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Semin Hear 2014; 35(02): 131-144
DOI: 10.1055/s-0034-1372529
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Tinnitus: Mechanisms Induced from Human Functional Neuroimaging Studies

Audrey Maudoux
1   Cyclotron Research Centre, University of Liège (ULg)
2   Department of Oto-Rhino-Laryngology, Head and Neck Surgery, Erasme Hospital, University of Brussels (ULB), Brussels, Belgium
,
Philippe Lefebvre
3   Department of Oto-Rhino-Laryngology, Head and Neck Surgery, University Hospital of Liège, University of Liège (ULg), Liège, Belgium
› Author Affiliations
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Publication History

Publication Date:
29 April 2014 (online)

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Abstract

The past 15 years has provided an unprecedented collection of discoveries that bear upon our scientific understanding of the pathophysiology of tinnitus. Highlighted among these discoveries is the fact that changes of brain activity accompany tinnitus. All tinnitus theories refer to common concepts. First, peripheral lesions in the cochlea or the auditory nerve produce dysfunctional input to central auditory structures and induce changes in the auditory system. Associated to plastic changes in central auditory structures, neuroimaging studies show signs of the implication of extra-auditory regions in tinnitus pathophysiology. Collectively, these observations have led to important new insights into the understanding of tinnitus. Here, we review the advances made in this field of research using human functional neuroimaging methods.

Keywords

Neuroimaging methods - tinnitus - functional magnetic resonance imaging - positron emission tomography - electroencephalography - magnetoencephalography - connectivity - resting state
 

  • References

  • 1 Joel SE, Caffo BS, van Zijl PC, Pekar JJ. On the relationship between seed-based and ICA-based measures of functional connectivity. Magn Reson Med 2011; 66 (3) 644-657
    CrossrefPubMedGoogle Scholar
  • 2 Saunders JC. The role of central nervous system plasticity in tinnitus. J Commun Disord 2007; 40 (4) 313-334
    CrossrefPubMedGoogle Scholar
  • 3 Van den Bergh O, Winters W, Devriese S, Van Diest I. Learning subjective health complaints. Scand J Psychol 2002; 43 (2) 147-152
    CrossrefPubMedGoogle Scholar
  • 4 Husain FT, Medina RE, Davis CW , et al. Neuroanatomical changes due to hearing loss and chronic tinnitus: a combined VBM and DTI study. Brain Res 2011; 1369: 74-88
    CrossrefPubMedGoogle Scholar
  • 5 Noreña AJ, Eggermont JJ. Changes in spontaneous neural activity immediately after an acoustic trauma: implications for neural correlates of tinnitus. Hear Res 2003; 183 (1–2) 137-153
    CrossrefPubMedGoogle Scholar
  • 6 Seki S, Eggermont JJ. Changes in spontaneous firing rate and neural synchrony in cat primary auditory cortex after localized tone-induced hearing loss. Hear Res 2003; 180 (1–2) 28-38
    CrossrefPubMedGoogle Scholar
  • 7 Andersson G, Lyttkens L, Hirvelä C, Furmark T, Tillfors M, Fredrikson M. Regional cerebral blood flow during tinnitus: a PET case study with lidocaine and auditory stimulation. Acta Otolaryngol 2000; 120 (8) 967-972
    CrossrefPubMedGoogle Scholar
  • 8 Lockwood AH, Salvi RJ, Coad ML, Towsley ML, Wack DS, Murphy BW. The functional neuroanatomy of tinnitus: evidence for limbic system links and neural plasticity. Neurology 1998; 50 (1) 114-120
    CrossrefPubMedGoogle Scholar
  • 9 Giraud AL, Chéry-Croze S, Fischer G , et al. A selective imaging of tinnitus. Neuroreport 1999; 10 (1) 1-5
