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Journal of the Association for Research in Otolaryngology

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Open Access 28-11-2023 | Tinnitus | Review

Eavesdropping on Tinnitus Using MEG: Lessons Learned and Future Perspectives

Authors: Lisa Reisinger, Gianpaolo Demarchi, Nathan Weisz

Published in: Journal of the Association for Research in Otolaryngology | Issue 6/2023

Abstract

Tinnitus has been widely investigated in order to draw conclusions about the underlying causes and altered neural activity in various brain regions. Existing studies have based their work on different tinnitus frameworks, ranging from a more local perspective on the auditory cortex to the inclusion of broader networks and various approaches towards tinnitus perception and distress. Magnetoencephalography (MEG) provides a powerful tool for efficiently investigating tinnitus and aberrant neural activity both spatially and temporally. However, results are inconclusive, and studies are rarely mapped to theoretical frameworks. The purpose of this review was to firstly introduce MEG to interested researchers and secondly provide a synopsis of the current state. We divided recent tinnitus research in MEG into study designs using resting state measurements and studies implementing tone stimulation paradigms. The studies were categorized based on their theoretical foundation, and we outlined shortcomings as well as inconsistencies within the different approaches. Finally, we provided future perspectives on how to benefit more efficiently from the enormous potential of MEG. We suggested novel approaches from a theoretical, conceptual, and methodological point of view to allow future research to obtain a more comprehensive understanding of tinnitus and its underlying processes.

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Henry JA, Reavis KM, Griest SE et al (2020) Tinnitus: an epidemiologic perspective. Otolaryngol Clin North Am 53(4):481–499CrossRefPubMed

Jarach CM, Lugo A, Scala M et al (2022) Global prevalence and incidence of tinnitus: a systematic review and meta-analysis. JAMA Neurol. https://doi.org/10.1001/jamaneurol.2022.2189CrossRefPubMedPubMedCentral

Dobie RA (2003) Depression and tinnitus. Otolaryngol Clin North Am 36(2):383–388. https://doi.org/10.1016/S0030-6665(02)00168-8CrossRefPubMed

Eggermont JJ, Roberts LE (2004) The neuroscience of tinnitus. Trends Neurosci 27:676–682. https://doi.org/10.1016/j.tins.2004.08.010CrossRefPubMed

Kim HJ, Lee HJ, An SY et al (2015) Analysis of the prevalence and associated risk factors of tinnitus in adults. PLoS ONE 10(5):e0127578. https://doi.org/10.1371/journal.pone.0127578CrossRefPubMedPubMedCentral

Wallhäusser-Franke E, D’Amelio R, Glauner A et al (2017) Transition from acute to chronic tinnitus: predictors for the development of chronic distressing tinnitus. Front Neurol 8:605. https://doi.org/10.3389/fneur.2017.00605CrossRefPubMedPubMedCentral

Ivansic D, Besteher B, Gantner J et al (2019) Psychometric assessment of mental health in tinnitus patients, depressive and healthy controls. Psychiatry Res 281:112582. https://doi.org/10.1016/j.psychres.2019.112582CrossRefPubMed

Ivansic D, Guntinas-Lichius O, Müller B, Volk GF, Schneider G, Dobel C (2017) Impairments of speech comprehension in patients with tinnitus - a review. Front Aging Neurosci 9:224. https://doi.org/10.3389/fnagi.2017.00224CrossRefPubMedPubMedCentral

Eggermont JJ (2003) Central tinnitus. Auris Nasus Larynx 30:7–12. https://doi.org/10.1016/S0385-8146(02)00122-0CrossRef

10.

Tonndorf J (1987) The analogy between tinnitus and pain: a suggestion for a physiological basis of chronic tinnitus. Hear Res 28(2–3):271–275. https://doi.org/10.1016/0378-5955(87)90054-2CrossRefPubMed

11.

Baguley DM, Axon P, Winter IM, Moffat DA (2002) The effect of vestibular nerve section upon tinnitus. Clin Otolaryngol Allied Sci 27(4):219–226. https://doi.org/10.1046/j.1365-2273.2002.00566.xCrossRefPubMed

12.

Møller MB, Møller AR, Jannetta PJ, Jho HD (1993) Vascular decompression surgery for severe tinnitus: selection criteria and results. Laryngoscope 103(4):421–427. https://doi.org/10.1002/lary.5541030410CrossRefPubMed

13.

Brüggemann 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. https://doi.org/10.3389/fnhum.2016.00341CrossRefPubMedPubMedCentral

14.

Adjamian P (2014) The application of electro-and magneto-encephalography in tinnitus research–methods and interpretations. Front Neurol 5:228. https://doi.org/10.3389/fneur.2014.00228CrossRefPubMedPubMedCentral

15.

Eggermont JJ, Roberts LE (2015) Tinnitus: animal models and findings in humans. Cell Tissue Res 361:311–336. https://doi.org/10.1007/s00441-014-1992-8CrossRefPubMed

16.

Kaltenbach JA (2011) Tinnitus: models and mechanisms. Hear Res 276(1–2):52–60. https://doi.org/10.1016/j.heares.2010.12.003CrossRefPubMed

17.

De Ridder D, Elgoyhen AB, Romo R, Langguth B (2011) Phantom percepts: tinnitus and pain as persisting aversive memory networks. National Academy of Sciences 108(20):8075–8080. https://doi.org/10.1073/pnas.101846610CrossRef

18.

Flor H, Elbert T, Knecht S et al (1995) Phantom-limb pain as a perceptual correlate of cortical reorganization following arm amputation. Nature 375(6531):482–484. https://doi.org/10.1038/375482a0CrossRefPubMed

19.

Mühlnickel W, Elbert T, Taub E, Flor H (1998) Reorganization of auditory cortex in tinnitus. National Academy of Sciences 95(17):10340–10343. https://doi.org/10.1073/pnas.95.17.10340CrossRef

20.

