Tinnitus induction in animals and its impact on auditory system structure
,
Abstract
Background and Aim: Tinnitus is a perception of sound in ears or head in the absence of any external stimuli. Despite its high prevalence in various age groups, tinnitus has still no effective treatment because its physiological and pathological mechanisms have remained unknown. Since the study of cellular-molecular mechanisms of tinnitus production and stability in human is not feasible, animal models have been used to shed some light on tinnitus induction and propagation mechanisms. This study reviewed some of these research studies. The present review article is based on articles published during 1967-2018 in which keywords such as “salicylate,” “noise,” “tinnitus in the animal model,” and “tinnitus mechanism” were used. These articles were searched in databases such as Science Direct, Google Scholar, PubMed, and Scopus.
Recent Findings: Despite differences in the mechanisms of tinnitus induction, the structural changes initiated from the cochlea and continued to cortex reflect the extent of the affected regions in the creation, development, and preservation of tinnitus.
Conclusion: Animal models (exposed to noise or ototoxic drugs such as salicylate) are ideal tools for studying tinnitus and understanding the details of its propagation and unknown mechanisms.
1. Berger JI, Coomber B, Shackleton TM, Palmer AR, Wallace MN. A novel behavioural approach to detecting tinnitus in the guinea pig. J Neurosci Methods. 2013;213(2):188-95. doi: 10.1016/j.jneumeth.2012.12.023
2. Turner J, Larsen D, Hughes L, Moechars D, Shore S. Time course of tinnitus development following noise exposure in mice. J Neurosci Res. 2012;90(7):1480-8. doi: 10.1002/jnr.22827
3. Kiefer L, Schauen A, Abendroth S, Gaese BH, Nowotny M. Variation in acoustic overstimulation changes tinnitus characteristics. Neuroscience. 2015;310:176-87. doi: 10.1016/j.neuroscience.2015.09.023
4. Chrbolka P, Palúch Z, Hill M, Alušík Š. Circulating steroids negatively correlate with tinnitus. Steroids. 2017;123:37-42. doi: 10.1016/j.steroids.2017.04.004
5. Berger JI, Owen W, Wilson CA, Hockley A, Coomber B, Palmer AR, et al. Gap-induced reductions of evoked potentials in the auditory cortex: A possible objective marker for the presence of tinnitus in animals. Brain Res. 2018;1679:101-8. doi: 10.1016/j.brainres.2017.11.026
6. Coomber B, Berger JI, Kowalkowski VL, Shackleton TM, Palmer AR, Wallace MN. Neural changes accompanying tinnitus following unilateral acoustic trauma in the guinea pig. Eur J Neurosci. 2014;40(2):2427-41. doi: 10.1111/ejn.12580
7. Zhang J, Luo H, Pace E, Li L, Liu B. Psychophysical and neural correlates of noised-induced tinnitus in animals: Intra- and inter-auditory and non-auditory brain structure studies. Hear Res. 2016;334:7-19. doi: 10.1016/j.heares.2015.08.006
8. Lauer AM, Larkin G, Jones A, May BJ. Behavioral animal model of the emotional response to tinnitus and hearing loss. J Assoc Res Otolaryngol. 2018;19(1):67-81. doi: 10.1007/s10162-017-0642-8
9. Leggett K, Mendis V, Mulders W. Divergent responses in the gap prepulse inhibition of the acoustic startle reflex in two different guinea pig colonies. Int Tinnitus J. 2018;22(1):1-9. doi: 10.5935/0946-5448.20180001
10. Paul AK, Lobarinas E, Simmons R, Wack D, Luisi JC, Spernyak J, et al. Metabolic imaging of rat brain during phar-macologically-induced tinnitus Neuroimage. 2009;44(2):312-8. doi: 10.1016/j.neuroimage.2008.09.024
11. Wan I, Pokora O, Chiu T, Lansky P, Poon PW. Altered intensity coding in the salicylate-overdose animal model of tinnitus. Biosystems. 2015;136:113-9. doi: 10.1016/j.biosystems.2015.06.010
