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27.02.2018 | Original Article

Tinnitus and temporary hearing loss result in differential noise-induced spatial reorganization of brain activity

verfasst von: Antonela Muca, Emily Standafer, Aaron K. Apawu, Farhan Ahmad, Farhad Ghoddoussi, Mirabela Hali, James Warila, Bruce A. Berkowitz, Avril Genene Holt

Erschienen in: Brain Structure and Function | Ausgabe 5/2018

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Abstract

Loud noise frequently results in hyperacusis or hearing loss (i.e., increased or decreased sensitivity to sound). These conditions are often accompanied by tinnitus (ringing in the ears) and changes in spontaneous neuronal activity (SNA). The ability to differentiate the contributions of hyperacusis and hearing loss to neural correlates of tinnitus has yet to be achieved. Towards this purpose, we used a combination of behavior, electrophysiology, and imaging tools to investigate two models of noise-induced tinnitus (either with temporary hearing loss or with permanent hearing loss). Manganese (Mn²⁺) uptake was used as a measure of calcium channel function and as an index of SNA. Manganese uptake was examined in vivo with manganese-enhanced magnetic resonance imaging (MEMRI) in key auditory brain regions implicated in tinnitus. Following acoustic trauma, MEMRI, the SNA index, showed evidence of spatially dependent rearrangement of Mn²⁺ uptake within specific brain nuclei (i.e., reorganization). Reorganization of Mn²⁺ uptake in the superior olivary complex and cochlear nucleus was dependent upon tinnitus status. However, reorganization of Mn²⁺ uptake in the inferior colliculus was dependent upon hearing sensitivity. Furthermore, following permanent hearing loss, reduced Mn²⁺ uptake was observed. Overall, by combining testing for hearing sensitivity, tinnitus, and SNA, our data move forward the possibility of discriminating the contributions of hyperacusis and hearing loss to tinnitus.

Altschuler RA, Dolan DF, Halsey K, Kanicki A, Deng N, Martin C, Eberle J, Kohrman DC, Miller RA, Schacht J (2015) Age-related changes in auditory nerve-inner hair cell connections, hair cell numbers, auditory brain stem response and gap detection in UM-HET4 mice. Neuroscience 292:22–33CrossRefPubMedPubMedCentral

Auerbach BD, Rodrigues PV, Salvi RJ (2014) Central gain control in tinnitus and hyperacusis. Front Neurol 5:206CrossRefPubMedPubMedCentral

Baizer JS, Manohar S, Paolone NA, Weinstock N, Salvi RJ (2012) Understanding tinnitus: The dorsal cochlear nucleus, organization and plasticity. Brain Res 1485:40–53CrossRefPubMedPubMedCentral

Basta D, Ernest A (2004) Noise-induced changes of neuronal spontaneous activity in mice inferior colliculus brain slices. Neurosci Lett 368(3):297–302CrossRefPubMed

Bissig D, Berkowitz BA (2014) Testing the calcium hypothesis of aging in the rat hippocampus in vivo using manganese-enhanced MRI. Neurobiol Aging 35(6):1453–1458CrossRefPubMed

Brozoski TJ, Bauer CA, Caspary DM (2002) Elevated fusiform cell activity in the dorsal cochlear nucleus of chinchillas with psychophysical evidence of tinnitus. J Neurosci 22(6):2383–2390CrossRefPubMed

Brozoski TJ, Ciobanu L, Bauer CA (2007) Central neural activity in rats with tinnitus evaluated with manganese-enhanced magnetic resonance imaging (MEMRI). Hear Res 228(1–2):168–179CrossRefPubMed

Brozoski TJ et al (2010) The effect of supplemental dietary taurine on tinnitus and auditory discrimination in an animal model. Hear Res 270(1–2):71–80CrossRefPubMedPubMedCentral

Brozoski TJ, Wisner KW, Odintsov B, Bauer CA (2013) Local NMDA receptor blockade attenuates chronic tinnitus and associated brain activity in an animal model. Plos One 8(10):e77674CrossRefPubMedPubMedCentral

Bures Z, Grécová J, Popelár J, Syka J (2010) Noise exposure during early development impairs the processing of sound intensity in adult rats. Eur J Neurosci 32:155–164CrossRefPubMed

Cacace AT, Brozoski T, Berkowitz B, Bauer C, Odintsov B, Bergkvist M, Castracane J, Zhang J, Holt AG (2014) Manganese enhanced magnetic resonance imaging (MEMRI): a powerful new imaging method to study tinnitus. Hear Res 311:49–62CrossRefPubMed

