Skip to main content
Log in

Neuromodulation for tinnitus treatment: an overview of invasive and non-invasive techniques

神经调节方法治疗耳鸣——侵入性和非侵入性技术概述

  • Review
  • Published:
Journal of Zhejiang University-SCIENCE B Aims and scope Submit manuscript

Abstract

Tinnitus is defined as a perception of sound without any external sound source. Chronic tinnitus is a frequent condition that can affect the quality of life. So far, no causal cure for tinnitus has been documented, and most pharmacologic and psychosomatic treatment modalities aim to diminish tinnitus’ impact on the quality of life. Neuromodulation, a novel therapeutic modality, which aims at alternating nerve activity through a targeted delivery of a stimulus, has emerged as a potential option in tinnitus treatment. This review provides a brief overview of the current neuromodulation techniques as tinnitus treatment options. The main intention is to provide updated knowledge especially for medical professionals counselling tinnitus patients in this emerging field of medicine. Non-invasive methods such as repetitive transcranial magnetic stimulation, transcranial electrical stimulation, neurofeedback, and transcutaneous vagus nerve stimulation were included, as well as invasive methods such as implanted vagus nerve stimulation and invasive brain stimulation. Some of these neuromodulation techniques revealed promising results; nevertheless, further research is needed, especially regarding the pathophysiological principle as to how these neuromodulation techniques work and what neuronal change they induce. Various studies suggest that individually different brain states and networks are involved in the generation and perception of tinnitus. Therefore, in the future, individually tailored neuromodulation strategies could be a promising approach in tinnitus treatment for achieving a more substantial and longer lasting improvement of complaints.

概 要

耳鸣被定义为非外部声音产生的听觉感知, 慢性耳鸣是一种影响生活质量的常见病症。 目前为止, 尚无任何针对耳鸣诱因的治疗方法, 大部分的药理和心理治疗方法都旨在减少耳鸣对生活 质量的影响。 神经调节是一种新型的治疗方式, 该方法通过定向刺激来改变神经活动, 已经成为耳鸣治疗的一个潜在选择。 本文就当前神经调节技术治疗耳鸣做了简要概述, 主要目的是为相关人士提供更新的知识介绍, 特别是在这个新兴医学领域的专业工作者。 本文介绍了包括经颅磁重复刺激、 经颅电刺激、 神经反馈和经皮迷走神经刺激等非侵入性方法, 以及植入的迷走神经刺激和侵入性脑刺激等侵入性方法。 虽然一些研究已经展示了神经调节技术的良好应用前景, 但是相关的研究还需要加强, 尤其是关于神经调节的病理生理学原理, 即这些神经调节技术如何发挥作用以及神经调节所引起的神经元变化。 多项研究表明, 不同个体的大脑活动状态和神经连接网络都参与了对耳鸣的产生和感知。 因此, 未来个性化定制的神经调节策略可能是一个有前景的耳鸣治疗方法, 从而更显著、 更持久地改善这个常见病症状。

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Adjamian P, Hall DA, Palmer AR, et al., 2014. Neuroanatomical abnormalities in chronic tinnitus in the human brain. Neurosci Biobehav Rev, 45:119–133. https://doi.org/10.1016/j.neubiorev.2014.05.013

    Article  PubMed  PubMed Central  Google Scholar 

  • Anders M, Dvorakova J, Rathova L, et al., 2010. Efficacy of repetitive transcranial magnetic stimulation for the treatment of refractory chronic tinnitus: a randomized, placebo controlled study. Neuro Endocrinol Lett, 31(2):238–249.

    PubMed  Google Scholar 

  • Axelsson A, Ringdahl A, 1989. Tinnitus—a study of its prevalence and characteristics. Br J Audiol, 23(1):53–62. https://doi.org/10.3109/03005368909077819

    Article  CAS  PubMed  Google Scholar 

  • Bittar RG, Burn SC, Bain PG, et al., 2005a. Deep brain stimulation for movement disorders and pain. J Clin Neurosci, 12(4):457–463. https://doi.org/10.1016/j.jocn.2004.09.001

    Article  PubMed  Google Scholar 

  • Bittar RG, Kar-Purkayastha I, Owen SL, et al., 2005b. Deep brain stimulation for pain relief: a meta-analysis. J Clin Neurosci, 12(5):515–519. https://doi.org/10.1016/j.jocn.2004.10.005

    Article  PubMed  Google Scholar 

  • Chen R, Classen J, Gerloff C, et al., 1997. Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology, 48(5):1398–1403. https://doi.org/10.1212/WNL.48.5.1398

    Article  CAS  PubMed  Google Scholar 

  • Cheung SW, Larson PS, 2010. Tinnitus modulation by deep brain stimulation in locus of caudate neurons (area LC). Neuroscience, 169(4):1768–1778. https://doi.org/10.1016/j.neuroscience.2010.06.007

