Noise-induced inner hair cell ribbon loss disturbs central arc mobilization: A novel molecular paradigm for understanding tinnitus

Molecular Neurobiology

Volumn 47, Issue 1, 2013, Pages 261-279

  Singer, Wibke ^a   Zuccotti, Annalisa ^a   Jaumann, Mirko ^a   Lee, Sze Chim ^a   Panford Walsh, Rama ^a   Xiong, Hao ^a   Zimmermann, Ulrike ^a   Franz, Christoph ^a   Geisler, Hyun Soon ^a   Köpschall, Iris ^a   Rohbock, Karin ^a   Varakina, Ksenya ^a   Verpoorten, Sandrine ^a   Reinbothe, Thomas ^a   Schimmang, Thomas ^b   Rüttiger, Lukas ^a   Knipper, Marlies ^a  

^a UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^b Universidad de Valladolid y Consejo Superior de Investigaciones Científicas   (Spain)

Author keywords

Arc; Behavioral animal model; Hyperacusis; Ribbon synapse; Stress; Tinnitus

Indexed keywords

ACTIVITY REGULATED CYTOSKELETON ASSOCIATED PROTEIN; CORTICOSTEROID;

ANIMAL EXPERIMENT; ANIMAL MODEL; AUDITORY CORTEX; AUDITORY NERVOUS SYSTEM; AUDITORY THRESHOLD; BASOLATERAL AMYGDALA; CONTROLLED STUDY; DEAFFERENTATION; EVOKED BRAIN STEM RESPONSE; FEMALE; HAIR CELL; HEARING IMPAIRMENT; HIPPOCAMPAL CA1 REGION; LOUDNESS RECRUITMENT; NOISE; NONHUMAN; PROTEIN EXPRESSION; RAT; REVIEW; TINNITUS;

EID: 84872495311     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-012-8372-8     Document Type: Review

References (94)

