Presbycusis and tinnitus are the two most common hearing related pathologies. Although both of these conditions presumably originate in the inner ear, there are several reports concerning their central components. Interestingly, the onset of presbycusis coincides with the highest occurrence of tinnitus. The aim of this study was to identify age, hearing loss, and tinnitus related functional changes, within the auditory system and its associated structures. Seventy-eight participants were selected for the study based on their age, hearing, and tinnitus, and they were divided into six groups: young controls (Y-NH-NT), subjects with mild presbycusis (O-NH-NT) or expressed presbycusis (O-HL-NT), young subjects with tinnitus (Y-NH-T), subjects with mild presbycusis and tinnitus (O-NH-T), and subjects with expressed presbycusis and tinnitus (O-HL-T). An MRI functional study was performed with a 3T MRI system, using an event related design (different types of acoustic and visual stimulations and their combinations). The amount of activation of the auditory cortices (ACs) was dependent on the complexity of the stimuli; higher complexity resulted in a larger area of the activated cortex. Auditory stimulation produced a slightly greater activation in the elderly, with a negative effect of hearing loss (lower activation). The congruent audiovisual stimulation led to an increased activity within the default mode network, whereas incongruent stimulation led to increased activation of the visual cortex. The presence of tinnitus increased activation of the AC, specifically in the aged population, with a slight prevalence in the left AC. The occurrence of tinnitus was accompanied by increased activity within the insula and hippocampus bilaterally. Overall, we can conclude that expressed presbycusis leads to a lower activation of the AC, compared to the elderly with normal hearing; aging itself leads to increased activity in the right AC. The complexity of acoustic stimuli plays a major role in the activation of the AC, its support by visual stimulation leads to minimal changes within the AC. Tinnitus causes changes in the activity of the limbic system, as well as in the auditory AC, where it is bound to the left hemisphere.

Department of Auditory Neuroscience Institute of Experimental Medicine The Czech Academy of Sciences Prague Czechia

Department of Otorhinolaryngology 3rd Faculty of Medicine Faculty Hospital Královské Vinohrady Charles University Prague Czechia

Department of Otorhinolaryngology Head and Neck Surgery 1st Faculty of Medicine Charles University Prague and University Hospital Motol Prague Czechia

MR Unit Institute for Clinical and Experimental Medicine Prague Czechia

Zobrazit více v PubMed

Arons B. (1992). A review of the cocktail party effect. J. Am. Voice Soc. 12 35–50.

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

Berlot E., Arts R., Smit J., George E., Gulban O. F., Moerel M., et al. (2020). A 7 Tesla fMRI investigation of human tinnitus percept in cortical and subcortical auditory areas. Neuroimage Clin. 25:102166. 10.1016/j.nicl.2020.102166 PubMed DOI PMC

Bischoff M., Walter B., Blecker C. R., Morgen K., Vaitl D., Sammer G. (2007). Utilizing the ventriloquism-effect to investigate audio-visual binding. Neuropsychologia 45 578–586. 10.1016/j.neuropsychologia.2006.03.008 PubMed DOI

Bizley J. K., King A. J. (2009). Visual influences on ferret auditory cortex. Hear. Res. 258 55–63. 10.1016/j.heares.2009.06.017 PubMed DOI PMC

Boemio A., Fromm S., Braun A., Poeppel D. (2005). Hierarchical and asymmetric temporal sensitivity in human auditory cortices. Nat. Neurosci. 8 389–395. 10.1038/nn1409 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

Cardon E., Jacquemin L., Mertens G., Van de Heyning P., Vanderveken O. M., Topsakal V., et al. (2019). Cognitive performance in chronic tinnitus patients: a cross-sectional study using the RBANS-H. Otol. Neurotol. 40 e876–e882. 10.1097/MAO.0000000000002403 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

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

Dlouhá O., Vokrál J., Cerný L. (2012). Test vetné srozumitelnosti v hovorovém šumu u osob s vadou sluchu. Otorhinolaryngol. Phoniatr. 61 240–244.