    Article  CAS  PubMed  Google Scholar 

  • Chung HK, Tsai CH, Lin YC, et al., 2012. Effectiveness of theta-burst repetitive transcranial magnetic stimulation for treating chronic tinnitus. Audiol Neurotol, 17(2):112–120. https://doi.org/10.1159/000330882

    Article  Google Scholar 

  • Claes L, Stamberger H, van de Heyning P, et al., 2014. Auditory cortex tACS and tRNS for tinnitus: single versus multiple sessions. Neural Plast, 2014:436713. https://doi.org/10.1155/2014/436713

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.2011.02.003

    Article  PubMed  Google Scholar 

  • Datta A, Bansal V, Diaz J, et al., 2009. Gyri-precise head model of transcranial direct current stimulation: improved spatial focality using a ring electrode versus conventional rectangular pad. Brain Stimul, 2(4):201–207. https://doi.org/10.1016/j.brs.2009.03.005

    Article  PubMed  PubMed Central  Google Scholar 

  • Davis A, Rafaie EA, 2000. Epidemiology of tinnitus. In: Tyler RS (Ed.), Tinnitus Handbook.

  • Singular, San Diego, CA. de Ridder D, Vanneste S, 2012. EEG driven tDCS versus bifrontal tDCS for tinnitus. Front Psychiatry, 3:84. https://doi.org/10.3389/fpsyt.2012.00084

    Google Scholar 

  • de Ridder D, Vanneste S, 2014. Targeting the parahippocampal area by auditory cortex stimulation in tinnitus. Brain Stimul, 7(5):709–717. https://doi.org/10.1016/j.brs.2014.04.004

    Article  PubMed  Google Scholar 

  • de Ridder D, de Mulder G, Walsh V, et al., 2004. Magnetic and electrical stimulation of the auditory cortex for intractable tinnitus: case report. J Neurosurg, 100(3):560–564.

    Article  PubMed  Google Scholar 

  • de Ridder D, de Mulder G, Verstraeten E, et al., 2006. Primary and secondary auditory cortex stimulation for intractable tinnitus. ORL J Otorhinolaryngol Relat Spec, 68(1):48–54, discussion 54–55. https://doi.org/10.1159/000090491

    Article  PubMed  Google Scholar 

  • de Ridder D, van der Loo E, van der Kelen K, et al., 2007a. Theta, alpha and beta burst transcranial magnetic stimulation: brain modulation in tinnitus. Int J Med Sci, 4(5): 237–241.

    Article  PubMed  PubMed Central  Google Scholar 

  • de Ridder D, van der Loo E, van der Kelen K, et al., 2007b. Do tonic and burst TMS modulate the lemniscal and extralemniscal system differentially? Int J Med Sci, 4(5): 242–246.

    Article  PubMed  PubMed Central  Google Scholar 

  • de Ridder D, Elgoyhen AB, Romo R, et al., 2011a. Phantom percepts: tinnitus and pain as persisting aversive memory networks. Proc Natl Acad Sci USA, 108(20):8075–8080. https://doi.org/10.1073/pnas.1018466108

    Article  PubMed  Google Scholar 

  • de Ridder D, van der Loo E, Vanneste S, et al., 2011b. Thetagamma dysrhythmia and auditory phantom perception. J Neurosurg, 114(4):912–921. https://doi.org/10.3171/2010.11.JNS10335

    Article  PubMed  Google Scholar 

  • de Ridder D, Song JJ, Vanneste S, 2013. Frontal cortex TMS for tinnitus. Brain Stimul, 6(3):355–362. https://doi.org/10.1016/j.brs.2012.07.002

    Article  PubMed  Google Scholar 

  • de Ridder D, Vanneste S, Weisz N, et al., 2014a. An integrative model of auditory phantom perception: tinnitus as a unified percept of interacting separable subnetworks. Neurosci Biobehav Rev, 44:16–32. https://doi.org/10.1016/j.neubiorev.2013.03.021

    Article  PubMed  Google Scholar 

  • de Ridder D, Vanneste S, Engineer ND, et al., 2014b. Safety and efficacy of vagus nerve stimulation paired with tones for the treatment of tinnitus: a case series. Neuromodulation, 17(2):170–179. https://doi.org/10.1111/ner.12127

    Article  PubMed  Google Scholar 

  • de Ridder D, Kilgard M, Engineer N, et al., 2015a. Placebocontrolled vagus nerve stimulation paired with tones in a patient with refractory tinnitus: a case report. Otol Neurotol, 36(4):575–580. https://doi.org/10.1097/MAO.0000000000000704

