Download PDF
Int Arch Otorhinolaryngol 2015; 19(03): 259-265
DOI: 10.1055/s-0035-1548671
Systematic Review
Thieme Publicações Ltda Rio de Janeiro, Brazil

Tinnitus Neural Mechanisms and Structural Changes in the Brain: The Contribution of Neuroimaging Research

Patricia Simonetti
1   Department of Otolaryngology, School of Medicine, University of São Paulo, Brazil
,
Jeanne Oiticica
1   Department of Otolaryngology, School of Medicine, University of São Paulo, Brazil
› Author Affiliations
Further Information

Publication History

18 November 2014

09 February 2015

Publication Date:
30 March 2015 (online)

   Permissions and Reprints

Abstract

Introduction Tinnitus is an abnormal perception of sound in the absence of an external stimulus. Chronic tinnitus usually has a high impact in many aspects of patients' lives, such as emotional stress, sleep disturbance, concentration difficulties, and so on. These strong reactions are usually attributed to central nervous system involvement. Neuroimaging has revealed the implication of brain structures in the auditory system.

Objective This systematic review points out neuroimaging studies that contribute to identifying the structures involved in the pathophysiological mechanism of generation and persistence of various forms of tinnitus.

Data Synthesis Functional imaging research reveals that tinnitus perception is associated with the involvement of the nonauditory brain areas, including the front parietal area; the limbic system, which consists of the anterior cingulate cortex, anterior insula, and amygdala; and the hippocampal and parahippocampal area.

Conclusion The neuroimaging research confirms the involvement of the mechanisms of memory and cognition in the persistence of perception, anxiety, distress, and suffering associated with tinnitus.

Keywords

tinnitus - functional neuroimaging - auditory cortex - neural networks - limbic system
 

