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Brain Structure and Function

, Volume 223, Issue 5, pp 2343–2360 | Cite as

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

  • Antonela Muca
  • Emily Standafer
  • Aaron K. Apawu
  • Farhan Ahmad
  • Farhad Ghoddoussi
  • Mirabela Hali
  • James Warila
  • Bruce A. Berkowitz
  • Avril Genene HoltEmail author
Original Article

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.

Keywords

Tinnitus Hyperacusis Neuronal activity Hyperactivity Neuroplasticity Hearing loss Permanent threshold shift Temporary threshold shift Manganese enhanced MRI Gap detection MEMRI Acoustic startle reflex 

Notes

Acknowledgements

We thank Mohanned Ahmed, Ahmad Ali Nassar, Sharowyn Wilson, and Nour Arafat for their help with experiments, analysis and creating macros for data analysis. A special thank you to Drs. P. D. Walker and R. Braun for providing feedback on the article prior to submission.

Funding

This work was supported by the Department of Veterans Affairs (Grant 1I01RX001095-01U.S to A.G.H); the National Institute for Occupational Safety and Health, Centers for Disease Control and Prevention (training Grant T42 OH008455 to AGH and AKA); the National Institutes of Health (Grant EY021619 to BAB); and Research to Prevent Blindness (unrestricted Grant to BAB). The views expressed do not necessarily reflect the official policies of the Department of Health and Human Services, nor does mention of trade names, commercial practices, or organizations imply endorsement by the US Government.