    Article  PubMed  Google Scholar 

  • de Ridder D, Vanneste S, Langguth B, et al., 2015b. Thalamocortical dysrhythmia: a theoretical update in tinnitus. Front Neurol, 6:124. https://doi.org/10.3389/fneur.2015.00124

    Article  PubMed  PubMed Central  Google Scholar 

  • de Ridder D, Joos K, Vanneste S, 2016. Anterior cingulate implants for tinnitus: report of 2 cases. J Neurosurg, 124(4): 893–901. https://doi.org/10.3171/2015.3.JNS142880

    Article  PubMed  Google Scholar 

  • Dobie RA, 2003. Depression and tinnitus. Otolaryngol Clin North Am, 36(2):383–388.

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Dohrmann K, Elbert T, Schlee W, et al., 2007b. Tuning the tinnitus percept by modification of synchronous brain activity. Restor Neurol Neurosci, 25(3–4): 371–378.

    PubMed  Google Scholar 

  • Edwards D, Cortes M, Datta A, et al., 2013. Physiological and modeling evidence for focal transcranial electrical brain stimulation in humans: a basis for high-definition tDCS. NeuroImage, 74:266–275. https://doi.org/10.1016/j.neuroimage.2013.01.042

    Article  PubMed  PubMed Central  Google Scholar 

  • Eggermont JJ, Roberts LE, 2004. The neuroscience of tinnitus. Trends Neurosci, 27(11):676–682. https://doi.org/10.1016/j.tins.2004.08.010

    Article  CAS  PubMed  Google Scholar 

  • Engineer ND, Moller AR, Kilgard MP, 2013. Directing neural plasticity to understand and treat tinnitus. Hear Res, 295: 58–66. https://doi.org/10.1016/j.heares.2012.10.001

    Article  PubMed  Google Scholar 

  • Faber M, Vanneste S, Fregni F, et al., 2012. Top down prefrontal affective modulation of tinnitus with multiple sessions of tDCS of dorsolateral prefrontal cortex. Brain Stimul, 5(4):492–498. https://doi.org/10.1016/j.brs.2011.09.003

    Article  PubMed  Google Scholar 

  • Fertonani A, Pirulli C, Miniussi C, 2011. Random noise stimulation improves neuroplasticity in perceptual learning. J Neurosci, 31(43):15416–15423. https://doi.org/10.1523/JNEUROSCI.2002-11.2011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Folmer RL, Griest SE, Meikle MB, et al., 1999. Tinnitus severity, loudness, and depression. Otolaryngol Head Neck Surg, 121(1):48–51. https://doi.org/10.1016/S0194-5998(99)70123-3

    Article  CAS  PubMed  Google Scholar 

  • Frank E, Schecklmann M, Landgrebe M, et al., 2012. Treatment of chronic tinnitus with repeated sessions of prefrontal transcranial direct current stimulation: outcomes from an open-label pilot study. J Neurol, 259(2):327–333. https://doi.org/10.1007/s00415-011-6189-4

    Article  PubMed  Google Scholar 

  • Fregni F, Marcondes R, Boggio PS, et al., 2006. Transient tinnitus suppression induced by repetitive transcranial magnetic stimulation and transcranial direct current stimulation. Eur J Neurol, 13(9):996–1001. https://doi.org/10.1111/j.1468-1331.2006.01414.x

    Article  CAS  PubMed  Google Scholar 

  • Garin P, Gilain C, van Damme JP, et al., 2011. Short- and long-lasting tinnitus relief induced by transcranial direct current stimulation. J Neurol, 258(11):1940–1948. https://doi.org/10.1007/s00415-011-6037-6

    Article  PubMed  PubMed Central  Google Scholar 

  • Gosepath K, Nafe B, Ziegler E, et al., 2001. Neurofeedback in therapy of tinnitus. HNO, 49(1):29–35 (in German). https://doi.org/10.1007/s001060050704

    Article  CAS  PubMed  Google Scholar 

  • Hartmann T, Lorenz I, Müller N, et al., 2014. The effects of neurofeedback on oscillatory processes related to tinnitus. Brain Topogr, 27(1):149–157. https://doi.org/10.1007/s10548-013-0295-9

    Article  PubMed  Google Scholar 

  • Hoare DJ, Stacey PC, Hall DA, 2010. The efficacy of auditory perceptual training for tinnitus: a systematic review. Ann Behav Med, 40(3):313–324. https://doi.org/10.1007/s12160-010-9213-5

    Article  PubMed  PubMed Central  Google Scholar 

  • Hoare DJ, van Labeke N, McCormack A, et al., 2014. Gameplay as a source of intrinsic motivation in a randomized controlled trial of auditory training for tinnitus. PLoS ONE, 9(9):e107430. https://doi.org/10.1371/journal.pone.0107430

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoare DJ, Adjamian P, Sereda M, 2016. Electrical stimulation of the ear, head, cranial nerve, or cortex for the treatment of tinnitus: a scoping review. Neural Plast, 2016:5130503. https://doi.org/10.1155/2016/5130503

    Article  PubMed  PubMed Central  Google Scholar 

  • Hoffman HJ, Reed GW, 2004. Epidemiology of tinnitus. In: Snow JB (Ed.), Tinnitus: Theory and Management. BC Decker Inc., Hamilton, London, p.16-41.

