Age related hearing loss (presbycusis) is one of the most common sensory deficits in the aging population. The main subjective ailment in the elderly is the deterioration of speech understanding, especially in a noisy environment, which cannot solely be explained by increased hearing thresholds. The examination methods used in presbycusis are primarily focused on the peripheral pathologies (e.g., hearing sensitivity measured by hearing thresholds), with only a limited capacity to detect the central lesion. In our study, auditory tests focused on central auditory abilities were used in addition to classical examination tests, with the aim to compare auditory abilities between an elderly group (elderly, mean age 70.4 years) and young controls (young, mean age 24.4 years) with clinically normal auditory thresholds, and to clarify the interactions between peripheral and central auditory impairments. Despite the fact that the elderly were selected to show natural age-related deterioration of hearing (auditory thresholds did not exceed 20 dB HL for main speech frequencies) and with clinically normal speech reception thresholds (SRTs), the detailed examination of their auditory functions revealed deteriorated processing of temporal parameters [gap detection threshold (GDT), interaural time difference (ITD) detection] which was partially responsible for the altered perception of distorted speech (speech in babble noise, gated speech). An analysis of interactions between peripheral and central auditory abilities, showed a stronger influence of peripheral function than temporal processing ability on speech perception in silence in the elderly with normal cognitive function. However, in a more natural environment mimicked by the addition of background noise, the role of temporal processing increased rapidly.

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

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

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

Department of Technical Studies College of Polytechnics Jihlava Czechia

Eye Clinic Liberec Liberec Czechia

See more in PubMed

Abel S. M. (1972). Duration discrimination of noise and tone bursts. J. Acoust. Soc. Am. 51, 1219–1223. 10.1121/1.1912963 PubMed DOI

Abel S. M., Giguère C., Consoli A., Papsin B. C. (2000). The effect of aging on horizontal plane sound localization. J. Acoust. Soc. Am. 108, 743–752. 10.1121/1.429607 PubMed DOI

Abel S. M., Hay V. H. (1996). Sound localization. The interaction of aging, hearing loss and hearing protection. Scand. Audiol. 25, 3–12. 10.3109/01050399609047549 PubMed DOI

Akeroyd M. A. (2008). Are individual differences in speech reception related to individual differences in cognitive ability? A survey of twenty experimental studies with normal and hearing-impaired adults. Int. J. Audiol. 47, S53–S71. 10.1080/14992020802301142 PubMed DOI

Anderson S., Parbery-Clark A., White-Schwoch T., Kraus N. (2012). Aging affects neural precision of speech encoding. J. Neurosci. 32, 14156–14164. 10.1523/JNEUROSCI.2176-12.2012 PubMed DOI PMC

Babkoff H., Muchnik C., Ben-David N., Furst M., Even-Zohar S., Hildesheimer M. (2002). Mapping lateralization of click trains in younger and older populations. Hear. Res. 165, 117–127. 10.1016/s0378-5955(02)00292-7 PubMed DOI

Bopp K. L., Verhaeghen P. (2009). Working memory and aging: separating the effects of content and context. Psychol. Aging 24, 968–980. 10.1037/a0017731 PubMed DOI PMC

Caspary D. M., Schatteman T. A., Hughes L. F. (2005). Age-related changes in the inhibitory response properties of dorsal cochlear nucleus output neurons: role of inhibitory inputs. J. Neurosci. 25, 10952–10959. 10.1523/JNEUROSCI.2451-05.2005 PubMed DOI PMC

CHABA . (1998). Speech understanding and aging. working group on speech understanding and aging. committee on hearing, bioacoustics and biomechanics, commission on behavioral and social sciences and education, national research council. J. Acoust. Soc. Am. 83, 859–895. PubMed

Dlouhá O., Vokřál J., Cerny L. (2013). Test of sentence intelligibility in babble noise in persons with normal hearing. Otorhinolaryngol. Foniatrie 61, 240–244.