Eckert M. A., Vaden K. I., Dubno J. R. (2019). Age-Related hearing loss associations with changes in brain morphology. Trends Hear. 23:2331216519857267. 10.1177/2331216519857267 PubMed DOI PMC

Eggermont J. J. (2017). “Chapter 7 - epidemiology and genetics of hearing loss and tinnitus,” in Hearing Loss, ed. Eggermont J. J. (Cambridge, MA: Academic Press; ), 209–234. 10.1016/B978-0-12-805398-0.00007-4 DOI

Eggermont J. J., Roberts L. E. (2012). The neuroscience of tinnitus: understanding abnormal and normal auditory perception. Front. Syst. Neurosci. 6:53. 10.3389/fnsys.2012.00053 PubMed DOI PMC

Fogerty D., Ahlstrom J. B., Bologna W. J., Dubno J. R. (2015). Sentence intelligibility during segmental interruption and masking by speech-modulated noise: effects of age and hearing loss. J. Acoust. Soc. Am. 137 3487–3501. 10.1121/1.4921603 PubMed DOI PMC

Forster B., Cavina-Pratesi C., Aglioti S. M., Berlucchi G. (2002). Redundant target effect and intersensory facilitation from visual-tactile interactions in simple reaction time. Exp. Brain Res. 143 480–487. 10.1007/s00221-002-1017-9 PubMed DOI

Fuksa J., Profant O., Chovanec M., Syka J. (2021). Vztah mezi presbyakuzí a poruchou kognitivních funkcí ve stárí. Otorhinolaryngol. Phoniatr. 70 223–233.

Gates G. A., Mills J. H. (2005). Presbycusis. Lancet 366 1111–1120. 10.1016/S0140-6736(05)67423-5 PubMed DOI

Geven L. I., de Kleine E., Willemsen A. T. M., van Dijk P. (2014). Asymmetry in primary auditory cortex activity in tinnitus patients and controls. Neuroscience 256 117–125. 10.1016/j.neuroscience.2013.10.015 PubMed DOI

Gilles A., Schlee W., Rabau S., Wouters K., Fransen E., Van de Heyning P. (2016). Decreased speech-in-noise understanding in young adults with tinnitus. Front. Neurosci. 10. Available online at: https://www.frontiersin.org/article/10.3389/fnins.2016.00288 (accessed April 2, 2022). PubMed DOI PMC

Giroud N., Hirsiger S., Muri R., Kegel A., Dillier N., Meyer M. (2017). Neuroanatomical and resting state EEG power correlates of central hearing loss in older adults. Brain Struct. Funct. 223 145–163. 10.1007/s00429-017-1477-0 PubMed DOI

Glick H., Sharma A. (2017). Cross-modal plasticity in developmental and age-related hearing loss: clinical implications. Hear. Res. 343 191–201. 10.1016/j.heares.2016.08.012 PubMed DOI PMC

Grose J. H., Mamo S. K. (2010). Processing of temporal fine structure as a function of age. Ear Hear. 31 755–760. 10.1097/AUD.0b013e3181e627e7 PubMed DOI PMC

Hallam R. S., McKenna L., Shurlock L. (2004). Tinnitus impairs cognitive efficiency. Int. J. Audiol. 43 218–226. 10.1080/14992020400050030 PubMed DOI

Heller A. J. (2003). Classification and epidemiology of tinnitus. Otolaryngol. Clin. N. Am. 36 239–248. 10.1016/S0030-6665(02)00160-3 PubMed DOI

Hofmeier B., Wolpert S., Aldamer E. S., Walter M., Thiericke J., Braun C., et al. (2018). Reduced sound-evoked and resting-state BOLD fMRI connectivity in tinnitus. Neuroimage Clin. 20 637–649. 10.1016/j.nicl.2018.08.029 PubMed DOI PMC

House J. W., Brackmann D. E. (1981). Tinnitus: surgical treatment. Ciba Found. Symp. 85 204–216. 10.1002/9780470720677.ch12 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

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

Keller M., Neuschwander P., Meyer M. (2019). When right becomes less right: neural dedifferentiation during suprasegmental speech processing in the aging brain. Neuroimage 189 886–895. 10.1016/j.neuroimage.2019.01.050 PubMed DOI

Khan R. A., Husain F. T. (2020). Tinnitus and cognition: can load theory help us refine our understanding? Laryngoscope Investig. Otolaryngol. 5 1197–1204. 10.1002/lio2.501 PubMed DOI PMC

Khan R. A., Sutton B. P., Tai Y., Schmidt S. A., Shahsavarani S., Husain F. T. (2021). A large-scale diffusion imaging study of tinnitus and hearing loss. Sci. Rep. 11:23395. 10.1038/s41598-021-02908-6 PubMed DOI PMC

