The neuropsychiatry of tinnitus: A circuit-based approach to the causes and treatments available

Journal of Neurology, Neurosurgery and Psychiatry

Volumn 85, Issue 10, 2014, Pages 1138-1144

  Minen, Mia T ^a,b   Camprodon, Joan ^a,b   Nehme, Romy ^a   Chemali, Zeina ^a,b,c  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c MASSACHUSETTS EYE AND EAR INFIRMARY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIDEPRESSANT AGENT; BENZODIAZEPINE DERIVATIVE; MOOD STABILIZER; NEUROLEPTIC AGENT; PSYCHOTROPIC AGENT;

ACUPUNCTURE; ANXIETY DISORDER; BRAIN DECOMPRESSION; BRAIN ELECTROPHYSIOLOGY; COGNITIVE BEHAVIORAL THERAPY; COGNITIVE DEFECT; DISEASE ASSOCIATION; ELECTROENCEPHALOGRAPHY; HABITUATION; HEADACHE; HUMAN; MAGNETOENCEPHALOGRAPHY; MOOD DISORDER; NERVE CELL NETWORK; NEUROIMAGING; NEUROPATHOLOGY; NEUROPSYCHIATRY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PERSONALITY DISORDER; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; REVIEW; SLEEP DISORDER; STEREOTACTIC RADIOSURGERY; STRESS; TINNITUS; TRANSCRANIAL MAGNETIC STIMULATION; TRAUMATIC BRAIN INJURY; AUDITORY NERVOUS SYSTEM; BEHAVIOR THERAPY; BEHAVIOURAL DISORDER; BIOLOGICAL MODEL; BRAIN; COGNITION; MENTAL DISEASE; NEURORADIOLOGY; NEUROTOLOGY; PATHOPHYSIOLOGY;

BEHAVIOURAL DISORDER; COGNITION; NEUROOTOLOGY; NEUROPSYCHIATRY; NEURORADIOLOGY;

AUDITORY PATHWAYS; BEHAVIOR THERAPY; BRAIN; HUMANS; MENTAL DISORDERS; MODELS, NEUROLOGICAL; NEUROIMAGING; PSYCHOTROPIC DRUGS; TINNITUS; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 84908317293     PISSN: 00223050     EISSN: 1468330X     Source Type: Journal    
DOI: 10.1136/jnnp-2013-307339     Document Type: Review

References (127)

1. Davis A, Rafaie A. Epidemiology of tinnitus. San Diego, California: Singulair; 2000:1-23.
2. House JW Treatment of severe tinnitus with biofeedback training. Laryngoscope 1978; 88:406-12.
3. House PR Personality of the tinnitus patient. Ciba Found Symp 1981; 85:193-203.
4. Moller AR Pathophysiology of tinnitus. Ann Otol Rhinol Laryngol 1984; 93(1 Pt 1):39-44.
5. Barnea G, Attias J, Gold S, et al. Tinnitus with normal hearing sensitivity: extended high-frequency audiometry and auditory-nerve brain-stem-evoked responses. Audiology 1990; 29:36-45.
6. Langguth B, Kreuzer PM, Kleinjung T, et al. Tinnitus: causes and clinical management. Lancet Neurol 2013; 12:920-30.
7. Matthies C, Samii M. Management of 1000 vestibular schwannomas (acoustic neuromas): clinical presentation. Neurosurgery 1997; 40:1-9;discussion 9-10
8. Vasconcelos, Carlos Augusto Carvalho de, Fazan VPS, et al. Transmission electron microscopy studies of the vestibulocochlear nerve in chronic diabetic rats. Int J Morphol 2011; 29:272-7.
9. Jastreboff PJ, Hazell JW. A neurophysiological approach to tinnitus: clinical implications. Br J Audiol 1993; 27:7-17.
10. Amoodi HA, Mick PT, Shipp DB, et al. The effects of unilateral cochlear implantation on the tinnitus handicap inventory and the influence on quality of life. Laryngoscope 2011; 121:1536-40.
11. Bledsoe SC Jr, Koehler S, Tucci DL, et al. Ventral cochlear nucleus responses to contralateral sound are mediated by commissural and olivocochlear pathways. J Neurophysiol 2009; 102:886-900.