Carlson S, Willott JF (1996) The behavioral salience of tones as indicated by prepulse inhibition of the startle response: relationship to hearing loss and central neural plasticity in C57BL/6J mice. Hear Res 99(1–2):168–175CrossRefPubMed

Campolo J, Lobarinas E, Salvi R (2013) Does tinnitus “fill in” the silent gaps? Noise Health 15(67):398–405CrossRefPubMed

Chen GD, Sheppard A, Salvi R (2016) Noise trauma induced plastic changes in brain regions outside the classical auditory pathway. Neuroscience 315:228–245CrossRefPubMed

Chuang KH, Koretsky AP, Sotak CH (2009) Temporal changes in the T1 and T2 relaxation rates (DeltaR1 and DeltaR2) in the rat brain are consistent with the tissue-clearance rates of elemental manganese. Magn Reson Med 61(6):1528–1532CrossRefPubMedPubMedCentral

Davis (1984) The mammalian startle response. In: Eaton RC (ed) Neural mechanisms of startle behavior. Plenum Press, New York, pp 287–351

Eggermont JJ, Roberts LE (2004) The neuroscience of tinnitus. Trends Neurosci 27(11):676–682CrossRefPubMed

Galazyuk A, Hébert S (2015) Gap-prepulse inhibition of the acoustic startle reflex (GPIAS) for tinnitus assessment: current status and future directions. Front Neurol 6:88CrossRefPubMedPubMedCentral

Gerken GM, Saunders SS, Paul RE (1984) Hypersensitivity to electrical stimulation of auditory nuclei follows hearing loss in cats. Hear Res 13(3):249–259CrossRefPubMed

Grécová J, Bures Z, Popelár J, Suta D, Syka J (2009) Brief exposure of juvenile rats to noise impairs the development of the response properties of inferior colliculus neurons. Eur J Neurosci 29:1921–1930CrossRefPubMed

Hackett TA, Barkat TR, O’Brien BM, Hensch TK, Polley DB (2011) Linking topography to tonotopy in the mouse auditory thalamocortical circuit. J Neurosci 31(8):2983–2995CrossRefPubMedPubMedCentral

Heffner HE (2011) A two-choice sound localization procedure for detecting lateralized tinnitus in animals. Behav Res Methods 43(2):577–589CrossRefPubMed

Heffner HE, Harrington IA (2002) Tinnitus in hamsters following exposure to intense sound. Hear Res 170(1–2):83–95CrossRefPubMed

Hickox AE, Liberman MC (2014) Is noise-induced cochlear neuropathy key to the generation of hyperacusis or tinnitus? J Neurophysiol 111

Holt AG, Bissig D, Mirza N, Rajah G, Berkowitz B (2010) Evidence of key tinnitus-related brain regions documented by a unique combination of manganese-enhanced MRI and acoustic startle reflex testing. Plos One 5(12):e14260CrossRefPubMedPubMedCentral

Huang CM, Fex J (1986) Tonotopic organization in the inferior colliculus of the rat demonstrated with the 2-deoxyglucose method. Exp Brain Res 61(3):506–512CrossRefPubMed

Ison JR, Allen PD (2003) Low-frequency tone pips elicit exaggerated startle reflexes in C57BL/6J mice with hearing loss. J Assoc Res Otolaryngol 4(4):495–504CrossRefPubMedPubMedCentral

Jastreboff PJ, Hazell JWP (1993) A neurophysiological approach to tinnitus—clinical implications. Br J Audiol 27(1):7–17CrossRefPubMed

Jones LS, Disterhoft JF (1983) The effect of auditory stimulus rate on [14C]2-deoxyglucose uptake in rabbit inferior colliculus. Brain Res 279(1–2):85–91CrossRefPubMed

Kaltenbach JA, Zhang J, Afman CE (2000) Plasticity of spontaneous neural activity in the dorsal cochlear nucleus after intense sound exposure. Hear Res 147(1–2):282–292CrossRefPubMed

Kaltenbach JA, Zhang J, Finlayson P (2005) Tinnitus as a plastic phenomenon and its possible neural underpinnings in the dorsal cochlear nucleus. Hear Res 206(1–2):200–226CrossRefPubMed

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

Koch (1999) The neurobiology of startle. Prog Neurobiol 59:107–128CrossRefPubMed

Kujawa SG, Liberman MC (2009) Adding insult to injury: cochlear nerve degeneration after “temporary” noise-induced hearing loss. J Neurosci 29(45):14077–14085CrossRefPubMedPubMedCentral