12. Evans EF, Wilson JP, Borerwe TA. Animal models of tinnitus. Ciba Found Symp. 1981;85:108-38.
13. Stolzberg D, Salvi RJ, Allman BL. Salicylate toxicity model of tinnitus. Front Syst Neurosci. 2012;6:28. doi: 10.3389/fnsys.2012.00028
14. Ralli M, Lobarinas E, Fetoni AR, Stolzberg D, Paludetti G, Salvi R. Comparison of salicylate- and quinine-induced tinnitus in rats: development, time course, and evaluation of audiologic correlates. Otol Neurotol. 2010;31(5):823-31. doi: 10.1097/MAO.0b013e3181de4662
15. Su YY, Luo B, Wang HT, Chen L. Differential effects of sodium salicylate on current-evoked firing of pyramidal neurons and fast-spiking interneurons in slices of rat auditory cortex. Hear Res. 2009;253(1-2):60-6. doi: 10.1016/j.heares.2009.03.007
16. Yi B, Hu S, Zuo C, Jiao F, Lv J, Chen D, et al. Effects of long-term salicylate administration on synaptic ultrastructure and metabolic activity in the rat CNS. Sci Rep. 2016;6:24428. doi: 10.1038/srep24428
17. Radziwon KE, Stolzberg DJ, Urban ME, Bowler RA, Salvi RJ. Salicylate-induced hearing loss and gap detection deficits in rats. Front Neurol. 2015;6:31. doi: 10.3389/fneur.2015.00031
18. Kizawa K, Kitahara T, Horii A, Maekawa C, Kuramasu T, Kawashima T, et al. Behavioral assessment and identification of a molecular marker in a salicylate-induced tinnitus in rats. Neuroscience. 2010;165(4):1323-32. doi: 10.1016/j.neuroscience.2009.11.048
19. Deng A, Lu J, Sun W. Temporal processing in inferior colliculus and auditory cortex affected by high doses of salicylate. Brain Res. 2010;1344:96-103. doi: 10.1016/j.brainres.2010.04.077
20. Lobarinas E, Yang G, Sun W, Ding D, Mirza N, Dalby-Brown W, et al. Salicylate- and quinine-induced tinnitus and effects of memantine. Acta Otolaryngol Suppl. 2006;(556):13-9. doi: 10.1080/03655230600895408
21. Sun W, Deng A, Jayaram A, Gibson B. Noise exposure enhances auditory cortex responses related to hyperacusis behavior. Brain Res. 2012;1485:108-16. doi: 10.1016/j.brainres.2012.02.008
22. Yang G, Lobarinas E, Zhang L, Turner J, Stolzberg D, Salvi R, et al. Salicylate induced tinnitus: behavioral measures and neural activity in auditory cortex of awake rats. Hear Res. 2007;226(1-2):244-53. doi: 10.1016/j.heares.2006.06.013
23. Stolzberg D, Chen GD, Allman BL, Salvi RJ. Salicylate-induced peripheral auditory changes and tonotopic reorganization of auditory cortex. Neuroscience. 2011;180:157-64. doi: 10.1016/j.neuroscience.2011.02.005
24. Zheng Y, Hamilton E, Begum S, Smith PF, Darlington CL. The effects of acoustic trauma that can cause tinnitus on spatial performance in rats. Neuroscience. 2011;186:48-56. doi: 10.1016/j.neuroscience.2011.04.052
25. Eggermont JJ. Can animal models contribute to understanding tinnitus heterogeneity in humans? Front Aging Neurosci. 2016;8:265. doi: 10.3389/fnagi.2016.00265
26. Jin Y, Luo B, Su YY, Wang XX, Chen L, Wang M, et al. Sodium salicylate suppresses GABAergic inhibitory activity in neurons of rodent dorsal raphe nucleus. PLoS One. 2015;10(5):e0126956. doi: 10.1371/journal.pone.0126956
27. Yu H, Vikhe Patil K, Han C, Fabella B, Canlon B, Someya S, et al. GLAST deficiency in mice exacerbates gap detection deficits in a model of salicylate-induced tinnitus. Front Behav Neurosci. 2016;10:158. doi: 10.3389/fnbeh.2016.00158
28. Lu YG, Tang ZQ, Ye ZY, Wang HT, Huang YN, Zhou KQ, et al. Salicylate, an aspirin metabolite, specifically inhibits the current mediated by glycine receptors containing alpha1-subunits. Br J Pharmacol. 2009;157(8):1514-22. doi: 10.1111/j.1476-5381.2009.00321.x
29. Wang XX, Jin Y, Luo B, Sun JW, Zhang J, Wang M, et al. Sodium salicylate potentiates the GABAB-GIRK pathway to suppress rebound depolarization in neurons of the rat's medial geniculate body. Hear Res. 2016;332:104-12. doi: 10.1016/j.heares.2015.11.013
30. Ruel J, Chabbert C, Nouvian R, Bendris R, Eybalin M, Leger CL, et al. Salicylate enables cochlear arachidonic-acid-sensitive NMDA receptor responses. J Neurosci. 2008;28(29):7313-23. doi: 10.1523/JNEUROSCI.5335-07.2008
31. Jin ZH, Kikuchi T, Tanaka K, Kobayashi T. Expression of glutamate transporter GLAST in the developing mouse cochlea. Tohoku J Exp Med. 2003;200(3):137-44.
