke B., et al. . (2018). Mapping cortical brain asymmetry in 17,141 healthy individuals worldwide via the ENIGMA Consortium. Proc. Natl. Acad. Sci. U.S.A. 115, E5154–E5163. 10.1073/pnas.1718418115 PubMed DOI PMC

Koops E. A., Renken R. J., Lanting C. P., van Dijk P. (2020). Cortical tonotopic map changes in humans are larger in hearing loss than in additional tinnitus. J. Neurosci. 40, 3178–3185. 10.1523/JNEUROSCI.2083-19.2020 PubMed DOI PMC

Landgrebe M., Langguth B., Rosengarth K., Braun S., Koch A., Kleinjung T., et al. . (2009). Structural brain changes in tinnitus: grey matter decrease in auditory and non-auditory brain areas. Neuroimage 46, 213–218. 10.1016/j.neuroimage.2009.01.069 PubMed DOI

Langers D. R. M., de Kleine E., van Dijk P. (2012). Tinnitus does not require macroscopic tonotopic map reorganization. Front. Syst. Neurosci. 6:2. 10.3389/fnsys.2012.00002 PubMed DOI PMC

Langguth B., Kreuzer P. M., Kleinjung T., De Ridder D. (2013). Tinnitus: causes and clinical management. Lancet Neurol. 12, 920–930. 10.1016/S1474-4422(13)70160-1 PubMed DOI

Lanting C. P., de Kleine E., van Dijk P. (2009). Neural activity underlying tinnitus generation: results from PET and fMRI. Hear. Res. 255, 1–13. 10.1016/j.heares.2009.06.009 PubMed DOI

Lenhardt M. L., Shulman A., Goldstein B. A. (2008). The role of the insula cortex in the final common pathway for tinnitus: experience using ultra-high-frequency therapy. Int. Tinnitus J. 14, 13–16. PubMed

Li W., Li J., Xian J., Lv B., Li M., Wang C., et al. . (2013). Alterations of grey matter asymmetries in adolescents with prelingual deafness: a combined VBM and cortical thickness analysis. Restor. Neurol. Neurosci. 31, 1–17. 10.3233/RNN-2012-120269 PubMed DOI

Li X., Wang H., Tian Y., Zhou S., Li X., Wang K., et al. . (2016). Impaired white matter connections of the limbic system networks associated with impaired emotional memory in Alzheimer's disease. Front. Aging Neurosci. 8:250. 10.3389/fnagi.2016.00250 PubMed DOI PMC

Lin F. R., Ferrucci L., Metter E. J., An Y., Zonderman A. B., Resnick S. M. (2011). Hearing loss and cognition in the Baltimore longitudinal study of aging. Neuropsychology 25, 763–770. 10.1037/a0024238 PubMed DOI PMC

Lin F. R., Yaffe K., Xia J., Xue Q.-L., Harris T. B., Purchase-Helzner E., et al. . (2013). Hearing loss and cognitive decline in older adults. JAMA Intern. Med. 173, 293–299. 10.1001/jamainternmed.2013.1868 PubMed DOI PMC

Maguire E. A., Frackowiak R. S., Frith C. D. (1996). Learning to find your way: a role for the human hippocampal formation. Proc. Biol. Sci. 263, 1745–1750. 10.1098/rspb.1996.0255 PubMed DOI

McCombe A., Baguley D., Coles R., McKenna L., McKinney C., Windle-Taylor P., et al. . (2001). Guidelines for the grading of tinnitus severity: the results of a working group commissioned by the British association of otolaryngologists, head and neck surgeons, 1999. Clin. Otolaryngol. Allied Sci. 26, 388–393. 10.1046/j.1365-2273.2001.00490.x PubMed DOI

Momi S. K., Wolber L. E., Fabiane S. M., MacGregor A. J., Williams F. M. K. (2015). Genetic and environmental factors in age-related hearing impairment. Twin Res. Hum. Genet. 18, 383–392. 10.1017/thg.2015.35 PubMed DOI

