Skip to main content
SpringerLink
Log in

Hearing loss and brain plasticity: the hyperactivity phenomenon

  • Review
  • Published:
Brain Structure and Function Aims and scope Submit manuscript

Abstract

Many aging adults experience some form of hearing problems that may arise from auditory peripheral damage. However, it has been increasingly acknowledged that hearing loss is not only a dysfunction of the auditory periphery but also results from changes within the entire auditory system, from periphery to cortex. Damage to the auditory periphery is associated with an increase in neural activity at various stages throughout the auditory pathway. Here, we review neurophysiological evidence of hyperactivity, auditory perceptual difficulties that may result from hyperactivity, and outline open conceptual and methodological questions related to the study of hyperactivity. We suggest that hyperactivity alters all aspects of hearing—including spectral, temporal, spatial hearing—and, in turn, impairs speech comprehension when background sound is present. By focusing on the perceptual consequences of hyperactivity and the potential challenges of investigating hyperactivity in humans, we hope to bring animal and human electrophysiologists closer together to better understand hearing problems in older adulthood.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abel SM, Giguere C, Consoli A, Papsin BC (2000) The effect of aging on horizontal plane sound localization. J Acoust Soc Am 108:743–752

    Article  CAS  PubMed  Google Scholar 

  • Abolafia JM, Vergara R, Arnold MM, Reig R, Sanchez-Vives MV (2011) Cortical auditory adaptation in the awake rat and the role of potassium currents. Cereb Cortex 21:977–990

    Article  PubMed  Google Scholar 

  • Aizenberg M, Mwilambwe-Tshilobo L, Briguglio JJ, Natan RG, Geffen MN (2015) Bidirectional regulation of innate and learned behaviors that rely on frequency discrimination by cortical inhibitory neurons. PLoS Biol 13:e1002308

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Alain C, McDonald K, Van Roon P (2012) Effects of age and background noise on processing a mistuned harmonic in an otherwise periodic complex sound. Hear Res 283:126–135

    Article  PubMed  Google Scholar 

  • Alain C, Roye A, Salloum C (2014) Effects of age-related hearing loss and background noise on neuromagnetic activity from auditory cortex. Front Syst Neurosci. https://doi.org/10.3389/fnsys.2014.00008

    Article  PubMed  PubMed Central  Google Scholar 

  • Allen PD, Burkard RF, Ison JR, Walton JP (2003) Impaired gap encoding in aged mouse inferior colliculus at moderate but not high stimulus levels. Hear Res 186:17–29

    Article  PubMed  Google Scholar 

  • Allman B, Keniston LP, Meredith MA (2009) Adult deafness induces somatosensory conversion of ferret auditory cortex. Proc Natl Acad Sci 106:5925–5930

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Amenedo E, Díaz F (1999) Ageing-related changes in the processing of attended and unattended standard stimuli. NeuroReport 10:2383–2388

    Article  CAS  PubMed  Google Scholar 

  • Anari M, Axelsson A, Eliasson A, Magnusson L (1999) Hypersensitivity to sound: questionnaire data, audiometry and classification. Scand Audiol 28:219–230

    Article  CAS  PubMed  Google Scholar 

  • Anderer P, Semlitsch HV, Saletu B (1996) Multichannel auditory event-related brain potentials: effects of normal aging on the scalp distribution of N1, P2, N2 and P300 latencies and amplitudes. Electroencephalogr Clin Neurophysiol 99:458–472

    Article  CAS  PubMed  Google Scholar 

  • Anderson S, Kraus N (2010) Objective neural indices of speech-in-noise perception. Trends Amplif 14:73–83

    Article  PubMed  PubMed Central  Google Scholar 

  • Anderson S, Parbery-Clark A, White-Schwoch T, Kraus N (2012) Aging affects neural precision of speech encoding. J Neurosci 32:14156–14164

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arnott SR, Binns MA, Grady CL, Alain C (2004) Assessing the auditory dual-pathway model in humans. Neuroimage 22:401–408

    Article  PubMed  Google Scholar 

  • Asokan MM, Williamson RS, Hancock KE, Polley DB (2018) Sensory overamplification in layer 5 auditory corticofugal projection neurons following cochlear nerve synaptic damage. Nat Commun 9:2468

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Auerbach BD, Rodrigues PV, Salvi RJ (2014) Central gain control in tinnitus and hyperacusis. Front Neurol. https://doi.org/10.3389/fneur.2014.00206

    Article  PubMed  PubMed Central  Google Scholar 

  • Bäckman L, Dixon RA (1992) Psychological compensation: a theoretical framework. Psychol Bull 112:259–283

    Article  PubMed  Google Scholar 

  • Backoff PM, Palombi PS, Caspary DM (1999) γ-Aminobutyric acidergic and glycinergic inputs shape coding of amplitude modulation in the chinchilla cochlear nucleus. Hear Res 134:77–88

    Article  CAS  PubMed  Google Scholar 

  • Bacon SP, Gleitman RM (1992) Modulation detection in subjects with relatively flat hearing losses. J Speech Hear Res 35:642–653

    Article  CAS  PubMed  Google Scholar 

  • Baguley DM (2003) Hyperacusis. J R Soc Med 96:582–585

    Article  PubMed  PubMed Central  Google Scholar 

  • Baguley DM, McFerran D, Hall AD (2013) Tinnitus. Lancet 382:1600–1607

    Article  PubMed  Google Scholar 

  • Balaram P, Hackett TA, Polley DB (2019) Synergistic transcriptional changes in AMPA and GABAA receptor genes support compensatory plasticity following unilateral hearing loss. Neuroscience 407:108–119

    Article  CAS  PubMed  Google Scholar 

  • Bandyopadhyay S, Shamma SA, Kanold PO (2010) Dichotomy of functional organization in the mouse auditory cortex. Nat Neurosci 13:361–368

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bao J, Ohlemiller KK (2010) Age-related loss of spiral ganglion neurons. Hear Res 264:93–97

    Article  PubMed  Google Scholar 

  • Barsz K, Wilson WW, Walton JP (2007) Reorganization of receptive fields following hearing loss in inferior colliculus neurons. Neuroscience 147:532–545

    Article  CAS  PubMed  Google Scholar 

  • Bartlett EL, Sadagopan S, Wang X (2011) Fine frequency tuning in monkey auditory cortex and thalamus. J Neurophysiol 106:849–859

    Article  PubMed  PubMed Central  Google Scholar 

  • Bauer CA, Turner JG, Caspary DM, Myers KS, Brozoski TJ (2008) Tinnitus and inferior colliculus activity in chinchillas related to three distinct patterns of cochlear trauma. J Neurosci Res 86:2564–2578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baumann S, Petkov CI, Griffiths TD (2013) A unified framework for the organization of the primate auditory cortex. Front Syst Neurosci. https://doi.org/10.3389/fnsys.2013.00011

    Article  PubMed  PubMed Central  Google Scholar 

  • Bidelman GM, Villafuerte JW, Moreno S, Alain C (2014) Age-related changes in the subcorticalecortical encoding and categorical perception of speech. Neurobiol Aging 35:2526–2540

    Article  PubMed  Google Scholar 

  • Blackwell JM, Geffen MN (2017) Progress and challenges for understanding the function of cortical microcircuits in auditory processing. Nat Commun 8:2165

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Brewer AA, Barton B (2016) Maps of the auditory cortex. Annu Rev Neurosci 39:385–407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brotherton H, Plack CJ, Schaette R, Munro KJ (2016) Time course and frequency specificity of sub-cortical plasticity in adults following acute unilateral deprivation. Hear Res 341:210–219

    Article  PubMed  Google Scholar 

  • Brotherton H, Plack CJ, Schaette R, Munro KJ (2017) Using acoustic reflex threshold, auditory brainstem response and loudness judgments to investigate changes in neural gain following acute unilateral deprivation in normal hearing adults. Hear Res 345:88–95

    Article  PubMed  Google Scholar 

  • Brotherton H, Turtle C, Plack CJ, Munro KJ, Schaette R (2019) Earplug-induced changes in acoustic reflex thresholds suggest that increased subcortical neural gain may be necessary but not sufficient for the occurrence of tinnitus. Neuroscience 407:192–199

    Article  CAS  PubMed  Google Scholar 

  • Brown CH (1984) Directional hearing in aging rats. Exp Aging Res 10:35–38

    Article  PubMed  Google Scholar 

  • Bu J, Sathyendra V, Nagykery N, Geula C (2003) Age-related changes in calbindin-D28k, calretinin, and parvalbumin-immunoreactive neurons in the human cerebral cortex. Exp Neurol 182:220–231