Knipper M., van Dijk P., Schulze H., Mazurek B., Krauss P., Scheper V., et al. (2020). The neural bases of tinnitus: lessons from deafness and cochlear implants. J. Neurosci. 40 7190–7202. 10.1523/JNEUROSCI.1314-19.2020 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

Kraus N., White-Schwoch T. (2015). Unraveling the biology of auditory learning: a cognitive-sensorimotor-reward framework. Trends Cogn. Sci. 19 642–654. 10.1016/j.tics.2015.08.017 PubMed DOI PMC

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

Lanting C., WoźAniak A., van Dijk P., Langers D. R. M. (2016). Tinnitus- and task-related differences in resting-state networks. Adv. Exp. Med. Biol. 894 175–187. 10.1007/978-3-319-25474-6_19 PubMed DOI

Lavie N., Hirst A., de Fockert J. W., Viding E. (2004). Load theory of selective attention and cognitive control. J. Exp. Psychol. Gen. 133 339–354. 10.1037/0096-3445.133.3.339 PubMed DOI

Leaver A. M., Seydell-Greenwald A., Rauschecker J. P. (2016). Auditory-limbic interactions in chronic tinnitus: challenges for neuroimaging research. Hear. Res. 334 49–57. 10.1016/j.heares.2015.08.005 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

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

McGettigan C., Scott S. K. (2012). Cortical asymmetries in speech perception: what’s wrong, what’s right and what’s left? Trends Cogn. Sci. 16 269–276. 10.1016/j.tics.2012.04.006 PubMed DOI PMC

Moon I. J., Won J. H., Kang H. W., Kim D. H., An Y.-H., Shim H. J. (2015). Influence of tinnitus on auditory spectral and temporal resolution and speech perception in tinnitus patients. J. Neurosci. 35 14260–14269. 10.1523/JNEUROSCI.5091-14.2015 PubMed DOI PMC

Moore B. C. J. (2016). Effects of age and hearing loss on the processing of auditory temporal fine structure. Adv. Exp. Med. Biol. 894 1–8. 10.1007/978-3-319-25474-6_1 PubMed DOI

Musacchia G., Schroeder C. E. (2009). Neuronal mechanisms, response dynamics and perceptual functions of multisensory interactions in auditory cortex. Hear. Res. 258 72–79. 10.1016/j.heares.2009.06.018 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

Nuesse T., Wiercinski B., Brand T., Holube I. (2019). Measuring speech recognition with a matrix test using synthetic speech. Trends Hear. 23:2331216519862982. 10.1177/2331216519862982 PubMed DOI PMC

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

Piccirillo J. F., Rodebaugh T. L., Lenze E. J. (2020). Tinnitus. JAMA 323:1497. 10.1001/jama.2020.0697 PubMed DOI

Pichora-Fuller M. K., Singh G. (2006). Effects of age on auditory and cognitive processing: implications for hearing aid fitting and audiologic rehabilitation. Trends Amplif. 10 29–59. 10.1177/108471380601000103 PubMed DOI PMC

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., Škoch A., Tintěra J., Svobodová V., Kuchárová D., Svobodová Burianová J., et al. (2020). The influence of aging, hearing, and tinnitus on the morphology of cortical gray matter, amygdala, and hippocampus. Front. Aging Neurosci. 12:553461. 10.3389/fnagi.2020.553461 PubMed DOI PMC

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

Refat F., Wertz J., Hinrichs P., Klose U., Samy H., Abdelkader R. M., et al. (2021). Co-occurrence of hyperacusis accelerates with tinnitus burden over time and requires medical care. Front. Neurol. 12:627522. 10.3389/fneur.2021.627522 PubMed DOI PMC

Rosemann S., Smith D., Dewenter M., Thiel C. M. (2020). Age-related hearing loss influences functional connectivity of auditory cortex for the McGurk illusion. Cortex 129 266–280. 10.1016/j.cortex.2020.04.022 PubMed DOI

Rosen S., Wise R. J. S., Chadha S., Conway E.-J., Scott S. K. (2011). Hemispheric asymmetries in speech perception: sense, nonsense and modulations. PLoS One 6:e24672. 10.1371/journal.pone.0024672 PubMed DOI PMC