Mühlau M., Rauschecker J. P., Oestreicher E., Gaser C., Röttinger M., Wohlschlüger A. M., et al. . (2006). Structural brain changes in tinnitus. Cereb. Cortex 16, 1283–1288. 10.1093/cercor/bhj070 PubMed DOI

Munoz-Lopez M. M., Mohedano-Moriano A., Insausti R. (2010). Anatomical pathways for auditory memory in primates. Front. Neuroanat. 4:129. 10.3389/fnana.2010.00129 PubMed DOI PMC

Newman C. W., Jacobson G. P., Spitzer J. B. (1996). Development of the tinnitus handicap inventory. Arch. Otolaryngol. Head Neck Surg. 122, 143–148. 10.1001/archotol.1996.01890140029007 PubMed DOI

Norena A., Micheyl C., Chéry-Croze S., Collet L. (2002). Psychoacoustic characterization of the tinnitus spectrum: implications for the underlying mechanisms of tinnitus. Audiol. Neurootol. 7, 358–369. 10.1159/000066156 PubMed DOI

Ouda L., Profant O., Syka J. (2015). Age-related changes in the central auditory system. Cell Tissue Res. 361, 337–358. 10.1007/s00441-014-2107-2 PubMed DOI

Pearson J. D., Morrell C. H., Gordon-Salant S., Brant L. J., Metter E. J., Klein L. L., et al. . (1995). Gender differences in a longitudinal study of age-associated hearing loss. J. Acoust. Soc. Am. 97, 1196–1205. 10.1121/1.412231 PubMed DOI

Penhune V. B., Cismaru R., Dorsaint-Pierre R., Petitto L. A., Zatorre R. J. (2003). The morphometry of auditory cortex in the congenitally deaf measured using MRI. Neuroimage 20, 1215–1225. 10.1016/S1053-8119(03)00373-2 PubMed DOI

Pinheiro J., Bates D. (2010). Mixed-Effects Models in S and S-PLUS. New York, NY: Springer.

Profant O., Balogová Z., Dezortová M., Wagnerová D., Hájek M., Syka J. (2013). Metabolic changes in the auditory cortex in presbycusis demonstrated by MR spectroscopy. Exp. Gerontol. 48, 795–800. 10.1016/j.exger.2013.04.012 PubMed DOI

Profant O., Jilek M., Bures Z., Vencovsky V., Kucharova D., Svobodova V., et al. . (2019). Functional age-related changes within the human auditory system studied by audiometric examination. Front. Aging Neurosci. 11:26. 10.3389/fnagi.2019.00026 PubMed DOI PMC

Profant O., Škoch A., Balogová Z., Tintěra J., Hlinka J., Syka J. (2014). Diffusion tensor imaging and MR morphometry of the central auditory pathway and auditory cortex in aging. Neuroscience 260, 87–97. 10.1016/j.neuroscience.2013.12.010 PubMed DOI

Profant O., Tintěra J., Balogová Z., Ibrahim I., Jilek M., Syka J. (2015). Functional changes in the human auditory cortex in ageing. PLoS ONE 10:e0116692. 10.1371/journal.pone.0116692 PubMed DOI PMC

Rauschecker J. P., Leaver A. M., Mühlau M. (2010). Tuning out the noise: limbic-auditory interactions in tinnitus. Neuron 66, 819–826. 10.1016/j.neuron.2010.04.032 PubMed DOI PMC

Resnick S. M., Pham D. L., Kraut M. A., Zonderman A. B., Davatzikos C. (2003). Longitudinal magnetic resonance imaging studies of older adults: a shrinking brain. J. Neurosci. 23, 3295–3301. 10.1523/JNEUROSCI.23-08-03295.2003 PubMed DOI PMC