1. Lockwood AH, Salvi RJ, Burkard RF (2002) Tinnitus. N Engl J Med 347(12):904-910
2. MØller AR (2003) Pathophysiology of tinnitus. Otolaryngol Clin North Am 36(2):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(8):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, Rauschecker JP (2011) Dysregulation of limbic and auditory networks in tinnitus. Neuron 69(1):33-43. doi: 10.1016/j.neuron.2010.12.002
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(10):1835-1845
8. Langguth B, Salvi R, Elgoyhen AB (2009) Emerging pharmacotherapy of tinnitus. Expert Opin Emerg Drugs 14(4):687-702
9. Kim DK, Park SN, Kim HM, Son HR, Kim NG, Park KH, Yeo SW (2011) Prevalence and significance of high-frequency hearing loss in subjectively normal-hearing patients with tinnitus. Ann Otol Rhinol Laryngol 120(8):523-528
10. Roberts LE, Eggermont JJ, Caspary DM, Shore SE, Melcher JR, Kaltenbach JA (2010) Ringing ears: the neuroscience of tinnitus. J Neurosci 30(45):14972-14979. doi: 10.1523/JNEUROSCI.4028-10.2010
11. 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(1-2):108-114
12. Geven LI, de Kleine E, Free RH, van Dijk P (2011) Contralateral suppression of otoacoustic emissions in tinnitus patients. Otol Neurotol 32(2):315-321. doi: 10.1097/MAO.0b013e3181fcf180
13. Bauer CA, Brozoski TJ, Myers K (2007) Primary afferent dendrite degeneration as a cause of tinnitus. J Neurosci Res 85(7):1489-1498
14. Knipper M, Müller M, Zimmermann U (2012) Molecular mechanism of tinnitus. In: Fay RR, Popper AN, Eggermont JJ (eds) Springer handbook of auditory research: neural correlates of tinnitus. Springer, New York
15. Knipper M, Zimmermann U, Müller M (2010) Molecular aspects of tinnitus. Hear Res 266(1-2):60-69. doi: 10.1016/j.heares.2009.07.013
16. Baguley DM (2003) Hyperacusis. J R Soc Med 96(12):582-585
17. Gu JW, Halpin CF, Nam EC, Levine RA, Melcher JR (2010) Tinnitus, diminished sound-level tolerance, and elevated auditory activity in humans with clinically normal hearing sensitivity. J Neurophysiol 104(6):3361-3370. doi: 10.1152/jn.00226.2010
18. Kujawa SG, Liberman MC (2009) Adding insult to injury: cochlear nerve degeneration after temporary noise-induced hearing loss. J Neurosci 29(45):14077-14085
19. Rauschecker JP, Leaver AM, Mühlau M (2010) Tuning out the noise: limbic-auditory interactions in tinnitus. Neuron 66(6):819-826. doi: 10.1016/j.neuron.2010.04.032
20. Salvi RJ, Wang J, Ding D (2000) Auditory plasticity and hyperactivity following cochlear damage. Hear Res 147(1-2):261-274
21. 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):2383-2390
22. Kaltenbach JA (2007) The dorsal cochlear nucleus as a contributor to tinnitus: mechanisms underlying the induction of hyperactivity. Prog Brain Res 166:89-106
23. Middleton JW, Kiritani T, Pedersen C, Turner JG, Shepherd GM, Tzounopoulos T (2011) Mice with behavioral evidence of tinnitus exhibit dorsal cochlear nucleus hyperactivity because of decreased GABAergic inhibition. Proc Natl Acad Sci USA 108(18):7601-7606. doi: 10.1073/pnas.1100223108
24. 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(36):14974-14979. doi: 10.1073/pnas.1107998108
25. 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(5):1660-1671. doi: 10.1523/JNEUROSCI.4608-11.2012
26. Schaette R, Kempter R (2012) Computational models of neurophysiological correlates of tinnitus. Front Syst Neurosci 6:34. doi: 10.3389/fnsys.2012.00034
27. 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(1):5-22. doi: 10.1007/s10162-008-0142-y
28. Szczepaniak WS, MØller AR (1996) Evidence of neuronal plasticity within the inferior colliculus after noise exposure: a study of evoked potentials in the rat. Electroencephalogr Clin Neurophysiol 100(2):158-164
29. Turner JG (2007) Behavioral measures of tinnitus in laboratory animals. Prog Brain Res 166:147-156
30. 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(1-2):39-50
