Skip to main content

Neurobiology of Stress-Induced Tinnitus

  • Chapter
  • First Online:
The Behavioral Neuroscience of Tinnitus

Part of the book series: Current Topics in Behavioral Neurosciences ((CTBN,volume 51))

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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Adoga AA, Adoga AS, Obindo JT (2008) Tinnitus and the prevalence of co-morbid psychological stress. Niger J Med 17:95–97

    Article  CAS  PubMed  Google Scholar 

  • Aldskogius H, Kozlova EN (1998) Central neuron-glial and glial-glial interactions following axon injury. Prog Neurobiol 55:1–26

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Axelsson A, Borg E, Hornstrand C (1983) Noise effects on the cochlear vasculature in normotensive and spontaneously hypertensive rats. Acta Otolaryngol 96:215–225

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Betz LT, Muhlberger A, Langguth B, Schecklmann M (2017) Stress reactivity in chronic tinnitus. Sci Rep 7:41521

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bhatt JM, Bhattacharyya N, Lin HW (2017) Relationships between tinnitus and the prevalence of anxiety and depression. Laryngoscope 127:466–469

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Borg E, Viberg A (1987) Age-related hair cell loss in spontaneously hypertensive and normotensive rats. Hear Res 30:111–118

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Bryant RA (2018) The current evidence for acute stress disorder. Curr Psychiatry Rep 20:111

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Canlon B, Theorell T, Hasson D (2013) Associations between stress and hearing problems in humans. Hear Res 295:9–15

    Article  PubMed  Google Scholar 

  • Cannon WB (1922) Bodily changes in pain, hunger, fear and rage: an account of recent researches into the function of emotional excitement. D. Appleton

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Caspary DM, Llano DA (2017) Auditory thalamic circuits and GABA(A) receptor function: putative mechanisms in tinnitus pathology. Hear Res 349:197–207

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Cortada M, Levano S, Bodmer D (2017) Brimonidine protects auditory hair cells from in vitro-induced toxicity of gentamicin. Audiol Neurootol 22:125–134

    Article  CAS  PubMed  Google Scholar 

  • Craske MG, Stein MB (2016) Anxiety. Lancet 388:3048–3059

    Article  PubMed  Google Scholar 

  • Crawley BK, Keithley EM (2011) Effects of mitochondrial mutations on hearing and cochlear pathology with age. Hear Res 280:201–208

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Curtis J (1841) Tinnitus aurium. Lancet 36:828–829

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Eggermont JJ (1990) On the pathophysiology of tinnitus; a review and a peripheral model. Hear Res 48:111–123

    Article  CAS  PubMed  Google Scholar 

  • Eggermont JJ, Roberts LE (2015) Tinnitus: animal models and findings in humans. Cell Tissue Res 361:311–336

    Article  PubMed  Google Scholar 

  • El Ganzoury MM, Kamel TB, Khalil LH, Seliem AM (2012) Cochlear dysfunction in children following cardiac bypass surgery. ISRN Pediatr 2012:375038

    Article  PubMed  PubMed Central  Google Scholar 

  • Evans P, Halliwell B (1999) Free radicals and hearing. Cause, consequence, and criteria. Ann N Y Acad Sci 884:19–40

    Article  CAS  PubMed  Google Scholar 

  • Figueiredo RR, Azevedo AA, Penido NO (2016) Positive association between tinnitus and arterial hypertension. Front Neurol 7:171

    Article  PubMed  PubMed Central  Google Scholar 

  • Figueiredo RR, De Azevedo AA, Penido Nde O (2015) Tinnitus and arterial hypertension: a systematic review. Eur Arch Otorhinolaryngol 272:3089–3094

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Fortier C, Selye H (1949) Adrenocorticotrophic effect of stress after severance of the hypothalamo-hypophyseal pathways. Am J Physiol 159:433–439. illust

    Article  CAS  PubMed  Google Scholar 

  • Frye MD, Ryan AF, Kurabi A (2019) Inflammation associated with noise-induced hearing loss. J Acoust Soc Am 146:4020

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Gupta MA, Jarosz P, Gupta AK (2017) Posttraumatic stress disorder (PTSD) and the dermatology patient. Clin Dermatol 35:260–266

    Article  PubMed  Google Scholar 

  • Haider HF, Bojić T, Ribeiro SF, Paço J, Hall DA, Szczepek AJ (2018) Pathophysiology of subjective tinnitus: triggers and maintenance. Front Neurosci 12

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hébert S, Lupien SJ (2007) The sound of stress: blunted cortisol reactivity to psychosocial stress in tinnitus sufferers. Neurosci Lett 411:138–142

    Article  PubMed  CAS  Google Scholar 

  • Heim C, Nemeroff CB (2009) Neurobiology of posttraumatic stress disorder. CNS Spectr 14:13–24

    PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Horner K (2003) The emotional ear in stress. Neurosci Biobehav Rev 27:437–446

    Article  CAS  PubMed  Google Scholar 

  • Hu BH, Zhang C, Frye MD (2018) Immune cells and non-immune cells with immune function in mammalian cochleae. Hear Res 362:14–24

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Jastreboff PJ (1990) Phantom auditory perception (tinnitus): mechanisms of generation and perception. Neurosci Res 8:221–254

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Kapolowicz MR, Thompson LT (2020) Plasticity in limbic regions at early time points in experimental models of tinnitus. Front Syst Neurosci 13

    Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Kokotas H, Petersen MB, Willems PJ (2007) Mitochondrial deafness. Clin Genet 71:379–391

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Leaver AM, Seydell-Greenwald A, Rauschecker JP (2016) Auditory-limbic interactions in chronic tinnitus: challenges for neuroimaging research. Hear Res 334:49–57

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Levin SG, Godukhin OV (2017) Modulating effect of cytokines on mechanisms of synaptic plasticity in the brain. Biochemistry (Mosc) 82:264–274

    Article  CAS  Google Scholar 

  • Liberman MC, Kujawa SG (2017) Cochlear synaptopathy in acquired sensorineural hearing loss: manifestations and mechanisms. Hear Res 349:138–147

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mazurek B, Boecking B, Brueggemann P (2019) Association between stress and tinnitus-new aspects. Otol Neurotol 40:e467–e473

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Mazurek B, Szczepek A, Hebert S (2015) Stress and tinnitus. HNO 63:258–265

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Michaelides A, Zis P (2019) Depression, anxiety and acute pain: links and management challenges. Postgrad Med 131:438–444

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  PubMed Central  Google Scholar 

  • Oyola MG, Handa RJ (2017) Hypothalamic-pituitary-adrenal and hypothalamic-pituitary-gonadal axes: sex differences in regulation of stress responsivity. Stress 20:476–494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pickles JO (2004) Mutation in mitochondrial DNA as a cause of presbyacusis. Audiol Neurootol 9:23–33

    Article  CAS  PubMed  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rauschecker JP, Leaver AM, Mühlau M (2010) Tuning out the noise: limbic-auditory interactions in tinnitus. Neuron 66:819–826

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ryan D, Bauer CA (2016) Neuroscience of tinnitus. Neuroimaging Clin N Am 26:187–196

    Article  PubMed  Google Scholar 

  • Rybak LP, Mukherjea D, Ramkumar V (2019) Mechanisms of cisplatin-induced ototoxicity and prevention. Semin Hear 40:197–204

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Sahley TL, Nodar RH (2001) A biochemical model of peripheral tinnitus. Hear Res 152:43–54

    Article  CAS  PubMed  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Selye H (1937) The significance of the adrenals for adaptation. Science 85:247–248

    Article  CAS  PubMed  Google Scholar 

  • Selye H (1950) Stress and the general adaptation syndrome. Br Med J 1:1383–1392

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Selye H, Fortier C (1949) Adaptive reactions to stress. Res Publ Assoc Res Nerv Ment Dis 29:3–18

    CAS  PubMed  Google Scholar 

  • Sheth S, Mukherjea D, Rybak LP, Ramkumar V (2017) Mechanisms of cisplatin-induced ototoxicity and otoprotection. Front Cell Neurosci 11:338

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shirane M, Harrison RV (1987) The effects of hypoxia on sensory cells of the cochlea in chinchilla. Scanning Microsc 1:1175–1183

    CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Sliwinska-Kowalska M, Davis A (2012) Noise-induced hearing loss. Noise Health 14:274–280

    Article  PubMed  Google Scholar 

  • Szczepek A, Mazurek B (2017) Tinnitus and stress. Springer, Cham

    Book  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Waechter S, Brännström KJ (2015) The impact of tinnitus on cognitive performance in normal-hearing individuals. Int J Audiol 54(11):845–851

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Yao X, Rarey KE (1996) Localization of the mineralocorticoid receptor in rat cochlear tissue. Acta Otolaryngol 116:493–496

    Article  CAS  PubMed  Google Scholar 

  • Yip J, Geng X, Shen J, Ding Y (2016) Cerebral gluconeogenesis and diseases. Front Pharmacol 7:521

    PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Zöger S, Svedlund J, Holgers KM (2006) Relationship between tinnitus severity and psychiatric disorders. Psychosomatics 47:282–288

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Agnieszka J. Szczepek .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2021 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Szczepek, A.J., Mazurek, B. (2021). Neurobiology of Stress-Induced Tinnitus. In: Searchfield, G.D., Zhang, J. (eds) The Behavioral Neuroscience of Tinnitus. Current Topics in Behavioral Neurosciences, vol 51. Springer, Cham. https://doi.org/10.1007/7854_2020_215

Download citation

Publish with us

Policies and ethics