    CrossrefPubMedGoogle Scholar
  • 10 Osaki Y, Nishimura H, Takasawa M , et al. Neural mechanism of residual inhibition of tinnitus in cochlear implant users. Neuroreport 2005; 16 (15) 1625-1628
    CrossrefPubMedGoogle Scholar
  • 11 Reyes SA, Salvi RJ, Burkard RF , et al. Brain imaging of the effects of lidocaine on tinnitus. Hear Res 2002; 171 (1–2) 43-50
    CrossrefPubMedGoogle Scholar
  • 12 Lockwood AH, Wack DS, Burkard RF , et al. The functional anatomy of gaze-evoked tinnitus and sustained lateral gaze. Neurology 2001; 56 (4) 472-480
    CrossrefPubMedGoogle Scholar
  • 13 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 (3) 238-246
    CrossrefPubMedGoogle Scholar
  • 14 Eggermont JJ, Kenmochi M. Salicylate and quinine selectively increase spontaneous firing rates in secondary auditory cortex. Hear Res 1998; 117 (1–2) 149-160
    CrossrefPubMedGoogle Scholar
  • 15 Eggermont JJ, Roberts LE. The neuroscience of tinnitus. Trends Neurosci 2004; 27 (11) 676-682
    CrossrefPubMedGoogle Scholar
  • 16 Eggermont JJ. Tinnitus: neurobiological substrates. Drug Discov Today 2005; 10 (19) 1283-1290
    CrossrefPubMedGoogle Scholar
  • 17 Salvi RJ, Saunders SS, Gratton MA, Arehole S, Powers N. Enhanced evoked response amplitudes in the inferior colliculus of the chinchilla following acoustic trauma. Hear Res 1990; 50 (1–2) 245-257
    CrossrefPubMedGoogle Scholar
  • 18 Wang J, Ding D, Salvi RJ. Functional reorganization in chinchilla inferior colliculus associated with chronic and acute cochlear damage. Hear Res 2002; 168 (1–2) 238-249
    CrossrefPubMedGoogle Scholar
  • 19 Melcher JR, Sigalovsky IS, Guinan Jr JJ, Levine RA. Lateralized tinnitus studied with functional magnetic resonance imaging: abnormal inferior colliculus activation. J Neurophysiol 2000; 83 (2) 1058-1072
    CrossrefPubMedGoogle Scholar
  • 20 Melcher JR, Levine RA, Bergevin C, Norris B. The auditory midbrain of people with tinnitus: abnormal sound-evoked activity revisited. Hear Res 2009; 257 (1–2) 63-74
    CrossrefPubMedGoogle Scholar
  • 21 Lanting CP, De Kleine E, Bartels H, Van Dijk P. Functional imaging of unilateral tinnitus using fMRI. Acta Otolaryngol 2008; 128 (4) 415-421
    CrossrefPubMedGoogle Scholar
  • 22 Lanting CP, de Kleine E, Eppinga RN, van Dijk P. Neural correlates of human somatosensory integration in tinnitus. Hear Res 2010; 267 (1–2) 78-88
    CrossrefPubMedGoogle Scholar
  • 23 Smits M, Kovacs S, de Ridder D, Peeters RR, van Hecke P, Sunaert S. Lateralization of functional magnetic resonance imaging (fMRI) activation in the auditory pathway of patients with lateralized tinnitus. Neuroradiology 2007; 49 (8) 669-679
    CrossrefPubMedGoogle Scholar
  • 24 Husain FT, Pajor NM, Smith JF , et al. Discrimination task reveals differences in neural bases of tinnitus and hearing impairment. PLoS ONE 2011; 6 (10) e26639
    CrossrefPubMedGoogle Scholar
  • 25 Moller AR , et al. Tinnitus Retraining Therapy. In: Moller AR, Langguth B, Ridder D, Kleinjung T, , ed. Textbook of Tinnitus. New York, NY: Springer; 2011
    CrossrefGoogle Scholar
  • 26 Mirz F, Gjedde A, Ishizu K, Pedersen CB. Cortical networks subserving the perception of tinnitus—a PET study. Acta Otolaryngol Suppl 2000; 543: 241-243
    PubMedGoogle Scholar
  • 27 Leaver AM, Renier L, Chevillet MA, Morgan S, Kim HJ, Rauschecker JP. Dysregulation of limbic and auditory networks in tinnitus. Neuron 2011; 69 (1) 33-43
    CrossrefPubMedGoogle Scholar
  • 28 Petacchi A, Laird AR, Fox PT, Bower JM. Cerebellum and auditory function: an ALE meta-analysis of functional neuroimaging studies. Hum Brain Mapp 2005; 25 (1) 118-128
