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Current topics in behavioral neurosciences
2021;51 327-347.

Neurobiology of Stress-Induced Tinnitus.

Agnieszka J Szczepek, Birgit Mazurek
Author Information
  1. Agnieszka J Szczepek: Department of Otorhinolaryngology, Head and Neck Surgery, Charité-Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany. agnes.szczepek@charite.de.
  2. Birgit Mazurek: Tinnitus Center, Charité-Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany.
PMID: 33604876 DOI: 10.1007/7854_2020_215

Abstract

Emotional stress has accompanied humans since the dawn of time and has played an essential role not only in positive selection and adaptation to an ever-changing environment, but also in the acceleration or even initiation of many illnesses. The three main somatic mechanisms induced by stress are the hypothalamus-pituitary-adrenal axis (HPA axis), the sympathetic-adreno-medullar (SAM) axis, and the immune axis. In this chapter, the stress-induced mechanisms that can affect cochlear physiology are presented and discussed in the context of tinnitus generation and auditory neurobiology. It is concluded that all of the presented mechanisms need to be further investigated. It is advised that clinical practitioners ask patients about stressful events or chronic stress preceding the tinnitus onset and measure the vital signs. Finally, taking into account that tinnitus itself acts as a stressor, the implementation of anti-stress therapies for tinnitus treatment is recommended.

Keywords

Catecholamines Cytokines Glucocorticoids Glutamate excitotoxicity HPA axis Immune axis SAM axis The cochlea

References

  1. Adoga AA, Adoga AS, Obindo JT (2008) Tinnitus and the prevalence of co-morbid psychological stress. Niger J Med 17:95–97 [PMID: 18390143]
  2. Aldskogius H, Kozlova EN (1998) Central neuron-glial and glial-glial interactions following axon injury. Prog Neurobiol 55:1–26 [PMID: 9602498]
  3. Altschuler RA, Halsey K, Kanicki A, Martin C, Prieskorn D, Deremer S, Dolan DF (2019) Small arms fire-like noise: effects on hearing loss, gap detection and the influence of preventive treatment. Neuroscience 407:32–40 [PMID: 30053484]
  4. Arranz L, De Vicente A, Muñoz M, De La Fuente M (2009) Impaired immune function in a homeless population with stress-related disorders. Neuroimmunomodulation 16:251–260 [PMID: 19365149]
  5. Axelsson A, Borg E, Hornstrand C (1983) Noise effects on the cochlear vasculature in normotensive and spontaneously hypertensive rats. Acta Otolaryngol 96:215–225 [PMID: 6637443]
  6. Aydin N, Searchfield GD (2019) Changes in tinnitus and physiological biomarkers of stress in response to short-term broadband noise and sounds of nature. Complement Ther Med 46:62–68 [PMID: 31519289]
  7. Baigi A, Oden A, Almlid-Larsen V, Barrenäs ML, Holgers KM (2011) Tinnitus in the general population with a focus on noise and stress: a public health study. Ear Hear 32:787–789 [PMID: 21716113]
  8. Barald KF, Shen YC, Bianchi LM (2018) Chemokines and cytokines on the neuroimmunoaxis: inner ear neurotrophic cytokines in development and disease. Prospects for repair? Exp Neurol 301:92–99 [PMID: 29080793]
  9. Bertolaso L, Martini A, Bindini D, Lanzoni I, Parmeggiani A, Vitali C, Kalinec G, Kalinec F, Capitani S, Previati M (2001) Apoptosis in the OC-k3 immortalized cell line treated with different agents. Audiology 40:327–335 [PMID: 11781046]
  10. Besteher B, Gaser C, Ivanšić D, Guntinas-Lichius O, Dobel C, Nenadić I (2019) Chronic tinnitus and the limbic system: reappraising brain structural effects of distress and affective symptoms. Neuroimage Clin 24:101976 [PMID: 31494400]