    Article  CAS  PubMed  Google Scholar 

  • Butler BE, Chabot NA, Lomber SG (2016) Quantifying and comparing the pattern of thalamic and cortical projections to the posterior auditory field in hearing and deaf cats. J Comp Neurol 524:3042–3063

    Article  CAS  PubMed  Google Scholar 

  • Butler BE, de la Rua A, Ward-Able T, Lomber SG (2018) Cortical and thalamic connectivity to the second auditory cortex of the cat is resilient to the onset of deafness. Brain Struct Funct 223:819–835

    Article  PubMed  Google Scholar 

  • Canlon B, Borg E, Flock A (1988) Protection against noise trauma by pre-exposure to a low-level acoustic stimulus. Hear Res 34:197–200

    Article  CAS  PubMed  Google Scholar 

  • Cannon WB, Rosenblueth A (1949) The supersensitivity of denervated structures: a law of denervation. The Macmillan Company, New York

    Google Scholar 

  • Caspary DM, Schatteman TA, Hughes LF (2005) Age-related changes in the inhibitory response properties of dorsal cochlear nucleus output neurons: role of inhibitory inputs. J Neurosci 25:10952–10959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Caspary DM, Ling L, Turner JG, Hughes LF (2008) Inhibitory neurotransmission, plasticity and aging in the mammalian central auditory system. J Exp Biol 211:1781–1791

    Article  CAS  PubMed  Google Scholar 

  • Chabot NA, Butler BE, Lomber SG (2015) Differential modification of cortical and thalamic projections to cat primary auditory cortex following early-and late-onset deafness. J Comp Neurol 529:2297–2232

    Article  Google Scholar 

  • Chambers AR, Salazar JJ, Polley DB (2016a) Persistent thalamic sound processing despite profound cochlear denervation. Front Neural Circuits. https://doi.org/10.3389/fncir.2016.00072

    Article  PubMed  PubMed Central  Google Scholar 

  • Chambers AR, Resnik J, Yuan Y, Whitton JP, Edge AS, Liberman MC, Polley DB (2016b) Central gain restores auditory processing following near-complete cochlear denervation. Neuron 89:867–879

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cisneros-Franco JM, de Villers-Sidani É (2019) Reactivation of critical period plasticity in adult auditory cortex through chemogenetic silencing of parvalbumin-positive interneurons. Proc Natl Acad Sci 116:26329–26331

    Article  CAS  PubMed Central  Google Scholar 

  • Cisneros-Franco JM, Ouellet L, Kamal B, de Villers-Sidani E (2018) A brain without brakes: reduced inhibition is associated with enhanced but dysregulated plasticity in the aged rat auditory cortex. eNeuro 5:0051

    Article  Google Scholar 

  • Clinard CG, Tremblay KL (2013) Aging degrades the neural encoding of simple and complex sounds in the human brainstem. J Am Acad Audiol 24:590–599

    Article  PubMed  Google Scholar 

  • Clinard CG, Tremblay KL, Krishnan AR (2010) Aging alters the perception and physiological representation of frequency: evidence from human frequency-following response recordings. Hear Res 264:48–55

    Article  PubMed  Google Scholar 

  • Coomber B, Berger JI, Kowalkowski VL, Shackleton TM, Palmer AR, Wallace MN (2014) Neural changes accompanying tinnitus following unilateral acoustic trauma in the guinea pig. Eur J Neurosci 40:2427–2441

    Article  PubMed  PubMed Central  Google Scholar 

  • Cruickshanks KJ, Wiley TL, Tweed TS, Klein BEK, Klein R, Mares-Perlman JA, Nondahl DM (1998) Prevalence of hearing loss in older adults in Beaver Dam, Wisconsin. Am J Epidemiol 148:879–886

    Article  CAS  PubMed  Google Scholar 

  • Da Costa S, van der Zwaag W, Marques JP, Frackowiak RSJ, Clarke S, Saenz M (2011) Human primary auditory cortex follows the shape of Heschl’s Gyrus. J Neurosci 31:14067–14075

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Day RO, Graham GG, Bieri D, Brown M, Cairns D, Harris G, Hounsell J, Platt-Hepworth S, Reeve R, Sambrook PN, Smith J (1989) Concentration-response relationships for salicylate-induced ototoxicity in normal volunteers. Br J Clin Pharmacol 28:695–702

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Villers-Sidani E, Alzghoul L, Zhou X, Simpson KL, Lin RCS, Merzenich MM (2010) Recovery of functional and structural age-related changes in the rat primary auditory cortex with operant training. Proc Natl Acad Sci 107:13900–13905

    Article  PubMed  PubMed Central  Google Scholar 

  • Dobri SGJ, Ross B (2021) Total GABA level in human auditory cortex is associated with speech-in-noise understanding in older age. Neuroimage 225:117474

    Article  CAS  PubMed  Google Scholar 

  • Drullman R (1995) Temporal envelope and fine structure cues for speech intelligibility. J Acoustical Soc Am 97:585–592

    Article  CAS  Google Scholar 

  • Dubno JR, Eckert MA, Lee F-S, Matthews LJ, Schmiedt RA (2013) Classifying human audiometric phenotypes of age-related hearing loss from animal models. J Assoc Res Otolaryngol 14:687–701

    Article  PubMed  PubMed Central  Google Scholar 

  • Dziorny AC, Scott LL, Luebke AE, Walton JP (2020) Rescuing auditory temporal processing with a novel augmented acoustic environment in a mouse model of congenital SNHL. BioRxiv. https://doi.org/10.1101/2020.08.19.256396

    Article  Google Scholar 

  • Edwards E, Chang EF (2013) Syllabic (~2-5 Hz) and fluctuation (~1-10 Hz) ranges in speech and auditory processing. Hear Res 305:113–134

    Article  PubMed  Google Scholar 

  • Eggermont JJ (2012) The neural synchrony model of tinnitus. In: Eggermont JJ (ed) The neuroscience of tinnitus. Oxford University Press, UK, pp 154–173

    Chapter  Google Scholar 

  • Eggermont JJ (2015) Animal models of spontaneous activity in the healthy and impaired auditory system. Front Neural Circuits 9:19

    Article  PubMed  PubMed Central  Google Scholar 

  • Eggermont JJ, Roberts LE (2004) The neuroscience of tinnitus. Trends Neurosci 27:676–682

    Article  CAS  PubMed  Google Scholar 

  • Eggermont JJ, Tass PA (2015) Maladaptive neural synchrony in tinnitus: origin and restoration. Front Neurol 6:29–29

    Article  PubMed  PubMed Central  Google Scholar 

  • Ernst SM, Moore BCJ (2012) The role of time and place cues in the detection of frequency modulation by hearing impaired listeners. J Acoustical Soc Am 131:4722–4731

    Article  Google Scholar 

  • Feder K, Michaud D, Ramage-Morin P, McNamee J, Beauregard Y (2015) Prevalence of hearing loss among Canadians aged 20 to 79: Audiometric results from the 2012/2013 Canadian Health Measures Survey. Health Rep 26:18–25

    PubMed  Google Scholar 

  • Fitzgibbons PJ, Gordon-Salant S (1996) Auditory temporal processing in elderly listeners. J Am Acad Audiol 7:183–189

    CAS  PubMed  Google Scholar 

  • Fitzgibbons PJ, Gordon-Salant S (2010) Behavioral studies with aging humans: hearing sensitivity and psychoacoustics. In: Gordon-Salant S, Frisina RD, Popper AN, Fay RR (eds) The aging auditory system. Springer-Verlag, New York, USA, pp 111–134

    Chapter  Google Scholar 

  • Fournier P, Schönwiesner M, Hébert S (2014) Loudness modulation after transient and permanent hearing loss: implications for tinnitus and hyperacusis. Neuroscience 283:64–77

    Article  CAS  PubMed  Google Scholar 

  • Frisina DR, Frisina RD, Snell KB, Burkard R, Walton JP, Ison JR (2001) Auditory temporal processing during Aging. In: Hof PR, Mobbs CV (eds) Functional neurobiology of aging. Academic Press, San Diego, pp 565–579

    Chapter  Google Scholar 

  • Froemke RC, Martins ARO (2011) Spectrotemporal dynamics of auditory cortical synaptic receptive field plasticity. Hear Res 279:149–161

    Article  PubMed  PubMed Central  Google Scholar 

  • Fromby C, Sherlock LP, Gold SL, Hawley ML (2007) Adaptive recalibration of chronic auditory gain. Semin Hear 28:295–302

    Article  Google Scholar 

  • Fukushima N, White P, Harrison RV (1990) Influence of acoustic deprivation on recovery of hair cells after acoustic trauma. Hear Res 50:107–118

    Article  CAS  PubMed  Google Scholar 

  • Füllgrabe C, Meyer B, Lorenzi C (2003) Effect of cochlear damage on the detection of complex temporal envelopes. Hear Res 178:35–43