    CrossrefPubMedGoogle Scholar
  • 29 Mirz F, Pedersen B, Ishizu K , et al. Positron emission tomography of cortical centers of tinnitus. Hear Res 1999; 134 (1–2) 133-144
    CrossrefPubMedGoogle Scholar
  • 30 Bauer CA, Kurt W, Sybert LT, Brozoski TJ. The cerebellum as a novel tinnitus generator. Hear Res 2013; 295: 130-139
    CrossrefPubMedGoogle Scholar
  • 31 Lanting CP, de Kleine E, van Dijk P. Neural activity underlying tinnitus generation: results from PET and fMRI. Hear Res 2009; 255 (1–2) 1-13
    CrossrefPubMedGoogle Scholar
  • 32 Fox MD, Raichle ME. Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 2007; 8 (9) 700-711
    CrossrefPubMedGoogle Scholar
  • 33 Bressler SL, Menon V. Large-scale brain networks in cognition: emerging methods and principles. Trends Cogn Sci 2010; 14 (6) 277-290
    CrossrefPubMedGoogle Scholar
  • 34 Rosazza C, Minati L. Resting-state brain networks: literature review and clinical applications. Neurol Sci 2011; 32 (5) 773-785
    CrossrefPubMedGoogle Scholar
  • 35 Demertzi A, Soddu A, Faymonville ME , et al. Hypnotic modulation of resting state fMRI default mode and extrinsic network connectivity. Prog Brain Res 2011; 193: 309-322
    PubMedGoogle Scholar
  • 36 Boveroux P, Vanhaudenhuyse A, Bruno MA , et al. Breakdown of within- and between-network resting state functional magnetic resonance imaging connectivity during propofol-induced loss of consciousness. Anesthesiology 2010; 113 (5) 1038-1053
    CrossrefPubMedGoogle Scholar
  • 37 Zhou J, Greicius MD, Gennatas ED , et al. Divergent network connectivity changes in behavioural variant frontotemporal dementia and Alzheimer's disease. Brain 2010; 133 (Pt 5) 1352-1367
    CrossrefPubMedGoogle Scholar
  • 38 Greicius MD, Srivastava G, Reiss AL, Menon V. Default-mode network activity distinguishes Alzheimer's disease from healthy aging: evidence from functional MRI. Proc Natl Acad Sci U S A 2004; 101 (13) 4637-4642
    CrossrefPubMedGoogle Scholar
  • 39 Greicius MD, Flores BH, Menon V , et al. Resting-state functional connectivity in major depression: abnormally increased contributions from subgenual cingulate cortex and thalamus. Biol Psychiatry 2007; 62 (5) 429-437
    CrossrefPubMedGoogle Scholar
  • 40 Vanhaudenhuyse A, Noirhomme Q, Tshibanda LJ , et al. Default network connectivity reflects the level of consciousness in non-communicative brain-damaged patients. Brain 2010; 133 (Pt 1) 161-171
    CrossrefPubMedGoogle Scholar
  • 41 Boly M, Phillips C, Tshibanda L , et al. Intrinsic brain activity in altered states of consciousness: how conscious is the default mode of brain function?. Ann N Y Acad Sci 2008; 1129: 119-129
    CrossrefPubMedGoogle Scholar
  • 42 Hunter MD, Eickhoff SB, Miller TW, Farrow TF, Wilkinson ID, Woodruff PW. Neural activity in speech-sensitive auditory cortex during silence. Proc Natl Acad Sci U S A 2006; 103 (1) 189-194
    CrossrefPubMedGoogle Scholar
  • 43 Dosenbach NU, Fair DA, Miezin FM , et al. Distinct brain networks for adaptive and stable task control in humans. Proc Natl Acad Sci U S A 2007; 104 (26) 11073-11078
    CrossrefPubMedGoogle Scholar
  • 44 Arnold W, Bartenstein P, Oestreicher E, Römer W, Schwaiger M. Focal metabolic activation in the predominant left auditory cortex in patients suffering from tinnitus: a PET study with [18F]deoxyglucose. ORL J Otorhinolaryngol Relat Spec 1996; 58 (4) 195-199
    CrossrefPubMedGoogle Scholar
  • 45 Wang H, Tian J, Yin D , et al. Regional glucose metabolic increases in left auditory cortex in tinnitus patients: a preliminary study with positron emission tomography. Chin Med J (Engl) 2001; 114 (8) 848-851