References

  1. 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 292:22–33CrossRefPubMedPubMedCentralGoogle Scholar
  2. Auerbach BD, Rodrigues PV, Salvi RJ (2014) Central gain control in tinnitus and hyperacusis. Front Neurol 5:206CrossRefPubMedPubMedCentralGoogle Scholar
  3. Baizer JS, Manohar S, Paolone NA, Weinstock N, Salvi RJ (2012) Understanding tinnitus: The dorsal cochlear nucleus, organization and plasticity. Brain Res 1485:40–53CrossRefPubMedPubMedCentralGoogle Scholar
  4. Basta D, Ernest A (2004) Noise-induced changes of neuronal spontaneous activity in mice inferior colliculus brain slices. Neurosci Lett 368(3):297–302CrossRefPubMedGoogle Scholar
  5. 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):1453–1458CrossRefPubMedGoogle Scholar
  6. 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):2383–2390CrossRefPubMedGoogle Scholar
  7. 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):168–179CrossRefPubMedGoogle Scholar
  8. 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):71–80CrossRefPubMedPubMedCentralGoogle Scholar
  9. 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):e77674CrossRefPubMedPubMedCentralGoogle Scholar
  10. 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 32:155–164CrossRefPubMedGoogle Scholar
  11. 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 311:49–62CrossRefPubMedGoogle Scholar
  12. 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):168–175CrossRefPubMedGoogle Scholar
  13. Campolo J, Lobarinas E, Salvi R (2013) Does tinnitus “fill in” the silent gaps? Noise Health 15(67):398–405CrossRefPubMedGoogle Scholar
  14. Chen GD, Sheppard A, Salvi R (2016) Noise trauma induced plastic changes in brain regions outside the classical auditory pathway. Neuroscience 315:228–245CrossRefPubMedGoogle Scholar
  15. 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):1528–1532CrossRefPubMedPubMedCentralGoogle Scholar
  16. Davis (1984) The mammalian startle response. In: Eaton RC (ed) Neural mechanisms of startle behavior. Plenum Press, New York, pp 287–351Google Scholar
  17. Eggermont JJ, Roberts LE (2004) The neuroscience of tinnitus. Trends Neurosci 27(11):676–682CrossRefPubMedGoogle Scholar
  18. Galazyuk A, Hébert S (2015) Gap-prepulse inhibition of the acoustic startle reflex (GPIAS) for tinnitus assessment: current status and future directions. Front Neurol 6:88CrossRefPubMedPubMedCentralGoogle Scholar
  19. Gerken GM, Saunders SS, Paul RE (1984) Hypersensitivity to electrical stimulation of auditory nuclei follows hearing loss in cats. Hear Res 13(3):249–259CrossRefPubMedGoogle Scholar
  20. 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 29:1921–1930CrossRefPubMedGoogle Scholar
  21. 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):2983–2995CrossRefPubMedPubMedCentralGoogle Scholar
  22. Heffner HE (2011) A two-choice sound localization procedure for detecting lateralized tinnitus in animals. Behav Res Methods 43(2):577–589CrossRefPubMedGoogle Scholar
  23. Heffner HE, Harrington IA (2002) Tinnitus in hamsters following exposure to intense sound. Hear Res 170(1–2):83–95CrossRefPubMedGoogle Scholar
  24. Hickox AE, Liberman MC (2014) Is noise-induced cochlear neuropathy key to the generation of hyperacusis or tinnitus? J Neurophysiol 111Google Scholar
  25. 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):e14260CrossRefPubMedPubMedCentralGoogle Scholar
  26. 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):506–512CrossRefPubMedGoogle Scholar
  27. 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):495–504CrossRefPubMedPubMedCentralGoogle Scholar
  28. Jastreboff PJ, Hazell JWP (1993) A neurophysiological approach to tinnitus—clinical implications. Br J Audiol 27(1):7–17CrossRefPubMedGoogle Scholar
  29. 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):85–91CrossRefPubMedGoogle Scholar
  30. 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):282–292CrossRefPubMedGoogle Scholar
  31. 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):200–226CrossRefPubMedGoogle Scholar
  32. 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 111:17–33CrossRefPubMedGoogle Scholar
  33. Koch (1999) The neurobiology of startle. Prog Neurobiol 59:107–128CrossRefPubMedGoogle Scholar
  34. Kujawa SG, Liberman MC (2009) Adding insult to injury: cochlear nerve degeneration after “temporary” noise-induced hearing loss. J Neurosci 29(45):14077–14085CrossRefPubMedPubMedCentralGoogle Scholar
  35. 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):81–82CrossRefPubMedGoogle Scholar
  36. 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):114–120CrossRefPubMedGoogle Scholar
  37. Longenecker RJ, Galazyuk AV (2011) Development of tinnitus in CBA/CaJ mice following sound exposure. J Assoc Res Otolaryngol 12(5):647–658CrossRefPubMedPubMedCentralGoogle Scholar
  38. Longenecker RJ, Galazyuk AV (2012) Methodological optimization of tinnitus assessment using prepulse inhibition of the acoustic startle reflex. Brain Res 1485:54–62CrossRefPubMedGoogle Scholar
  39. 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):1–13CrossRefGoogle Scholar
  40. 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):1466–1477CrossRefPubMedGoogle Scholar
  41. McCormack A, Edmondson-Jones M, Somerset S, Hall D (2016) A systematic review of the reporting of tinnitus prevalence and severity. Hear Res 337:70–79CrossRefPubMedGoogle Scholar