12. Eggermont JJ, Kenmochi M. Salicylate and quinine selectively increase spontaneous firing rates in secondary auditory cortex. Hear Res 1998; 117:149-60.
13. Eggermont JJ, Roberts LE. The neuroscience of tinnitus. Trends Neurosci 2004; 27:676-82.
14. Kaltenbach JA Summary of evidence pointing to a role of the dorsal cochlear nucleus in the etiology of tinnitus. Acta Otolaryngol Suppl 2006; (556):20-6.
15. Ma WL, Hidaka H, May BJ. Spontaneous activity in the inferior colliculus of CBA/J mice after manipulations that induce tinnitus. Hear Res 2006; 212:9-21.
16. Mulders WH, Robertson D. Hyperactivity in the auditory midbrain after acoustic trauma: dependence on cochlear activity. Neuroscience 2009; 164:733-46.
17. Norena AJ, Eggermont JJ. Changes in spontaneous neural activity immediately after an acoustic trauma: implications for neural correlates of tinnitus. Hear Res 2003; 183:137-53.
18. Dong S, Mulders WH, Rodger J, et al. Acoustic trauma evokes hyperactivity and changes in gene expression in guinea-pig auditory brainstem. Eur J Neurosci 2010; 31:1616-28.
19. Syka J. Plastic changes in the central auditory system after hearing loss, restoration of function, and during learning. Physiol Rev 2002; 82:601-36.
20. Syka J, Rybalko N, Popelar J. Enhancement of the auditory cortex evoked responses in awake guinea pigs after noise exposure. Hear Res 1994; 78:158-68.
21. Popelar J, Syka J, Berndt H. Effect of noise on auditory evoked responses in awake guinea pigs. Hear Res 1987; 26:239-47.
22. Wang J, McFadden SL, Caspary D, et al. Gamma-aminobutyric acid circuits shape response properties of auditory cortex neurons. Brain Res 2002; 944:219-31.
23. Foeller E, Vater M, Kossl M. Laminar analysis of inhibition in the gerbil primary auditory cortex. J Assoc Res Otolaryngol 2001; 2:279-96.
24. Kanold PO, Young ED. Proprioceptive information from the pinna provides somatosensory input to cat dorsal cochlear nucleus. J Neurosci 2001; 21:7848-58.
25. Levine RA Somatic (craniocervical) tinnitus and the dorsal cochlear nucleus hypothesis. Am J Otolaryngol 1999; 20:351-62.
26. Pinchoff RJ, Burkard RF, Salvi RJ, et al. Modulation of tinnitus by voluntary jaw movements. Am J Otol 1998; 19:785-9.
27. Shore S, Zhou J, Koehler S. Neural mechanisms underlying somatic tinnitus. Prog Brain Res 2007; 166:107-23.
28. Shore SE Sensory nuclei in tinnitus. In: Snow JB, ed. Tinnitus:Theory and management. Ontario, CA: Decker, 2005:125-41.
29. Mazurek B, Haupt H, Olze H, et al. Stress and tinnitus-from bedside to bench and back. Front Syst Neurosci 2012; 6:47.
30. Hebert S, Paiement P, Lupien SJ. A physiological correlate for the intolerance to both internal and external sounds. Hear Res 2004; 190:1-9.
31. Ashton H, Reid K, Marsh R, et al. High frequency localised "hot spots" in temporal lobes of patients with intractable tinnitus: a quantitative electroencephalographic (QEEG) study. Neurosci Lett 2007; 426:23-8.
32. Vanneste S, De Ridder D. The auditory and non-auditory brain areas involved in tinnitus. an emergent property of multiple parallel overlapping subnetworks. Front Syst Neurosci 2012; 6:31.
33. Gu JW, Herrmann BS, Levine RA, et al. Brainstem auditory evoked potentials suggest a role for the ventral cochlear nucleus in tinnitus. J Assoc Res Otolaryngol 2012; 13:819-33.
34. Cassvan A, Ralescu S, Moshkovski FG, et al. Brainstem auditory evoked potential studies in patients with tinnitus and/or vertigo. Arch Phys Med Rehabil 1990; 71:583-6.