31. Tan J, Rüttiger L, Panford-Walsh R, Singer W, Schulze H, Kilian SB, Hadjab S, Zimmermann U, Köpschall I, Rohbock K, Knipper M (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(2):715-726
32. 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(5):605-616. doi: 10.1007/s10162-011-0277-0
33. Melcher JR, Kiang NY (1996) Generators of the brainstem auditory evoked potential in cat. III: identified cell populations. Hear Res 93(1-2):52-71
34. Zuccotti A, Kuhn S, Johnson SL, Franz C, Singer W, Hecker D, Geisler HS, Köpschall I, Rohbock K, Gutsche K, Dlugaiczyk J, Schick B, Marcotti W, Rüttiger L, Schimmang T, Knipper M (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
35. Bramham CR, Alme MN, Bittins M, Kuipers SD, Nair RR, Pai B, Panja D, Schubert M, Soule J, Tiron A, Wibrand K (2010) The Arc of synaptic memory. Exp Brain Res 200(2):125-140. doi: 10.1007/s00221-009-1959-2
36. Gao M, Sossa K, Song L, Errington L, Cummings L, Hwang H, Kuhl D, Worley P, Lee HK (2010) A specific requirement of Arc/Arg3.1 for visual experience-induced homeostatic synaptic plasticity in mouse primary visual cortex. J Neurosci 30(21):7168-7178. doi: 10.1523/JNEUROSCI.1067-10.2010
37. Korb E, Finkbeiner S (2012) Arc in synaptic plasticity: from gene to behavior. Trends Neurosci 34(11):591-598. doi: 10.1016/j.tins.2011.08.007[doi]
38. Kozlovsky N, Matar MA, Kaplan Z, Kotler M, Zohar J, Cohen H (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(2):107-116. doi: 10.1016/j.euroneuro.2007.04.009
39. 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(11):2043-2052. doi: 10.1111/j.1460-9568.2010.07242.x
40. Turner BB (1986) Tissue differences in the up-regulation of glucocorticoid-binding proteins in the rat. Endocrinology 118(3):1211-1216
41. Chavez CM, McGaugh JL, Weinberger NM (2009) The basolateral amygdala modulates specific sensory memory representations in the cerebral cortex. Neurobiol Learn Mem 91(4):382-392. doi: 10.1016/j.nlm.2008.10.010
42. Knipper M, Zinn C, Maier H, Praetorius M, Rohbock K, Köpschall I, Zimmermann U (2000) Thyroid hormone deficiency before the onset of hearing causes irreversible damage to peripheral and central auditory systems. J Neurophysiol 83(5):3101-3112
43. Schimmang T, Tan J, Müller M, Zimmermann U, Rohbock K, Köpschall I, Limberger A, Minichiello L, Knipper M (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(19):4741-4750
44. Engel J, Braig C, Rüttiger L, Kuhn S, Zimmermann U, Blin N, Sausbier M, Kalbacher H, Münkner S, Rohbock K, Ruth P, Winter H, Knipper M (2006) Two classes of outer hair cells along the tonotopic axis of the cochlea. Neuroscience 143:837-849
45. Blanchard RJ, McKittrick CR, Blanchard DC (2001) Animal models of social stress: effects on behavior and brain neurochemical systems. Physiol Behav 73(3):261-271
46. Haller J, Fuchs E, Halasz J, Makara GB (1999) Defeat is a major stressor in males while social instability is stressful mainly in females: towards the development of a social stress model in female rats. Brain Res Bull 50(1):33-39
47. Heidrych P, Zimmermann U, Kuhn S, Franz C, Engel J, Duncker SV, Hirt B, Pusch CM, Ruth P, Pfister M, Marcotti W, Blin N, Knipper M (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
48. Panford-Walsh R, Singer W, Rüttiger L, Hadjab S, Tan J, Geisler HS, Zimmermann U, Köpschall I, Rohbock K, Vieljans A, Oestreicher E, Knipper M (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(3):595-604. doi: 10.1124/mol.108. 046375
49. Ramirez-Amaya V, Vazdarjanova A, Mikhael D, Rosi S, Worley PF, Barnes CA (2005) Spatial exploration-induced Arc mRNA and protein expression: evidence for selective, network-specific reactivation. J Neurosci 25(7):1761-1768
50. Müller M (1991) Frequency representation in the rat cochlea. Hear Res 51(2):247-254
51. 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(4):345-360