  11. Betz LT, Muhlberger A, Langguth B, Schecklmann M (2017) Stress reactivity in chronic tinnitus. Sci Rep 7:41521 [PMID: 28134346]
  12. Bhatt JM, Bhattacharyya N, Lin HW (2017) Relationships between tinnitus and the prevalence of anxiety and depression. Laryngoscope 127:466–469 [PMID: 27301552]
  13. Biehl R, Boecking B, Brueggemann P, Grosse R, Mazurek B (2019) Personality traits, perceived stress, and tinnitus-related distress in patients with chronic tinnitus: support for a vulnerability-stress model. Front Psychol 10:3093 [PMID: 32116880]
  14. Borg E, Viberg A (1987) Age-related hair cell loss in spontaneously hypertensive and normotensive rats. Hear Res 30:111–118 [PMID: 3680059]
  15. Brueggemann P, Seydel C, Schaefer C, Szczepek AJ, Amarjargal N, Boecking B, Rose M, Mazurek B (2019) ICD-10 symptom rating questionnaire for assessment of psychological comorbidities in patients with chronic tinnitus. HNO 67:46–50 [PMID: 30927015]
  16. Bruggemann P, Szczepek AJ, Rose M, Mckenna L, Olze H, Mazurek B (2016) Impact of multiple factors on the degree of tinnitus distress. Front Hum Neurosci 10:341 [PMID: 27445776]
  17. Bryant RA (2018) The current evidence for acute stress disorder. Curr Psychiatry Rep 20:111 [PMID: 30315408]
  18. Cai J, Li J, Mao Y, Bai X, Xu L, Wang H (2013) Immunohistochemical localization of α2-adrenergic receptors in the neonatal rat cochlea and the vestibular labyrinth. J Mol Neurosci 51:1010–1020 [PMID: 23975628]
  19. Canlon B, Theorell T, Hasson D (2013) Associations between stress and hearing problems in humans. Hear Res 295:9–15 [PMID: 22982334]
  20. Cannon WB (1922) Bodily changes in pain, hunger, fear and rage: an account of recent researches into the function of emotional excitement. D. Appleton
  21. Carrasco VN, Prazma J, Faber JE, Triana RJ, Pillsbury HC (1990) Cochlear microcirculation. Effect of adrenergic agonists on arteriole diameter. Arch Otolaryngol Head Neck Surg 116:411–417 [PMID: 1969284]
  22. Caspary DM, Llano DA (2017) Auditory thalamic circuits and GABA(A) receptor function: putative mechanisms in tinnitus pathology. Hear Res 349:197–207 [PMID: 27553899]
  23. Conrad I, Kleinstauber M, Jasper K, Hiller W, Andersson G, Weise C (2015) The role of dysfunctional cognitions in patients with chronic tinnitus. Ear Hear 36
  24. Cortada M, Levano S, Bodmer D (2017) Brimonidine protects auditory hair cells from in vitro-induced toxicity of gentamicin. Audiol Neurootol 22:125–134 [PMID: 28889125]
  25. Craske MG, Stein MB (2016) Anxiety. Lancet 388:3048–3059 [PMID: 27349358]
  26. Crawley BK, Keithley EM (2011) Effects of mitochondrial mutations on hearing and cochlear pathology with age. Hear Res 280:201–208 [PMID: 21664445]
  27. Cui W, Wang H, Cheng Y, Ma X, Lei Y, Ruan X, Shi L, Lv M (2019) Long-term treatment with salicylate enables NMDA receptors and impairs AMPA receptors in C57BL/6J mice inner hair cell ribbon synapse. Mol Med Rep 19:51–58 [PMID: 30431080]
  28. Curtis J (1841) Tinnitus aurium. Lancet 36:828–829 [DOI: 10.1016/S0140-6736(02)97637-3]
  29. Danioth L, Brotschi G, Croy I, Friedrich H, Caversaccio MD, Negoias S (2020) Multisensory environmental sensitivity in patients with chronic tinnitus. J Psychosom Res 135:110155 [PMID: 32534321]
  30. Değirmenci H, Bakırcı EM, Salcan İ, Demirelli S, Duman H, Ceyhun G, Küçüksu Z (2014) Determination of correlation among heart rate variability, left atrium global strain, and nighttime blood pressure among patients with tinnitus. Med Sci Monit 20:1714–1719 [PMID: 25249354]