    PubMedGoogle Scholar
  • 46 Langguth B, Hajak G, Kleinjung T, Pridmore S, Sand P, Eichhammer P. Repetitive transcranial magnetic stimulation and chronic tinnitus. Acta Otolaryngol Suppl 2006; (556) 102-105
    PubMedGoogle Scholar
  • 47 Schecklmann M, Landgrebe M, Poeppl TB , et al. Neural correlates of tinnitus duration and distress: a positron emission tomography study. Hum Brain Mapp 2013; 34 (1) 233-240
    CrossrefPubMedGoogle Scholar
  • 48 Weisz N, Müller S, Schlee W, Dohrmann K, Hartmann T, Elbert T. The neural code of auditory phantom perception. J Neurosci 2007; 27 (6) 1479-1484
    CrossrefPubMedGoogle Scholar
  • 49 Weisz N, Moratti S, Meinzer M, Dohrmann K, Elbert T. Tinnitus perception and distress is related to abnormal spontaneous brain activity as measured by magnetoencephalography. PLoS Med 2005; 2 (6) e153
    CrossrefPubMedGoogle Scholar
  • 50 van den Heuvel MP, Mandl RC, Kahn RS, Hulshoff Pol HE. Functionally linked resting-state networks reflect the underlying structural connectivity architecture of the human brain. Hum Brain Mapp 2009; 30 (10) 3127-3141
    CrossrefPubMedGoogle Scholar
  • 51 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 (5) 413-417
    CrossrefPubMedGoogle Scholar
  • 52 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
    CrossrefPubMedGoogle Scholar
  • 53 Maudoux A, Lefebvre P, Cabay JE , et al. Auditory resting-state network connectivity in tinnitus: a functional MRI study. PLoS ONE 2012; 7 (5) e36222
    CrossrefPubMedGoogle Scholar
  • 54 Burton H, Wineland A, Bhattacharya M, Nicklaus J, Garcia KS, Piccirillo JF. Altered networks in bothersome tinnitus: a functional connectivity study. BMC Neurosci 2012; 13: 3
    CrossrefPubMedGoogle Scholar
  • 55 Wineland AM, Burton H, Piccirillo J. Functional connectivity networks in nonbothersome tinnitus. Otolaryngol Head Neck Surg 2012; 147 (5) 900-906
    CrossrefPubMedGoogle Scholar
  • 56 Schlee W, Hartmann T, Langguth B, Weisz N. Abnormal resting-state cortical coupling in chronic tinnitus. BMC Neurosci 2009; 10: 11
    CrossrefPubMedGoogle Scholar
  • 57 Vanneste S, Focquaert F, Van de Heyning P, De Ridder D. Different resting state brain activity and functional connectivity in patients who respond and not respond to bifrontal tDCS for tinnitus suppression. Exp Brain Res 2011; 210 (2) 217-227
    CrossrefPubMedGoogle Scholar
  • 58 Vanneste S, Plazier M, van der Loo E, Van de Heyning P, De Ridder D. The difference between uni- and bilateral auditory phantom percept. Clin Neurophysiol 2011; 122 (3) 578-587
    CrossrefPubMedGoogle Scholar
  • 59 Vanneste S, van de Heyning P, De Ridder D. The neural network of phantom sound changes over time: a comparison between recent-onset and chronic tinnitus patients. Eur J Neurosci 2011; 34 (5) 718-731
    CrossrefPubMedGoogle Scholar
  • 60 Vanneste S, Plazier M, van der Loo E, Van de Heyning P, De Ridder D. The differences in brain activity between narrow band noise and pure tone tinnitus. PLoS ONE 2010; 5 (10) e13618
    CrossrefPubMedGoogle Scholar
  • 61 Vanneste S, Plazier M, der Loo Ev, de Heyning PV, Congedo M, De Ridder D. The neural correlates of tinnitus-related distress. Neuroimage 2010; 52 (2) 470-480
    CrossrefPubMedGoogle Scholar
  • 62 van der Loo E, Gais S, Congedo M , et al. Tinnitus intensity dependent gamma oscillations of the contralateral auditory cortex. PLoS ONE 2009; 4 (10) e7396
    CrossrefPubMedGoogle Scholar
  • 63 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
    PubMedGoogle Scholar