    Article  PubMed  Google Scholar 

  • Gao F, Wang G, Ma W, Ren F, Li M, Dong Y, Liu C, Liu B, Bai X, Zhao B, Edden RAE (2015) Decreased auditory GABA+concentrations in presbycusis demonstrated by edited magnetic resonance spectroscopy. Neuroimage 106:311–316

    Article  CAS  PubMed  Google Scholar 

  • Gates GA, Mills JH (2005) Presbycusis. Lancet 366:1111–1120

    Article  PubMed  Google Scholar 

  • Gerken GM (1979) Central denervation hypersensitivity in the auditory system of the cat. J Acoustical Soc Am 66:721–727

    Article  CAS  Google Scholar 

  • Giraud A-L, Poeppel D (2012) Cortical oscillations and speech processing: emerging computational principles and operations. Nat Neurosci 15(4):511–517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Glasberg BR, Moore BC, Bacon SP (1987) Gap detection and masking in hearing-impaired and normal-hearing subjects. J Acoust Soc Am 81:1546–1556

    Article  CAS  PubMed  Google Scholar 

  • Goman AM, Lin FR (2016) Prevalence of hearing loss by severity in the United States. Am J Public Health 106:1820–1822

    Article  PubMed  PubMed Central  Google Scholar 

  • Goossens T, Vercammen C, Wouters J, van Wieringen A (2016) Aging affects neural synchronization to speech-related acoustic modulations. Front Aging Neurosci 8:133

    Article  PubMed  PubMed Central  Google Scholar 

  • Goossens T, Vercammen C, Wouters J, Van Wieringen A (2018) Neural envelope encoding predicts speech perception performance for normal-hearing and hearing-impaired adults. Hear Res 370:189–200

    Article  PubMed  Google Scholar 

  • Goossens T, Vercammen C, Wouters J, Van Wieringen A (2019) The association between hearing impairment and neural envelope encoding at different ages. Neurobiol Aging 74:202–212

    Article  PubMed  Google Scholar 

  • Gordon-Salant S, Fitzgibbons PJ (1993) Temporal factors and speech recognition performance in young and elderly listeners. J Speech Lang Hear Res 36:1276–1285

    Article  CAS  Google Scholar 

  • Gordon-Salant S, Fitzgibbons PJ (1999) Profile of auditory temporal processing in older listeners. Journal of Speech, Language, and Hearing Research : JSLHR 42:300–311

    Article  CAS  PubMed  Google Scholar 

  • Gratton MA, Vázquez AE (2003) Age-related hearing loss: current research. Curr Opin Otolaryngol Head Neck Surg 11:367–371

    Article  PubMed  Google Scholar 

  • Hackett TA (2011) Information flow in the auditory cortical network. Hear Res 271:133–146

    Article  PubMed  Google Scholar 

  • Harkrider AW, Plyler PN, Hedrick MS (2005) Effects of age and spectral shaping on perception and neural representation of stop consonant stimuli. Clin Neurophysiol 116:2153–2164

    Article  PubMed  Google Scholar 

  • Harris KC, Wilson S, Eckert MA, Dubno JR (2012) Human evoked cortical activity to silent gaps in noise: effects of age, attention, and cortical processing speed. Ear Hear 33:330–339

    Article  PubMed  PubMed Central  Google Scholar 

  • Hattori R, Kuchibhotla KV, Froemke RC, Komiyama T (2017) Functions and dysfunctions of neocortical inhibitory neuron subtypes. Nat Neurosci 20:1199–1208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hayes SH, Radziwon KE, Stolzberg DJ, Salvi RJ (2014) Behavioral models of tinnitus and hyperacusis in animals. Front Neurol 5:179

    Article  PubMed  PubMed Central  Google Scholar 

  • Hayes SH, Schormans AL, Sigela G, Beha K, Herrmann B, Allman BL (2021) Uncovering the contribution of enhanced central gain and altered cortical oscillations to tinnitus generation. Prog Neurobiol 196:101893

    Article  CAS  PubMed  Google Scholar 

  • Hebert S, Fournier P, Noreña A (2013) The auditory sensitivity is increased in tinnitus ears. J Neurosci 33:2356–2364

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Helfer KS, Merchant GR, Wasiuk PA (2017) Age-related changes in objective and subjective speech perception in complex listening environments. J Speech Lang Hear Res 60:3009–3018

    Article  PubMed  PubMed Central  Google Scholar 

  • Henry JA, Schechter MA, Zaugg TL, Griest S, Jastreboff PJ, Vernon JA, Kaelin C, Meikle MB, Lyons KS, Stewart BJ (2006) Clinical trial to compare tinnitus masking and tinnitus retraining therapy. Acta Otolaryngol Suppl 556:64–69

    Article  Google Scholar 

  • Henry MJ, Herrmann B, Obleser J (2014) Entrained neural oscillations in multiple frequency bands co-modulate behavior. Proc Natl Acad Sci 111:14935–14940

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Henry MJ, Herrmann B, Kunke D, Obleser J (2017) Aging affects the balance of neural entrainment and top-down neural modulation in the listening brain. Nat Commun 8:15801

    Article  PubMed  PubMed Central  Google Scholar 

  • Herrmann B, Maess B, Hahne A, Schröger E, Friederici AD (2011) Syntactic and auditory spatial processing in the human temporal cortex: an MEG study. Neuroimage 57:624–633

    Article  PubMed  Google Scholar 

  • Herrmann B, Henry MJ, Scharinger M, Obleser J (2013a) Auditory filter width affects response magnitude but not frequency specificity in auditory cortex. Hear Res 304:128–136

    Article  PubMed  Google Scholar 

  • Herrmann B, Henry MJ, Grigutsch M, Obleser J (2013b) Oscillatory phase dynamics in neural entrainment underpin illusory percepts of time. J Neurosci 33:15799–15809

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Herrmann B, Henry MJ, Johnsrude IS, Obleser J (2016) Altered temporal dynamics of neural adaptation in the aging human auditory cortex. Neurobiol Aging 45:10–22

    Article  PubMed  Google Scholar 

  • Herrmann B, Parthasarathy A, Bartlett EL (2017) Aging affects dual encoding of periodicity and envelope shape in rat inferior colliculus neurons. Eur J Neurosci 45:299–311

    Article  PubMed  Google Scholar 

  • Herrmann B, Maess B, Johnsrude IS (2018) Aging affects adaptation to sound-level statistics in human auditory cortex. J Neurosci 38:1989–1999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Herrmann B, Buckland C, Johnsrude IS (2019) Neural signatures of temporal regularity processing in sounds differ between younger and older adults. Neurobiol Aging 83:73–85

    Article  CAS  PubMed  Google Scholar 

  • Holmes E, Griffiths TD (2019) ‘Normal’ hearing thresholds and fundamental auditory grouping processes predict difficulties with speech-in-noise perception. Sci Rep 9:16771

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hopkins J (1994) Orchestrating an indoor city: ambient noise inside a mega-mall. Environ Behav 26:785–812

    Article  Google Scholar 

  • Hughes LF, Turner JG, Parrish JL, Caspary DM (2010) Processing of broadband stimuli across A1 layers in young and aged rats. Hear Res 264:79–85

    Article  PubMed  Google Scholar 

  • Humes LE, Busey TA, Craig JC, Kewley-Port D (2009) The effects of age on sensory thresholds and temporal gap detection in hearing, vision, and touch. Atten Percept Psychophys 71:860–871

    Article  PubMed  PubMed Central  Google Scholar 

  • Huotilainen M, Winkler I, Alho K, Escera C, Virtanen J, Ilmoniemi RJ, Jääskeläinen IP, Pekkonen E, Näätänen R (1998) Combined mapping of human auditory EEG and MEG responses. Electroencephalogr Clin Neurophysiol 108:370–379

    Article  CAS  PubMed  Google Scholar 

  • Ibrahim BA, Llano DA (2019) Aging and central auditory disinhibition: is it a reflection of homeostatic downregulation or metabolic vulnerability? Brain Sci 9:351

    Article  CAS  PubMed Central  Google Scholar 

  • Imam L, Hannan SA (2017) Noise-induced hearing loss: a modern epidemic? Br J Hosp Med 78:286–290

    Article  Google Scholar 

  • Isaacson JS, Scanziani M (2011) How inhibition shapes cortical activity. Neuron 72:231–243

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ivansic D, Guntinas-Lichius O, Müller B, Volk GF, Schneider G, Dobel C (2017) Impairments of speech comprehension in patients with Tinnitus-a review. Front Aging Neurosci 9:224

    Article  PubMed  PubMed Central  Google Scholar 

  • Izquierdo MA, Gutiérrez-Conde PM, Merchán MA, Malmierca MS (2008) Non-plastic reorganization of frequency coding in the inferior colliculus of the rat following noise-induced hearing loss. Neuroscience 154:355–369