  31. Desa DE, Nichols MG, Smith HJ (2018) Aminoglycosides rapidly inhibit NAD(P)H metabolism increasing reactive oxygen species and cochlear cell demise. J Biomed Opt 24:1–14 [PMID: 30411553]
  32. Eggermont JJ (1990) On the pathophysiology of tinnitus; a review and a peripheral model. Hear Res 48:111–123 [PMID: 2249954]
  33. Eggermont JJ, Roberts LE (2015) Tinnitus: animal models and findings in humans. Cell Tissue Res 361:311–336 [PMID: 25266340]
  34. El Ganzoury MM, Kamel TB, Khalil LH, Seliem AM (2012) Cochlear dysfunction in children following cardiac bypass surgery. ISRN Pediatr 2012:375038 [PMID: 22811927]
  35. Evans P, Halliwell B (1999) Free radicals and hearing. Cause, consequence, and criteria. Ann N Y Acad Sci 884:19–40 [PMID: 10842581]
  36. Figueiredo RR, Azevedo AA, Penido NO (2016) Positive association between tinnitus and arterial hypertension. Front Neurol 7:171 [PMID: 27761128]
  37. Figueiredo RR, De Azevedo AA, Penido Nde O (2015) Tinnitus and arterial hypertension: a systematic review. Eur Arch Otorhinolaryngol 272:3089–3094 [PMID: 25190255]
  38. Fischel-Ghodsian N, Prezant TR, Chaltraw WE, Wendt KA, Nelson RA, Arnos KS, Falk RE (1997) Mitochondrial gene mutation is a significant predisposing factor in aminoglycoside ototoxicity. Am J Otolaryngol 18:173–178 [PMID: 9164619]
  39. Fortier C, Selye H (1949) Adrenocorticotrophic effect of stress after severance of the hypothalamo-hypophyseal pathways. Am J Physiol 159:433–439. illust [PMID: 15401087]
  40. Frye MD, Ryan AF, Kurabi A (2019) Inflammation associated with noise-induced hearing loss. J Acoust Soc Am 146:4020 [PMID: 31795714]
  41. Furuta H, Mori N, Sato C, Hoshikawa H, Sakai S, Iwakura S, Doi K (1994) Mineralocorticoid type I receptor in the rat cochlea: mRNA identification by polymerase chain reaction (PCR) and in situ hybridization. Hear Res 78:175–180 [PMID: 7982810]
  42. Gauvin DV, Yoder J, Zimmermann ZJ, Tapp R (2018) Ototoxicity: the radical drum beat and rhythm of cochlear hair cell life and death. Int J Toxicol 37:195–206 [PMID: 29575954]
  43. Gomaa MA, Elmagd MH, Elbadry MM, Kader RM (2014) Depression, anxiety and stress scale in patients with tinnitus and hearing loss. Eur Arch Otorhinolaryngol 271:2177–2184 [PMID: 24071860]
  44. Guest H, Munro KJ, Prendergast G, Howe S, Plack CJ (2017) Tinnitus with a normal audiogram: relation to noise exposure but no evidence for cochlear synaptopathy. Hear Res 344:265–274 [PMID: 27964937]
  45. Gupta MA, Jarosz P, Gupta AK (2017) Posttraumatic stress disorder (PTSD) and the dermatology patient. Clin Dermatol 35:260–266 [PMID: 28511822]
  46. Haider HF, Bojić T, Ribeiro SF, Paço J, Hall DA, Szczepek AJ (2018) Pathophysiology of subjective tinnitus: triggers and maintenance. Front Neurosci 12
  47. Haider HF, Ribeiro SF, Martins C, Ribeiro D, Trigueiros N, Szczepek AJ, Caria H, Hoare DJ, Paço J, Borrego LM (2020) Tinnitus, hearing loss and inflammatory processes in an older portuguese population. Int J Audiol 59:323–332 [PMID: 31829778]
  48. Han BR, Lin SC, Espinosa K, Thorne PR, Vlajkovic SM (2019) Inhibition of the adenosine A(2A) receptor mitigates excitotoxic injury in organotypic tissue cultures of the rat cochlea. Cell 8
  49. Hasson D, Theorell T, Bergquist J, Canlon B (2013) Acute stress induces hyperacusis in women with high levels of emotional exhaustion. PLoS One 8:e52945 [PMID: 23301005]
  50. Hébert S, Canlon B, Hasson D, Magnusson Hanson LL, Westerlund H, Theorell T (2012) Tinnitus severity is reduced with reduction of depressive mood – a prospective population study in Sweden. PLoS One 7:e37733 [PMID: 22629449]