35. Muhlau M, Rauschecker JP, Oestreicher E, et al. Structural brain changes in tinnitus. Cereb Cortex 2006; 16:1283-8.
36. Landgrebe M, Langguth B, Rosengarth K, et al. Structural brain changes in tinnitus: grey matter decrease in auditory and non-auditory brain areas. Neuroimage 2009; 46:213-18.
37. Giraud AL, Chery-Croze S, Fischer G, et al. A selective imaging of tinnitus. Neuroreport 1999; 10:1-5.
38. Lockwood AH, Salvi RJ, Coad ML, et al. The functional neuroanatomy of tinnitus: evidence for limbic system links and neural plasticity. Neurology 1998; 50:114-20.
39. Mirz F, Pedersen B, Ishizu K, et al. Positron emission tomography of cortical centers of tinnitus. Hear Res 1999; 134:133-44.
40. Mirz F, Gjedde A, Ishizu K, et al. Cortical networks subserving the perception of tinnitus-a PET study. Acta Otolaryngol Suppl 2000; 543:241-3.
41. Plewnia C, Reimold M, Najib A, et al. Moderate therapeutic efficacy of positron emission tomography-navigated repetitive transcranial magnetic stimulation for chronic tinnitus: a randomised, controlled pilot study. J Neurol Neurosurg Psychiatry 2007; 78:152-6.
42. Lanting CP, de Kleine E, van Dijk P. Neural activity underlying tinnitus generation: results from PET and fMRI. Hear Res 2009; 255:1-13.
43. Roberts LE, Eggermont JJ, Caspary DM, et al. Ringing ears: the neuroscience of tinnitus. J Neurosci 2010; 30:14972-9.
44. Melcher JR, Levine RA, Bergevin C, et al. The auditory midbrain of people with tinnitus: abnormal sound-evoked activity revisited. Hear Res 2009; 257:63-74.
45. Maudoux A, Lefebvre P, Cabay JE, et al. Connectivity graph analysis of the auditory resting state network in tinnitus. Brain Res 2012; 1485:10-21.
46. Kim JY, Kim YH, Lee S, et al. Alteration of functional connectivity in tinnitus brain revealed by resting-state fMRI? A pilot study. Int J Audiol 2012; 51:413-17.
47. Burton H, Wineland A, Bhattacharya M, et al. Altered networks in bothersome tinnitus: a functional connectivity study. BMC Neurosci 2012; 13:3.-2202-13-3.
48. Schlee W, Weisz N, Bertrand O, et al. Using auditory steady state responses to outline the functional connectivity in the tinnitus brain. PLoS ONE 2008; 3: e3720.
49. Price JL, Drevets WC. Neurocircuitry of mood disorders. Neuropsychopharmacology 2010; 35:192-216.
50. Ploghaus A, Tracey I, Gati JS, et al. Dissociating pain from its anticipation in the human brain. Science 1999; 284:1979-81.
51. Wager TD, Rilling JK, Smith EE, et al. Placebo-induced changes in FMRI in the anticipation and experience of pain. Science 2004; 303:1162-7.
52. Marciano E, Carrabba L, Giannini P, et al. Psychiatric comorbidity in a population of outpatients affected by tinnitus. Int J Audiol 2003; 42:4-9.
53. Belli S, Belli H, Bahcebasi T, et al. Assessment of psychopathological aspects and psychiatric comorbidities in patients affected by tinnitus. Eur Arch Otorhinolaryngol 2008; 265:279-85.
54. Hebert S, Canlon B, Hasson D. Emotional exhaustion as a predictor of tinnitus. Psychother Psychosom 2012; 81:324-6.
55. Hebert S, Canlon B, Hasson D, et al. Tinnitus severity is reduced with reduction of depressive mood-a prospective population study in sweden. PLoS ONE 2012; 7: e37733.
56. Lewis JE, Stephens SD, McKenna L. Tinnitus and suicide. Clin Otolaryngol Allied Sci 1994; 19:50-4.
57. Jacobson GP, McCaslin DL. A search for evidence of a direct relationship between tinnitus and suicide. J Am Acad Audiol 2001; 12:493-6.
58. Shargorodsky J, Curhan GC, Farwell WR. Prevalence and characteristics of tinnitus among US adults. Am J Med 2010; 123:711-18.