Fitzgibbons P. J., Gordon-Salant S. (1994). Age effects on measures of auditory duration discrimination. J. Speech Hear. Res. 37, 662–670. 10.1044/jshr.3703.662 PubMed DOI

Fitzgibbons P. J., Gordon-Salant S. (1995). Age effects on duration discrimination with simple and complex stimuli. J. Acoust. Soc. Am. 98, 3140–3145. 10.1121/1.413803 PubMed DOI

Fitzgibbons P. J., Gordon-Salant S. (2011). Age effects in discrimination of repeating sequence intervals. J. Acoust. Soc. Am. 129, 1490–1500. 10.1121/1.3533728 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

Fowler E. P., Sabine P. E. (1942). Tentative standard procedure for evaluating the percentage of useful hearing loss in medicolegal cases. JAMA 119, 1108–1109.

Frisina D. R., Frisina R. D. (1997). Speech recognition in noise and presbycusis: relations to possible neural mechanisms. Hear. Res. 106, 95–104. 10.1016/s0378-5955(97)00006-3 PubMed DOI

Frisina R. D., Walton J. P. (2006). Age-related structural and functional changes in the cochlear nucleus. Hear. Res. 216–223. 10.1016/j.heares.2006.02.003 PubMed DOI

Füllgrabe C., Moore B. C. J. (2014). Effects of age and hearing loss on stream segregation based on interaural time differences. J. Acoust. Soc. Am. 136, EL185–EL191. 10.1121/1.4890201 PubMed DOI

Gardner G., Robertson J. H. (1988). Hearing preservation in unilateral acoustic neuroma surgery. Ann. Otol. Rhinol. Laryngol. 97, 55–66. 10.1177/000348948809700110 PubMed DOI

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

Gates G. A., Cooper J. C., Kannel W. B., Miller N. J. (1990). Hearing in the elderly: the Framingham cohort, 1983-1985. Part I. Basic audiometric test results. Ear Hear. 11, 247–256. PubMed

Giroud N., Hirsiger S., Muri R., Kegel A., Dillier N., Meyer M. (2018). 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

Gordon-Salant S., Fitzgibbons P. J. (1993). Temporal factors and speech recognition performance in young and elderly listeners. J. Speech Hear. Res. 36, 1276–1285. 10.1044/jshr.3606.1276 PubMed DOI

Gordon-Salant S., Fitzgibbons P. J. (1997). Selected cognitive factors and speech recognition performance among young and elderly listeners. J. Speech Lang. Hear. Res. JSLHR 40, 423–431. 10.1044/jslhr.4002.423 PubMed DOI

Gordon-Salant S., Zion D. J., Espy-Wilson C. (2014). Recognition of time-compressed speech does not predict recognition of natural fast-rate speech by older listeners. J. Acoust. Soc. Am. 136, EL268–274. 10.1121/1.4895014 PubMed DOI PMC

Grady C. L. (2008). Cognitive neuroscience of aging. Ann. N Y Acad. Sci. 1124, 127–144. 10.1196/annals.1440.009 PubMed DOI

Grassi M., Borella E. (2013). The role of auditory abilities in basic mechanisms of cognition in older adults. Front. Aging Neurosci. 5:59. 10.3389/fnagi.2013.00059 PubMed DOI PMC

Greenber S. (1996). “Auditory processing of speech,” in Principles of Experimental Phonetics, ed. Lass N. (St. Louis: Mosby; ), 364–407.

Grose J. H., Hall J. W., Buss E. (2006). Temporal processing deficits in the pre-senescent auditory system. J. Acoust. Soc. Am. 119, 2305–2315. PubMed 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

He N. J., Horwitz A. R., Dubno J. R., Mills J. H. (1999). Psychometric functions for gap detection in noise measured from young and aged subjects. J. Acoust. Soc. Am. 106, 966–978. 10.1121/1.427109 PubMed DOI

Helleman H. W., Jansen E. J. M., Dreschler W. A. (2010). Otoacoustic emissions in a hearing conservation program: general applicability in longitudinal monitoring and the relation to changes in pure-tone thresholds. Int. J. Audiol. 49, 410–419. 10.3109/14992020903527616 PubMed DOI