  51. Hébert S, Lupien SJ (2007) The sound of stress: blunted cortisol reactivity to psychosocial stress in tinnitus sufferers. Neurosci Lett 411:138–142 [PMID: 17084027]
  52. Heim C, Nemeroff CB (2009) Neurobiology of posttraumatic stress disorder. CNS Spectr 14:13–24 [PMID: 19169190]
  53. Hermann R, Biallas B, Predel HG, Petrowski K (2019) Physical versus psychosocial stress: effects on hormonal, autonomic, and psychological parameters in healthy young men. Stress 22:103–112 [PMID: 30345865]
  54. Herr RM, Bosch JA, Theorell T, Loerbroks A (2018) Bidirectional associations between psychological distress and hearing problems: an 18-year longitudinal analysis of the British household panel survey. Int J Audiol 57:816–824 [PMID: 30052099]
  55. Hirose K, Rutherford MA, Warchol ME (2017) Two cell populations participate in clearance of damaged hair cells from the sensory epithelia of the inner ear. Hear Res 352:70–81 [PMID: 28526177]
  56. Hoang KN, Dinh CT, Bas E, Chen S, Eshraghi AA, Van De Water TR (2009) Dexamethasone treatment of naïve organ of corti explants alters the expression pattern of apoptosis-related genes. Brain Res 1301:1–8 [PMID: 19747459]
  57. Horner K (2003) The emotional ear in stress. Neurosci Biobehav Rev 27:437–446 [PMID: 14505685]
  58. Hu BH, Zhang C, Frye MD (2018) Immune cells and non-immune cells with immune function in mammalian cochleae. Hear Res 362:14–24 [PMID: 29310977]
  59. Huang T, Cheng AG, Stupak H, Liu W, Kim A, Staecker H, Lefebvre PP, Malgrange B, Kopke R, Moonen G, Van De Water TR (2000) Oxidative stress-induced apoptosis of cochlear sensory cells: otoprotective strategies. Int J Dev Neurosci 18:259–270 [PMID: 10715580]
  60. Hunter RG, Seligsohn M, Rubin TG, Griffiths BB, Ozdemir Y, Pfaff DW, Datson NA, Mcewen BS (2016) Stress and corticosteroids regulate rat hippocampal mitochondrial DNA gene expression via the glucocorticoid receptor. Proc Natl Acad Sci U S A 113:9099–9104 [PMID: 27457949]
  61. Hwang JH, Chen JC, Yang SY, Wang MF, Chan YC (2011) Expression of tumor necrosis factor-α and interleukin-1β genes in the cochlea and inferior colliculus in salicylate-induced tinnitus. J Neuroinflammation 8:30 [PMID: 21477330]
  62. Iguchi H, Yamane H, Konishi K, Nakagawa T, Shibata S, Takayama M, Nishimura K, Sunami K, Nakai Y (1997) Asialo GM1-positive cells in mouse cochlea. Acta Otolaryngol Suppl 528:6–9 [PMID: 9288228]
  63. Jastreboff PJ (1990) Phantom auditory perception (tinnitus): mechanisms of generation and perception. Neurosci Res 8:221–254 [PMID: 2175858]
  64. Jung YH, Shin NY, Jang JH, Lee WJ, Lee D, Choi Y, Choi SH, Kang DH (2019) Relationships among stress, emotional intelligence, cognitive intelligence, and cytokines. Medicine (Baltimore) 98:e15345 [DOI: 10.1097/MD.0000000000015345]
  65. Kapolowicz MR, Thompson LT (2020) Plasticity in limbic regions at early time points in experimental models of tinnitus. Front Syst Neurosci 13
  66. Karst H, Berger S, Turiault M, Tronche F, Schütz G, Joëls M (2005) Mineralocorticoid receptors are indispensable for nongenomic modulation of hippocampal glutamate transmission by corticosterone. Proc Natl Acad Sci U S A 102:19204–19207 [PMID: 16361444]
  67. Kaur T, Clayman AC, Nash AJ, Schrader AD, Warchol ME, Ohlemiller KK (2019) Lack of fractalkine receptor on macrophages impairs spontaneous recovery of ribbon synapses after moderate noise trauma in C57BL/6 mice. Front Neurosci 13:620 [PMID: 31263398]
  68. Keithley EM (2020) Pathology and mechanisms of cochlear aging. J Neurosci Res 98(9):1674–1684. https://doi.org/10.1002/jnr.24439 . Epub 2019 May 7