    Article  CAS  PubMed  Google Scholar 

  • Jastreboff MM (2007) Sound therapies for tinnitus management. Prog Brain Res 166:435–440

    Article  PubMed  Google Scholar 

  • Juarez-Salinas DL, Engle JR, Navarro XO, Recanzone GH (2010) Hierarchical and serial processing in the spatial auditory cortical pathway is degraded by natural aging. J Neurosci 30:14795–14804

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kalappa BI, Brozoski TJ, Turner JG, Caspary DM (2014) Single unit hyperactivity and bursting in the auditory thalamus of awake rats directly correlates with behavioural evidence of tinnitus. J Physiol 592:5065–5078

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaltenbach JA, Rachel JD, Mathog TA, Zhang J, Falzarano PR, Lewandowski M (2002) Cisplatin-induced hyperactivity in the dorsal cochlear nucleus and its relation to outer hair cell loss: relevance to tinnitus. J Neurophysiol 88:699–714

    Article  CAS  PubMed  Google Scholar 

  • Kamal B, Holman C, de Villers-Sidani E (2013) Shaping the aging brain: role of auditory input patterns in the emergence of auditory cortical impairments. Front Syst Neurosci 7:52

    Article  PubMed  PubMed Central  Google Scholar 

  • Kandler K, Clause A, Noh J (2009) Tonotopic reorganization of developing auditory brainstem circuits. Nat Neurosci 12:711–717

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kato HK, Asinof SK, Isaacson JS (2017) Network-level control of frequency tuning in auditory cortex. Neuron 95:412–423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaur S, Lazar R, Metherate R (2004) Intracortical pathways determine breadth of subthreshold frequency receptive fields in primary auditory cortex. J Neurophysiol 91:2551–2567

    Article  PubMed  Google Scholar 

  • Keck T, Toyoizumi T, Chen L, Doiron B, Feldman DE, Fox K, Gerstner W, Haydon PG, Hübener M, Lee H-K, Lisman JE, Rose T, Sengpiel F, Stellwagen D, Stryker MP, Turrigiano GG, van Rossum MC (2017) Integrating Hebbian and homeostatic plasticity: the current state of the field and future research directions. Philos Trans R Soc B 372:20160158

    Article  CAS  Google Scholar 

  • Keithley EM (2020) Pathology and mechanisms of cochlear aging. J Neurosci Res 98:1674–1684

    Article  CAS  PubMed  Google Scholar 

  • Kerlin JR, Shahin AJ, Miller LM (2010) Attentional gain control of ongoing cortical speech representations in a “Cocktail Party.” J Neurosci 30:620–628

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • King AJ, Bajo VM, Bizley JK, Campbell RAA, Nodal FR, Schulz AL, Schnupp JWH (2007) Physiological and behavioral studies of spatial coding in the auditory cortex. Hear Res 229:106–115

    Article  PubMed  PubMed Central  Google Scholar 

  • Knipper M, Van Dijk P, Nunes I, Rüttiger L, Zimmermann U (2013) Advances in the neurobiology of hearing disorders: Recent developments regarding the basis of tinnitus and hyperacusis. Prog Neurobiol 111:17–33

    Article  PubMed  Google Scholar 

  • Knipper M, van Dijk P, Schulze H, Mazurek B, Krauss P, Scheper V, Warnecke A, Schlee W, Schwabe K, Singer W, Braun C, Delano PH, Fallgatter AJ, Ehlis A-C, Searchfield GD, Munk MHJ, Baguley DM, Rüttiger L (2020) The neural bases of tinnitus: lessons from deafness and cochlear implants. J Neurosci 40:7190–7202

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koehnke J, Besing JM (2001) The effects of aging on binaural and spatial hearing. Semin Hear 22:241–254

    Article  Google Scholar 

  • Koops EA, Renken RJ, Lanting CP, van Dijk P (2020) Cortical tonotopic map changes in humans are larger in hearing loss than in additional tinnitus. J Neurosci 40:3178–3185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kotak VC, Fujisawa S, Lee FA, Karthikeyan O, Aoki C, Sanes DH (2005) Hearing loss raises excitability in the auditory cortex. J Neurosci 25:3908–3918

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kujawa SG, Liberman MC (2009) Adding insult to injury: cochlear nerve degeneration after “temporary” noise-induced hearing loss. J Neurosci 29:14077–14085

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laffont F, Bruneau N, Roux S, Agar N, Minz M, Cathala HP (1989) Effects of age on auditory evoked responses (AER) and augmenting-reducing. Clin Neurophysiol 19:15–23

    Article  CAS  Google Scholar 

  • Leong UC, Barsz K, Allen PD, Walton JP (2011) Neural correlates of age-related declines in frequency selectivity in the auditory midbrain. Neurobiol Aging 32:168–178

    Article  PubMed  Google Scholar 

  • Li S, Choi V, Tzounopoulos T (2013) Pathogenic plasticity of Kv7.2/3 channel activity is essential for the induction of tinnitus. Proc Natl Acad Sci USA 110:9980–9985

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li S, Kalappa BI, Tzounopoulos T (2015) Noise-induced plasticity of KCNQ2/3 and HCN channels underlies vulnerability and resilience to tinnitus. Elife. https://doi.org/10.7554/eLife.07242

    Article  PubMed  PubMed Central  Google Scholar 

  • Liberman MC, Kujawa SG (2017) Cochlear synaptopathy in acquired sensorineural hearing loss: manifestations and mechanisms. Hear Res 349:138–147

    Article  PubMed  PubMed Central  Google Scholar 

  • Liberman MC, Epstein MJ, Cleveland SS, Wang H, Maison SF (2016) Toward a differential diagnosis of hidden hearing loss in humans. PLoS ONE 11:e0162726

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lister JJ, Maxfield ND, Pitt GJ, Gonzalez VB (2011) Auditory evoked response to gaps in noise: older adults. Int J Audiol 50:211–225

    Article  PubMed  PubMed Central  Google Scholar 

  • Llano DA, Turner J, Caspary DM (2012) Diminished cortical inhibition in an aging mouse model of chronic tinnitus. J Neurosci 32:16141–16148

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lobarinas E, Salvi R, Ding D (2013) Insensitivity of the audiogram to carboplatin induced inner hair cell loss in chinchillas. Hear Res 302:113–120

    Article  CAS  PubMed  Google Scholar 

  • Lorenzi C, Gilbert G, Héloise C, Garnier S, Moore BCJ (2006) Speech perception problems of the hearing impaired reflect inability to use temporal fine structure. Proc Natl Acad Sci 103:18866–18869

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maess B, Jacobsen T, Schröger E, Friederici AD (2007) Localizing pre-attentive auditory memory-based comparison: magnetic mismatch negativity to pitch change. Neuroimage 37:561–571

    Article  PubMed  Google Scholar 

  • Manunta Y, Edeline J-M (1997) Effects of noradrenaline on frequency tuning of rat auditory cortex neurons. Eur J Neurosci 9:833–847

    Article  CAS  PubMed  Google Scholar 

  • Manzoor NF, Licari FG, Klapchar M, Elkin RL, Gao Y, Chen G, Kaltenbach JA (2012) Noise-induced hyperactivity in the inferior colliculus: its relationship with hyperactivity in the dorsal cochlear nucleus. J Neurophysiol 108:976–988

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin del Campo HN, Measor KR, Razak KA (2012) Parvalbumin immunoreactivity in the auditory cortex of a mouse model of presbycusis. Hear Res 294:31–39

    Article  CAS  PubMed  Google Scholar 

  • McCormack A, Edmondson-Jones M, Somerset S, Hall DA (2016) A systematic review of the reporting of tinnitus prevalence and severity. Hear Res 337:70–79

    Article  PubMed  Google Scholar 

  • Mepani AM, Kirk SA, Hancock KE, Bennett K, de Gruttola V, Liberman MC, Maison SF (2020) Middle ear muscle reflex and word recognition in “normal-hearing” adults: evidence for cochlear synaptopathy? Ear Hear 41:25–38

    Article  PubMed  PubMed Central  Google Scholar 

  • Miller LM, Escabí MA, Read HL, Schreiner CE (2002) Spectrotemporal receptive fields in the lemniscal auditory thalamus and cortex. J Neurophysiol 87:516–527

    Article  PubMed  Google Scholar 

  • Millman RE, Mattys SL, Gouws AD, Prendergast G (2017) Magnified neural envelope coding predicts deficits in speech perception in noise. J Neurosci 37:7727–7736