Reuter M., Rosas H. D., Fischl B. (2010). Highly accurate inverse consistent registration: a robust approach. Neuroimage 53, 1181–1196. 10.1016/j.neuroimage.2010.07.020 PubMed DOI PMC

Reuter M., Schmansky N. J., Rosas H. D., Fischl B. (2012). Within-subject template estimation for unbiased longitudinal image analysis. Neuroimage 61, 1402–1418. 10.1016/j.neuroimage.2012.02.084 PubMed DOI PMC

Sandu A.-L., Artiges E., Galinowski A., Gallarda T., Bellivier F., Lemaitre H., et al. . (2017). Amygdala and regional volumes in treatment-resistant versus nontreatment-resistant depression patients. Depress. Anxiety 34, 1065–1071. 10.1002/da.22675 PubMed DOI

Saygin Z. M., Kliemann D., Iglesias J. E., van der Kouwe A. J. W., Boyd E., Reuter M., et al. . (2017). High-resolution magnetic resonance imaging reveals nuclei of the human amygdala: manual segmentation to automatic atlas. Neuroimage 155, 370–382. 10.1016/j.neuroimage.2017.04.046 PubMed DOI PMC

Schmidt S. A., Akrofi K., Carpenter-Thompson J. R., Husain F. T. (2013). Default mode, dorsal attention and auditory resting state networks exhibit differential functional connectivity in tinnitus and hearing loss. PLoS ONE 8:e76488. 10.1371/journal.pone.0076488 PubMed DOI PMC

Schmidt S. A., Zimmerman B., Bido Medina R. O., Carpenter-Thompson J. R., Husain F. T. (2018). Changes in gray and white matter in subgroups within the tinnitus population. Brain Res. 1679, 64–74. 10.1016/j.brainres.2017.11.012 PubMed DOI

Schnack H. G., van Haren N. E. M., Brouwer R. M., Evans A., Durston S., Boomsma D. I., et al. . (2015). Changes in thickness and surface area of the human cortex and their relationship with intelligence. Cereb. Cortex 25, 1608–1617. 10.1093/cercor/bht357 PubMed DOI

Schneider P., Andermann M., Wengenroth M., Goebel R., Flor H., Rupp A., et al. . (2009). Reduced volume of Heschl's gyrus in tinnitus. Neuroimage 45, 927–939. 10.1016/j.neuroimage.2008.12.045 PubMed DOI

Seeley W. W., Menon V., Schatzberg A. F., Keller J., Glover G. H., Kenna H., et al. . (2007). Dissociable intrinsic connectivity networks for salience processing and executive control. J. Neurosci. 27, 2349–2356. 10.1523/JNEUROSCI.5587-06.2007 PubMed DOI PMC

Ségonne F., Dale A. M., Busa E., Glessner M., Salat D., Hahn H. K., et al. . (2004). A hybrid approach to the skull stripping problem in MRI. Neuroimage 22, 1060–1075. 10.1016/j.neuroimage.2004.03.032 PubMed DOI

Shargorodsky J., Curhan G. C., Farwell W. R. (2010). Prevalence and characteristics of tinnitus among US adults. Am. J. Med. 123, 711–718. 10.1016/j.amjmed.2010.02.015 PubMed DOI

Shiell M. M., Champoux F., Zatorre R. J. (2016). The right hemisphere planum temporale supports enhanced visual motion detection ability in deaf people: evidence from cortical thickness. Neural Plast. 2016:7217630. 10.1155/2016/7217630 PubMed DOI PMC

Shore S. E., Roberts L. E., Langguth B. (2016). Maladaptive plasticity in tinnitus–triggers, mechanisms and treatment. Nat. Rev. Neurol. 12, 150–160. 10.1038/nrneurol.2016.12 PubMed DOI PMC

Sluimer J. D., van der Flier W. M., Karas G. B., van Schijndel R., Barnes J., Boyes R. G., et al. . (2009). Accelerating regional atrophy rates in the progression from normal aging to Alzheimer's disease. Eur. Radiol. 19, 2826–2833. 10.1007/s00330-009-1512-5 PubMed DOI PMC

