The Reduced Cochlear Output and the Failure to Adapt the Central Auditory Response Causes Tinnitus in Noise Exposed Rats

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Rüttiger, Lukas ^a   Singer, Wibke ^a   Panford Walsh, Rama ^a   Matsumoto, Masahiro ^a   Lee, Sze Chim ^a   Zuccotti, Annalisa ^a   Zimmermann, Ulrike ^a   Jaumann, Mirko ^a   Rohbock, Karin ^a   Xiong, Hao ^a   Knipper, Marlies ^a  

^a UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVITY REGULATED CYTOSKELETON ASSOCIATED PROTEIN; MESSENGER RNA;

ACTIVITY REGULATED CYTOSKELETON ASSOCIATED GENE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUDITORY CORTEX; BRAIN REGION; COCHLEA POTENTIAL; COCHLEAR NERVE; CONTROLLED STUDY; DISEASE SEVERITY; EVOKED BRAIN STEM AUDITORY RESPONSE; FEMALE; GENE EXPRESSION; HAIR CELL; HEARING IMPAIRMENT; NEUROPATHOLOGY; NONHUMAN; PROTEIN EXPRESSION; RAT; SENSORY DEPRIVATION; TINNITUS;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; AUDITORY CORTEX; AUDITORY THRESHOLD; BEHAVIOR, ANIMAL; COCHLEA; CYTOSKELETAL PROTEINS; EVOKED POTENTIALS, AUDITORY, BRAIN STEM; FEMALE; HAIR CELLS, AUDITORY, INNER; HEARING LOSS, NOISE-INDUCED; IMMUNOHISTOCHEMISTRY; NERVE TISSUE PROTEINS; NOISE; RATS; TINNITUS;

EID: 84874846057     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0057247     Document Type: Article

References (97)

1. Lockwood AH, Salvi RJ, Burkard RF, (2002) Tinnitus. N Engl J Med 347: 904-910.
2. Møller AR (2003) Pathophysiology of tinnitus. Otolaryngol Clin North Am 36: 249-266, v-vi.
3. Jastreboff PJ, (2007) Tinnitus retraining therapy. Prog Brain Res 166: 415-423.
4. Zenner HP, Pfister M, Birbaumer N, (2006) Tinnitus sensitization: Sensory and psychophysiological aspects of a new pathway of acquired centralization of chronic tinnitus. Otol Neurotol 27: 1054-1063.
5. Puel JL, Guitton MJ, (2007) Salicylate-induced tinnitus: molecular mechanisms and modulation by anxiety. Prog Brain Res 166: 141-146.
6. Leaver AM, Renier L, Chevillet MA, Morgan S, Kim HJ, et al. (2011) Dysregulation of limbic and auditory networks in tinnitus. Neuron 69: 33-43.
7. Meltser I, Tahera Y, Canlon B, (2009) Glucocorticoid receptor and mitogen-activated protein kinases activity after restraint stress and acoustic trauma. J Neurotrauma 26: 1835-1845.
8. Langguth B, Salvi R, Elgoyhen AB, (2009) Emerging pharmacotherapy of tinnitus. Expert Opin Emerg Drugs 14: 687-702.
9. Roberts LE, Eggermont JJ, Caspary DM, Shore SE, Melcher JR, et al. (2010) Ringing ears: the neuroscience of tinnitus. J Neurosci 30: 14972-14979.
10. Knipper M, Zimmermann U, Müller M, (2010) Molecular aspects of tinnitus. Hear Res 266: 60-69.
11. Rauschecker JP, Leaver AM, Mühlau M, (2010) Tuning out the noise: limbic-auditory interactions in tinnitus. Neuron 66: 819-826.
12. Salvi RJ, Wang J, Ding D, (2000) Auditory plasticity and hyperactivity following cochlear damage. Hear Res 147: 261-274.
13. 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: 2383-2390.
14. Kaltenbach JA, (2007) The dorsal cochlear nucleus as a contributor to tinnitus: mechanisms underlying the induction of hyperactivity. Prog Brain Res 166: 89-106.
15. Schaette R, Kempter R, (2009) Predicting tinnitus pitch from patients' audiograms with a computational model for the development of neuronal hyperactivity. J Neurophysiol 101: 3042-3052.