  • References

  • 1 House JW, Brackmann DE. Tinnitus: surgical treatment. Ciba Found Symp 1981; 85: 204-216
    Google Scholar
  • 2 Jastreboff PJ. Phantom auditory perception (tinnitus): mechanisms of generation and perception. Neurosci Res 1990; 8 (4) 221-254
    CrossrefPubMedGoogle Scholar
  • 3 Eggermont JJ, Roberts LE. The neuroscience of tinnitus. Trends Neurosci 2004; 27 (11) 676-682
    CrossrefGoogle Scholar
  • 4 Eggermont JJ, Roberts LE. The neuroscience of tinnitus: understanding abnormal and normal auditory perception. Front Syst Neurosci 2012; 6: 53
    Google Scholar
  • 5 Noreña AJ. An integrative model of tinnitus based on a central gain controlling neural sensitivity. Neurosci Biobehav Rev 2011; 35 (5) 1089-1109
    CrossrefGoogle Scholar
  • 6 Schaette R, McAlpine D. Tinnitus with a normal audiogram: physiological evidence for hidden hearing loss and computational model. J Neurosci 2011; 31 (38) 13452-13457
    CrossrefPubMedGoogle Scholar
  • 7 Engineer ND, Møller AR, Kilgard MP. Directing neural plasticity to understand and treat tinnitus. Hear Res 2013; 295: 58-66
    CrossrefGoogle Scholar
  • 8 Roberts LE, Eggermont JJ, Caspary DM, Shore SE, Melcher JR, Kaltenbach JA. Ringing ears: the neuroscience of tinnitus. J Neurosci 2010; 30 (45) 14972-14979
    CrossrefGoogle Scholar
  • 9 Levine RA. Somatic (craniocervical) tinnitus and the dorsal cochlear nucleus hypothesis. Am J Otolaryngol 1999; 20 (6) 351-362
    CrossrefGoogle Scholar
  • 10 Shore SE. Multisensory integration in the dorsal cochlear nucleus: unit responses to acoustic and trigeminal ganglion stimulation. Eur J Neurosci 2005; 21 (12) 3334-3348
    CrossrefGoogle Scholar
  • 11 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
  • 12 Davies J, Gander PE, Andrews M, Hall DA. Auditory network connectivity in tinnitus patients: a resting-state fMRI study. Int J Audiol 2014; 53 (3) 192-198
    CrossrefGoogle Scholar
  • 13 Rogers BP, Morgan VL, Newton AT, Gore JC. Assessing functional connectivity in the human brain by fMRI. Magn Reson Imaging 2007; 25 (10) 1347-1357
    CrossrefGoogle Scholar
  • 14 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
  • 15 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 (1) 213-218
    CrossrefGoogle Scholar
  • 16 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
    CrossrefGoogle Scholar
  • 17 Simmons R, Dambra C, Lobarinas E, Stocking C, Salvi R. Head, Neck, and Eye Movements That Modulate Tinnitus. Semin Hear 2008; 29 (4) 361-370
    Article in Thieme ConnectGoogle Scholar
  • 18 Giraud AL, Chéry-Croze S, Fischer G , et al. A selective imaging of tinnitus. Neuroreport 1999; 10 (1) 1-5
    CrossrefGoogle Scholar
  • 19 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
    CrossrefGoogle Scholar
  • 20 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
    CrossrefGoogle Scholar
  • 21 Boyen K, de Kleine E, van Dijk P, Langers DR. Tinnitus-related dissociation between cortical and subcortical neural activity in humans with mild to moderate sensorineural hearing loss. Hear Res 2014; 312: 48-59
    CrossrefGoogle Scholar
  • 22 Mühlau M, Rauschecker JP, Oestreicher E , et al. Structural brain changes in tinnitus. Cereb Cortex 2006; 16 (9) 1283-1288
    Google Scholar
  • 23 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
  • 24 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
  • 25 Seydell-Greenwald A, Leaver AM, Turesky TK, Morgan S, Kim HJ, Rauschecker JP. Functional MRI evidence for a role of ventral prefrontal cortex in tinnitus. Brain Res 2012; 1485: 22-39
    CrossrefPubMedGoogle Scholar
  • 26 Leaver AM, Seydell-Greenwald A, Turesky TK, Morgan S, Kim HJ, Rauschecker JP. Cortico-limbic morphology separates tinnitus from tinnitus distress. Front Syst Neurosci 2012; 6: 21
    Google Scholar
  • 27 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
    CrossrefGoogle Scholar
  • 28 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
    CrossrefGoogle Scholar
  • 29 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
  • 30 Schmidt SA, Akrofi K, Carpenter-Thompson JR, Husain FT. Default mode, dorsal attention and auditory resting state networks exhibit differential functional connectivity in tinnitus and hearing loss. PLoS ONE 2013; 8 (10) e76488
    CrossrefGoogle Scholar
  • 31 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
    CrossrefGoogle Scholar
  • 32 Song JJ, De Ridder D, Van de Heyning P, Vanneste S. Mapping tinnitus-related brain activation: an activation-likelihood estimation metaanalysis of PET studies. J Nucl Med 2012; 53 (10) 1550-1557
    CrossrefGoogle Scholar
  • 33 Langguth B, Schecklmann M, Lehner A , et al. Neuroimaging and neuromodulation: complementary approaches for identifying the neuronal correlates of tinnitus. Front Syst Neurosci 2012; 6: 15
    Google Scholar
  • 34 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
    CrossrefGoogle Scholar
  • 35 Elgoyhen AB, Langguth B, Vanneste S, De Ridder D. Tinnitus: network pathophysiology-network pharmacology. Front Syst Neurosci 2012; 6: 1
    Google Scholar
  • 36 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
    CrossrefGoogle Scholar
  • 37 Schlee W, Weisz N, Bertrand O, Hartmann T, Elbert T. Using auditory steady state responses to outline the functional connectivity in the tinnitus brain. PLoS ONE 2008; 3 (11) e3720
    CrossrefGoogle Scholar
  • 38 Rubinstein B, Axelsson A, Carlsson GE. Prevalence of signs and symptoms of craniomandibular disorders in tinnitus patients. J Craniomandib Disord 1990; 4 (3) 186-192
    Google Scholar
  • 39 Pinchoff RJ, Burkard RF, Salvi RJ, Coad ML, Lockwood AH. Modulation of tinnitus by voluntary jaw movements. Am J Otol 1998; 19 (6) 785-789
    Google Scholar
  • 40 Shore S, Zhou J, Koehler S. Neural mechanisms underlying somatic tinnitus. Prog Brain Res 2007; 166: 107-123
    Google Scholar
  • 41 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
    CrossrefGoogle Scholar
  • 42 van Gendt MJ, Boyen K, de Kleine E, Langers DR, van Dijk P. The relation between perception and brain activity in gaze-evoked tinnitus. J Neurosci 2012; 32 (49) 17528-17539
    CrossrefGoogle Scholar