32. Bartels H, Staal MJ, Albers FW. Tinnitus and neural plasticity of the brain. Otol Neurotol. 2007;28(2):178-84. doi: 10.1097/MAO.0b013e31802b3248
33. Engineer ND, Riley JR, Seale JD, Vrana WA, Shetake JA, Sudanagunta SP, et al. Reversing pathological neural activity using targeted plasticity. Nature. 2011;470(7332):101-4. doi: 10.1038/nature09656
34. Mao JC, Pace E, Pierozynski P, Kou Z, Shen Y, VandeVord P, et al. Blast-induced tinnitus and hearing loss in rats: behavioral and imaging assays. J Neurotrauma. 2012;29(2):430-44. doi: 10.1089/neu.2011.1934
35. Marques APC, Miranda Filho AL, Monteiro GTR. Prevalence of hearing loss in adolescents and young adults as a result of social noise exposure: meta-analysis. Revista CEFAC. 2015;17(6):2056-64. doi: 10.1590/1982-021620151761115
36. Rabinowitz PM, Slade MD, Galusha D, Dixon-Ernst C, Cullen MR. Trends in the prevalence of hearing loss among young adults entering an industrial workforce 1985 to 2004. Ear Hear. 2006;27(4):369-75. doi: 10.1097/01.aud.0000224125.12338.9a
37. Rauschecker JP, Leaver AM, Mühlau M. Tuning out the noise: limbic-auditory interactions in tinnitus. Neuron. 2010;66(6):819-26. doi: 10.1016/j.neuron.2010.04.032
38. Rüttiger L, Singer W, Panford-Walsh R, Matsumoto M, Lee SC, Zuccotti A, et al. The reduced cochlear output and the failure to adapt the central auditory response causes tinnitus in noise exposed rats. PLoS One. 2013;8(3):e57247. doi: 10.1371/journal.pone.0057247
39. Zheng Y, McPherson K, Reid P, Smith PF. The anti-inflammatory selective melanocortin receptor subtype 4 agonist, RO27-3225, fails to prevent acoustic trauma-induced tinnitus in rats. Eur J Pharmacol. 2015;761:206-10. doi: 10.1016/j.ejphar.2015.05.007
40. Ropp TJ, Tiedemann KL, Young ED, May BJ. Effects of unilateral acoustic trauma on tinnitus-related spontaneous activity in the inferior colliculus. J Assoc Res Otolaryngol. 2014;15(6):1007-22. doi: 10.1007/s10162-014-0488-2
41. Middleton JW, Kiritani T, Pedersen C, Turner JG, Shepherd GM, Tzounopoulos T. Mice with behavioral evidence of tinnitus exhibit dorsal cochlear nucleus hyperactivity because of decreased GABAergic inhibition. Proc Natl Acad Sci U S A. 2011;108(18):7601-6. doi: 10.1073/pnas.1100223108
42. Dong S, Mulders WH, Rodger J, Woo S, Robertson D. Acoustic trauma evokes hyperactivity and changes in gene expression in guinea-pig auditory brainstem. Eur J Neurosci. 2010;31(9):1616-28. doi: 10.1111/j.1460-9568.2010.07183.x
43. Mulders WH, Ding D, Salvi R, Robertson D. Relationship between auditory thresholds, central spontaneous activity, and hair cell loss after acoustic trauma. J Comp Neurol. 2011;519(13):2637-47. doi: 10.1002/cne.22644
44. Hickox AE, Liberman MC. Is noise-induced cochlear neuropathy key to the generation of hyperacusis or tinnitus? J Neurophysiol. 2014;111(3):552-64. doi: 10.1152/jn.00184.2013
45. Shi L, Guo X, Shen P, Liu L, Tao S, Li X, et al. Noise-induced damage to ribbon synapses without permanent threshold shifts in neonatal mice. Neuroscience. 2015;304:368-77. doi: 10.1016/j.neuroscience.2015.07.066