Schaette R, Kempter R (2012) Computational models of neurophysiological correlates of tinnitus. Front Syst Neurosci 6:34. https://doi.org/10.3389/fnsys.2012.00034CrossRefPubMedPubMedCentral

21.

Eggermont JJ, Roberts LE (2012) The neuroscience of tinnitus: understanding abnormal and normal auditory perception. Front Syst Neurosci 6:53. https://doi.org/10.3389/fnsys.2012.00053CrossRefPubMedPubMedCentral

22.

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(1):114–120. https://doi.org/10.1212/WNL.50.1.114CrossRefPubMed

23.

Lockwood AH, Salvi RJ, Burkard RF (2002) Tinnitus. N Engl J Med 347(12):904–910. https://doi.org/10.1056/NEJMra013395CrossRefPubMed

24.

Lockwood AH, Wack DS, Burkard RF et al (2001) The functional anatomy of gaze-evoked tinnitus and sustained lateral gaze. Neurology 56(4):472–480. https://doi.org/10.1212/WNL.56.4.472CrossRefPubMed

25.

Irvine DR, Rajan R, McDermott HJ (2000) Injury-induced reorganization in adult auditory cortex and its perceptual consequences. Hear Res 147:188–199. https://doi.org/10.1016/S0378-5955(00)00131-3CrossRefPubMed

26.

Leaver AM, Seydell-Greenwald A, Rauschecker JP (2016) Auditory–limbic interactions in chronic tinnitus: challenges for neuroimaging research. Hear Res 334:49–57. https://doi.org/10.1016/j.heares.2015.08.005CrossRefPubMed

27.

Norena AJ, Eggermont JJ (2006) Enriched acoustic environment after noise trauma abolishes neural signs of tinnitus. NeuroReport 17(6):559–563CrossRefPubMed

28.

Roberts LE, Eggermont JJ, Caspary DM, Shore SE, Melcher JR, Kaltenbach JA (2010) Ringing ears: the neuroscience of tinnitus. J Neurosci 30(45):14972–14979. https://doi.org/10.1523/JNEUROSCI.4028-10.2010CrossRefPubMedPubMedCentral

29.

Engineer ND, Riley JR, Seale JD et al (2011) Reversing pathological neural activity using targeted plasticity. Nature 470:101–104. https://doi.org/10.1038/nature09656CrossRefPubMedPubMedCentral

30.

Yang S, Weiner BD, Zhang LS, Cho SJ, Bao S (2011) Homeostatic plasticity drives tinnitus perception in an animal model. National Academy of Sciences 108(36):14974–14979. https://doi.org/10.1073/pnas.1107998108CrossRef

31.

Langers DR, Kleine ED, Dijk PV (2012) Tinnitus does not require macroscopic tonotopic map reorganization. Front Syst Neurosci 6:2. https://doi.org/10.3389/fnsys.2012.00002CrossRefPubMedPubMedCentral

32.

Koops EA, Renken RJ, Lanting CP, van Dijk P (2020) Cortical tonotopic map changes in humans are larger in hearing loss than in additional tinnitus. J Neurosci 40(16):3178–3185. https://doi.org/10.1523/JNEUROSCI.2083-19.2020CrossRefPubMedPubMedCentral

33.

Wienbruch C, Paul I, Weisz N, Elbert T, Roberts LE (2006) Frequency organization of the 40-Hz auditory steady-state response in normal hearing and in tinnitus. Neuroimage 33(1):180–194. https://doi.org/10.1016/j.neuroimage.2006.06.023CrossRefPubMed

34.

Llinás RR, Ribary U, Jeanmonod D, Kronberg E, Mitra pp. (1999) Thalamocortical dysrhythmia: a neurological and neuropsychiatric syndrome characterized by magnetoencephalography. National Academy of Sciences 96(26):15222–15227. https://doi.org/10.1073/pnas.96.26.15222CrossRef

35.

Llinás R, Urbano FJ, Leznik E, Ramírez RR, Van Marle HJ (2005) Rhythmic and dysrhythmic thalamocortical dynamics: GABA systems and the edge effect. Trends Neurosci 28(6):325–333. https://doi.org/10.1016/j.tins.2005.04.006CrossRefPubMed

36.

Van der Loo E, Gais S, Congedo M et al (2009) Tinnitus intensity dependent gamma oscillations of the contralateral auditory cortex. PLoS ONE 4(10):e7396. https://doi.org/10.1371/journal.pone.0007396CrossRefPubMedPubMedCentral

37.

Weisz N, Müller S, Schlee W, Dohrmann K, Hartmann T, Elbert T (2007) The neural code of auditory phantom perception. J Neurosci 27(6):1479–1484. https://doi.org/10.1523/JNEUROSCI.3711-06.2007CrossRefPubMedPubMedCentral

38.

Sedley W (2019) Tinnitus: does gain explain? Neuroscience 407:213–228. https://doi.org/10.1016/j.neuroscience.2019.01.027CrossRefPubMed

39.

Schaette R, Kempter R (2006) Development of tinnitus-related neuronal hyperactivity through homeostatic plasticity after hearing loss: a computational model. Eur J Neurosci 23(11):3124–3138. https://doi.org/10.1111/j.1460-9568.2006.04774.xCrossRefPubMed

40.

Mühlmeier G, Baguley D, Cox T, Suckfüll M, Meyer T (2016) Characteristics and spontaneous recovery of tinnitus related to idiopathic sudden sensorineural hearing loss. Otol Neurotol 37(6):634. https://doi.org/10.1097/MAO.0000000000001081CrossRefPubMedPubMedCentral

41.

Vielsmeier V, Santiago Stiel R, Kwok P, Langguth B, Schecklmann M (2020) From acute to chronic tinnitus: pilot data on predictors and progression. Front Neurol 11:997. https://doi.org/10.3389/fneur.2020.00997CrossRefPubMedPubMedCentral

42.