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mishra J, de Villers-Sidani E, Merzenich MM, Gazzaley A (2014) Adaptive training diminishes distractibility in aging across species. Neuron 84:1091–1103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moerel M, De Martino F, Formisano E (2014) An anatomical and functional topography of human auditory cortical areas. Front Neurosci 8:225

    Article  PubMed  PubMed Central  Google Scholar 

  • Möhrle D, Ni K, Varakina K, Bing D, Lee SC, Zimmermann U, Knipper M, Rüttiger L (2016) Loss of auditory sensitivity from inner hair cell synaptopathy can be centrally compensated in the young but not old brain. Neurobiol Aging 44:173–184

    Article  PubMed  Google Scholar 

  • Moore DR (1987) Physiology of higher auditory system. Br Med Bull 43:856–870

    Article  CAS  PubMed  Google Scholar 

  • Moore BCJ (2007) Cochlear hearing loss: physiological, psychological and technical issues. John Wiley & Sons Ltd, West Sussex, England

    Book  Google Scholar 

  • Moore BCJ (2014) Auditory processing of temporal fine structure: effects of age and hearing loss. World Scientific, Singapore

    Book  Google Scholar 

  • Moore BC, Glasberg BR (1988) Gap detection with sinusoids and noise in normal, impaired, and electrically stimulated ears. J Acoust Soc Am 83:1093–1101

    Article  CAS  PubMed  Google Scholar 

  • Moore BCJ, Skrodzka E (2002) Detection of frequency modulation by hearing-impaired listeners: effects of carrier frequency, modulation rate, and added amplitude modulation. J Acoustical Soc Am 111:327–335

    Article  Google Scholar 

  • Moore BCJ, Peters RW, Glasberg BR (1992) Detection of temporal gaps in sinusoids by elderly subjects with and without hearing loss. J Acoustical Soc Am 92:1923–1932

    Article  CAS  Google Scholar 

  • Moore BCJ, Wojtczak M, Vickers D (1996) Effect of loudness recruitment on the perception of amplitude modulation. J Acoust Soc Am 100:481–489

    Article  Google Scholar 

  • Moore BCJ, Mariathasan S, Sęk AP (2019) Effects of age and hearing loss on the discrimination of amplitude and frequency modulation for 2- and 10-Hz rates. Trends Hear 23:2331216519853963

    PubMed  PubMed Central  Google Scholar 

  • Moser T, Starr A (2016) Auditory neuropathy—neural and synaptic mechanisms. Nat Rev Neurol 12:135–149

    Article  CAS  PubMed  Google Scholar 

  • Mühlnickel W, Elbert T, Taub E, Flor H (1998) Reorganization of auditory cortex in tinnitus. Proc Natl Acad Sci 95:10340–10343

    Article  PubMed  PubMed Central  Google Scholar 

  • Mulders WHAM, Robertson D (2013) Development of hyperactivity after acoustic trauma in the guinea pig inferior colliculus. Hear Res 298:104–108

    Article  CAS  PubMed  Google Scholar 

  • Munguia R, Pienkowski M, Eggermont JJ (2013) Spontaneous firing rate changes in cat primary auditory cortex following long-term exposure to non-traumatic noise: tinnitus without hearing loss? Neurosci Lett 546:46–50

    Article  CAS  PubMed  Google Scholar 

  • Munro KJ, Turtle C, Schaette R (2014) Plasticity and modified loudness following short-term unilateral deprivation: evidence of multiple gain mechanisms within the auditory system. J Acoustical Soc Am 135:315–322

    Article  Google Scholar 

  • Näätänen R, Picton TW (1987) The N1 wave of the human electric and magnetic response to sound: a review and an analysis of the component structure. Psychophysiology 24:375–425

    Article  PubMed  Google Scholar 

  • Nahmani M, Turrigiano GG (2014) Adult cortical plasticity following injury: recapitulation of critical period mechanisms? Neuroscience 283:4–16

    Article  CAS  PubMed  Google Scholar 

  • Natan RG, Briguglio JJ, Mwilambwe-Tshilobo L, Jones SI, Aizenberg M, Goldberg EM, Geffen MN (2015) Complementary control of sensory adaptation by two types of cortical interneurons. Elife 4:e09868

    Article  PubMed  PubMed Central  Google Scholar 

  • Natan RG, Rao W, Geffen MN (2017) Cortical interneurons differentially shape frequency tuning following adaptation. Cell Rep 21:878–890

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nelson DA, Freyman RL (1986) Psychometric functions for frequency discrimination from listeners with sensorineural hearing loss. J Acoustical Soc Am 79:799–805

    Article  CAS  Google Scholar 

  • Ng C-W, Recanzone GH (2018) Age-related changes in temporal processing of rapidly-presented sound sequences in the macaque auditory cortex. Cereb Cortex 28:3775–3796

    Article  PubMed  Google Scholar 

  • Niu X, Tahera Y, Canlon B (2004) Protection against acoustic trauma by forward and backward sound conditioning. Audiol Neurootol 9:265–273

    Article  PubMed  Google Scholar 

  • Niu X, Tahera Y, Canlon B (2007) Environmental enrichment to sound activates dopaminergic pathways in the auditory system. Physiol Behav 92:34–39

    Article  CAS  PubMed  Google Scholar 

  • Noelle O’Connell M, Barczak A, Schroeder CE, Lakatos P (2014) Layer specific sharpening of frequency tuning by selective attention in primary auditory cortex. J Neurosci 34:16496–16508

    Article  CAS  Google Scholar 

  • Norena AJ, Chery-Croze S (2007) Enriched acoustic environment rescales auditory sensitivity. NeuroReport 18:1251–1255

    Article  PubMed  Google Scholar 

  • Norena AJ, Eggermont JJ (2006) Enriched acoustic environment after noise trauma abolishes neural signs of tinnitus. NeuroReport 17:559–563

    Article  PubMed  Google Scholar 

  • Norena AJ, Tomita M, Eggermont JJ (2003) Neural changes in cat auditory cortex after a transient pure-tone trauma. J Neurophysiol 90:2387–2401

    Article  PubMed  Google Scholar 

  • Noreña AJ, Gourévitch B, Aizawa N, Eggermont JJ (2006) Spectrally enhanced acoustic environment disrupts frequency representation in cat auditory cortex. Nat Neurosci 7:932–939

    Article  CAS  Google Scholar 

  • Oliver DL, Izquierdo MA, Malmierca MS (2011) Persistent effects of early augmented acoustic environment on the auditory brainstem. Neuroscience 184:75–87

    Article  CAS  PubMed  Google Scholar 

  • Olsen WO (1998) Average speech levels and spectra in various speaking/listening conditions: a summary of the Pearson, Bennett, & Fidell (1977) report. Am J Audiol 7:21–25

    Article  PubMed  Google Scholar 

  • Ouda L, Profant O, Syka J (2015) Age-related changes in the central auditory system. Cell Tissue Res 361:337–358

    Article  PubMed  Google Scholar 

  • Ouellet L, de Villers-Sidani E (2014) Trajectory of the main GABAergic interneuron populations from early development to old age in the rat primary auditory cortex. Front Neuroanatomy 8:40

    Article  CAS  Google Scholar 

  • Overton JA, Recanzone GH (2016) Effects of aging on the response of single neurons to amplitude-modulated noise in primary auditory cortex of rhesus macaque. J Neurophysiol 115:2911–2923

    Article  PubMed  PubMed Central  Google Scholar 

  • Palombi PS, Backoff PM, Caspary DM (2001) Responses of young and aged rat inferior colliculus neurons to sinusoidally amplitude modulated stimuli. Hear Res 153:174–180

    Article  Google Scholar 

  • Parmentier FBR, Andrés P (2010) The involuntary capture of attention by sound novelty and postnovelty distraction in young and older adults. Exp Psychol 57:68–76

    Article  PubMed  Google Scholar 

  • Parry LV, Maslin MRD, Schaette R, Moore DR, Munro KJ (2019) Increased auditory cortex neural response amplitude in adults with chronic unilateral conductive hearing impairment. Hear Res 372:10–16

    Article  PubMed  Google Scholar 

  • Parthasarathy A, Herrmann B, Bartlett EL (2019) Aging alters envelope representations of speech-like sounds in the inferior colliculus. Neurobiol Aging 73:30–40

    Article  PubMed  Google Scholar 

  • Parthasarathy A, Hancock KE, Bennett K, DeGruttola V, Polley DB (2020) Bottom-up and top-down neural signatures of disordered multi-talker speech perception in adults with normal hearing. Elife 9:e51419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peelle JE, Davis MH (2013) Neural oscillations carry speech rhythm through to comprehension. Front Psychol 3:320

    Google Scholar 

  • Pfeffer CK, Xue M, He M, Huang ZJ, Scanziani M (2013) Inhibition of inhibition in visual cortex: the logic of connections between molecularly distinct interneurons. Nat Neurosci 16:1068–1076