16. Middleton JW, Kiritani T, Pedersen C, Turner JG, Shepherd GM, et al. (2011) Mice with behavioral evidence of tinnitus exhibit dorsal cochlear nucleus hyperactivity because of decreased GABAergic inhibition. Proc Natl Acad Sci USA 108: 7601-7606.
17. Schaette R, McAlpine D, (2011) Tinnitus with a normal audiogram: physiological evidence for hidden hearing loss and computational model. J Neurosci 31: 13452-13457.
18. Yang S, Weiner BD, Zhang LS, Cho SJ, Bao S, (2011) Homeostatic plasticity drives tinnitus perception in an animal model. Proc Natl Acad Sci USA 108: 14974-14979.
19. Dehmel S, Pradhan S, Koehler S, Bledsoe S, Shore S, (2012) Noise overexposure alters long-term somatosensory- auditory processing in the dorsal cochlear nucleus-possible basis for tinnitus-related hyperactivity? J Neurosci 32: 1660-1671.
20. Dong S, Mulders WH, Rodger J, Robertson D, (2009) Changes in neuronal activity and gene expression in guinea-pig auditory brainstem after unilateral partial hearing loss. Neuroscience 159: 1164-1174.
21. Turner JG, (2007) Behavioral measures of tinnitus in laboratory animals. Prog Brain Res 166: 147-156.
22. Rüttiger L, Ciuffani J, Zenner HP, Knipper M, (2003) A behavioral paradigm to judge acute sodium salicylate-induced sound experience in rats: a new approach for an animal model on tinnitus. Hear Res 180: 39-50.
23. Tan J, Rüttiger L, Panford-Walsh R, Singer W, Schulze H, et al. (2007) Tinnitus behavior and hearing function correlate with the reciprocal expression patterns of BDNF and Arg3.1/arc in auditory neurons following acoustic trauma. Neuroscience 145: 715-726.
24. Kujawa SG, Liberman MC, (2009) Adding insult to injury: cochlear nerve degeneration after "temporary" noise-induced hearing loss. J Neurosci 29: 14077-14085.
25. Zuccotti A, Kuhn S, Johnson SL, Franz C, Singer W, et al. (2012) Lack of brain-derived neurotrophic factor hampers inner hair cell synapse physiology, but protects against noise induced hearing loss. J Neurosci 32, 8545-8553.
26. Ramirez-Amaya V, Vazdarjanova A, Mikhael D, Rosi S, Worley PF, et al. (2005) Spatial exploration-induced Arc mRNA and protein expression: evidence for selective, network-specific reactivation. J Neurosci 25: 1761-1768.
27. Bramham CR, Alme MN, Bittins M, Kuipers SD, Nair RR, et al. (2010) The Arc of synaptic memory. Exp Brain Res 200: 125-140.
28. Goel A, Lee HK, (2007) Persistence of experience-induced homeostatic synaptic plasticity through adulthood in superficial layers of mouse visual cortex. J Neurosci 27: 6692-6700.
29. Gao M, Sossa K, Song L, Errington L, Cummings L, et al. (2010) A specific requirement of Arc/Arg3.1 for visual experience-induced homeostatic synaptic plasticity in mouse primary visual cortex. J Neurosci 30: 7168-7178.
30. Knipper M, Zinn C, Maier H, Praetorius M, Rohbock K, et al. (2000) Thyroid hormone deficiency before the onset of hearing causes irreversible damage to peripheral and central auditory systems. J Neurophysiol 83: 3101-3112.
31. Schimmang T, Tan J, Müller M, Zimmermann U, Rohbock K, et al. (2003) Lack of Bdnf and TrkB signalling in the postnatal cochlea leads to a spatial reshaping of innervation along the tonotopic axis and hearing loss. Development 130: 4741-4750.
32. Engel J, Braig C, Rüttiger L, Kuhn S, Zimmermann U, et al. (2006) Two classes of outer hair cells along the tonotopic axis of the cochlea. Neuroscience 143: 837-849.
33. Kehrle HM, Granjeiro RC, Sampaio AL, Bezerra R, Almeida VF, et al. (2008) Comparison of auditory brainstem response results in normal-hearing patients with and without tinnitus. Arch Otolaryngol Head Neck Surg 134: 647-651.
34. Heidrych P, Zimmermann U, Kuhn S, Franz C, Engel J, et al. (2009) Otoferlin interacts with myosin VI: implications for maintenance of the basolateral synaptic structure of the inner hair cell. Hum Mol Genet 18: 2779-2790.