52. Sarro EC, Kotak VC, Sanes DH, Aoki C (2008) Hearing loss alters the subcellular distribution of presynaptic GAD and postsynaptic GABAA receptors in the auditory cortex. Cereb Cortex 18(12):2855-2867. doi: 10.1093/cercor/bhn044
53. 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(12):1290-1301. doi: 10.1002/hipo.20838
54. Wang H, Brozoski TJ, Turner JG, Ling L, Parrish JL, Hughes LF, Caspary DM (2009) Plasticity at glycinergic synapses in dorsal cochlear nucleus of rats with behavioral evidence of tinnitus. Neuroscience 164(2):747-759. doi: 10.1016/j.neuroscience.2009.08.026
55. Vogler DP, Robertson D, Mulders WH (2011) Hyperactivity in the ventral cochlear nucleus after cochlear trauma. J Neurosci 31(18):6639-6645. doi: 10.1523/JNEUROSCI.6538-10.2011
56. Glowatzki E, Fuchs PA (2002) Transmitter release at the hair cell ribbon synapse. Nat Neurosci 5(2):147-154
57. Buran BN, Strenzke N, Neef A, Gundelfinger ED, Moser T, Liberman MC (2010) Onset coding is degraded in auditory nerve fibers from mutant mice lacking synaptic ribbons. J Neurosci 30(22):7587-7597. doi: 10.1523/JNEUROSCI. 0389-10.2010
58. Johnson DH, Kiang NY (1976) Analysis of discharges recorded simultaneously from pairs of auditory nerve fibers. Biophys J 16(7):719-734
59. Schaette R, Kempter R (2009) Predicting tinnitus pitch from patients' audiograms with a computational model for the development of neuronal hyperactivity. J Neurophysiol 101(6):3042-3052
60. 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(1-2):153-171
61. Zeng FG (2012) An active loudness model suggesting tinnitus as increased central noise and hyperacusis as increased nonlinear gain. Hear Res. doi: 10.1016/j.heares.2012.05.009
62. Schaette R, McAlpine D (2011) Tinnitus with a normal audiogram: physiological evidence for hidden hearing loss and computational model. J Neurosci 31(38):13452-13457. doi: 10.1523/JNEUROSCI.2156-11.2011
63. Malmierca M, Merchan M (2004) The auditory system. In: Paxinos G (ed) The rat nervous system. Academic, San Diego, pp 997-1082
64. Shepherd JD, Rumbaugh G, Wu J, Chowdhury S, Plath N, Kuhl D, Huganir RL, Worley PF (2006) Arc/Arg3.1 mediates homeostatic synaptic scaling of AMPA receptors. Neuron 52(3):475-484
65. 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(12):1120-1124
66. 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(1-2):50-56
67. 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(2):816-821. doi: 10.1073/pnas.1017914108
68. Kotak VC, Fujisawa S, Lee FA, Karthikeyan O, Aoki C, Sanes DH (2005) Hearing loss raises excitability in the auditory cortex. J Neurosci 25(15):3908-3918
69. Peebles CL, Yoo J, Thwin MT, Palop JJ, Noebels JL, Finkbeiner S (2010) Arc regulates spine morphology and maintains network stability in vivo. Proc Natl Acad Sci U S A 107(42):18173-18178. doi: 10.1073/pnas.1006546107
70. Eggermont JJ, Roberts LE (2004) The neuroscience of tinnitus. Trends Neurosci 27(11):676-682
71. Noreña AJ, Tomita M, Eggermont JJ (2003) Neural changes in cat auditory cortex after a transient pure-tone trauma. J Neurophysiol 90(4):2387-2401
72. Schecklmann M, Vielsmeier V, Steffens T, Landgrebe M, Langguth B, Kleinjung T (2012) Relationship between audiometric slope and tinnitus pitch in tinnitus patients: insights into the mechanisms of tinnitus generation. PLoS One 7(4):e34878. doi: 10.1371/journal.pone.0034878
73. Mangiamele LA, Thomson CJ, Lebonville CL, Burmeister SS (2010) Characterization of the plasticity-related gene, Arc, in the frog brain. Dev Neurobiol 70(12):813-825. doi: 10.1002/dneu.20817
74. Hawley ML, Melcher JR, Fullerton BC (2005) Effects of sound bandwidth on fMRI activation in human auditory brainstem nuclei. Hear Res 204(1-2):101-110. doi: 10.1016/j.heares.2005.01.005
75. Rajan R (1998) Receptor organ damage causes loss of cortical surround inhibition without topographic map plasticity. Nat Neurosci 1(2):138-143. doi: 10.1038/388