  69. Kil SH, Kalinec F (2013) Expression and dexamethasone-induced nuclear translocation of glucocorticoid and mineralocorticoid receptors in guinea pig cochlear cells. Hear Res 299:63–78 [PMID: 23403298]
  70. Kim KX, Payne S, Yang-Hood A, Li SZ, Davis B, Carlquist J, V-Ghaffari B, Gantz JA, Kallogjeri D, Fitzpatrick JAJ, Ohlemiller KK, Hirose K, Rutherford MA (2019) Vesicular glutamatergic transmission in noise-induced loss and repair of cochlear ribbon synapses. J Neurosci 39:4434–4447 [PMID: 30926748]
  71. Kirschbaum C, Pirke KM, Hellhammer DH (1993) The ‘Trier Social Stress Test’ – a tool for investigating psychobiological stress responses in a laboratory setting. Neuropsychobiology 28:76–81 [PMID: 8255414]
  72. Kishimoto I, Okano T, Nishimura K, Motohashi T, Omori K (2019) Early development of resident macrophages in the mouse cochlea depends on Yolk Sac hematopoiesis. Front Neurol 10:1115 [PMID: 31695671]
  73. Kokotas H, Petersen MB, Willems PJ (2007) Mitochondrial deafness. Clin Genet 71:379–391 [PMID: 17489842]
  74. Landgrebe M, Langguth B, Rosengarth K, Braun S, Koch A, Kleinjung T, May A, De Ridder D, Hajak G (2009) Structural brain changes in tinnitus: grey matter decrease in auditory and non-auditory brain areas. Neuroimage 46:213–218 [PMID: 19413945]
  75. Le TN, Straatman LV, Lea J, Westerberg B (2017) Current insights in noise-induced hearing loss: a literature review of the underlying mechanism, pathophysiology, asymmetry, and management options. J Otolaryngol Head Neck Surg 46:41 [PMID: 28535812]
  76. Leaver AM, Seydell-Greenwald A, Rauschecker JP (2016) Auditory-limbic interactions in chronic tinnitus: challenges for neuroimaging research. Hear Res 334:49–57 [PMID: 26299843]
  77. Lechowicz U, Pollak A, Raj-Koziak D, Dziendziel B, Skarżyński PH, Skarżyński H, Ołdak M (2018) Tinnitus in patients with hearing loss due to mitochondrial DNA pathogenic variants. Eur Arch Otorhinolaryngol 275:1979–1985 [PMID: 29936625]
  78. Levin SG, Godukhin OV (2017) Modulating effect of cytokines on mechanisms of synaptic plasticity in the brain. Biochemistry (Mosc) 82:264–274 [DOI: 10.1134/S000629791703004X]
  79. Liberman MC, Kujawa SG (2017) Cochlear synaptopathy in acquired sensorineural hearing loss: manifestations and mechanisms. Hear Res 349:138–147 [PMID: 28087419]
  80. Lie A, Skogstad M, Johannessen HA, Tynes T, Mehlum IS, Nordby KC, Engdahl B, Tambs K (2016) Occupational noise exposure and hearing: a systematic review. Int Arch Occup Environ Health 89:351–372 [PMID: 26249711]
  81. Liu W, Molnar M, Garnham C, Benav H, Rask-Andersen H (2018) Macrophages in the human cochlea: saviors or predators – a study using super-resolution immunohistochemistry. Front Immunol 9:223 [PMID: 29487598]
  82. Liu W, Rask-Andersen H (2019) Super-resolution immunohistochemistry study on CD4 and CD8 cells and the relation to macrophages in human cochlea. J Otol 14:1–5 [PMID: 30936894]
  83. Liu Y, Niu H, Zhu J, Zhao P, Yin H, Ding H, Gong S, Yang Z, Lv H, Wang Z (2019) Morphological neuroimaging biomarkers for tinnitus: evidence obtained by applying machine learning. Neural Plast 2019:1712342 [PMID: 31915431]
  84. 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 50:114–120 [PMID: 9443467]
  85. Lupien SJ, Mcewen BS, Gunnar MR, Heim C (2009) Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci 10:434–445 [PMID: 19401723]
  86. Martin S, Henley JM, Holman D, Zhou M, Wiegert O, Van Spronsen M, Joëls M, Hoogenraad CC, Krugers HJ (2009) Corticosterone alters AMPAR mobility and facilitates bidirectional synaptic plasticity. PLoS One 4:e4714 [PMID: 19305644]