59. Hiller W, Janca A, Burke KC. Association between tinnitus and somatoform disorders. J Psychosom Res 1997; 43:613-24.
60. Baigi A, Oden A, Almlid-Larsen V, et al. Tinnitus in the general population with a focus on noise and stress: a public health study. Ear Hear 2011; 32:787-9.
61. Hasson D, Theorell T, Wallen MB, et al. Stress and prevalence of hearing problems in the Swedish working population. BMC Public Health 2011; 11:130.
62. Falkenberg ES, Tungland OP, Skollerud S. Habituation therapy of chronic distressing tinnitus: a presentation of a treatment prpgramme and an evaluation of its effects. Audiol Med 2003; 1:132-7.
63. McEwen BS, Wingfield JC. The concept of allostasis in biology and biomedicine. Horm Behav 2003; 43:2-15.
64. Axelsson A, Ringdahl A. Tinnitus-a study of its prevalence and characteristics. Br J Audiol 1989; 23:53-62.
65. Jakes SC, Hallam RS, Chambers C, et al. A factor analytical study of tinnitus complaint behaviour. Audiology 1985; 24:195-206.
66. Tyler RS, Baker LJ, Armstrong-Bednall G. Difficulties experienced by hearing-aid candidates and hearing-aid users. Br J Audiol 1983; 17:191-201.
67. Alster J, Shemesh Z, Ornan M, et al. Sleep disturbance associated with chronic tinnitus. Biol Psychiatry 1993; 34:84-90.
68. Burgos I, Feige B, Hornyak M, et al. Chronic tinnitus and associated sleep disturbance. Somnologie 2005; 9:133-8.
69. Cronlein T, Langguth B, Geisler P, et al. Tinnitus and insomnia. Prog Brain Res 2007; 166:227-33.
70. Hebert S, Fullum S, Carrier J. Polysomnographic and quantitative electroencephalographic correlates of subjective sleep complaints in chronic tinnitus. J Sleep Res 2011; 20(1 Pt 1):38-44.
71. Bauer CA, Brozoski TJ. Assessing tinnitus and prospective tinnitus therapeutics using a psychophysical animal model. J Assoc Res Otolaryngol 2001; 2:54-64.
72. Fausti SA, Wilmington DJ, Gallun FJ, et al. Auditory and vestibular dysfunction associated with blast-related traumatic brain injury. J Rehabil Res Dev 2009; 46:797-810.
73. Folmer RL, Griest SE. Chronic tinnitus resulting from head or neck injuries. Laryngoscope 2003; 113:821-7.
74. Hinton DE, Chhean D, Pich V, et al. Tinnitus among cambodian refugees: relationship to PTSD severity. J Trauma Stress 2006; 19:541-6.
75. Langguth B, Landgrebe M, Kleinjung T, et al. Tinnitus and depression. World J Biol Psychiatry 2011; 12:489-500.
76. Boniver R. Temporomandibular joint dysfunction in whiplash injuries: association with tinnitus and vertigo. Int Tinnitus J 2002; 8:129-31.
77. Kreuzer PM, Landgrebe M, Schecklmann M, et al. The TRI Database Study Group. Trauma-associated tinnitus: Audiological, demographic and clinical characteristics. PLoS ONE 2012; 7:e45599.
78. Farri A, Enrico A, Lacilla M, et al. Tinnitus during headache: clinical-instrumental evaluation. Acta Otorhinolaryngol Ital 1999; 19:70-5.
79. Sturzenegger MH, Meienberg O. Basilar artery migraine: a follow-up study of 82 cases. Headache 1985; 25:408-15.
80. Volcy M, Sheftell FD, Tepper SJ, et al. Tinnitus in migraine: an allodynic symptom secondary to abnormal cortical functioning? Headache 2005; 45:1083-7.
81. Lee H, Whitman GT, Lim JG, et al. Hearing symptoms in migrainous infarction. Arch Neurol 2003; 60:113-16.
82. Digre KB Idiopathic intracranial hypertension headache. Curr Pain Headache Rep 2002; 6:217-25.
83. Wang SJ, Silberstein SD, Patterson S, et al. Idiopathic intracranial hypertension without papilledema: a case-control study in a headache center. Neurology 1998; 51:245-9.