46. Dehmel S, Pradhan S, Koehler S, Bledsoe S, Shore S. Noise overexposure alters long-term somatosensory-auditory proce-ssing in the dorsal cochlear nucleus--possible basis for tinnitus-related hyperactivity? J Neurosci. 2012;32(5):1660-71. doi: 10.1523/JNEUROSCI.4608-11.2012
47. Shore SE, Koehler S, Oldakowski M, Hughes LF, Syed S. Dorsal cochlear nucleus responses to somatosensory stimulation are enhanced after noise-induced hearing loss. Eur J Neurosci. 2008;27(1):155-68. doi: 10.1111/j.1460-9568.2007.05983.x
48. Zeng C, Nannapaneni N, Zhou J, Hughes LF, Shore S. Cochlear damage changes the distribution of vesicular glutamate transporters associated with auditory and nonauditory inputs to the cochlear nucleus. J Neurosci. 2009;29(13):4210-7. doi: 10.1523/JNEUROSCI.0208-09.2009
49. Ma WL, Young ED. Dorsal cochlear nucleus response properties following acoustic trauma: response maps and spontaneous activity. Hear Res. 2006;216-217:176-88. doi: 10.1016/j.heares.2006.03.011
50. Brozoski TJ, Wisner KW, Sybert LT, Bauer CA. Bilateral dorsal cochlear nucleus lesions prevent acoustic-trauma induced tinnitus in an animal model. J Assoc Res Otolaryngol. 2012;13(1):55-66. doi: 10.1007/s10162-011-0290-3
51. Manzoor NF, Licari FG, Klapchar M, Elkin RL, Gao Y, Chen G, et al. Noise-induced hyperactivity in the inferior colliculus: its relationship with hyperactivity in the dorsal cochlear nucleus. J Neurophysiol. 2012;108(4):976-88. doi: 10.1152/jn.00833.2011
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2. Turner J, Larsen D, Hughes L, Moechars D, Shore S. Time course of tinnitus development following noise exposure in mice. J Neurosci Res. 2012;90(7):1480-8. doi: 10.1002/jnr.22827
3. Kiefer L, Schauen A, Abendroth S, Gaese BH, Nowotny M. Variation in acoustic overstimulation changes tinnitus characteristics. Neuroscience. 2015;310:176-87. doi: 10.1016/j.neuroscience.2015.09.023
4. Chrbolka P, Palúch Z, Hill M, Alušík Š. Circulating steroids negatively correlate with tinnitus. Steroids. 2017;123:37-42. doi: 10.1016/j.steroids.2017.04.004
5. Berger JI, Owen W, Wilson CA, Hockley A, Coomber B, Palmer AR, et al. Gap-induced reductions of evoked potentials in the auditory cortex: A possible objective marker for the presence of tinnitus in animals. Brain Res. 2018;1679:101-8. doi: 10.1016/j.brainres.2017.11.026
6. Coomber B, Berger JI, Kowalkowski VL, Shackleton TM, Palmer AR, Wallace MN. Neural changes accompanying tinnitus following unilateral acoustic trauma in the guinea pig. Eur J Neurosci. 2014;40(2):2427-41. doi: 10.1111/ejn.12580
7. Zhang J, Luo H, Pace E, Li L, Liu B. Psychophysical and neural correlates of noised-induced tinnitus in animals: Intra- and inter-auditory and non-auditory brain structure studies. Hear Res. 2016;334:7-19. doi: 10.1016/j.heares.2015.08.006
8. Lauer AM, Larkin G, Jones A, May BJ. Behavioral animal model of the emotional response to tinnitus and hearing loss. J Assoc Res Otolaryngol. 2018;19(1):67-81. doi: 10.1007/s10162-017-0642-8
9. Leggett K, Mendis V, Mulders W. Divergent responses in the gap prepulse inhibition of the acoustic startle reflex in two different guinea pig colonies. Int Tinnitus J. 2018;22(1):1-9. doi: 10.5935/0946-5448.20180001