  87. Mazurek B, Boecking B, Brueggemann P (2019) Association between stress and tinnitus-new aspects. Otol Neurotol 40:e467–e473 [PMID: 30870382]
  88. Mazurek B, Haupt H, Joachim R, Klapp BF, Stöver T, Szczepek AJ (2010a) Stress induces transient auditory hypersensitivity in rats. Hear Res 259:55–63 [PMID: 19840840]
  89. Mazurek B, Stöver T, Haupt H, Klapp B, Adli M, Gross J, Szczepek A (2010b) The significance of stress: its role in the auditory system and the pathogenesis of tinnitus. HNO 58:162–172 [PMID: 19795102]
  90. Mazurek B, Szczepek A, Hebert S (2015) Stress and tinnitus. HNO 63:258–265 [PMID: 25862619]
  91. Mazurek B, Winter E, Fuchs J, Haupt H, Gross J (2003) Susceptibility of the hair cells of the newborn rat cochlea to hypoxia and ischemia. Hear Res 182:2–8 [PMID: 12948595]
  92. Mcgregor BA, Murphy KM, Albano DL, Ceballos RM (2016) Stress, cortisol, and B lymphocytes: a novel approach to understanding academic stress and immune function. Stress 19:185–191 [PMID: 26644211]
  93. Michaelides A, Zis P (2019) Depression, anxiety and acute pain: links and management challenges. Postgrad Med 131:438–444 [PMID: 31482756]
  94. Misiewicz Z, Iurato S, Kulesskaya N, Salminen L, Rodrigues L, Maccarrone G, Martins J, Czamara D, Laine MA, Sokolowska E, Trontti K, Rewerts C, Novak B, Volk N, Park DI, Jokitalo E, Paulin L, Auvinen P, Voikar V, Chen A, Erhardt A, Turck CW, Hovatta I (2019) Multi-omics analysis identifies mitochondrial pathways associated with anxiety-related behavior. PLoS Genet 15:e1008358 [PMID: 31557158]
  95. Moghaddam B (1993) Stress preferentially increases extraneuronal levels of excitatory amino acids in the prefrontal cortex: comparison to hippocampus and basal ganglia. J Neurochem 60:1650–1657 [PMID: 8097232]
  96. Moossavi A, Sadeghijam M, Akbari M (2019) The hypothetical relation between the degree of stress and auditory cortical evoked potentials in tinnitus sufferers. Med Hypotheses 130:109266 [PMID: 31383346]
  97. Mosnier I, Teixeira M, Loiseau A, Fernandes I, Sterkers O, Amiel C, Ferrary E (2001) Effects of acute and chronic hypertension on the labyrinthine barriers in rat. Hear Res 151(1–2):227–236. https://doi.org/10.1016/s0378-5955(00)00229-x
  98. Mostafa H, Saad M, El-Attar A, Ahmed G, Berrettini S, Forli F, Siciliano G, Mancuso M (2014) Mitochondrial DNA (mtDNA) haplotypes and dysfunctions in presbyacusis. Acta Otorhinolaryngol Ital 34:54–61 [PMID: 24711684]
  99. Mühlau M, Rauschecker JP, Oestreicher E, Gaser C, Röttinger M, Wohlschläger AM, Simon F, Etgen T, Conrad B, Sander D (2006) Structural brain changes in tinnitus. Cereb Cortex 16:1283–1288 [PMID: 16280464]
  100. National Guideline (2020) Evidence review for psychological therapies: tinnitus: assessment and management: evidence review L. National Institute for Health and Care Excellence (UK), London. Copyright © NICE 2020
  101. O’reilly M, Young L, Kirkwood NK, Richardson GP, Kros CJ, Moore AL (2019) Gentamicin affects the bioenergetics of isolated mitochondria and collapses the mitochondrial membrane potential in cochlear sensory hair cells. Front Cell Neurosci 13:416 [PMID: 31572129]
  102. Op De Beeck K, Schacht J, Van Camp G (2011) Apoptosis in acquired and genetic hearing impairment: the programmed death of the hair cell. Hear Res 281:18–27 [>PMCID: ]
  103. Oyola MG, Handa RJ (2017) Hypothalamic-pituitary-adrenal and hypothalamic-pituitary-gonadal axes: sex differences in regulation of stress responsivity. Stress 20:476–494 [PMID: 28859530]
  104. Pickles JO (2004) Mutation in mitochondrial DNA as a cause of presbyacusis. Audiol Neurootol 9:23–33 [PMID: 14676471]