84. Llinas RR, Ribary U, Jeanmonod D, et al. Thalamocortical dysrhythmia: a neurological and neuropsychiatric syndrome characterized by magnetoencephalography. Proc Natl Acad Sci USA 1999; 96:15222-7.
85. Muhlnickel W, Elbert T, Taub E, et al. Reorganization of auditory cortex in tinnitus. Proc Natl Acad Sci USA 1998; 95:10340-3.
86. Andersson G, Eriksson J, Lundh LG, et al. Tinnitus and cognitive interference: a stroop paradigm study. J Speech Lang Hear Res 2000; 43:1168-73.
87. Stevens C, Walker G, Boyer M, et al. Severe tinnitus and its effect on selective and divided attention. Int J Audiol 2007; 46:208-16.
88. Rossiter S, Stevens C, Walker G. Tinnitus and its effect on working memory and attention. J Speech Lang Hear Res 2006; 49:150-60.
89. Hallam RS, McKenna L, Shurlock L. Tinnitus impairs cognitive efficiency. Int J Audiol 2004; 43:218-26.
90. Das SK, Wineland A, Kallogjeri D, et al. Cognitive speed as an objective measure of tinnitus. Laryngoscope 2012; 122:2533-8.
91. Kim YH, Jung HJ, Kang SI, et al. Tinnitus in children: association with stress and trait anxiety. Laryngoscope 2012; 122:2279-84.
92. Bulbul SF, Muluk NB, Cakir EP, et al. Subjective tinnitus and hearing problems in adolescents. Int J Pediatr Otorhinolaryngol 2009; 73:1124-31.
93. Shargorodsky J, Curhan SG, Curhan GC, et al. Change in prevalence of hearing loss in US adolescents. JAMA 2010; 304:772-8.
94. Gananca MM, Caovilla HH, Gananca FF, et al. Clonazepam in the pharmacological treatment of vertigo and tinnitus. Int Tinnitus J 2002; 8:50-3.
95. Jalali MM, Kousha A, Naghavi SE, et al. The effects of alprazolam on tinnitus: a cross-over randomized clinical trial. Med Sci Monit 2009; 15:PI55-60.
96. Panford-Walsh R, Singer W, Ruttiger L, et al. Midazolam reverses salicylate-induced changes in brain-derived neurotrophic factor and arg3.1 expression: Implications for tinnitus perception and auditory plasticity. Mol Pharmacol 2008; 74:595-604.
97. Robinson SK, Viirre ES, Bailey KA, et al. Randomized placebo-controlled trial of a selective serotonin reuptake inhibitor in the treatment of nondepressed tinnitus subjects. Psychosom Med 2005; 67:981-8.
98. Dobie RA, Sakai CS, Sullivan MD, et al. Antidepressant treatment of tinnitus patients: report of a randomized clinical trial and clinical prediction of benefit. Am J Otol 1993; 14:18-23.
99. Zoger S, Svedlund J, Holgers KM. The effects of sertraline on severe tinnitus suffering-a randomized, double-blind, placebo-controlled study. J Clin Psychopharmacol 2006; 26:32-9.
100. Brantberg K. Paroxysmal staccato tinnitus: a carbamazepine responsive hyperactivity dysfunction symptom of the eighth cranial nerve. J Neurol Neurosurg Psychiatry 2010; 81:451-5.
101. Pondrom MF, Brahm NC. Venlafaxine-associated tinnitus. Am J Health Syst Pharm 2009; 66:1606, 1608.
102. Ahmad S. Venlafaxine and severe tinnitus. Am Fam Physician 1995; 51:1830.
103. De Marinis M, Santilli V. Tinnitus in postherpetic neuralgia. J Headache Pain 2010; 11:83-4.
104. Clewes J. A case report of onset of tinnitus following discontinuation of antidepressant and a review of the literature. Prim Care Companion CNS Disord 2012; 14:PCC.11br01218. Epub 2012 Feb 16.
105. Lopez-Gonzalez MA, Moliner-Peiro F, Alfaro-Garcia J, et al. Sulpiride plus hydroxyzine decrease tinnitus perception. Auris Nasus Larynx 2007; 34:23-7.