35. Panford-Walsh R, Singer W, Rüttiger L, Hadjab S, Tan J, et al. (2008) Midazolam reverses salicylate-induced changes in brain-derived neurotrophic factor and arg3.1 expression: implications for tinnitus perception and auditory plasticity. Mol Pharmacol 74: 595-604.
36. Doron NN, Ledoux JE, Semple MN, (2002) Redefining the tonotopic core of rat auditory cortex: physiological evidence for a posterior field. J Comp Neurol 453: 345-360.
37. Sheets L, Trapani JG, Mo W, Obholzer N, Nicolson T, (2011) Ribeye is required for presynaptic Ca(V)1.3a channel localization and afferent innervation of sensory hair cells. Development 138: 1309-1319.
38. Müller M, (1991) Frequency representation in the rat cochlea. Hearing Research 51: 247-254.
39. Buran BN, Strenzke N, Neef A, Gundelfinger ED, Moser T, et al. (2010) Onset coding is degraded in auditory nerve fibers from mutant mice lacking synaptic ribbons. J Neurosci 30: 7587-7597.
40. Johnson DH, Kiang NY, (1976) Analysis of discharges recorded simultaneously from pairs of auditory nerve fibers. Biophys J 16: 719-734.
41. Melcher JR, Kiang NY, (1996) Generators of the brainstem auditory evoked potential in cat. III: Identified cell populations. Hear Res 93: 52-71.
42. Yates GK, Winter IM, Robertson D, (1990) Basilar membrane nonlinearity determines auditory nerve rate-intensity functions and cochlear dynamic range. Hear Res 45: 203-219.
43. Pettigrew AM, Liberman MC, Kiang NY (1984) Click-evoked gross potentials and single-unit thresholds in acoustically traumatized cats. Ann Otol Rhinol Laryngol Suppl 112: 83-96.
44. Don M, Eggermont JJ, (1978) Analysis of the click-evoked brainstem potentials in man unsing high-pass noise masking. Journal of the Acoustical Society of America 63: 1084-1092.
45. Korb E, Finkbeiner S, (2012) Arc in synaptic plasticity: from gene to behavior. Trends Neurosci 34: 591-598.
46. Bauer CA, Brozoski TJ, Myers K, (2007) Primary afferent dendrite degeneration as a cause of tinnitus. J Neurosci Res 85: 1489-1498.
47. Weisz N, Hartmann T, Dohrmann K, Schlee W, Noreña A, (2006) High-frequency tinnitus without hearing loss does not mean absence of deafferentation. Hear Res 222: 108-114.
48. Geven LI, de Kleine E, Free RH, van Dijk P, (2011) Contralateral suppression of otoacoustic emissions in tinnitus patients. Otol Neurotol 32: 315-321.
49. Knipper M, Müller M, Zimmermann U (2012) Molecular Mechanism of Tinnitus. In: Fay RR, Popper AN, Eggermont JJ, editors. Springer Handbook of Audidory Research: Neural Correlates of Tinnitus. New York. Springer: 49-82.
50. Roberts LE, Moffat G, Baumann M, Ward LM, Bosnyak DJ, (2008) Residual inhibition functions overlap tinnitus spectra and the region of auditory threshold shift. J Assoc Res Otolaryngol 9: 417-435.
51. Noreña AJ, Eggermont JJ, (2003) Changes in spontaneous neural activity immediately after an acoustic trauma: implications for neural correlates of tinnitus. Hear Res 183: 137-153.
52. Engineer ND, Riley JR, Seale JD, Vrana WA, Shetake JA, et al. (2011) Reversing pathological neural activity using targeted plasticity. Nature 470: 101-104.
53. Glowatzki E, Fuchs PA, (2002) Transmitter release at the hair cell ribbon synapse. Nat Neurosci 5: 147-154.
54. Matthews G, Fuchs P, (2010) The diverse roles of ribbon synapses in sensory neurotransmission. Nat Rev Neurosci 11: 812-822.
55. Westerman LA, Smith RL, (1984) Rapid and short-term adaptation in auditory nerve responses. Hear Res 15: 249-260.
56. Kim DK, Park SN, Kim HM, Son HR, Kim NG, et al. (2011) Prevalence and significance of high-frequency hearing loss in subjectively normal-hearing patients with tinnitus. Ann Otol Rhinol Laryngol 120: 523-528.