Lobarinas E, Salvi R, Baizer J, Altman C, Allman B (2013) Noise and health special issue: advances in the neuroscience of tinnitus. Noise Health 15(63):81–82CrossRefPubMed

Lockwood AH, Salvi RJ, Coad ML, Towsley ML, Wack DS, Murphy BW (1998) The functional neuroanatomy of tinnitus—evidence for limbic system links and neural plasticity. Neurology 50(1):114–120CrossRefPubMed

Longenecker RJ, Galazyuk AV (2011) Development of tinnitus in CBA/CaJ mice following sound exposure. J Assoc Res Otolaryngol 12(5):647–658CrossRefPubMedPubMedCentral

Longenecker RJ, Galazyuk AV (2012) Methodological optimization of tinnitus assessment using prepulse inhibition of the acoustic startle reflex. Brain Res 1485:54–62CrossRefPubMed

Longenecker RJ, Chonko KT, Maricich SM, Galazyuk AV (2014) Age effects on tinnitus and hearing loss in CBA/CaJ mice following sound exposure. SpringerPlus 3(1):1–13CrossRef

Luo H, Pace E, Zhang X, Zhang J (2014) Blast-Induced tinnitus and spontaneous firing changes in the rat dorsal cochlear nucleus. J Neurosci Res 92(11):1466–1477CrossRefPubMed

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

Mulders WHAM, Robertson D (2011) Progressive centralization of midbrain hyperactivity after acoustic trauma. Neuroscience 192:753–760CrossRefPubMed

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

Mulders WH, Ding D, Salvi R, Robertson D (2011) Relationship between auditory thresholds, central spontaneous activity, and hair cell loss after acoustic trauma. J Comp Neurol 519(13):2637–2647CrossRefPubMedPubMedCentral

Ono M, Bishop DC, Oliver DL (2016) Long-lasting sound-evoked afterdischarge in the auditory midbrain. Sci Rep 6:20757CrossRefPubMedPubMedCentral

Paxinos G, Watson C (2007) The rat brain in stereotaxic coordinates. Elsevier, Amsterdam

Pienkowski M, Eggermont JJ (2012) Reversible long-term changes in auditory processing in mature auditory cortex in the absence of hearing loss induced by passive, moderate-level sound exposure. Ear Hear 33:305–314CrossRef

Robertson D, Bester C, Vogler D, Mulders WHAM. (2013) Spontaneous hyperactivity in the auditory midbrain: Relationship to afferent input. Hear Res 295:124–129CrossRefPubMed

Romand R, Ehret G (1990) Development of tonotopy in the inferior colliculus. I. Electrophysiological mapping in house mice. Brain Res Dev Brain Res 54(2):221–234CrossRefPubMed

Ropp TJ, Tiedemann KL, Young ED, May BJ (2014) Effects of unilateral acoustic trauma on tinnitus-related spontaneous activity in the inferior colliculus. J Assoc Res Otolaryngol JARO 15(6):1007–1022CrossRefPubMed

Rorden C, Brett M (2000) Stereotaxic display of brain lesions. Behav Neurol 12(4):191–200CrossRefPubMed

Ryan AF, Axelsson GA, Woolf NK (1992) Central auditory metabolic activity induced by intense noise exposure. Hear Res 61(1–2):24–30CrossRefPubMed

Rybalko N, Bureš Z, Burianová J, Popelář J, Grécová J, Syka J (2011) Noise exposure during early development influences the acoustic startle reflex in adult rats. Physiol Behav 102:453–458CrossRefPubMed

Salvi RJ, Arehole S (1985) Gap detection in chinchillas with temporary high-frequency hearing-loss. J Acoust Soc Am 77(3):1173–1177CrossRefPubMed

Salloum RH, Yurosko C, Santiago L, Sandridge SA, Kaltenbach JA (2014) Induction of enhanced acoustic startle response by noise exposure: dependence on exposure conditions and testing parameters and possible relevance to hyperacusis. PLoS One 9(10):e111747CrossRefPubMedPubMedCentral

Shargorodsky J, Curhan GC, Farwell WR (2010) Prevalence and characteristics of tinnitus among US adults. Am J Med 123

Shore S, Zhou JX, Koehler S (2007) Neural mechanisms underlying somatic tinnitus. Prog Brain Res 166:107–123CrossRefPubMedPubMedCentral

Silva AC, Bock NA (2008) Manganese-enhanced MRI: an exceptional tool in translational neuroimaging. Schizophr Bull 34(4):595–604CrossRefPubMedPubMedCentral

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(1):325–334CrossRefPubMed

Swerdlow N et al (2001) Neural circuit regulation of prepulse inhibition of startle in the rat: current knowledge and future challenges. Psychopharmacology (Berl) 156(2-3):194–215CrossRefPubMed