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pichora-Fuller MK (2003) Processing speed and timing in aging adults: psychoacoustics, speech perception, and comprehension. Int J Audiol 42:S59–S67

    Article  Google Scholar 

  • Pichora-Fuller MK, Kramer SE, Eckert MA, Edwards B, Hornsby BWY, Humes LE, Lemke U, Lunner T, Matthen M, Mackersie CL, Naylor G, Phillips NA, Richter M, Rudner M, Sommers MS, Tremblay KL, Wingfield A (2016) Hearing impairment and cognitive energy: the framework for understanding effortful listening (FUEL). Ear Hear 37(Suppl 1):5S-27S

    Article  PubMed  Google Scholar 

  • Picton TW, John SM, Dimitrijevic A, Purcell DW (2003) Human auditory steady-state responses. Int J Audiol 42:177–219

    Article  PubMed  Google Scholar 

  • Plack CJ (2014) The sense of hearing. Psychology Press, New York, USA

    Google Scholar 

  • Plack CJ, Barker D, Prendergast G (2014) Perceptual consequences of “hidden” hearing loss. Trends Hearing 18:1–11

    Article  Google Scholar 

  • Popelár J, Syka J, Berndt H (1987) Effect of noise on auditory evoked responses in awake guinea pigs. Hear Res 26:239–247

    Article  PubMed  Google Scholar 

  • Prendergast G, Guest H, Munro KJ, Kluk K, Leger A, Hall AD, Heinz MG, Plack CJ (2017a) Effects of noise exposure on young adults with normal audiograms I: electrophysiology. Hear Res 344:68–81

    Article  PubMed  PubMed Central  Google Scholar 

  • Prendergast G, Millman RE, Guest H, Munro KJ, Kluk K, Dewey RS, Hall DA, Heinz MG, Plack CJ (2017b) Effects of noise exposure on young adults with normal audiograms II: behavioral measures. Hear Res 356:74–86

    Article  PubMed  PubMed Central  Google Scholar 

  • Presacco A, Simon JZ, Anderson S (2016a) Evidence of degraded representation of speech in noise, in the aging midbrain and cortex. J Neurophysiol 116:2346–2355

    Article  PubMed  PubMed Central  Google Scholar 

  • Presacco A, Simon JZ, Anderson S (2016b) Effect of informational content of noise on speech representation in the aging midbrain and cortex. J Neurophysiol 116:2356–2367

    Article  PubMed  PubMed Central  Google Scholar 

  • Presacco A, Simon JZ, Anderson S (2019) Speech-in-noise representation in the aging midbrain and cortex: Effects of hearing loss. PLoS ONE 14:e0213899

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ptito M, Kupers R, Lomber S, Pietrini P (2012) Sensory deprivation and brain plasticity. Neural Plast 2012:810370

    Article  PubMed  PubMed Central  Google Scholar 

  • Purcell DW, John SM, Schneider BA, Picton TW (2004) Human temporal auditory acuity as assessed by envelope following responses. J Acoustical Soc Am 116:3581–3593

    Article  Google Scholar 

  • Qiu C, Salvi R, Ding D, Burkard R (2000) Inner hair cell loss leads to enhanced response amplitudes in auditory cortex of unanesthetized chinchillas: evidence for increased system gain. Hear Res 139:153–171

    Article  CAS  PubMed  Google Scholar 

  • Rabang CF, Parthasarathy A, Venkataraman Y, Fisher ZL, Gardner SM, Bartlett EL (2012) A computational model of inferior colliculus responses to amplitude modulated sounds in young and aged rats. Front Neural Circuits 6:77

    Article  PubMed  PubMed Central  Google Scholar 

  • Rachel JD, Kaltenbach JA, Janisse J (2002) Increases in spontaneous neural activity in the hamster dorsal cochlear nucleus following cisplatin treatment: a possible basis for cisplatin-induced tinnitus. Hear Res 164:206–214

    Article  CAS  PubMed  Google Scholar 

  • Radziwon KE, Stolzberg DJ, Urban ME, Bowler RA, Salvi RJ (2015) Salicylate-induced hearing loss and gap detection deficits in rats. Front Neurol. https://doi.org/10.3389/fneur.2015.00031

    Article  PubMed  PubMed Central  Google Scholar 

  • Radziwon K, Hayes SH, Sheppard AM, Ding D, Salvi R (2016) Drug-induced tinnitus. In: Baguley DM, Fagelson M (eds) Tinnitus: clinical and research perspectives. Plural Publishing, pp 89–109

    Google Scholar 

  • Radziwon KE, Holfoth D, Lindner J, Kaier-Green Z, Bowler R, Urban M, Salvi R (2017) Salicylate-induced hyperacusis in rats: dose- and frequency-dependent effects. Hear Res 350:133–138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ramachandran R, Davis KA, May BJ (1999) Single-unit responses in the inferior colliculus of decerebrate cats. I. Classification based on frequency response maps. J Neurophysiol 82:152–163

    Article  CAS  PubMed  Google Scholar 

  • Rauschecker JP (2011) An expanded role for the dorsal auditory pathway in sensorimotor control and integration. Hear Res 271:16–25

    Article  PubMed  Google Scholar 

  • Rauschecker JP, Scott SK (2009) Maps and streams in the auditory cortex: nonhuman primates illuminate human speech processing. Nat Neurosci 12:718–724

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rauschecker JP, Tian B (2000) Mechanisms and streams for processing of “what” and “where” in auditory cortex. Proc Natl Acad Sci 97:11800–11806

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Resnik J, Polley DB (2017) Fast-spiking GABA circuit dynamics in the auditory cortex predict recovery of sensory processing following peripheral nerve damage. Elife 6:e21452

    Article  PubMed  PubMed Central  Google Scholar 

  • Resnik J, Polley DB (2021) Cochlear neural degeneration disrupts hearing in background noise by increasing auditory cortex internal noise. Neuron 109:984–996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rogalla MM, Hildebrandt KJ (2020) Aging but not age-related hearing loss dominates the decrease of parvalbumin immunoreactivity in the primary auditory cortex of mice. eNeuro. https://doi.org/10.1523/ENEURO.0511-19.2020

    Article  PubMed  PubMed Central  Google Scholar 

  • Rosen S (1992) Temporal information in speech: acoustic, auditory and linguistic aspects. Philos Trans Biol Sci 336:367–373

    Article  CAS  Google Scholar 

  • Rosen MJ, Sarro EC, Kelly JB, Sanes DH (2012) Diminished behavioral and neural sensitivity to sound modulation is associated with moderate developmental hearing loss. PLoS ONE 7:e41514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ross B, Tremblay KL (2009) Stimulus experience modifies auditory neuromagnetic responses in young and older listeners. Hear Res 248:48–59

    Article  PubMed  Google Scholar 

  • Ross B, Schneider B, Snyder JS, Alain C (2010) Biological markers of auditory gap detection in young, middle-aged, and older adults. PLoS ONE 5:10101

    Article  CAS  Google Scholar 

  • Saenz M, Langers DRM (2014) Tonotopic mapping of human auditory cortex. Hear Res 307:42–52

    Article  PubMed  Google Scholar 

  • Salthouse TA (1995) Refining the concept of psychological compensation. In: Dixon RA, Backman L (eds) Compensating for psychological deficits and declines: Managing losses and promoting gains. Lawrence Erlbaum Associates Inc, pp 21–34

    Google Scholar 

  • Salvi R, Sun W, Ding D, Chen G-D, Lobarinas E, Wang J, Radziwon K, Auerbach BD (2017) Inner hair cell loss disrupts hearing and cochlear function leading to sensory deprivation and enhanced central auditory gain. Front Neurosci 10:621

    Article  PubMed  PubMed Central  Google Scholar 

  • Salvi RJ, Auerbach BD, Lau C, Chen Y-C, Manohar S, Liu X, Ding D, Chen G-D (2020) Functional neuroanatomy of salicylate- and noise-induced tinnitus and hyperacusis. In: Geyer MA, Ellenbroek BA, Marsden CA, Barnes TRE, Andersen SL, Paulus MP (eds) Current topics in behavioral neurosciences. Springer, Berlin, Heidelberg

    Google Scholar 

  • Sanes DH, Kotak VC (2011) Developmental plasticity of auditory cortical inhibitory synapses. Hear Res 279:140–148

    Article  PubMed  PubMed Central  Google Scholar 

  • Sanes DH, Sarro EC, Takesian AE, Aoki C, Kotak VC (2010) Regulation of inhibitory synapse function in the developing auditory CNS. In: Pallas SL (ed) Developmental plasticity of inhibitory circuitry. Springer, US, Boston, MA, pp 43–69