  42. Mulders WHAM, Robertson D (2011) Progressive centralization of midbrain hyperactivity after acoustic trauma. Neuroscience 192:753–760CrossRefPubMedGoogle Scholar
  43. Mulders WHAM., Robertson D (2013) Development of hyperactivity after acoustic trauma in the guinea pig inferior colliculus. Hear Res 298:104–108CrossRefPubMedGoogle Scholar
  44. 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):2637–2647CrossRefPubMedPubMedCentralGoogle Scholar
  45. Ono M, Bishop DC, Oliver DL (2016) Long-lasting sound-evoked afterdischarge in the auditory midbrain. Sci Rep 6:20757CrossRefPubMedPubMedCentralGoogle Scholar
  46. Paxinos G, Watson C (2007) The rat brain in stereotaxic coordinates. Elsevier, AmsterdamGoogle Scholar
  47. 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 33:305–314CrossRefGoogle Scholar
  48. Robertson D, Bester C, Vogler D, Mulders WHAM. (2013) Spontaneous hyperactivity in the auditory midbrain: Relationship to afferent input. Hear Res 295:124–129CrossRefPubMedGoogle Scholar
  49. 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):221–234CrossRefPubMedGoogle Scholar
  50. 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):1007–1022CrossRefPubMedGoogle Scholar
  51. Rorden C, Brett M (2000) Stereotaxic display of brain lesions. Behav Neurol 12(4):191–200CrossRefPubMedGoogle Scholar
  52. Ryan AF, Axelsson GA, Woolf NK (1992) Central auditory metabolic activity induced by intense noise exposure. Hear Res 61(1–2):24–30CrossRefPubMedGoogle Scholar
  53. 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 102:453–458CrossRefPubMedGoogle Scholar
  54. Salvi RJ, Arehole S (1985) Gap detection in chinchillas with temporary high-frequency hearing-loss. J Acoust Soc Am 77(3):1173–1177CrossRefPubMedGoogle Scholar
  55. 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):e111747CrossRefPubMedPubMedCentralGoogle Scholar
  56. Shargorodsky J, Curhan GC, Farwell WR (2010) Prevalence and characteristics of tinnitus among US adults. Am J Med 123Google Scholar
  57. Shore S, Zhou JX, Koehler S (2007) Neural mechanisms underlying somatic tinnitus. Prog Brain Res 166:107–123CrossRefPubMedPubMedCentralGoogle Scholar
  58. Silva AC, Bock NA (2008) Manganese-enhanced MRI: an exceptional tool in translational neuroimaging. Schizophr Bull 34(4):595–604CrossRefPubMedPubMedCentralGoogle Scholar
  59. 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):325–334CrossRefPubMedGoogle Scholar
  60. 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):194–215CrossRefPubMedGoogle Scholar
  61. Takeda A (2003) Manganese action in brain function. Brain Res Rev 41(1):79–87CrossRefPubMedGoogle Scholar
  62. 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 334:30–36CrossRefPubMedGoogle Scholar
  63. Turner JG, Parrish J (2008) Gap detection methods for assessing salicylate-induced tinnitus and hyperacusis in rats. Am J Audiol 17(2):S185–S192CrossRefGoogle Scholar
  64. 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):188–195CrossRefPubMedGoogle Scholar
  65. 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):1480–1488CrossRefPubMedPubMedCentralGoogle Scholar
  66. 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 34:151–159CrossRefGoogle Scholar
  67. Turrigiano GG (1999) Homeostatic plasticity in neuronal networks: the more things change, the more they stay the same. Trends Neurosci 22:221–227Google Scholar
  68. Turrigiano G (2011) Too many cooks? Intrinsic and synaptic homeostatic mechanisms in cortical circuit refinement. Annu Rev Neurosci 34:89–103CrossRefGoogle Scholar
  69. Turrigiano GG, Nelson SB (2004) Homeostatic plasticity in the developing nervous system. Nat Rev Neurosci 5:97–107CrossRefGoogle Scholar
  70. 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):402–419CrossRefPubMedGoogle Scholar
  71. 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):432–446CrossRefPubMedPubMedCentralGoogle Scholar
  72. 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):244–253CrossRefPubMedGoogle Scholar
  73. Young JS, Fechter LD (1983) Reflex inhibition procedures for animal audiometry: a technique for assessing ototoxicity. J Acoust Soc Am 73(5):1686–1693CrossRefPubMedGoogle Scholar
  74. Yu X, Wadghiri YZ, Sanes DH, Turnbull DH (2005) In vivo auditory brain mapping in mice with Mn-enhanced MRI. Nat Neurosci 8(7):961–968CrossRefPubMedPubMedCentralGoogle Scholar
  75. 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):12193–12198CrossRefPubMedPubMedCentralGoogle Scholar
  76. 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):223–230CrossRefPubMedGoogle Scholar
  77. 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):1251–1258CrossRefPubMedPubMedCentralGoogle Scholar
  78. 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):197–200CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Antonela Muca
    • 1
  • Emily Standafer
    • 1
  • Aaron K. Apawu
    • 1
  • Farhan Ahmad
    • 1
  • Farhad Ghoddoussi
    • 2
  • Mirabela Hali
    • 1
  • James Warila
    • 1
  • Bruce A. Berkowitz
    • 1
    • 3
  • Avril Genene Holt
    • 1
    • 4
    Email author
  1. 1.Department of Anatomy and Cell BiologyWayne State University School of MedicineDetroitUSA
  2. 2.Department of AnesthesiologyWayne State University School of MedicineDetroitUSA
  3. 3.Department of OphthalmologyWayne State University School of MedicineDetroitUSA
  4. 4.John D. Dingell VAMCDetroitUSA

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