  105. Pienkowski M (2018) Prolonged exposure of CBA/Ca mice to moderately loud noise can cause cochlear synaptopathy but not tinnitus or hyperacusis as assessed with the acoustic startle reflex. Trends Hear 22:2331216518758109 [PMID: 29532738]
  106. Poirrier AL, Pincemail J, Van Den Ackerveken P, Lefebvre PP, Malgrange B (2010) Oxidative stress in the cochlea: an update. Curr Med Chem 17:3591–3604 [PMID: 20738243]
  107. Polman JAE, Welten JE, Bosch DS, De Jonge RT, Balog J, Van Der Maarel SM, De Kloet ER, Datson NA (2012) A genome-wide signature of glucocorticoid receptor binding in neuronal PC12 cells. BMC Neurosci 13:118 [PMID: 23031785]
  108. Probst T, Pryss R, Langguth B, Schlee W (2016) Emotional states as mediators between tinnitus loudness and tinnitus distress in daily life: results from the “TrackYourTinnitus” application. Sci Rep 6:20382 [PMID: 26853815]
  109. Puel JL, Ruel J, Guitton M, Wang J, Pujol R (2002) The inner hair cell synaptic complex: physiology, pharmacology and new therapeutic strategies. Audiol Neurootol 7:49–54 [PMID: 11914527]
  110. Qu T, Qi Y, Yu S, Du Z, Wei W, Cai A, Wang J, Nie B, Liu K, Gong S (2019) Dynamic changes of functional neuronal activities between the auditory pathway and limbic systems contribute to noise-induced tinnitus with a normal audiogram. Neuroscience 408:31–45 [PMID: 30946875]
  111. Ralli M, Troiani D, Podda MV, Paciello F, Eramo SL, De Corso E, Salvi R, Paludetti G, Fetoni AR (2014) The effect of the NMDA channel blocker memantine on salicylate-induced tinnitus in rats. Acta Otorhinolaryngol Ital 34:198–204 [PMID: 24882929]
  112. Rauschecker JP, Leaver AM, Mühlau M (2010) Tuning out the noise: limbic-auditory interactions in tinnitus. Neuron 66:819–826 [PMID: 20620868]
  113. Reddy TE, Pauli F, Sprouse RO, Neff NF, Newberry KM, Garabedian MJ, Myers RM (2009) Genomic determination of the glucocorticoid response reveals unexpected mechanisms of gene regulation. Genome Res 19:2163–2171 [PMID: 19801529]
  114. Ryan D, Bauer CA (2016) Neuroscience of tinnitus. Neuroimaging Clin N Am 26:187–196 [PMID: 27154602]
  115. Rybak LP, Mukherjea D, Ramkumar V (2019) Mechanisms of cisplatin-induced ototoxicity and prevention. Semin Hear 40:197–204 [PMID: 31036996]
  116. Sahley TL, Hammonds MD, Musiek FE (2013) Endogenous dynorphins, glutamate and N-methyl-d-aspartate (NMDA) receptors may participate in a stress-mediated type-I auditory neural exacerbation of tinnitus. Brain Res 1499:80–108 [PMID: 23313584]
  117. Sahley TL, Nodar RH (2001) A biochemical model of peripheral tinnitus. Hear Res 152:43–54 [PMID: 11223280]
  118. Salviati M, Bersani FS, Terlizzi S, Melcore C, Panico R, Romano GF, Valeriani G, Macri F, Altissimi G, Mazzei F, Testugini V, Latini L, Delle Chiaie R, Biondi M, Cianfrone G (2014) Tinnitus: clinical experience of the psychosomatic connection. Neuropsychiatr Dis Treat 10:267–275 [PMID: 24550676]
  119. Sawada S, Mori N, Mount RJ, Harrison RV (2001) Differential vulnerability of inner and outer hair cell systems to chronic mild hypoxia and glutamate ototoxicity: insights into the cause of auditory neuropathy. J Otolaryngol 30:106–114 [PMID: 11770952]
  120. Seifert E, Lamprecht-Dinnesen A, Asfour B, Rotering H, Bone HG, Scheld HH (1998) The influence of body temperature on transient evoked otoacoustic emissions. Br J Audiol 32:387–398 [PMID: 10064421]
  121. Selye H (1937) The significance of the adrenals for adaptation. Science 85:247–248 [PMID: 17841381]
  122. Selye H (1950) Stress and the general adaptation syndrome. Br Med J 1:1383–1392 [PMID: 15426759]