76. Diesch E, Struve M, Rupp A, Ritter S, Hulse M, Flor H (2004) Enhancement of steady-state auditory evoked magnetic fields in tinnitus. Eur J Neurosci 19(4):1093-1104
77. Langers DR, de Kleine E, van Dijk P (2012) Tinnitus does not require macroscopic tonotopic map reorganization. Front Syst Neurosci 6:2. doi: 10.3389/fnsys.2012.00002
78. Campeau S, Watson SJ (1997) Neuroendocrine and behavioral responses and brain pattern of c-fos induction associated with audiogenic stress. J Neuroendocrinol 9(8):577-588
79. Karst H, Berger S, Erdmann G, Schutz G, Joëls M (2010) Metaplasticity of amygdalar responses to the stress hormone corticosterone. Proc Natl Acad Sci U S A 107(32):14449-14454. doi: 10.1073/pnas.0914381107
80. Tasker JG, Di S, Malcher-Lopes R (2006) Minireview: rapid glucocorticoid signaling via membrane-associated receptors. Endocrinology 147(12):5549-5556. doi: 10.1210/en.2006-0981
81. Groeneweg FL, Karst H, de Kloet ER, Joëls M (2011) Rapid non-genomic effects of corticosteroids and their role in the central stress response. J Endocrinol 209(2):153-167. doi: 10.1530/JOE-10-0472
82. Richter-Levin G, Maroun M (2010) Stress and amygdala suppression of metaplasticity in the medial prefrontal cortex. Cereb Cortex 20(10):2433-2441. doi: 10.1093/cercor/bhp311
83. Kozlovsky N, Matar MA, Kaplan Z, Zohar J, Cohen H (2009) A distinct pattern of intracellular glucocorticoid-related responses is associated with extreme behavioral response to stress in an animal model of post-traumatic stress disorder. Eur Neuropsychopharmacol 19(11):759-771. doi: 10.1016/j.euroneuro.2009.04.009
84. Abraham WC, Bear MF (1996) Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci 19(4):126-130
85. Wang Y, Liberman MC (2002) Restraint stress and protection from acoustic injury in mice. Hear Res 165(1-2):96-102
86. Terakado M, Kumagami H, Takahashi H (2011) Distribution of glucocorticoid receptors and 11 beta-hydroxysteroid dehydrogenase isoforms in the rat inner ear. Hear Res 280(1-2):148-156. doi: 10.1016/j.heares.2011.05.006
87. Yao X, Rarey KE (1996) Localization of the mineralocorticoid receptor in rat cochlear tissue. Acta Otolaryngol 116(3):493-496
88. Oitzl MS, Champagne DL, van der Veen R, de Kloet ER (2010) Brain development under stress: hypotheses of glucocorticoid actions revisited. Neurosci Biobehav Rev 34(6):853-866. doi: 10.1016/j.neubiorev.2009.07.006
89. Knapman A, Kaltwasser SF, Martins-de-Souza D, Holsboer F, Landgraf R, Turck CW, Czisch M, Touma C (2012) Increased stress reactivity is associated with reduced hippocampal activity and neuronal integrity along with changes in energy metabolism. Eur J Neurosci 35(3):412-422. doi: 10.1111/j.1460-9568.2011. 07968.x
90. Hebert S, Lupien SJ (2007) The sound of stress: blunted cortisol reactivity to psychosocial stress in tinnitus sufferers. Neurosci Lett 411(2):138-142
91. Eriksson TM, Delagrange P, Spedding M, Popoli M, Mathe AA, Ogren SO, Svenningsson P (2012) Emotional memory impairments in a genetic rat model of depression: involvement of 5-HT/MEK/Arc signaling in restoration. Mol Psychiatry 17(2):173-184. doi: 10.1038/mp.2010.131
92. Palop JJ, Chin J, Bien-Ly N, Massaro C, Yeung BZ, Yu GQ, Mucke L (2005) Vulnerability of dentate granule cells to disruption of arc expression in human amyloid precursor protein transgenic mice. J Neurosci 25(42):9686-9693
93. Wegenast-Braun BM, Fulgencio Maisch A, Eicke D, Radde R, Herzig MC, Staufenbiel M, Jucker M, Calhoun ME (2009) Independent effects of intra- and extracellular Abeta on learning-related gene expression. Am J Pathol 175(1):271-282. doi: 10.2353/ajpath.2009.090044
94. Goel A, Lee HK (2007) Persistence of experience-induced homeostatic synaptic plasticity through adulthood in superficial layers of mouse visual cortex. J Neurosci 27(25):6692-6700. doi: 10.1523/JNEUROSCI.5038-06.2007