57. Dominguez M, Becker S, Bruce I, Read H, (2006) A spiking neuron model of cortical correlates of sensorineural hearing loss: Spontaneous firing, synchrony, and tinnitus. Neural Comput 18: 2942-2958.
58. König O, Schaette R, Kempter R, Gross M, (2006) Course of hearing loss and occurrence of tinnitus. Hear Res 221: 59-64.
59. Parra LC, Pearlmutter BA, (2007) Illusory percepts from auditory adaptation. J Acoust Soc Am 121: 1632-1641.
60. Schaette R, Kempter R, (2012) Computational models of neurophysiological correlates of tinnitus. Front Syst Neurosci 6: 34.
61. Cai S, Ma WL, Young ED, (2009) Encoding intensity in ventral cochlear nucleus following acoustic trauma: implications for loudness recruitment. J Assoc Res Otolaryngol 10: 5-22.
62. 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.
63. Szczepaniak WS, Møller AR, (1996) Evidence of neuronal plasticity within the inferior colliculus after noise exposure: a study of evoked potentials in the rat. Electroencephalography and Clinical Neurophysiology 100: 158-164.
64. Zeng FG (2012) An active loudness model suggesting tinnitus as increased central noise and hyperacusis as increased nonlinear gain. Hear Res.
65. Penner MJ, (1986) Tinnitus as a source of internal noise. J Speech Hear Res 29: 400-406.
66. Vazdarjanova A, Ramirez-Amaya V, Insel N, Plummer TK, Rosi S, et al. (2006) Spatial exploration induces ARC, a plasticity-related immediate-early gene, only in calcium/calmodulin-dependent protein kinase II-positive principal excitatory and inhibitory neurons of the rat forebrain. J Comp Neurol 498: 317-329.
67. Kelly MP, Deadwyler SA, (2002) Acquisition of a novel behavior induces higher levels of Arc mRNA than does overtrained performance. Neuroscience 110: 617-626.
68. Daberkow DP, Riedy MD, Kesner RP, Keefe KA, (2007) Arc mRNA induction in striatal efferent neurons associated with response learning. Eur J Neurosci 26: 228-241.
69. Lonergan ME, Gafford GM, Jarome TJ, Helmstetter FJ, (2010) Time-dependent expression of Arc and zif268 after acquisition of fear conditioning. Neural Plast 2010: 139891.
70. Link W, Konietzko U, Kauselmann G, Krug M, Schwanke B, et al. (1995) Somatodendritic expression of an immediate early gene is regulated by synaptic activity. Proc Natl Acad Sci USA 92: 5734-5738.
71. Bramham CR, Worley PF, Moore MJ, Guzowski JF, (2008) The immediate early gene arc/arg3.1: regulation, mechanisms, and function. J Neurosci 28: 11760-11767.
72. Tzingounis AV, Nicoll RA, (2006) Arc/Arg3.1: linking gene expression to synaptic plasticity and memory. Neuron 52: 403-407.
73. Shepherd JD, Rumbaugh G, Wu J, Chowdhury S, Plath N, et al. (2006) Arc/Arg3.1 mediates homeostatic synaptic scaling of AMPA receptors. Neuron 52: 475-484.
74. Guzowski JF, McNaughton BL, Barnes CA, Worley PF, (1999) Environment-specific expression of the immediate-early gene Arc in hippocampal neuronal ensembles. Nat Neurosci 2: 1120-1124.
75. Moga DE, Shapiro ML, Morrison JH, (2006) Bidirectional redistribution of AMPA but not NMDA receptors after perforant path simulation in the adult rat hippocampus in vivo. Hippocampus 16: 990-1003.
76. Steward O, Wallace CS, Lyford GL, Worley PF, (1998) Synaptic activation causes the mRNA for the IEG Arc to localize selectively near activated postsynaptic sites on dendrites. Neuron 21: 741-751.
77. Okuno H, Akashi K, Ishii Y, Yagishita-Kyo N, Suzuki K, et al. (2012) Inverse synaptic tagging of inactive synapses via dynamic interaction of Arc/Arg3.1 with CaMKIIbeta. Cell 149: 886-898.
78. Beique JC, Na Y, Kuhl D, Worley PF, Huganir RL, (2010) Arc-dependent synapse-specific homeostatic plasticity. Proc Natl Acad Sci U S A 108: 816-821.