    Chapter  Google Scholar 

  • Saunders JC, Dear SP, Schneider ME (1985) The anatomical consequences of acoustic injury: a review and tutorial. J Acoustical Soc Am 78:833–860

    Article  CAS  Google Scholar 

  • Schaette R, McAlpine D (2011) Tinnitus with a normal audiogram: physiological evidence for hidden hearing loss and computational model. J Neurosci 31:13452–13457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schaette R, Turtle C, Munro KJ (2012) Reversible induction of phantom auditory sensations through simulated unilateral hearing loss. PLoS ONE 7:e35238

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schatteman TA, Hughes LF, Caspary DM (2008) Age-related loss of temporal processing: altered responses to amplitude modulated tones in rat dorsal cochlear nucleus. Neuroscience 154:329–337

    Article  CAS  PubMed  Google Scholar 

  • Schlittenlacher J, Moore BCJ (2016) Discrimination of amplitude-modulation depth by subjects with normal and impaired hearing. J Acoust Soc Am 140:3487–3495

    Article  PubMed  Google Scholar 

  • Schmiedt RA (2010) The physiology of cochlear Presbycusis. In: Gordon-Salant S, Frisina R, Popper A, Fay R (eds) The aging auditory system. Springer handbook of auditory research. Springer, New York, USA, pp 9–38

    Chapter  Google Scholar 

  • Schneider BA, Pichora-Fuller MK, Kowalchuk D, Lamb M (1994) Gap detection and the precedence effect in young and old adults. J Acoust Soc Am 95:980–991

    Article  CAS  PubMed  Google Scholar 

  • Schneider B, Speranza F, Pichora-Fuller MK (1998) Age-related changes in temporal resolution: envelope and intensity effects. Canad J Exp Psychol 52:184–191

    Article  CAS  Google Scholar 

  • Schormans AL, Typlt M, Allman B (2019) Adult-onset hearing impairment induces layer-specific cortical reorganization: evidence of crossmodal plasticity and central gain enhancement. Cereb Cortex 29:1875–1888

    Article  PubMed  Google Scholar 

  • Schreiner CE, Froemke RC, Atencio CA (2011) Spectral processing in auditory cortex. In: Winer JA, Schreiner CE (eds) The auditory cortex. Springer, USA, pp 275–308

    Chapter  Google Scholar 

  • Sedley W (2019) Tinnitus: does gain explain? Neuroscience 407:213–228

    Article  CAS  PubMed  Google Scholar 

  • Sedley W, Friston KJ, Gander PE, Kumar S, Griffiths TD (2016) An integrative tinnitus model based on sensory precision. Trends Neurosci 39(12):799–810

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sek A, Baer T, Crinnion W, Springgay A, Moore BCJ (2015) Modulation masking within and across carriers for subjects with normal and impaired hearing. J Acoustical Soc Am 138:1143–1153

    Article  Google Scholar 

  • Seki S, Eggermont JJ (2003) Changes in spontaneous firing rate and neural synchrony in cat primary auditory cortex after localized tone-induced hearing loss. Hear Res 180:28–38

    Article  PubMed  Google Scholar 

  • Sekiya K, Takahashi M, Murakami S, Kakigi R, Okamoto H (2017) Broadened population-level frequency tuning in the auditory cortex of tinnitus patients. J Neurophysiol 117:1379–1384

    Article  PubMed  PubMed Central  Google Scholar 

  • Shaheen LA, Liberman MC (2018) Cochlear synaptopathy changes sound-evoked activity without changing spontaneous discharge in the mouse inferior colliculus. Front Syst Neurosci 12:59

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shamma S, Lorenzi C (2013) On the balance of envelope and temporal fine structure in the encoding of speech in the early auditory system. J Acoustical Soc Am 133:2818–2833

    Article  Google Scholar 

  • Sheppard AM, Liu X, Ding D, Salvi RJ (2018) Auditory central gain compensates for changes in cochlear output afterprolonged low-level noise exposure. Neurosci Lett 687:183–188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sheppard A, Stocking C, Ralli M, Salvi RJ (2020) A review of auditory gain, low-level noise and sound therapy for tinnitus and hyperacusis. Int J Audiol 59:5–15

    Article  PubMed  Google Scholar 

  • Shew WL, Plenz D (2013) The functional benefits of criticality in the cortex. Neuroscientist 19:88–100

    Article  PubMed  Google Scholar 

  • Silver RA (2010) Neuronal arithmetic. Nat Rev Neurosci 11:474–489

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Slepecky N (1986) Overview of mechanical damage to the inner ear: noise as a tool to probe cochlear function. Hear Res 22:307–321

    Article  CAS  PubMed  Google Scholar 

  • Snell KB (1997) Age-related changes in temporal gap detection. J Acoust Soc Am 101:2214–2220

    Article  CAS  PubMed  Google Scholar 

  • Snell KB, Frisina DR (2000) Relationships among age-related differences in gap detection and word recognition. J Acoust Soc Am 107:1615–1626

    Article  CAS  PubMed  Google Scholar 

  • Sörös P, Treismann IK, Manemann E, Lütkenhöner B (2009) Auditory temporal processing in healthy aging: a magnetoencephalographic study. BMC Neurosci 10:34

    Article  PubMed  PubMed Central  Google Scholar 

  • Stolzberg D, Chrostowski M, Salvi RJ, Allman B (2012) Intracortical circuits amplify sound-evoked activity in primary auditory cortex following systemic injection of salicylate in the rat. J Neurophysiol 108:200–214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stolzberg D, Hayes SH, Kashanian N, Radziwon K, Salvi RJ, Allman BL (2013) A novel behavioral assay for the assessment of acute tinnitus in rats optimized for simultaneous recording of oscillatory neural activity. J Neurosci Methods 219:224–232

    Article  PubMed  PubMed Central  Google Scholar 

  • Stothart G, Kazanina N (2016) Auditory perception in the aging brain: the role of inhibition and facilitation in early processing. Neurobiol Aging 47:23–24

    Article  PubMed  PubMed Central  Google Scholar 

  • Sturm JJ, Zhang-Hooks YX, Roos H, Nguyen T, Kandler K (2017) Noise trauma-induced behavioral gap detection deficits correlate with reorganization of excitatory and inhibitory local circuits in the inferior colliculus and are prevented by acoustic enrichment. J Neurosci 37:6314–6330

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun W, Lu J, Stolzberg D, Gray L, Deng A, Lobarinas E, Salvi RJ (2009) Salicylate increases the gain of the central auditory system. Neuroscience 159:325–334

    Article  CAS  PubMed  Google Scholar 

  • Sun W, Deng A, Jayaram A, Gibson B (2012) Noise exposure enhances auditory cortex responses related to hyperacusis behavior. Brain Res 1485:108–116

    Article  CAS  PubMed  Google Scholar 

  • Syka J, Rybalko N, Popelár J (1994) Enhancement of the auditory cortex evoked responses in awake guinea pigs after noise exposure. Hear Res 78:158–168

    Article  CAS  PubMed  Google Scholar 

  • Takesian AE, Kotak VC, Sanes DH (2009) Developmental hearing loss disrupts synaptic inhibition: implications for auditory processing. Future Neurol 4:331–349

    Article  PubMed  PubMed Central  Google Scholar 

  • Takesian AE, Kotak VC, Sanes DH (2012) Age-dependent effect of hearing loss on cortical inhibitory synapse function. J Neurophysiol 107:937–947

    Article  CAS  PubMed  Google Scholar 

  • Teichert M, Liebmann L, Hübner CA, Bolz J (2017) Homeostatic plasticity and synaptic scaling in the adult mouse auditory cortex. Sci Rep 7:17423

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Thomas ME, Guercio GD, Drudik KM, de Villers-Sidani É (2019a) Evidence of hyperacusis in adult rats following non-traumatic sound exposure. Front Syst Neurosci 13:55

    Article  PubMed  PubMed Central  Google Scholar 

  • Thomas ME, Friedman NHM, Cisneros-Franco JM, Ouellet L, de Villers-Sidani E (2019b) The prolonged masking of temporal acoustic inputs with noise drives plasticity in the adult rat auditory cortex. Cereb Cortex 29:1032–1046

    Article  PubMed  Google Scholar 

  • Tremblay KL, Piskosz M, Souza P (2003) Effects of age and age-related hearing loss on the neural representation of speech cues. Clin Neurophysiol 114:1332–1343

    Article  PubMed  Google Scholar 

  • Tsai K-T, Lin M-D, Chen Y-H (2009) Noise mapping in urban environments: a Taiwan study. Appl Acoust 70:964–972

    Article  Google Scholar 

  • Turner CW, Nelson DA (1982) Frequency discrimination in regions of normal and impaired sensitivity. J Speech Hear Res 25:34–41