Hickox A. E., Larsen E., Heinz M. G., Shinobu L., Whitton J. P. (2017). Translational issues in cochlear synaptopathy. Hear. Res. 349, 164–171. 10.3410/f.727192264.793532887 PubMed DOI PMC

Humes L. E. (1996). Speech understanding in the elderly. J. Am. Acad. Audiol. 7, 161–167. PubMed

Humes L. E., Dubno J. R., Gordon-Salant S., Lister J. J., Cacace A. T., Cruickshanks K. J., et al. . (2012). Central presbycusis: a review and evaluation of the evidence. J. Am. Acad. Audiol. 23, 635–666. 10.3766/jaaa.23.8.5 PubMed DOI PMC

Jacobson M., Kim S., Romney J., Zhu X., Frisina R. D. (2003). Contralateral suppression of distortion-product otoacoustic emissions declines with age: a comparison of findings in CBA mice with human listeners. Laryngoscope 113, 1707–1713. 10.1097/00005537-200310000-00009 PubMed DOI

Jayakody D. M. P., Friedland P. L., Martins R. N., Sohrabi H. R. (2018). Impact of aging on the auditory system and related cognitive functions: a narrative review. Front. Neurosci. 12:125 10.3389/fnins.2018.00125 PubMed DOI PMC

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

Kim S., Frisina D. R., Frisina R. D. (2002). Effects of age on contralateral suppression of distortion product otoacoustic emissions in human listeners with normal hearing. Audiol. Neurootol. 7, 348–357. 10.1159/000066159 PubMed DOI

Kujawa S. G., Liberman M. C. (2009). Adding insult to injury: cochlear nerve degeneration after “temporary” noise-induced hearing loss. J. Neurosci. Off. J. Soc. Neurosci. 29, 14077–14085. 10.1523/JNEUROSCI.2845-09.2009 PubMed DOI PMC

Liberman M. C., Kujawa S. G. (2017). Cochlear synaptopathy in acquired sensorineural hearing loss: Manifestations and mechanisms. Hear. Res. 349, 138–147. 10.1016/j.heares.2017.01.003 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

Matthews L. J., Lee F. S., Mills J. H., Dubno J. R. (1997). Extended high-frequency thresholds in older adults. J. Speech Lang. Hear. Res. 40, 208–214. 10.1044/jslhr.4001.208 PubMed DOI

Mazelová J., Popelar J., Syka J. (2003). Auditory function in presbycusis: peripheral vs. central changes. Exp. Gerontol. 38, 87–94. 10.1016/s0531-5565(02)00155-9 PubMed DOI

Mitsudo T., Hironaga N., Mori S. (2014). Cortical activity associated with the detection of temporal gaps in tones: a magnetoencephalography study. Front. Hum. Neurosci. 8:763 10.3389/fnhum.2014.00763 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

Nasreddine Z. S., Phillips N. A., Bédirian V., Charbonneau S., Whitehead V., Collin I., et al. . (2005). The montreal cognitive assessment, MoCA: a brief screening tool for mild cognitive impairment. J. Am. Geriatr. Soc. 53, 695–699. 10.1111/j.1532-5415.2005.53221.x PubMed DOI

Noble W., Byrne D., Lepage B. (1994). Effects on sound localization of configuration and type of hearing impairment. J. Acoust. Soc. Am. 95, 992–1005. 10.1121/1.408404 PubMed DOI

Ouda L., Burianova J., Syka J. (2015). Age-related changes in calbindin and calretinin immunoreactivity in the central auditory system of the rat. Exp. Gerontol. 47, 497–506. 10.1016/j.exger.2012.04.003 PubMed DOI

Ozmeral E. J., Eddins A. C., Frisina D. R., Eddins D. A. (2016a). Large cross-sectional study of presbycusis reveals rapid progressive decline in auditory temporal acuity. Neurobiol. Aging 43, 72–78. 10.1016/j.neurobiolaging.2015.12.024 PubMed DOI PMC

Ozmeral E. J., Eddins D. A., Eddins A. C. (2016b). Reduced temporal processing in older, normal-hearing listeners evident from electrophysiological responses to shifts in interaural time difference. J. Neurophysiol. 116, 2720–2729. 10.1152/jn.00560.2016 PubMed DOI PMC