Sadaghiani S., Hesselmann G., Kleinschmidt A. (2009). Distributed and antagonistic contributions of ongoing activity fluctuations to auditory stimulus detection. J. Neurosci. 29 13410–13417. 10.1523/JNEUROSCI.2592-09.2009 PubMed DOI PMC

Schecklmann M., Landgrebe M., Poeppl T. B., Kreuzer P., Männer P., Marienhagen J., et al. (2011). Neural correlates of tinnitus duration and distress: a positron emission tomography study. Hum. Brain Mapp. 34 233–240. 10.1002/hbm.21426 PubMed DOI PMC

Schönwiesner M., Krumbholz K., Rübsamen R., Fink G. R., von Cramon D. Y. (2007). Hemispheric asymmetry for auditory processing in the human auditory brain stem, thalamus, and cortex. Cereb. Cortex 17 492–499. 10.1093/cercor/bhj165 PubMed DOI

Schuknecht H. F. (1974). Pathology of the Ear. Cambridge, MA: Harvard Univ. Press.

Schuknecht H. F., Gacek M. R. (1993). Cochlear pathology in presbycusis. Ann. Otol. Rhinol. Laryngol. 102 1–16. 10.1177/00034894931020S101 PubMed DOI

Smits M., Kovacs S., de Ridder D., Peeters R. R., van Hecke P., Sunaert S. (2007). Lateralization of functional magnetic resonance imaging (fMRI) activation in the auditory pathway of patients with lateralized tinnitus. Neuroradiology 49 669–679. 10.1007/s00234-007-0231-3 PubMed DOI

Specht K., Osnes B., Hugdahl K. (2009). Detection of differential speech-specific processes in the temporal lobe using fMRI and a dynamic “sound morphing” technique. Hum. Brain Mapp. 30 3436–3444. 10.1002/hbm.20768 PubMed DOI PMC

Stouffer J. L., Tyler R. S. (1990). Characterization of tinnitus by tinnitus patients. J. Speech Hear. Disord. 55 439–453. 10.1044/jshd.5503.439 PubMed DOI

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

Tramo M. J., Cariani P. A., Koh C. K., Makris N., Braida L. D. (2005). Neurophysiology and neuroanatomy of pitch perception: auditory cortex. Ann. N. Y. Acad. Sci. 1060 148–174. 10.1196/annals.1360.011 PubMed DOI

Tramo M. J., Shah G. D., Braida L. D. (2002). Functional role of auditory cortex in frequency processing and pitch perception. J. Neurophysiol. 87 122–139. PubMed

Tremblay P., Brisson V., Deschamps I. (2021). Brain aging and speech perception: effects of background noise and talker variability. Neuroimage 227:117675. 10.1016/j.neuroimage.2020.117675 PubMed DOI

Wayne R. V., Johnsrude I. S. (2015). A review of causal mechanisms underlying the link between age-related hearing loss and cognitive decline. Ageing Res. Rev. 23 154–166. 10.1016/j.arr.2015.06.002 PubMed DOI

Wilke M., Lidzba K. (2007). LI-tool: a new toolbox to assess lateralization in functional MR-data. J. Neurosci. Methods 163 128–136. 10.1016/j.jneumeth.2007.01.026 PubMed DOI

Wilke M., Schmithorst V. J. (2006). A combined bootstrap/histogram analysis approach for computing a lateralization index from neuroimaging data. Neuroimage 33 522–530. 10.1016/j.neuroimage.2006.07.010 PubMed DOI

Working Group on Speech Understanding (1988). Speech understanding and aging. J. Acoust. Soc. Am. 83 859–895. 10.1121/1.395965 PubMed DOI

Wu J., Li Q., Bai O., Touge T. (2009). Multisensory interactions elicited by audiovisual stimuli presented peripherally in a visual attention task: a behavioral and event-related potential study in humans. J. Clin. Neurophysiol. 26 407–413. 10.1097/WNP.0b013e3181c298b1 PubMed DOI

Zaehle T., Wüstenberg T., Meyer M., Jäncke L. (2004). Evidence for rapid auditory perception as the foundation of speech processing: a sparse temporal sampling fMRI study. Eur. J. Neurosci. 20 2447–2456. 10.1111/j.1460-9568.2004.03687.x PubMed DOI

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

The effect of aging, hearing loss, and tinnitus on white matter in the human auditory system revealed with fixel-based analysis