    Article  CAS  PubMed  Google Scholar 

  • Turner JG, Hughes LF, Caspary DM (2005) Affects of aging on receptive fields in rat primary auditory cortex layer V neurons. J Neurophysiol 94:2738–2747

    Article  PubMed  Google Scholar 

  • Turner JG, Brozoski TJ, Bauer CA, Parrish JL, Myers K, Hughes LF, Caspary DM (2006) Gap detection deficits in rats with tinnitus: a potential novel screening tool. Behav Neurosci 120:188–195

    Article  PubMed  Google Scholar 

  • Turrigiano GG (1999) Homeostatic plasticity in neuronal networks: the more things change, the more they stay the same. Trends Neurosci 22:221–227

    Article  CAS  PubMed  Google Scholar 

  • Turrigiano GG (2012) Homeostatic synaptic plasticity: local and global mechanisms for stabilizing neuronal function. Cold Spring Harbor Perspectives Biology 4:a005736

    Article  CAS  Google Scholar 

  • Turrigiano GG, Nelson SB (2000) Hebb and homeostasis in neuronal plasticity. Curr Opin Neurobiol 10:358–364

    Article  CAS  PubMed  Google Scholar 

  • Tyler RS, Pienkowski M, Roncancio ER, Jun HJ, Brozoski T, Dauman N, Coelho CB, Andersson G, Keiner AJ, Cacace AT, Martin N, Moore BCJ (2014) A review of hyperacusis and future directions: Part I. Definitions and manifestations. Am J Audiol 23:402–419

    Article  PubMed  Google Scholar 

  • Walton JP (2010) Timing is everything: temporal processing deficits in the aged auditory brainstem. Hear Res 264:63–69

    Article  PubMed  PubMed Central  Google Scholar 

  • Walton JP, Frisina RD, O’Neill WE (1998) Age-related alteration in processing of temporal sound features in the auditory midbrain of the CBA mouse. J Neurosci 18:2764–2776

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Walton JP, Simon H, Frisina RD (2002) Age-related alterations in the neural coding of envelope periodicities. J Neurophysiol 88:565–578

    Article  PubMed  Google Scholar 

  • Wang J, McFadden SL, Caspary DM, Salvi RJ (2002) Gamma-aminobutyric acid circuits shape response properties of auditory cortex neurons. Brain Res Interactive 944:219–231

    Article  CAS  Google Scholar 

  • Wang F, Zuo L, Hong B, Han D, Range EM, Zhao L, Sui Y, Guo W, Liu L (2013) Tonotopic reorganization and spontaneous firing in inferior colliculus during both short and long recovery periods after noise overexposure. J Biomed Sci 20:91

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wehr M, Zador AM (2003) Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426:442–446

    Article  CAS  PubMed  Google Scholar 

  • Weisz N, Moratti S, Meinzer M, Dohrmann K, Elbert T (2005) Tinnitus perception and distress is related to abnormal spontaneous brain activity as measured by magnetoencephalography. PloS Med 2:e153

    Article  PubMed  PubMed Central  Google Scholar 

  • Whitmire CJ, Stanley GB (2016) Rapid sensory adaptation redux: a circuit perspective. Neuron 92:298–315

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wieczerzak KB, Patel SV, MacNeil H, Scott KE, Schormans AL, Hayes SH, Herrmann B, Allman BL (2021) Differential plasticity in auditory and prefrontal cortices, and cognitive-behavioral deficits following noise-induced hearing loss. Neuroscience 455:1–18

    Article  CAS  PubMed  Google Scholar 

  • Willott JF (1986) Effects of aging, hearing loss, and anatomical location on thresholds of inferior colliculus neurons in C57BL/6 and CBA mice. J Neurophysiol 56:391–408

    Article  CAS  PubMed  Google Scholar 

  • Willott JF, Parham K, Hunter KP (1988a) Response properties of inferior colliculus neurons in middle-aged C57BL/6J mice with presbycusis. Hear Res 37:15–27

    Article  CAS  PubMed  Google Scholar 

  • Willott JF, Parham K, Hunter KP (1988b) Response properties of inferior colliculus neurons in young and very old CBA/J mice. Hear Res 37:1–14

    Article  CAS  PubMed  Google Scholar 

  • Wolak T, Ciesla K, Lorens A, Kochanek K, Lewandowska M, Rusiniak M, Pluta A, Wojcik J, Skarzynski H (2017) Tonotopic organisation of the auditory cortex in sloping sensorineural hearing loss. Hear Res 355:81–96

    Article  PubMed  Google Scholar 

  • Wood KC, Blackwell JM, Geffen MN (2017) Cortical inhibitory interneurons control sensory processing. Curr Opin Neurobiol 46:200–207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Woods DL, Alain C (2009) Functional imaging of human auditory cortex. Curr Opin Otolaryngol Head Neck Surg 17:407–411

    Article  PubMed  Google Scholar 

  • Woods TM, Lopez SE, Long JH, Rahman JE, Recanzone GH (2006) Effects of stimulus azimuth and intensity on the single-neuron activity in the auditory cortex of the alert macaque monkey. J Neurophysiol 96:3323–3337

    Article  PubMed  Google Scholar 

  • Wu P-z, O’Malley JT, de Gruttola V, Liberman MC (2020) Age-related hearing loss is dominated by damage to inner ear sensory cells, not the cellular battery that powers them. J Neurosci 40:6357–6366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang L, Pollak GD (1997) Differential response properties to amplitude modulated signals in the dorsal nucleus of the lateral lemniscus of the mustache bat and the roles of GABAergic inhibition. J Neurophysiol 77:324–340

    Article  CAS  PubMed  Google Scholar 

  • Yang G, Lobarinas E, Zhang L, Turnerc J, Stolzberg D, Salvi R, Sun W (2007) Salicylate induced tinnitus: behavioral measures and neuralactivity in auditory cortex of awake rats. Hear Res 226:244–253

    Article  CAS  PubMed  Google Scholar 

  • Yang S, Weiner BD, Zhang LS, Cho S-J, Bao S (2011) Homeostatic plasticity drives tinnitus perceptionin an animal model. Proc Natl Acad Sci 108:14974–14979

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshida N, Liberman MC (2000) Sound conditioning reduces noise-induced permanent threshold shift in mice. Hear Res 148:213–219

    Article  CAS  PubMed  Google Scholar 

  • Yuan Y, Shi F, Yin Y, Tong M, Lang H, Polley DB, Liberman MC, Edge AS (2014) Ouabain-induced cochlear nerve degeneration: synaptic loss and plasticity in a mouse model of auditory neuropathy. J Assoc Res Otolaryngol 15:31–43

    Article  PubMed  Google Scholar 

  • Zeng F-G (2013) An active loudness model suggesting tinnitus as increased central noise and hyperacusis as increased nonlinear gain. Hear Res 295:172–179

    Article  PubMed  Google Scholar 

  • Zeng FG, Richardson M, Turner K (2020) Tinnitus does not interfere with auditory and speech perception. J Neurosci 40:6007–6017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang JS, Kaltenbach JA (1998) Increases in spontaneous activity in the dorsal cochlear nucleus of the rat following exposure to high-intensity sound. Neurosci Lett 250:197–200

    Article  CAS  PubMed  Google Scholar 

  • Zhao Y, Song Q, Li X, Li C (2016) Neural hyperactivity of the central auditory system in response to peripheral damage. Neural Plast 2016:2162105

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhou X, Merzenich MM (2012) Environmental noise exposure degrades normal listening processes. Nat Commun 3:843

    Article  PubMed  CAS  Google Scholar 

Download references

Funding

BH was supported by the Canada Research Chair program.

Author information

Authors and Affiliations

  1. Rotman Research Institute, Baycrest, Toronto, ON, M6A 2E1, Canada

    Björn Herrmann

  2. Department of Psychology, University of Toronto, Toronto, ON, Canada

    Björn Herrmann

  3. Department of Psychology & The Brain and Mind Institute, University of Western Ontario, London, ON, Canada

    Blake E. Butler

  4. National Centre for Audiology, University of Western Ontario, London, ON, Canada

    Blake E. Butler

Authors
  1. Björn Herrmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Blake E. Butler
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

BH had the idea for the article. BH and BEB performed the literature search. BH drafted the manuscript. BH and BEB critically revised the manuscript.

Corresponding author

Correspondence to Björn Herrmann.

Ethics declarations

Conflict of interest

The authors have no conflict of interest/competing interests.

Consent for publication

BH and BEB consent to the publication.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Herrmann, B., Butler, B.E. Hearing loss and brain plasticity: the hyperactivity phenomenon. Brain Struct Funct 226, 2019–2039 (2021). https://doi.org/10.1007/s00429-021-02313-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-021-02313-9

Keywords

Search

Navigation