Syka J. (2002). Plastic changes in the central auditory system after hearing loss, restoration of function, and during learning. Physiol. Rev. 82, 601–636. 10.1152/physrev.00002.2002 PubMed DOI

Tervaniemi M., Hugdahl K. (2003). Lateralization of auditory-cortex functions. Brain Res. Rev. 43, 231–246. 10.1016/j.brainresrev.2003.08.004 PubMed DOI

Thambisetty M., Wan J., Carass A., An Y., Prince J. L., Resnick S. M. (2010). Longitudinal changes in cortical thickness associated with normal aging. Neuroimage 52, 1215–1223. 10.1016/j.neuroimage.2010.04.258 PubMed DOI PMC

Thompson P. M., Hayashi K. M., Sowell E. R., Gogtay N., Giedd J. N., Rapoport J. L., et al. . (2004). Mapping cortical change in Alzheimer's disease, brain development, and schizophrenia. Neuroimage 23, S2–S18. 10.1016/j.neuroimage.2004.03.040 PubMed DOI

Tu N. C., Friedman R. A. (2018). Age-related hearing loss: unraveling the pieces. Laryngoscope Investig Otolaryngol. 3, 68–72. 10.1002/lio2.134 PubMed DOI PMC

Uddin L. Q., Nomi J. S., Hébert-Seropian B., Ghaziri J., Boucher O. (2017). Structure and function of the human insula. J. Clin. Neurophysiol. 34, 300–306. 10.1097/WNP.0000000000000377 PubMed DOI PMC

Vanneste S., De Ridder D. (2012). The auditory and non-auditory brain areas involved in tinnitus. an emergent property of multiple parallel overlapping subnetworks. Front. Syst. Neurosci. 6:31. 10.3389/fnsys.2012.00031 PubMed DOI PMC

Vanneste S., Plazier M., van der Loo E., Van de Heyning P., De Ridder D. (2011). The difference between uni- and bilateral auditory phantom percept. Clin. Neurophysiol. 122, 578–587. 10.1016/j.clinph.2010.07.022 PubMed DOI

Vanneste S., Van De Heyning P., De Ridder D. (2015). Tinnitus: a large VBM-EEG correlational study. PLoS ONE 10:e0115122. 10.1371/journal.pone.0115122 PubMed DOI PMC

Watkins K. E., Paus T., Lerch J. P., Zijdenbos A., Collins D. L., Neelin P., et al. . (2001). Structural asymmetries in the human brain: a voxel-based statistical analysis of 142 MRI scans. Cereb. Cortex 11, 868–877. 10.1093/cercor/11.9.868 PubMed DOI

Weinberger N. M. (2007). Auditory associative memory and representational plasticity in the primary auditory cortex. Hear. Res. 229, 54–68. 10.1016/j.heares.2007.01.004 PubMed DOI PMC

Weisz N., Hartmann T., Dohrmann K., Schlee W., Norena A. (2006). High-frequency tinnitus without hearing loss does not mean absence of deafferentation. Hear. Res. 222, 108–114. 10.1016/j.heares.2006.09.003 PubMed DOI

Xu X.-M., Jiao Y., Tang T.-Y., Zhang J., Salvi R., Teng G.-J. (2019). Inefficient involvement of insula in sensorineural hearing loss. Front. Neurosci. 13:133. 10.3389/fnins.2019.00133 PubMed DOI PMC

Yoo H. B., De Ridder D., Vanneste S. (2016). The importance of aging in gray matter changes within tinnitus patients shown in cortical thickness, surface area and volume. Brain Topogr. 29, 885–896. 10.1007/s10548-016-0511-5 PubMed DOI

Zatorre R. J., Belin P. (2001). Spectral and temporal processing in human auditory cortex. Cereb. Cortex 11, 946–953. 10.1093/cercor/11.10.946 PubMed DOI

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