10. Paul AK, Lobarinas E, Simmons R, Wack D, Luisi JC, Spernyak J, et al. Metabolic imaging of rat brain during phar-macologically-induced tinnitus Neuroimage. 2009;44(2):312-8. doi: 10.1016/j.neuroimage.2008.09.024
11. Wan I, Pokora O, Chiu T, Lansky P, Poon PW. Altered intensity coding in the salicylate-overdose animal model of tinnitus. Biosystems. 2015;136:113-9. doi: 10.1016/j.biosystems.2015.06.010
12. Evans EF, Wilson JP, Borerwe TA. Animal models of tinnitus. Ciba Found Symp. 1981;85:108-38.
13. Stolzberg D, Salvi RJ, Allman BL. Salicylate toxicity model of tinnitus. Front Syst Neurosci. 2012;6:28. doi: 10.3389/fnsys.2012.00028
14. Ralli M, Lobarinas E, Fetoni AR, Stolzberg D, Paludetti G, Salvi R. Comparison of salicylate- and quinine-induced tinnitus in rats: development, time course, and evaluation of audiologic correlates. Otol Neurotol. 2010;31(5):823-31. doi: 10.1097/MAO.0b013e3181de4662
15. Su YY, Luo B, Wang HT, Chen L. Differential effects of sodium salicylate on current-evoked firing of pyramidal neurons and fast-spiking interneurons in slices of rat auditory cortex. Hear Res. 2009;253(1-2):60-6. doi: 10.1016/j.heares.2009.03.007
16. Yi B, Hu S, Zuo C, Jiao F, Lv J, Chen D, et al. Effects of long-term salicylate administration on synaptic ultrastructure and metabolic activity in the rat CNS. Sci Rep. 2016;6:24428. doi: 10.1038/srep24428
17. Radziwon KE, Stolzberg DJ, Urban ME, Bowler RA, Salvi RJ. Salicylate-induced hearing loss and gap detection deficits in rats. Front Neurol. 2015;6:31. doi: 10.3389/fneur.2015.00031
18. Kizawa K, Kitahara T, Horii A, Maekawa C, Kuramasu T, Kawashima T, et al. Behavioral assessment and identification of a molecular marker in a salicylate-induced tinnitus in rats. Neuroscience. 2010;165(4):1323-32. doi: 10.1016/j.neuroscience.2009.11.048
19. Deng A, Lu J, Sun W. Temporal processing in inferior colliculus and auditory cortex affected by high doses of salicylate. Brain Res. 2010;1344:96-103. doi: 10.1016/j.brainres.2010.04.077
20. Lobarinas E, Yang G, Sun W, Ding D, Mirza N, Dalby-Brown W, et al. Salicylate- and quinine-induced tinnitus and effects of memantine. Acta Otolaryngol Suppl. 2006;(556):13-9. doi: 10.1080/03655230600895408
21. Sun W, Deng A, Jayaram A, Gibson B. Noise exposure enhances auditory cortex responses related to hyperacusis behavior. Brain Res. 2012;1485:108-16. doi: 10.1016/j.brainres.2012.02.008
22. Yang G, Lobarinas E, Zhang L, Turner J, Stolzberg D, Salvi R, et al. Salicylate induced tinnitus: behavioral measures and neural activity in auditory cortex of awake rats. Hear Res. 2007;226(1-2):244-53. doi: 10.1016/j.heares.2006.06.013
23. Stolzberg D, Chen GD, Allman BL, Salvi RJ. Salicylate-induced peripheral auditory changes and tonotopic reorganization of auditory cortex. Neuroscience. 2011;180:157-64. doi: 10.1016/j.neuroscience.2011.02.005
24. Zheng Y, Hamilton E, Begum S, Smith PF, Darlington CL. The effects of acoustic trauma that can cause tinnitus on spatial performance in rats. Neuroscience. 2011;186:48-56. doi: 10.1016/j.neuroscience.2011.04.052