Sedley W, Friston KJ, Gander PE, Kumar S, Griffiths TD (2016) An integrative tinnitus model based on sensory precision. Trends Neurosci 39(12):799–812. https://doi.org/10.1016/j.tins.2016.10.004CrossRefPubMedPubMedCentral

43.

Von Helmholtz H (1867) Handbuch der physiologischen Optik: mit 213 in den Text eingedruckten Holzschnitten und 11 Tafeln. Voss, Leipzig

44.

De Ridder D, Vanneste S, Freeman W (2014) The Bayesian brain: phantom percepts resolve sensory uncertainty. Neurosci Biobehav Rev 44:4–15. https://doi.org/10.1016/j.neubiorev.2012.04.001CrossRefPubMed

45.

Hullfish J, Sedley W, Vanneste S (2019) Prediction and perception: insights for (and from) tinnitus. Neurosci Biobehav Rev 102:1–12. https://doi.org/10.1016/j.neubiorev.2019.04.008CrossRefPubMed

46.

Hu S, Hall DA, Zubler F et al (2021) Bayesian brain in tinnitus: computational modeling of three perceptual phenomena using a modified hierarchical Gaussian filter. Hear Res 410:108338. https://doi.org/10.1016/j.heares.2021.108338CrossRefPubMed

47.

Mohan A, Luckey A, Weisz N, Vanneste S (2022) Predisposition to domain-wide maladaptive changes in predictive coding in auditory phantom perception. Neuroimage 248:118813. https://doi.org/10.1016/j.neuroimage.2021.118813CrossRefPubMed

48.

Partyka M, Demarchi G, Roesch S et al (2019) Phantom auditory perception (tinnitus) is characterised by stronger anticipatory auditory predictions. Online-first. https://doi.org/10.1101/869842CrossRef

49.

Sedley W, Alter K, Gander PE, Berger J, Griffiths TD (2019) Exposing pathological-sensory predictions in tinnitus using auditory intensity deviant evoked responses. J Neurosci 39(50):10096–10103. https://doi.org/10.1523/JNEUROSCI.1308-19.2019CrossRefPubMedPubMedCentral

50.

Adjamian P, Sereda M, Zobay O, Hall DA, Palmer AR (2012) Neuromagnetic indicators of tinnitus and tinnitus masking in patients with and without hearing loss. J Assoc Res Otolaryngol 13:715–731. https://doi.org/10.1007/s10162-012-0340-5CrossRefPubMedPubMedCentral

51.

Longenecker RJ, Galazyuk AV (2016) Variable effects of acoustic trauma on behavioral and neural correlates of tinnitus in individual animals. Front Behav Neurosci 10:207. https://doi.org/10.3389/fnbeh.2016.00207CrossRefPubMedPubMedCentral

52.

Ropp TJF, Tiedemann KL, Young ED, May BJ (2014) Effects of unilateral acoustic trauma on tinnitus-related spontaneous activity in the inferior colliculus. JARO 15:1007–1022. https://doi.org/10.1007/s10162-014-0488-2CrossRefPubMedPubMedCentral

53.

Coomber B, Berger JI, Kowalkowski VL, Shackleton TM, Palmer AR, Wallace MN (2014) Neural changes accompanying tinnitus following unilateral acoustic trauma in the guinea pig. Eur J Neur 40(2):2427–2441. https://doi.org/10.1111/ejn.12580CrossRef

54.

Schlee W, Weisz N, Bertrand O, Hartmann T, Elbert T (2008) Using auditory steady state responses to outline the functional connectivity in the tinnitus brain. PLoS ONE 3(11):e3720. https://doi.org/10.1371/journal.pone.0003720CrossRefPubMedPubMedCentral

55.

Maudoux A, Lefebvre P, Cabay JE et al (2012) Auditory resting-state network connectivity in tinnitus: a functional MRI study. PLoS ONE 7(5):e36222. https://doi.org/10.1371/journal.pone.0036222CrossRefPubMedPubMedCentral

56.

Husain FT, Schmidt SA (2014) Using resting state functional connectivity to unravel networks of tinnitus. Hear Res 307:153–162. https://doi.org/10.1016/j.heares.2013.07.010CrossRefPubMed

57.

Burton H, Wineland A, Bhattacharya M, Nicklaus J, Garcia KS, Piccirillo JF (2012) Altered networks in bothersome tinnitus: a functional connectivity study. BMC Neurosci 13:1–15. https://doi.org/10.1186/1471-2202-13-3CrossRef

58.

Vanneste S, Van de Heyning P, De Ridder D (2011) The neural network of phantom sound changes over time: a comparison between recent-onset and chronic tinnitus patients. Eur J Neurosci 34(5):718–731. https://doi.org/10.1111/j.1460-9568.2011.07793.xCrossRefPubMed

59.

De Ridder D, Vanneste S, Song JJ, Adhia D (2022) Tinnitus and the triple network model: a perspective. Clin Exp Otorhinolaryngol 15(3):205–212. https://doi.org/10.21053/ceo.2022.00815

60.

Reisinger L, Schmidt F, Benz K et al (2023) Ageing as risk factor for tinnitus and its complex interplay with hearing loss - evidence from online and NHANES data. BMC Med 21(1):1–8. https://doi.org/10.1186/s12916-023-02998-1CrossRef

61.

Cohen D (1968) Magnetoencephalography: evidence of magnetic fields produced by alpha-rhythm currents. Science 161(3843):784–786CrossRefPubMed

62.

Hämäläinen MS (1992) Magnetoencephalography: a tool for functional brain imaging. Brain Topogr 5:95–102. https://doi.org/10.1007/BF01129036CrossRefPubMed

63.

Hämäläinen M, Hari R, Ilmoniemi RJ, Knuutila J, Lounasmaa OV (1993) Magnetoencephalography - theory, instrumentation, and applications to noninvasive studies of the working human brain. Rev Mod Phys 65(2):413. https://doi.org/10.1103/revmodphys.65.413CrossRef

64.