Pannese A., Grandjean D., Frühholz S. (2015). Subcortical processing in auditory communication. Hear. Res. 328, 67–77. 10.1016/j.heares.2015.07.003 PubMed DOI

Pearman A., Friedman L., Brooks J. O., Yesavage J. A. (2000). Hearing impairment and serial word recall in older adults. Exp. Aging Res. 26, 383–391. 10.1080/036107300750015769 PubMed DOI

Pecka M., Brand A., Behrend O., Grothe B. (2008). Interaural time difference processing in the mammalian medial superior olive: the role of glycinergic inhibition. J. Neurosci. 28, 6914–6925. 10.1523/jneurosci.1660-08.2008 PubMed DOI PMC

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

Pickett J. M. (1999). The Acoustics of Speech Communication: Fundamentals, Speech Perception Theory and Technology. Boston: Allyn and Bacon.

Popelář J., Rybalko N., Burianová J., Schwaller B., Syka J. (2013). The effect of parvalbumin deficiency on the acoustic startle response and prepulse inhibition in mice. Neurosci. Lett. 553, 216–220. 10.1016/j.neulet.2013.08.042 PubMed DOI

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., Roth J., Bureš Z., Balogová Z., Lišková I., Betka J., et al. (2017). Auditory dysfunction in patients with Huntington’s disease. Clin. Neurophysiol. 128, 1946–1953. 10.1016/j.clinph.2017.07.403 PubMed DOI

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

Pronk M., Deeg D. J., Festen J. M., Twisk J. W., Smits C., Comijs H. C., et al. . (2013). Decline in older persons’ ability to recognize speech in noise: the influence of demographic, health-related, environmental, and cognitive factors. Ear Hear. 34, 722–732. 10.1097/AUD.0b013e3182994eee PubMed DOI

Reban J. (2006). Montrealský kognitivni test /MoCA/: přínos k diagnostice predemencí. Čes Ger Revue 4, 224–229.

Rektorová I. (2011). Screeningové škály pro hodnocení demence. Neurol. Praxi 12, 37–45.

Ross B., Fujioka T., Tremblay K. L., Picton T. W. (2007). Aging in binaural hearing begins in mid-life: evidence from cortical auditory-evoked responses to changes in interaural phase. J. Neurosci. 27, 11172–11178. 10.1523/jneurosci.1813-07.2007 PubMed DOI PMC

Rybalko N., Suta D., Popelár J., Syka J. (2010). Inactivation of the left auditory cortex impairs temporal discrimination in the rat. Behav. Brain Res. 209, 123–130. 10.1016/j.bbr.2010.01.028 PubMed DOI

Schatteman T. A., Hughes L. F., Caspary D. M. (2008). Aged-related loss of temporal processing: altered responses to amplitude modulated tones in rat dorsal cochlear nucleus. Neuroscience 154, 329–337. 10.1016/j.neuroscience.2008.02.025 PubMed DOI PMC

Schuknecht H. F., Gacek M. R. (1993). Cochlear pathology in presbycusis. Ann. Otol. Rhinol. Laryngol. 102, 1–16. 10.1177/00034894931020s101 PubMed DOI

Seeman M., (1960). Czech Speech Audiometry. Prague: SZN.

Sergeyenko Y., Lall K., Liberman M. C., Kujawa S. G. (2013). Age-related cochlear synaptopathy: an early-onset contributor to auditory functional decline. J. Neurosci. 33, 13686–13694. 10.1523/jneurosci.1783-13.2013 PubMed DOI PMC

Sheldon S., Pichora-Fuller M. K., Schneider B. A. (2008). Priming and sentence context support listening to noise-vocoded speech by younger and older adults. J. Acoust. Soc. Am. 123, 489–499. 10.1121/1.2783762 PubMed DOI

Singh G., Pichora-Fuller M. K., Schneider B. A. (2008). The effect of age on auditory spatial attention in conditions of real and simulated spatial separation. J. Acoust. Soc. Am. 124, 1294–1305. 10.1121/1.2949399 PubMed DOI