106. Bauer CA, Brozoski TJ. Effect of gabapentin on the sensation and impact of tinnitus. Laryngoscope 2006; 116:675-81.
107. Mansbach AL, Freyens P. Tinnitus: current data and treatment with sodium valproate. Acta Otorhinolaryngol Belg 1983; 37:697-705.
108. Hulshof JH, Vermeij P. The value of carbamazepine in the treatment of tinnitus. ORL J Otorhinolaryngol Relat Spec 1985; 47:262-6.
109. Menkes DB, Larson PM. Sodium valproate for tinnitus. J Neurol Neurosurg Psychiatry 1998; 65:803.
110. Piccirillo JF, Finnell J, Vlahiotis A, et al. Relief of idiopathic subjective tinnitus: is gabapentin effective? Arch Otolaryngol Head Neck Surg 2007; 133:390-7.
111. She W, Dai Y, Du X, et al. Treatment of subjective tinnitus: a comparative clinical study of intratympanic steroid injection vs. oral carbamazepine. Med Sci Monit 2009; 15:PI35-9.
112. Zheng Y, Hooton K, Smith PF, et al. Carbamazepine reduces the behavioural manifestations of tinnitus following salicylate treatment in rats. Acta Otolaryngol 2008; 128:48-52.
113. Witsell DL, Hannley MT, Stinnet S, et al. Treatment of tinnitus with gabapentin: a pilot study. Otol Neurotol 2007; 28:11-15.
114. Hoekstra CE, Rynja SP, van Zanten GA, et al. Anticonvulsants for tinnitus. Cochrane Database Syst Rev 2011; (7):CD007960.
115. Hesser H, Weise C, Westin VZ, et al. A systematic review and meta-analysis of randomized controlled trials of cognitive-behavioral therapy for tinnitus distress. Clin Psychol Rev 2011; 31:545-53.
116. Falkenberg ES, Wie OB. Anxiety and depression in tinnitus patients: 5-year follow-up assessment after completion of habituation therapy. Int J Otolaryngol 2012; 2012:375460.
117. Rogha M, Rezvani M, Khodami AR. The effects of acupuncture on the inner ear originated tinnitus. J Res Med Sci 2011; 16:1217-23.
118. Bennett MH, Kertesz T, Perleth M, et al. Hyperbaric oxygen for idiopathic sudden sensorineural hearing loss and tinnitus. Cochrane Database Syst Rev 2012; 10: CD004739.
119. Hoare DJ, Kowalkowski VL, Kang S, et al. Systematic review and meta-analyses of randomized controlled trials examining tinnitus management. Laryngoscope 2011; 121:1555-64.
120. Soleymani T, Pieton D, Pezeshkian P, et al. Surgical approaches to tinnitus treatment: a review and novel approaches. Surg Neurol Int 2011; 2:154.
121. Plewnia C, Bartels M, Gerloff C. Transient suppression of tinnitus by transcranial magnetic stimulation. Ann Neurol 2003; 53:263-6.
122. Eichhammer P, Langguth B, Marienhagen J, et al. Neuronavigated repetitive transcranial magnetic stimulation in patients with tinnitus: A short case series. Biol Psychiatry 2003; 54:862-5.
123. Plewnia C, Reimold M, Najib A, et al. Dose-dependent attenuation of auditory phantom perception (tinnitus) by PET-guided repetitive transcranial magnetic stimulation. Hum Brain Mapp 2007; 28:238-46.
124. Vanneste S, van der Loo E, Plazier M, et al. Parietal double-cone coil stimulation in tinnitus. Exp Brain Res 2012; 221:337-43.
125. De Ridder D, Song JJ, Vanneste S. Frontal cortex TMS for tinnitus. Brain Stimul 2013; 6:355-62.
126. Song JJ, Vanneste S, Van de Heyning P, et al. Transcranial direct current stimulation in tinnitus patients: a systemic review and meta-analysis. ScientificWorldJournal 2012; 2012:427941.
127. De Ridder D, Vanneste S, Menovsky T, et al. Surgical brain modulation for tinnitus: the past, present and future. J Neurosurg Sci 2012; 56:323-40.