Gross J (2019) Magnetoencephalography in cognitive neuroscience: a primer. Neuron 104(2):189–204. https://doi.org/10.1016/j.neuron.2019.07.001CrossRefPubMed

65.

Murakami S, Okada Y (2006) Contributions of principal neocortical neurons to magnetoencephalography and electroencephalography signals. J Physiol 575(3):925–936. https://doi.org/10.1113/jphysiol.2006.105379CrossRefPubMedPubMedCentral

66.

Singh SP (2014) Magnetoencephalography: basic principles. Ann Indian Acad Neurol 17(Suppl 1):S107. https://doi.org/10.4103/0972-2327.128676CrossRefPubMedPubMedCentral

67.

Vorwerk J, Cho JH, Rampp S, Hamer H, Knösche TR, Wolters CH (2014) A guideline for head volume conductor modeling in EEG and MEG. Neuroimage 100:590–607. https://doi.org/10.1016/j.neuroimage.2014.06.040CrossRefPubMed

68.

Pizzo F, Roehri N, Medina Villalon S et al (2019) Deep brain activities can be detected with magnetoencephalography. Nat Com 10(1):971. https://doi.org/10.1038/s41467-019-08665-5CrossRef

69.

Ruzich E, Crespo-García M, Dalal SS, Schneiderman JF (2019) Characterizing hippocampal dynamics with MEG: a systematic review and evidence-based guidelines. Hum Brain Mapp 40(4):1353–1375. https://doi.org/10.1002/hbm.24445CrossRefPubMed

70.

Goldenholz DM, Ahlfors SP, Hämäläinen MS et al (2009) Mapping the signal-to-noise-ratios of cortical sources in magnetoencephalography and electroencephalography. Hum Brain Mapp 30(4):1077–1086. https://doi.org/10.1002/hbm.20571CrossRefPubMed

71.

Sato S, Balish M, Muratore R (1991) Principles of magnetoencephalography. J Clin Neurophysiol 8(2):144–156CrossRefPubMed

72.

Proudfoot M, Woolrich MW, Nobre AC, Turner MR (2014) Magnetoencephalography. Pract Neurol 14(5):336–343. https://doi.org/10.1136/practneurol-2013-000768CrossRefPubMedPubMedCentral

73.

Barkley GL (2004) Controversies in neurophysiology. MEG is superior to EEG in localization of interictal epileptiform activity: Pro. Clin Neurophysiol 115(5):1001–1009. https://doi.org/10.1016/j.clinph.2003.12.011

74.

Baillet S (2017) Magnetoencephalography for brain electrophysiology and imaging. Nat Neurosci 20(3):327–339. https://doi.org/10.1038/nn.4504CrossRefPubMed

75.

Schoffelen JM, Gross J (2009) Source connectivity analysis with MEG and EEG. Hum Brain Mapp 30(6):1857–1865. https://doi.org/10.1002/hbm.20745CrossRefPubMedPubMedCentral

76.

Schoffelen JM, Gross J (2019) Studying dynamic neural interactions with MEG. In: Supek S, Aine C (eds) Magnetoencephalography: from signals to dynamic cortical networks. Switzerland: Springer Nature

77.

Da Silva FL (2013) EEG and MEG: relevance to neuroscience. Neuron 80(5):1112–1128. https://doi.org/10.1016/j.neuron.2013.10.017CrossRef

78.

David O, Kilner JM, Friston KJ (2006) Mechanisms of evoked and induced responses in MEG/EEG. Neuroimage 31(4):1580–1591. https://doi.org/10.1016/j.neuroimage.2006.02.034CrossRefPubMed

79.

Siems M, Pape AA, Hipp JF, Siegel M (2016) Measuring the cortical correlation structure of spontaneous oscillatory activity with EEG and MEG. Neuroimage 129:345–355. https://doi.org/10.1016/j.neuroimage.2016.01.055CrossRefPubMed

80.

Puce A, Hämäläinen MS (2017) A review of issues related to data acquisition and analysis in EEG/MEG studies. Brain Sci 7(6):58. https://doi.org/10.3390/brainsci7060058CrossRefPubMedPubMedCentral

81.

Makeig S, Debener S, Onton J, Delorme A (2004) Mining event-related brain dynamics. Trends Cogn Sci 8(5):204–210. https://doi.org/10.1016/j.tics.2004.03.008CrossRefPubMed

82.

Varela F, Lachaux JP, Rodriguez E, Martinerie J (2001) The brainweb: phase synchronization and large-scale integration. Nat Rev Neurosci 2(4):229–239. https://doi.org/10.1038/35067550CrossRefPubMed

83.

Von Stein A, Sarnthein J (2000) Different frequencies for different scales of cortical integration: from local gamma to long range alpha/theta synchronization. Int J Psychophysiol 38(3):301–313. https://doi.org/10.1016/S0167-8760(00)00172-0CrossRef

84.

Pfurtscheller G, Da Silva FL (1999) Event-related EEG/MEG synchronization and desynchronization: basic principles. Clin Neurophysiol 110(11):1842–1857. https://doi.org/10.1016/S1388-2457(99)00141-8CrossRefPubMed

85.

Schaworonkow N, Nikulin VV (2022) Is sensor space analysis good enough? Spatial patterns as a tool for assessing spatial mixing of EEG/MEG rhythms. Neuroimage 253:119093. https://doi.org/10.1016/j.neuroimage.2022.119093CrossRefPubMed

86.

Näätänen R, Picton T (1987) The N1 wave of the human electric and magnetic response to sound: a review and an analysis of the component structure. Psychophysiol 24(4):375–425. https://doi.org/10.1111/j.1469-8986.1987.tb00311.xCrossRef

87.