  123. Selye H, Fortier C (1949) Adaptive reactions to stress. Res Publ Assoc Res Nerv Ment Dis 29:3–18 [PMID: 14854281]
  124. Sheth S, Mukherjea D, Rybak LP, Ramkumar V (2017) Mechanisms of cisplatin-induced ototoxicity and otoprotection. Front Cell Neurosci 11:338 [PMID: 29163050]
  125. Shirane M, Harrison RV (1987) The effects of hypoxia on sensory cells of the cochlea in chinchilla. Scanning Microsc 1:1175–1183 [PMID: 3659860]
  126. Slavich GM, Shields GS (2018) Assessing lifetime stress exposure using the stress and adversity inventory for adults (adult STRAIN): an overview and initial validation. Psychosom Med 80:17–27 [PMID: 29016550]
  127. Sliwinska-Kowalska M, Davis A (2012) Noise-induced hearing loss. Noise Health 14:274–280 [PMID: 23257577]
  128. Szczepek A, Mazurek B (2017) Tinnitus and stress. Springer, Cham [DOI: 10.1007/978-3-319-58397-6]
  129. Szczepek AJ, Haupt H, Klapp BF, Olze H, Mazurek B (2014) Biological correlates of tinnitus-related distress: an exploratory study. Hear Res 318:23–30 [PMID: 25445818]
  130. Tahera Y, Meltser I, Johansson P, Canlon B (2006a) Restraint stress modulates glucocorticoid receptors and nuclear factor kappa B in the cochlea. Neuroreport 17:879–882 [PMID: 16738480]
  131. Tahera Y, Meltser I, Johansson P, Hansson AC, Canlon B (2006b) Glucocorticoid receptor and nuclear factor-kappa B interactions in restraint stress-mediated protection against acoustic trauma. Endocrinology 147:4430–4437 [PMID: 16777974]
  132. Ten Cate WJ, Curtis LM, Small GM, Rarey KE (1993) Localization of glucocorticoid receptors and glucocorticoid receptor mRNAs in the rat cochlea. Laryngoscope 103:865–871 [PMID: 8361289]
  133. Waechter S, Brännström KJ (2015) The impact of tinnitus on cognitive performance in normal-hearing individuals. Int J Audiol 54(11):845–851 [PMID: 26107427]
  134. Wang W, Zhang LS, Zinsmaier AK, Patterson G, Leptich EJ, Shoemaker SL, Yatskievych TA, Gibboni R, Pace E, Luo H, Zhang J, Yang S, Bao S (2019) Neuroinflammation mediates noise-induced synaptic imbalance and tinnitus in rodent models. PLoS Biol 17:e3000307 [PMID: 31211773]
  135. Yang P, Ma W, Zheng Y, Yang H, Lin H (2015) A systematic review and meta-analysis on the association between hypertension and tinnitus. Int J Hypertens 2015:583493 [PMID: 26881064]
  136. Yao X, Rarey KE (1996) Localization of the mineralocorticoid receptor in rat cochlear tissue. Acta Otolaryngol 116:493–496 [PMID: 8790754]
  137. Yip J, Geng X, Shen J, Ding Y (2016) Cerebral gluconeogenesis and diseases. Front Pharmacol 7:521 [PMID: 28101056]
  138. Yu C-Y, Mayba O, Lee JV, Tran J, Harris C, Speed TP, Wang J-C (2010) Genome-wide analysis of glucocorticoid receptor binding regions in adipocytes reveal gene network involved in triglyceride homeostasis. PLoS One 5:e15188 [PMID: 21187916]
  139. Zirke N, Seydel C, Arsoy D, Klapp BF, Haupt H, Szczepek AJ, Olze H, Goebel G, Mazurek B (2013) Analysis of mental disorders in tinnitus patients performed with composite international diagnostic interview. Qual Life Res 22:2095–2104 [PMID: 23292277]
  140. Zöger S, Svedlund J, Holgers KM (2006) Relationship between tinnitus severity and psychiatric disorders. Psychosomatics 47:282–288 [PMID: 16844885]
  141. Zuo J, Curtis LM, Yao X, Ten Cate WJ, Bagger-Sjöbäck D, Hultcrantz M, Rarey KE (1995) Glucocorticoid receptor expression in the postnatal rat cochlea. Hear Res 87:220–227 [PMID: 8567439]

MeSH Term

Adaptation, Physiological
Humans
Hypothalamo-Hypophyseal System
Pituitary-Adrenal System
Stress, Psychological
Tinnitus
Journal Article

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