25. Eggermont JJ. Can animal models contribute to understanding tinnitus heterogeneity in humans? Front Aging Neurosci. 2016;8:265. doi: 10.3389/fnagi.2016.00265
26. Jin Y, Luo B, Su YY, Wang XX, Chen L, Wang M, et al. Sodium salicylate suppresses GABAergic inhibitory activity in neurons of rodent dorsal raphe nucleus. PLoS One. 2015;10(5):e0126956. doi: 10.1371/journal.pone.0126956
27. Yu H, Vikhe Patil K, Han C, Fabella B, Canlon B, Someya S, et al. GLAST deficiency in mice exacerbates gap detection deficits in a model of salicylate-induced tinnitus. Front Behav Neurosci. 2016;10:158. doi: 10.3389/fnbeh.2016.00158
28. Lu YG, Tang ZQ, Ye ZY, Wang HT, Huang YN, Zhou KQ, et al. Salicylate, an aspirin metabolite, specifically inhibits the current mediated by glycine receptors containing alpha1-subunits. Br J Pharmacol. 2009;157(8):1514-22. doi: 10.1111/j.1476-5381.2009.00321.x
29. Wang XX, Jin Y, Luo B, Sun JW, Zhang J, Wang M, et al. Sodium salicylate potentiates the GABAB-GIRK pathway to suppress rebound depolarization in neurons of the rat's medial geniculate body. Hear Res. 2016;332:104-12. doi: 10.1016/j.heares.2015.11.013
30. Ruel J, Chabbert C, Nouvian R, Bendris R, Eybalin M, Leger CL, et al. Salicylate enables cochlear arachidonic-acid-sensitive NMDA receptor responses. J Neurosci. 2008;28(29):7313-23. doi: 10.1523/JNEUROSCI.5335-07.2008
31. Jin ZH, Kikuchi T, Tanaka K, Kobayashi T. Expression of glutamate transporter GLAST in the developing mouse cochlea. Tohoku J Exp Med. 2003;200(3):137-44.
32. Bartels H, Staal MJ, Albers FW. Tinnitus and neural plasticity of the brain. Otol Neurotol. 2007;28(2):178-84. doi: 10.1097/MAO.0b013e31802b3248
33. Engineer ND, Riley JR, Seale JD, Vrana WA, Shetake JA, Sudanagunta SP, et al. Reversing pathological neural activity using targeted plasticity. Nature. 2011;470(7332):101-4. doi: 10.1038/nature09656
34. Mao JC, Pace E, Pierozynski P, Kou Z, Shen Y, VandeVord P, et al. Blast-induced tinnitus and hearing loss in rats: behavioral and imaging assays. J Neurotrauma. 2012;29(2):430-44. doi: 10.1089/neu.2011.1934
35. Marques APC, Miranda Filho AL, Monteiro GTR. Prevalence of hearing loss in adolescents and young adults as a result of social noise exposure: meta-analysis. Revista CEFAC. 2015;17(6):2056-64. doi: 10.1590/1982-021620151761115
36. Rabinowitz PM, Slade MD, Galusha D, Dixon-Ernst C, Cullen MR. Trends in the prevalence of hearing loss among young adults entering an industrial workforce 1985 to 2004. Ear Hear. 2006;27(4):369-75. doi: 10.1097/01.aud.0000224125.12338.9a
37. Rauschecker JP, Leaver AM, Mühlau M. Tuning out the noise: limbic-auditory interactions in tinnitus. Neuron. 2010;66(6):819-26. doi: 10.1016/j.neuron.2010.04.032
38. Rüttiger L, Singer W, Panford-Walsh R, Matsumoto M, Lee SC, Zuccotti A, et al. The reduced cochlear output and the failure to adapt the central auditory response causes tinnitus in noise exposed rats. PLoS One. 2013;8(3):e57247. doi: 10.1371/journal.pone.0057247
39. Zheng Y, McPherson K, Reid P, Smith PF. The anti-inflammatory selective melanocortin receptor subtype 4 agonist, RO27-3225, fails to prevent acoustic trauma-induced tinnitus in rats. Eur J Pharmacol. 2015;761:206-10. doi: 10.1016/j.ejphar.2015.05.007