Snell K. B. (1997). Age-related changes in temporal gap detection. J. Acoust. Soc. Am. 101, 2214–2220. 10.1121/1.418205 PubMed DOI

Strouse A., Ashmead D. H., Ohde R. N., Grantham D. W. (1998). Temporal processing in the aging auditory system. J. Acoust. Soc. Am. 104, 2385–2399. 10.1121/1.423748 PubMed DOI

Sussman E. S., Horváth J., Winkler I., Orr M. (2007). The role of attention in the formation of auditory streams. Percept. Psychophys. 69, 136–152. 10.3758/bf03194460 PubMed DOI

Suta D., Rybalko N., Pelánová J., Popelář J., Syka J. (2011). Age-related changes in auditory temporal processing in the rat. Exp. Gerontol. 46, 739–746. 10.1016/j.exger.2011.05.004 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. 10.1152/physrev.00002.2002 PubMed DOI

Syka J. (2010). The fischer 344 rat as a model of presbycusis. Hear. Res. 264, 70–78. 10.1016/j.heares.2009.11.003 PubMed DOI

Tadros S. F., Frisina S. T., Mapes F., Kim S., Frisina D. R., Frisina R. D. (2005). Loss of peripheral right-ear advantage in age-related hearing loss. Audiol. Neurootol. 10, 44–52. 10.1159/000082307 PubMed DOI

Ueberfuhr M. A., Fehlberg H., Goodman S. S., Withnell R. H. (2016). A DPOAE assessment of outer hair cell integrity in ears with age-related hearing loss. Hear. Res. 332, 137–150. 10.1016/j.heares.2015.11.006 PubMed DOI

Vielsmeier V., Lehner A., Strutz J., Steffens T., Kreuzer P. M., Schecklmann M., et al. . (2015). The relevance of the high frequency audiometry in tinnitus patients with normal hearing in conventional pure-tone audiometry. BioMed Res. Int. 2015:302515. 10.1155/2015/302515 PubMed DOI PMC

Walton J. P., Frisina R. D., O’Neill W. E. (1998). Age-related alteration in processing of temporal sound features in the auditory midbrain of the CBA mouse. J. Neurosci. 18, 2764–2776. 10.1523/jneurosci.18-07-02764.1998 PubMed DOI PMC

Wiley T. L., Cruickshanks K. J., Nondahl D. M., Tweed T. S., Klein R., Klein R., et al. . (1998). Aging and high-frequency hearing sensitivity. J. Speech Lang. Hear. Res. 41, 1061–1072. 10.1044/jslhr.4105.1061 PubMed DOI

Williamson T. T., Zhu X., Walton J. P., Frisina R. D. (2015). Auditory brainstem gap responses start to decline in mice in middle age: a novel physiological biomarker for age-related hearing loss. Cell Tissue Res. 361, 359–369. 10.1007/s00441-014-2003-9 PubMed DOI PMC

Willott J. F. (1996). Anatomic and physiologic aging: a behavioral neuroscience perspective. J. Am. Acad. Audiol. 7, 141–151. PubMed

Wingfield A. (1996). Cognitive factors in auditory performance: context, speed of processing, and constraints of memory. J. Am. Acad. Audiol. 7, 175–182. PubMed

Wingfield A., McCoy S. L., Peelle J. E., Tun P. A., Cox L. C. (2006). Effects of adult aging and hearing loss on comprehension of rapid speech varying in syntactic complexity. J. Am. Acad. Audiol. 17, 487–497. 10.3766/jaaa.17.7.4 PubMed DOI

Zeng F.-G., Kong Y.-Y., Michalewski H. J., Starr A. (2005). Perceptual consequences of disrupted auditory nerve activity. J. Neurophysiol. 93, 3050–3063. 10.1152/jn.00985.2004 PubMed DOI

Speech intelligibility and its relation to auditory temporal processing in Czech and Swiss German subjects with and without tinnitus

Functional changes in the auditory cortex and associated regions caused by different acoustic stimuli in patients with presbycusis and tinnitus

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

Speech Comprehension and Its Relation to Other Auditory Parameters in Elderly Patients With Tinnitus