Takeda A (2003) Manganese action in brain function. Brain Res Rev 41(1):79–87CrossRefPubMed

Turner JG, Larsen D (2016) Effects of noise exposure on development of tinnitus and hyperacusis: prevalence rates 12 months after exposure in middle-aged rats. Hear Res 334:30–36CrossRefPubMed

Turner JG, Parrish J (2008) Gap detection methods for assessing salicylate-induced tinnitus and hyperacusis in rats. Am J Audiol 17(2):S185–S192CrossRef

Turner JG, Brozoski TJ, Bauer CA, Parrish JL, Myers K (2006) Gap detection deficits in rats with tinnitus: a potential novel screening tool. Behav Neurosci 120(1):188–195CrossRefPubMed

Turner J, Larsen D, Hughes L, Moechars D, Shore S (2012) Time course of tinnitus development following noise exposure in mice. J Neurosci Res 90(7):1480–1488CrossRefPubMedPubMedCentral

Turner JG, Parrish JL, Zuiderveld L, Darr S, Hughes LF, Caspary DM, Idrezbegovic E, Canlon B (2013) Acoustic experience alters the aged auditory system. Ear Hear 34:151–159CrossRef

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

Turrigiano G (2011) Too many cooks? Intrinsic and synaptic homeostatic mechanisms in cortical circuit refinement. Annu Rev Neurosci 34:89–103CrossRef

Turrigiano GG, Nelson SB (2004) Homeostatic plasticity in the developing nervous system. Nat Rev Neurosci 5:97–107CrossRef

Tyler RS, Pienkowski M, Roncancio ER, Jun HJ, Brozoski T, Dauman N, Coelho CB, Andersson G, Keiner AJ, Cacace AT (2014) A review of hyperacusis and future directions: part I. Definitions and manifestations. Am J Audiol 23(4):402–419CrossRefPubMed

Van de Moortele PF, Auerbach EJ, Olman C, Yacoub E, Ugurbil K, Moeller S (2009) T1 weighted brain images at 7 T unbiased for Proton Density, T2* contrast and RF coil receive B1 sensitivity with simultaneous vessel visualization. Neuroimage 46(2):432–446CrossRefPubMedPubMedCentral

Yang G, Lobarinas E, Zhang L, Turner J, Stolzberg D, Salvi R, Sun W (2007) Salicylate induced tinnitus: behavioral measures and neural activity in auditory cortex of rats. Hear Res 226(1–2):244–253CrossRefPubMed

Young JS, Fechter LD (1983) Reflex inhibition procedures for animal audiometry: a technique for assessing ototoxicity. J Acoust Soc Am 73(5):1686–1693CrossRefPubMed

Yu X, Wadghiri YZ, Sanes DH, Turnbull DH (2005) In vivo auditory brain mapping in mice with Mn-enhanced MRI. Nat Neurosci 8(7):961–968CrossRefPubMedPubMedCentral

Yu X, Sanes DH, Aristizabal O, Wadghiri YZ, Turnbull DH (2007) Large-scale reorganization of the tonotopic map in mouse auditory midbrain revealed by MRI. Proc Natl Acad Sci USA 104(29):12193–12198CrossRefPubMedPubMedCentral

Yu X, Zou J, Babb JS, Johnson G, Sanes DH, Turnbull DH (2008) Statistical mapping of sound-evoked activity in the mouse auditory midbrain using Mn-enhanced MRI. NeuroImage 39(1):223–230CrossRefPubMed

Yu X, Nieman BJ, Sudarov A, Szulc KU, Abdollahian DJ, Bhatia N, Lalwani AK, Joyner AL, Turnbull DH (2011) Morphological and functional midbrain phenotypes in Fibroblast Growth Factor 17 mutant mice detected by Mn-enhanced MRI. Neuroimage 56(3):1251–1258CrossRefPubMedPubMedCentral

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(3):197–200CrossRefPubMed

Titel: Tinnitus and temporary hearing loss result in differential noise-induced spatial reorganization of brain activity
verfasst von: Antonela Muca
Emily Standafer
Aaron K. Apawu
Farhan Ahmad
Farhad Ghoddoussi
Mirabela Hali
James Warila
Bruce A. Berkowitz
Avril Genene Holt
Publikationsdatum: 27.02.2018
Verlag: Springer Berlin Heidelberg
Erschienen in: Brain Structure and Function / Ausgabe 5/2018
Print ISSN: 1863-2653
Elektronische ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-018-1635-z

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