40. Ropp TJ, Tiedemann KL, Young ED, May BJ. Effects of unilateral acoustic trauma on tinnitus-related spontaneous activity in the inferior colliculus. J Assoc Res Otolaryngol. 2014;15(6):1007-22. doi: 10.1007/s10162-014-0488-2
41. Middleton JW, Kiritani T, Pedersen C, Turner JG, Shepherd GM, Tzounopoulos T. Mice with behavioral evidence of tinnitus exhibit dorsal cochlear nucleus hyperactivity because of decreased GABAergic inhibition. Proc Natl Acad Sci U S A. 2011;108(18):7601-6. doi: 10.1073/pnas.1100223108
42. Dong S, Mulders WH, Rodger J, Woo S, Robertson D. Acoustic trauma evokes hyperactivity and changes in gene expression in guinea-pig auditory brainstem. Eur J Neurosci. 2010;31(9):1616-28. doi: 10.1111/j.1460-9568.2010.07183.x
43. Mulders WH, Ding D, Salvi R, Robertson D. Relationship between auditory thresholds, central spontaneous activity, and hair cell loss after acoustic trauma. J Comp Neurol. 2011;519(13):2637-47. doi: 10.1002/cne.22644
44. Hickox AE, Liberman MC. Is noise-induced cochlear neuropathy key to the generation of hyperacusis or tinnitus? J Neurophysiol. 2014;111(3):552-64. doi: 10.1152/jn.00184.2013
45. Shi L, Guo X, Shen P, Liu L, Tao S, Li X, et al. Noise-induced damage to ribbon synapses without permanent threshold shifts in neonatal mice. Neuroscience. 2015;304:368-77. doi: 10.1016/j.neuroscience.2015.07.066
46. Dehmel S, Pradhan S, Koehler S, Bledsoe S, Shore S. Noise overexposure alters long-term somatosensory-auditory proce-ssing in the dorsal cochlear nucleus--possible basis for tinnitus-related hyperactivity? J Neurosci. 2012;32(5):1660-71. doi: 10.1523/JNEUROSCI.4608-11.2012
47. Shore SE, Koehler S, Oldakowski M, Hughes LF, Syed S. Dorsal cochlear nucleus responses to somatosensory stimulation are enhanced after noise-induced hearing loss. Eur J Neurosci. 2008;27(1):155-68. doi: 10.1111/j.1460-9568.2007.05983.x
48. Zeng C, Nannapaneni N, Zhou J, Hughes LF, Shore S. Cochlear damage changes the distribution of vesicular glutamate transporters associated with auditory and nonauditory inputs to the cochlear nucleus. J Neurosci. 2009;29(13):4210-7. doi: 10.1523/JNEUROSCI.0208-09.2009
49. Ma WL, Young ED. Dorsal cochlear nucleus response properties following acoustic trauma: response maps and spontaneous activity. Hear Res. 2006;216-217:176-88. doi: 10.1016/j.heares.2006.03.011
50. Brozoski TJ, Wisner KW, Sybert LT, Bauer CA. Bilateral dorsal cochlear nucleus lesions prevent acoustic-trauma induced tinnitus in an animal model. J Assoc Res Otolaryngol. 2012;13(1):55-66. doi: 10.1007/s10162-011-0290-3
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| Files | ||
| Issue | Vol 28 No 4 (2019) | |
| Section | Review Article(s) | |
| DOI | https://doi.org/10.18502/avr.v28i4.1455 | |
| Keywords | ||
| Tinnitus; animal models of tinnitus; salicylate, noise | ||
| Rights and permissions | |
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Rezapour M, Moossavi A. Tinnitus induction in animals and its impact on auditory system structure. Aud Vestib Res. 2019;28(4):204-216.