Neukirch M, Hegerl U, Kötitz R, Dorn H, Gallinat U, Herrmann WM (2002) Comparison of the amplitude/intensity function of the auditory evoked N1m and N1 components. Neuropsychobiology 45(1):41–48. https://doi.org/10.1159/000048672CrossRefPubMed

88.

Gu JW, Halpin CF, Nam EC, Levine RA, Melcher JR (2010) Tinnitus, diminished sound-level tolerance, and elevated auditory activity in humans with clinically normal hearing sensitivity. J Neurophysiol 104(6):3361–3370. https://doi.org/10.1152/jn.00226.2010CrossRefPubMedPubMedCentral

89.

Korczak P, Smart J, Delgado R, Strobel TM, Bradford C (2012) Auditory steady-state responses. J Am Acad Audiol 23(03):146–170. https://doi.org/10.3766/jaaa.23.3.3CrossRefPubMed

90.

Regan D (1982) Comparison of transient and steady-state methods. Ann N Y Acad Sci 388:45–71CrossRefPubMed

91.

Galambos R, Makeig S, Talmachoff PJ (1981) A 40-Hz auditory potential recorded from the human scalp. National Academy of Sciences 78(4):2643–2647. https://doi.org/10.1073/pnas.78.4.2643CrossRef

92.

Gutschalk A, Mase R, Roth R et al (1999) Deconvolution of 40 Hz steady-state fields reveals two overlapping source activities of the human auditory cortex. Clin Neurophysiol 110(5):856–868. https://doi.org/10.1016/S1388-2457(99)00019-XCrossRefPubMed

93.

Pantev C, Roberts LE, Elbert T, Roβ B, Wienbruch C (1996) Tonotopic organization of the sources of human auditory steady-state responses. Hear Res 101(1–2):62–74. https://doi.org/10.1016/S0378-5955(96)00133-5CrossRefPubMed

94.

Hillebrand A, Singh KD, Holliday IE, Furlong PL, Barnes GR (2005) A new approach to neuroimaging with magnetoencephalography. Hum Brain Mapp 25(2):199–211. https://doi.org/10.1002/hbm.20102CrossRefPubMedPubMedCentral

95.

Friston KJ (1994) Functional and effective connectivity in neuroimaging: a synthesis. Hum Brain Mapp 2(1–2):56–78. https://doi.org/10.1002/hbm.460020107CrossRef

96.

Friston KJ (2011) Functional and effective connectivity: a review. Brain Connect 1(1):13–36. https://doi.org/10.1089/brain.2011.0008CrossRefPubMed

97.

Palva S, Palva JM (2012) Discovering oscillatory interaction networks with M/EEG: challenges and breakthroughs. Trends Cogn Sci 16(4):219–230. https://doi.org/10.1016/j.tics.2012.02.004CrossRefPubMed

98.

Kahlbrock N, Weisz N (2008) Transient reduction of tinnitus intensity is marked by concomitant reductions of delta band power. BMC Biol 6:1–9. https://doi.org/10.1186/1741-7007-6-4CrossRef

99.

Sedley W, Teki S, Kumar S, Barnes GR, Bamiou DE, Griffiths TD (2012) Single-subject oscillatory gamma responses in tinnitus. Brain 135(10):3089–3100. https://doi.org/10.1093/brain/aws220CrossRefPubMedPubMedCentral

100.

Müller N, Lorenz I, Langguth B, Weisz N (2013) rTMS induced tinnitus relief is related to an increase in auditory cortical alpha activity. PLoS ONE 8(2):e55557. https://doi.org/10.1371/journal.pone.0055557CrossRefPubMedPubMedCentral

101.

Weisz N, Moratti S, Meinzer M, Dohrmann K, Elbert T (2005) Tinnitus perception and distress is related to abnormal spontaneous brain activity as measured by magnetoencephalography. PLoS Med 2(6):e153. https://doi.org/10.1371/journal.pmed.0020153CrossRefPubMedPubMedCentral

102.

Schlee W, Schecklmann M, Lehner A et al (2014) Reduced variability of auditory alpha activity in chronic tinnitus. Neural Plast 2014:436146. https://doi.org/10.1155/2014/436146

103.

Lau P, Wollbrink A, Wunderlich R et al (2018) Targeting heterogeneous findings in neuronal oscillations in tinnitus: analyzing meg novices and mental health comorbidities. Front Psychol 9:235. https://doi.org/10.3389/fpsyg.2018.00235CrossRefPubMedPubMedCentral

104.

De Ridder D, Vanneste S, Langguth B, Llinas R (2015) Thalamocortical dysrhythmia: a theoretical update in tinnitus. Front Neurol 6:124. https://doi.org/10.3389/fneur.2015.00124CrossRefPubMedPubMedCentral

105.

Sedley W, Gander PE, Kumar S et al (2016) Neural signatures of perceptual inference elife 5:e11476. https://doi.org/10.7554/eLife.11476CrossRefPubMed

106.

Hartmann T, Lorenz I, Müller N, Langguth B, Weisz N (2014) The effects of neurofeedback on oscillatory processes related to tinnitus. Brain Topogr 27:149–157. https://doi.org/10.1007/s10548-013-0295-9CrossRefPubMed

107.

Crocetti A, Forti S, Del Bo L (2011) Neurofeedback for subjective tinnitus patients. Auris Nasus Larynx 38(6):735–738. https://doi.org/10.1016/j.anl.2011.02.003CrossRefPubMed

108.

Dohrmann K, Weisz N, Schlee W, Hartmann T, Elbert T (2007) Neurofeedback for treating tinnitus. Prog Brain Res 166:473–485. https://doi.org/10.1016/S0079-6123(07)66046-4CrossRefPubMed

109.

Zobay O, Adjamian P (2015) Source-space cross-frequency amplitude-amplitude coupling in tinnitus. BioMed Res Int 2015:489619. https://doi.org/10.1155/2015/489619

110.