79. Pinaud R, Penner MR, Robertson HA, Currie RW, (2001) Upregulation of the immediate early gene arc in the brains of rats exposed to environmental enrichment: implications for molecular plasticity. Brain Res Mol Brain Res 91: 50-56.
80. Kozlovsky N, Matar MA, Kaplan Z, Kotler M, Zohar J, et al. (2008) The immediate early gene Arc is associated with behavioral resilience to stress exposure in an animal model of posttraumatic stress disorder. Eur Neuropsychopharmacol 18: 107-116.
81. Ons S, Rotllant D, Marin-Blasco IJ, Armario A, (2010) Immediate-early gene response to repeated immobilization: Fos protein and arc mRNA levels appear to be less sensitive than c-fos mRNA to adaptation. Eur J Neurosci 31: 2043-2052.
82. Yilmaz-Rastoder E, Miyamae T, Braun AE, Thiels E, (2011) LTP- and LTD-inducing stimulations cause opposite changes in arc/arg3.1 mRNA level in hippocampal area CA1 in vivo. Hippocampus 21: 1290-1301.
83. Peebles CL, Yoo J, Thwin MT, Palop JJ, Noebels JL, et al. (2010) Arc regulates spine morphology and maintains network stability in vivo. Proc Natl Acad Sci U S A 107: 18173-18178.
84. Porcher C, Hatchett C, Longbottom RE, McAinch K, Sihra TS, et al. (2011) Positive feedback regulation between gamma-aminobutyric acid type A (GABA(A)) receptor signaling and brain-derived neurotrophic factor (BDNF) release in developing neurons. J Biol Chem 286: 21667-21677.
85. Ochi K, Eggermont JJ, (1997) Effects of quinine on neural activity in cat primary auditory cortex. Hear Res 105: 105-118.
86. Eggermont JJ, Roberts LE, (2004) The neuroscience of tinnitus. Trends Neurosci 27: 676-682.
87. Borsello T, Clarke PG, Hirt L, Vercelli A, Repici M, et al. (2003) A peptide inhibitor of c-Jun N-terminal kinase protects against excitotoxicity and cerebral ischemia. Nat Med 9: 1180-1186.
88. Singer W, Zuccotti A, Jaumann M, Lee SC, Panford-Walsh R, et al. (2012) Noise-Induced Inner Hair Cell Ribbon Loss Disturbs Central Arc Mobilization: A Novel Molecular Paradigm for Understanding Tinnitus. Mol Neurobiol.
89. Schecklmann M, Vielsmeier V, Steffens T, Landgrebe M, Langguth B, et al. (2012) Relationship between Audiometric slope and tinnitus pitch in tinnitus patients: insights into the mechanisms of tinnitus generation. PLoS One 7: e34878.
90. Lin HW, Furman AC, Kujawa SG, Liberman MC, (2011) Primary neural degeneration in the Guinea pig cochlea after reversible noise-induced threshold shift. J Assoc Res Otolaryngol 12: 605-616.
91. Wang Y, Liberman MC, (2002) Restraint stress and protection from acoustic injury in mice. Hear Res 165: 96-102.
92. Loeb M, Smith RP, (1967) Relation of induced tinnitus to physical characteristics of the inducing stimuli. J Acoust Soc Am 42: 453-455.
93. Atherley GR, Hempstock TI, Noble WG, (1968) Study of tinnitus induced temporarily by noise. J Acoust Soc Am 44: 1503-1506.
94. McFeely WJ Jr, Bojrab DI, Davis KG, Hegyi DF, (1999) Otologic injuries caused by airbag deployment. Otolaryngol Head Neck Surg 121: 367-373.
95. Mrena R, Paakkonen R, Back L, Pirvola U, Ylikoski J (2004) Otologic consequences of blast exposure: a Finnish case study of a shopping mall bomb explosion. Acta Otolaryngol Suppl 124: 946-952.
96. Nottet JB, Moulin A, Brossard N, Suc B, Job A, (2006) Otoacoustic emissions and persistent tinnitus after acute acoustic trauma. Laryngoscope 116: 970-975.
97. Schreiber BE, Agrup C, Haskard DO, Luxon LM, (2010) Sudden sensorineural hearing loss. Lancet 375: 1203-1211.