  • 64 De Ridder D, Elgoyhen AB, Romo R, Langguth B. Phantom percepts: tinnitus and pain as persisting aversive memory networks. Proc Natl Acad Sci U S A 2011; 108 (20) 8075-8080
    CrossrefPubMedGoogle Scholar
  • 65 Schlee W , et al. A Global Brain Model of Tinnitus. In: Moller AR, Lorenz I, Hartmann T, Muller N, Schulz H, Weisz N, , ed. Textbook of Tinnitus. New York, NY: Springer; 2011
    CrossrefGoogle Scholar
  • 66 Dehaene S, Changeux JP, Naccache L, Sackur J, Sergent C. Conscious, preconscious, and subliminal processing: a testable taxonomy. Trends Cogn Sci 2006; 10 (5) 204-211
    CrossrefPubMedGoogle Scholar
  • 67 Dehaene S, Kerszberg M, Changeux JP. A neuronal model of a global workspace in effortful cognitive tasks. Proc Natl Acad Sci U S A 1998; 95 (24) 14529-14534
    CrossrefPubMedGoogle Scholar
  • 68 Schlee W, Mueller N, Hartmann T, Keil J, Lorenz I, Weisz N. Mapping cortical hubs in tinnitus. BMC Biol 2009; 7: 80
    CrossrefPubMedGoogle Scholar
  • 69 Ueyama T, Donishi T, Ukai S , et al. Brain regions responsible for tinnitus distress and loudness: a resting-state FMRI study. PLoS ONE 2013; 8 (6) e67778
    CrossrefPubMedGoogle Scholar
  • 70 Rauschecker JP, Leaver AM, Mühlau M. Tuning out the noise: limbic-auditory interactions in tinnitus. Neuron 2010; 66 (6) 819-826
    CrossrefPubMedGoogle Scholar
  • 71 Llinás RR, Ribary U, Jeanmonod D, Kronberg E, Mitra PP. Thalamocortical dysrhythmia: a neurological and neuropsychiatric syndrome characterized by magnetoencephalography. Proc Natl Acad Sci U S A 1999; 96 (26) 15222-15227
    CrossrefPubMedGoogle Scholar
  • 72 Llinás R, Urbano FJ, Leznik E, Ramírez RR, van Marle HJ. Rhythmic and dysrhythmic thalamocortical dynamics: GABA systems and the edge effect. Trends Neurosci 2005; 28 (6) 325-333
    CrossrefPubMedGoogle Scholar
  • 73 Friston KJ, Harrison L, Penny W. Dynamic causal modelling. Neuroimage 2003; 19 (4) 1273-1302
    CrossrefPubMedGoogle Scholar
  • 74 Stephan KE, Penny WD, Moran RJ, den Ouden HE, Daunizeau J, Friston KJ. Ten simple rules for dynamic causal modeling. Neuroimage 2010; 49 (4) 3099-3109
    CrossrefPubMedGoogle Scholar
  • 75 Le Bihan D, Mangin JF, Poupon C , et al. Diffusion tensor imaging: concepts and applications. J Magn Reson Imaging 2001; 13 (4) 534-546
    CrossrefPubMedGoogle Scholar
  • 76 Aldhafeeri FM, Mackenzie I, Kay T, Alghamdi J, Sluming V. Neuroanatomical correlates of tinnitus revealed by cortical thickness analysis and diffusion tensor imaging. Neuroradiology 2012; 54 (8) 883-892
    CrossrefPubMedGoogle Scholar
  • 77 Cacace AT, Cousins JP, Parnes SM , et al. Cutaneous-evoked tinnitus. II. Review of neuroanatomical, physiological and functional imaging studies. Audiol Neurootol 1999; 4 (5) 258-268
    CrossrefPubMedGoogle Scholar
  • 78 Langguth B, Eichhammer P, Kreutzer A , et al. The impact of auditory cortex activity on characterizing and treating patients with chronic tinnitus—first results from a PET study. Acta Otolaryngol Suppl 2006; (556) 84-88
    PubMedGoogle Scholar
  • 79 Moazami-Goudarzi M, Michels L, Weisz N, Jeanmonod D. Temporo-insular enhancement of EEG low and high frequencies in patients with chronic tinnitus. QEEG study of chronic tinnitus patients. BMC Neurosci 2010; 11: 40
    CrossrefPubMedGoogle Scholar
  • 80 De Ridder D, Vanneste S, Congedo M. The distressed brain: a group blind source separation analysis on tinnitus. PLoS ONE 2011; 6 (10) e24273
    CrossrefPubMedGoogle Scholar
  • 81 Balkenhol T, Wallhäusser-Franke E, Delb W. Psychoacoustic tinnitus loudness and tinnitus-related distress show different associations with oscillatory brain activity. PLoS ONE 2013; 8 (1) e53180
    CrossrefPubMedGoogle Scholar