Zobay O, Palmer AR, Hall DA, Sereda M, Adjamian P (2015) Source space estimation of oscillatory power and brain connectivity in tinnitus. PLoS ONE 10(3):e0120123. https://doi.org/10.1371/journal.pone.0120123CrossRefPubMedPubMedCentral

111.

Schlee W, Lorenz I, Hartmann T, Müller N, Schulz H, Weisz N (2011) A global brain model of tinnitus. In Møller AR, Langguth B, De Ridder D, Kleinjung T (eds) Textbook of tinnitus. London: Springer

112.

Paraskevopoulos E, Dobel C, Wollbrink A, Salvari V, Bamidis PD, Pantev C (2019) Maladaptive alterations of resting state cortical network in tinnitus: a directed functional connectivity analysis of a larger MEG data set. Sci Rep 9(1):15452. https://doi.org/10.1038/s41598-019-51747-zCrossRefPubMedPubMedCentral

113.

Chen YC, Wang F, Wang J et al (2017) Resting-state brain abnormalities in chronic subjective tinnitus: a meta-analysis. Front Hum Neurosci 11:22. https://doi.org/10.3389/fnhum.2017.00022CrossRefPubMedPubMedCentral

114.

Chen YC, Xia W, Chen H et al (2017) Tinnitus distress is linked to enhanced resting-state functional connectivity from the limbic system to the auditory cortex. Hum Brain Mapp 38(5):2384–2397. https://doi.org/10.1002/hbm.23525CrossRefPubMedPubMedCentral

115.

Schmidt SA, Carpenter-Thompson J, Husain FT (2017) Connectivity of precuneus to the default mode and dorsal attention networks: a possible invariant marker of long-term tinnitus. Neuroimage Clin 16:196–204. https://doi.org/10.1016/j.nicl.2017.07.015CrossRefPubMedPubMedCentral

116.

Demopoulos C, Duong X, Hinkley LB et al (2020) Global resting-state functional connectivity of neural oscillations in tinnitus with and without hearing loss. Hum Brain Mapp 41(10):2846–2861. https://doi.org/10.1002/hbm.24981CrossRefPubMedPubMedCentral

117.

Schlee W, Hartmann T, Langguth B, Weisz N (2009) Abnormal resting-state cortical coupling in chronic tinnitus. BMC Neurosci 10:11. https://doi.org/10.1186/1471-2202-10-11CrossRefPubMedPubMedCentral

118.

Larson PS, Cheung SW (2012) Deep brain stimulation in area LC controllably triggers auditory phantom percepts. Neurosurg 70(2):398–406. https://doi.org/10.1227/NEU.0b013e3182320ab5CrossRef

119.

Larson PS, Cheung SW (2013) A stroke of silence: tinnitus suppression following placement of a deep brain stimulation electrode with infarction in area LC. J Neurosurg 118(1):192–194. https://doi.org/10.3171/2012.9.JNS12594CrossRefPubMed

120.

Li YH, Chi TS, Shiao AS, Li LPH, Hsieh JC (2022) Pros and cons in tinnitus brain: enhancement of global connectivity for alpha and delta waves. Prog Neuropsychopharmacol Biol Psychiatry 115:110497. https://doi.org/10.1016/j.pnpbp.2021.110497CrossRefPubMed

121.

Benoit O, Daurat A, Prado J (2000) Slow (0.7–2 Hz) and fast (2–4 Hz) delta components are differently correlated to theta, alpha and beta frequency bands during NREM sleep. Clin Neurophysiol 111(12):2103–2106. https://doi.org/10.1016/S1388-2457(00)00470-3

122.

Becker L, Keck A, Rohleder N, Müller-Voggel N (2022) Higher peripheral inflammation is associated with lower orbitofrontal gamma power in chronic tinnitus. Front Behav Neurosci 16:883926. https://doi.org/10.3389/fnbeh.2022.883926

123.

Elgoyhen AB, Langguth B, De Ridder D, Vanneste S (2015) Tinnitus: perspectives from human neuroimaging. Nat Rev Neurosci 16(10):632–642. https://doi.org/10.1038/nrn4003CrossRefPubMed

124.

Kennedy BK, Berger SL, Brunet A et al (2014) Geroscience: linking aging to chronic disease. Cell 159(4):709–713. https://doi.org/10.1016/j.cell.2014.10.039CrossRefPubMedPubMedCentral

125.

Noh TS, Kyong JS, Park MK et al (2019) Treatment outcome of auditory and frontal dual-site rTMS in tinnitus patients and changes in magnetoencephalographic functional connectivity after rTMS: double-blind randomized controlled trial. Audiol Neurotol 24(6):293–298. https://doi.org/10.1159/000503134CrossRef

126.

Kleinjung T, Eichhammer P, Landgrebe M et al (2008) Combined temporal and prefrontal transcranial magnetic stimulation for tinnitus treatment: a pilot study. Otolaryngol Head Neck Surg 138(4):497–501. https://doi.org/10.1016/j.otohns.2007.12.022CrossRefPubMed

127.

Sereda M, Adjamian P, Edmondson-Jones M, Palmer AR, Hall DA (2013) Auditory evoked magnetic fields in individuals with tinnitus. Hear Res 302:50–59. https://doi.org/10.1016/j.heares.2013.04.006CrossRefPubMedPubMedCentral

128.

Diesch E, Andermann M, Rupp A (2012) Is the effect of tinnitus on auditory steady-state response amplitude mediated by attention? Front Syst Neurosci 6:38. https://doi.org/10.3389/fnsys.2012.00038CrossRefPubMedPubMedCentral

129.

Müller N, Schlee W, Hartmann T, Lorenz I, Weisz N (2009) Top-down modulation of the auditory steady-state response in a task-switch paradigm. Front Hum Neurosci 3(1). https://doi.org/10.3389/neuro.09.001.2009

130.

Ross B, Picton TW, Herdman AT, Pantev C (2004) The effect of attention on the auditory steady-state response. Neurol Clin Neurophysiol 2004:22–22PubMed

131.

Salvi RJ, Wang J, Ding D (2000) Auditory plasticity and hyperactivity following cochlear damage. Hear Res 147:261–274. https://doi.org/10.1016/S0378-5955(00)00136-2CrossRefPubMed

132.

Diesch E, Andermann M, Flor H, Rupp A (2010) Interaction among the components of multiple auditory steady-state responses: enhancement in tinnitus patients, inhibition in controls. Neuroscience 167:540–553CrossRefPubMed

133.

McMahon CM, Ibrahim RK, Mathur A (2016) Cortical reorganisation during a 30-week tinnitus treatment program. PLoS ONE 11(2):e0148828. https://doi.org/10.1371/journal.pone.0148828CrossRefPubMedPubMedCentral

134.

Davis PB, Paki B, Hanley PJ (2007) Neuromonics tinnitus treatment: third clinical trial. Ear Hear 28(2):242–259CrossRefPubMed

135.

Lütkenhöner B, Krumbholz K, Seither-Preisler A (2003) Studies of tonotopy based on wave N100 of the auditory evoked field are problematic. Neuroimage 19(3):935–949. https://doi.org/10.1016/S1053-8119(03)00172-1CrossRefPubMed

136.

Falet JPR, Côté J, Tarka V et al (2021) Mapping the human auditory cortex using spectrotemporal receptive fields generated with magnetoencephalography. Neuroimage 238:118222. https://doi.org/10.1016/j.neuroimage.2021.118222CrossRefPubMed

137.

Su L, Zulfiqar I, Jamshed F, Fonteneau E, Marslen-Wilson W (2014) Mapping tonotopic organization in human temporal cortex: representational similarity analysis in EMEG source space. Front Neurosci 8:368. https://doi.org/10.3389/fnins.2014.00368CrossRefPubMedPubMedCentral

138.

Haxby JV, Guntupalli JS, Connolly AC et al (2011) A common, high-dimensional model of the representational space in human ventral temporal cortex. Neuron 72(2):404–416. https://doi.org/10.1016/j.neuron.2011.08.026CrossRefPubMedPubMedCentral

139.

Roberts LE (2007) Residual inhibition. Prog Brain Res 166:487–495. https://doi.org/10.1016/S0079-6123(07)66047-6CrossRefPubMed

140.

Sekiya K, Takahashi M, Murakami S, Kakigi R, Okamoto H (2017) Broadened population-level frequency tuning in the auditory cortex of tinnitus patients. J Neurophysiol 117(3):1379–1384. https://doi.org/10.1152/jn.00385.2016CrossRefPubMedPubMedCentral

141.

Okamoto H, Stracke H, Zwitserlood P, Roberts LE, Pantev C (2009) Frequency-specific modulation of population-level frequency tuning in human auditory cortex. BMC Neurosci 10(1):1–14. https://doi.org/10.1186/1471-2202-10-1CrossRefPubMedPubMedCentral

142.

Roberts LE, Bosnyak DJ, Bruce IC, Gander PE, Paul BT (2015) Evidence for differential modulation of primary and nonprimary auditory cortex by forward masking in tinnitus. Hear Res 327:9–27. https://doi.org/10.1016/j.heares.2015.04.011CrossRefPubMed

143.

Sams M, Salmelin R (1994) Evidence of sharp frequency tuning in the human auditory cortex. Hear Res 75(1–2):67–74. https://doi.org/10.1016/0378-5955(94)90057-4CrossRefPubMed

144.

Weisz N, Wienbruch C, Dohrmann K, Elbert T (2005) Neuromagnetic indicators of auditory cortical reorganization of tinnitus. Brain 128(11):2722–2731. https://doi.org/10.1093/brain/awh588CrossRefPubMed

145.

Salvari V, Korth D, Paraskevopoulos E et al (2023) Tinnitus-frequency specific activity and connectivity: a MEG study. NeuroImage Clin 38:103379. https://doi.org/10.1016/j.nicl.2023.103379

146.

Kok TE, Domingo D, Hassan J et al (2022) Resting-state networks in tinnitus: a scoping review. Clin Neuroradiol 32(4):903–922. https://doi.org/10.1007/s00062-022-01170-1CrossRefPubMedPubMedCentral

147.

Wunderlich R, Lau P, Stein A et al (2015) Impact of spectral notch width on neurophysiological plasticity and clinical effectiveness of the tailor-made notched music training. PLoS ONE 10(9):e0138595. https://doi.org/10.1371/journal.pone.0138595CrossRefPubMedPubMedCentral

148.

Pantev C, Okamoto H, Teismann H (2012) Tinnitus: the dark side of the auditory cortex plasticity. Ann N Y Acad Sci 1252(1):253–258. https://doi.org/10.1111/j.1749-6632.2012.06452.xCrossRefPubMed

149.

Pape J, Paraskevopoulos E, Bruchmann M, Wollbrink A, Rudack C, Pantev C (2014) Playing and listening to tailor-made notched music: cortical plasticity induced by unimodal and multimodal training in tinnitus patients. Neural Plast 2014:516163. https://doi.org/10.1155/2014/516163

150.

Okamoto H, Stracke H, Stoll W, Pantev C (2010) Listening to tailor-made notched music reduces tinnitus loudness and tinnitus-related auditory cortex activity. National Academy of Sciences 107(3):1207–1210. https://doi.org/10.1073/pnas.0911268107CrossRef

151.

Stein A, Engell A, Junghoefer M et al (2015) Inhibition-induced plasticity in tinnitus patients after repetitive exposure to tailor-made notched music. Clin Neurophysiol 126(5):1007–1015. https://doi.org/10.1016/j.clinph.2014.08.017CrossRefPubMed

152.

Stein A, Engell A, Lau P et al (2015) Enhancing inhibition-induced plasticity in tinnitus–spectral energy contrasts in tailor-made notched music matter. PLoS ONE 10(5):e0126494. https://doi.org/10.1371/journal.pone.0126494CrossRefPubMedPubMedCentral

153.

Stein A, Engell A, Okamoto H et al (2013) Modulatory effects of spectral energy contrasts on lateral inhibition in the human auditory cortex: an MEG study. PLoS ONE 8(12):e80899. https://doi.org/10.1371/journal.pone.0080899CrossRefPubMedPubMedCentral

154.

Li LPH, Shiao AS, Li CT et al (2019) Steady-state auditory evoked fields reflect long-term effects of repetitive transcranial magnetic stimulation in tinnitus. Clin Neurophysiol 130(9):1665–1672. https://doi.org/10.1016/j.clinph.2019.05.022CrossRefPubMed

155.

Li LPH, Shiao AS, Chen KC et al (2012) Neuromagnetic index of hemispheric asymmetry prognosticating the outcome of sudden hearing loss. PLoS ONE 7(4):e35055. https://doi.org/10.1371/journal.pone.0035055CrossRefPubMedPubMedCentral

156.

Li LPH, Chen KC, Lee PL et al (2013) Neuromagnetic index of hemispheric asymmetry predicting long-term outcome in sudden hearing loss. Neuroimage 64:356–364. https://doi.org/10.1016/j.neuroimage.2012.09.002CrossRefPubMed

157.

Wang KW, Chang HH, Hsu CC et al (2015) Extractions of steady-state auditory evoked fields in normal subjects and tinnitus patients using complementary ensemble empirical mode decomposition. Biomed Eng Online 14(1):1–18. https://doi.org/10.1186/s12938-015-0062-0CrossRef

158.

Brozoski TJ, Bauer CA (2016) Animal models of tinnitus. Hear Res 338:88–97. https://doi.org/10.1016/j.heares.2015.10.011CrossRefPubMed

159.

Rogenmoser L, Kuśmierek P, Archakov D, Rauschecker JP (2022) The blinking eye as a window into tinnitus: a new animal model of tinnitus in the macaque. Hear Res 420:108517. https://doi.org/10.1016/j.heares.2022.108517CrossRefPubMed

160.

Brozoski TJ, Bauer CA (2014) Auditory neuronal networks and chronic tinnitus. In: Faingold CL, Blumenfeld H (eds) Neuronal networks in brain function, CNS disorders, and therapeutics. Academic Press, Waltham, MA, USA. https://doi.org/10.1016/B978-0-12-415804-7.00020-4

161.

Von der Behrens W (2014) Animal models of subjective tinnitus. Neural Plast 2014. https://doi.org/10.1155/2014/741452

162.

Baguley D, McFerran D, Hall D (2013) Tinnitus Lancet 382(9904):1600–1607. https://doi.org/10.1016/S0140-6736(13)60142-7CrossRefPubMed

163.

Biswas R, Lugo A, Akeroyd MA, Schlee W, Gallus S, Hall DA (2022) Tinnitus prevalence in Europe: a multi-country cross-sectional population study. Lancet Reg Health Eur 12:100250. https://doi.org/10.1016/j.lanepe.2021.100250CrossRefPubMed

164.

Oosterloo BC, Croll PH, Baatenburg de Jong RJ, Ikram MK, Goedegebure A (2021) Prevalence of tinnitus in an aging population and its relation to age and hearing loss. Otolaryngol Head Neck Surg 164(4):859–868. https://doi.org/10.1177/0194599820957296CrossRefPubMed

165.

World Health Organization (2021) World report on hearing. World Health Organization

166.

Al-Swiahb J, Park SN (2016) Characterization of tinnitus in different age groups: a retrospective review. Noise Health 18(83):214. https://doi.org/10.4103/1463-1741.189240CrossRefPubMedPubMedCentral

167.

Corlett PR, Horga G, Fletcher PC, Alderson-Day B, Schmack K, Powers AR (2019) Hallucinations and strong priors. Trends Cogn Sci 23(2):114–127. https://doi.org/10.1016/j.tics.2018.12.001CrossRefPubMed

168.

Schubert J, Gehmacher Q, Schmidt F, Hartmann T, Weisz N (2023) Prediction tendency, eye movements, and attention in a unified framework of neural speech tracking. bioRxiv. https://doi.org/10.1101/2023.06.27.546746

169.

Demarchi G, Sanchez G, Weisz N (2019) Automatic and feature-specific prediction-related neural activity in the human auditory system. Nat Commun 10(1):3440. https://doi.org/10.1038/s41467-019-11440-1CrossRefPubMedPubMedCentral

170.

Vanneste S, Song JJ, De Ridder D (2018) Thalamocortical dysrhythmia detected by machine learning. Nat Commun 9:1103. https://doi.org/10.1038/s41467-018-02820-0CrossRefPubMedPubMedCentral

171.

Donoghue T, Haller M, Peterson EJ et al (2020) Parameterizing neural power spectra into periodic and aperiodic components. Nat Neurosci 23:1655–1665. https://doi.org/10.1038/s41593-020-00744-xCrossRefPubMedPubMedCentral

172.

Dang HB, Maloof AC, Romalis MV (2010) Ultrahigh sensitivity magnetic field and magnetization measurements with an atomic magnetometer. Appl Phys Lett 97(15):151110

Title: Eavesdropping on Tinnitus Using MEG: Lessons Learned and Future Perspectives
Authors: Lisa Reisinger
Gianpaolo Demarchi
Nathan Weisz
Publication date: 28-11-2023
Publisher: Springer US
Keywords: Tinnitus
Magnetoencephalography
Published in: Journal of the Association for Research in Otolaryngology / Issue 6/2023
Print ISSN: 1525-3961
Electronic ISSN: 1438-7573
DOI: https://doi.org/10.1007/s10162-023-00916-z

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Eavesdropping on Tinnitus Using MEG: Lessons Learned and Future Perspectives

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

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