  • Hoffman RE, Cavus I, 2002. Slow transcranial magnetic stimulation, long-term depotentiation, and brain hyperexcitability disorders. Am J Psychiatry, 159(7):1093–1102. https://doi.org/10.1176/appi.ajp.159.7.1093

    Article  PubMed  Google Scholar 

  • Hyvärinen P, Yrttiaho S, Lehtimäki J, et al., 2015. Transcutaneous vagus nerve stimulation modulates tinnitus-related beta- and gamma-band activity. Ear Hear, 36(3):e76-e85. https://doi.org/10.1097/AUD.0000000000000123

    Article  PubMed  Google Scholar 

  • Jackson P, 1985. A comparison of the effects of eighth nerve section with lidocaine on tinnitus. J Laryngol Otol, 99(7): 663–666.

    Article  CAS  PubMed  Google Scholar 

  • Jastreboff PJ, 1990. Phantom auditory perception (tinnitus): mechanisms of generation and perception. Neurosci Res, 8(4):221–254. https://doi.org/10.1016/0168-0102(90)90031-9

    Article  CAS  PubMed  Google Scholar 

  • Joliot M, Ribary U, Llinás R, 1994. Human oscillatory brain activity near 40Hz coexists with cognitive temporal binding. Proc Natl Acad Sci USA, 91(24):11748–11751.

    Article  CAS  PubMed  Google Scholar 

  • Joos K, de Ridder D, van de Heyning P, et al., 2014. Polarity specific suppression effects of transcranial direct current stimulation for tinnitus. Neural Plast, 2014:930860. https://doi.org/10.1155/2014/930860

    Article  PubMed  PubMed Central  Google Scholar 

  • Joos K, de Ridder D, Vanneste S, 2015. The differential effect of low-versus high-frequency random noise stimulation in the treatment of tinnitus. Exp Brain Res, 233(5): 1433–1440. https://doi.org/10.1007/s00221-015-4217-9

    Article  PubMed  Google Scholar 

  • Kaltenbach JA, Afman CE, 2000. Hyperactivity in the dorsal cochlear nucleus after intense sound exposure and its resemblance to tone-evoked activity: a physiological model for tinnitus. Hear Res, 140(1–2): 165–172. https://doi.org/10.1016/S0378-5955(99)00197-5

    Article  CAS  PubMed  Google Scholar 

  • Khedr EM, Rothwell JC, Ahmed MA, et al., 2008. Effect of daily repetitive transcranial magnetic stimulation for treatment of tinnitus: comparison of different stimulus frequencies. J Neurol Neurosurg Psychiat, 79(2):212–215. https://doi.org/10.1136/jnnp.2007.127712

    Article  CAS  PubMed  Google Scholar 

  • Khedr EM, Rothwell JC, El-Atar A, 2009. One-year follow up of patients with chronic tinnitus treated with left temporoparietal rTMS. Eur J Neurol, 16(3):404–408. https://doi.org/10.1111/j.1468-1331.2008.02522.x

    Article  CAS  PubMed  Google Scholar 

  • Kilgard MP, Merzenich MM, 1998a. Cortical map reorganization enabled by nucleus basalis activity. Science, 279(5357): 1714–1718. https://doi.org/10.1126/science.279.5357.1714

    Article  CAS  PubMed  Google Scholar 

  • Kilgard MP, Merzenich MM, 1998b. Plasticity of temporal information processing in the primary auditory cortex. Nat Neurosci, 1(8):727–731. https://doi.org/10.1038/3729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kleinjung T, Eichhammer P, Langguth B, et al., 2005. Longterm effects of repetitive transcranial magnetic stimulation (rTMS) in patients with chronic tinnitus. Otolaryngol Head Neck Surg, 132(4):566–569. https://doi.org/10.1016/j.otohns.2004.09.134

    Article  PubMed  Google Scholar 

  • 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.2007.12.022

    Article  PubMed  Google Scholar 

  • Koller WC, Lyons KE, Wilkinson SB, et al., 1999. Efficacy of unilateral deep brain stimulation of the VIM nucleus of the thalamus for essential head tremor. Movement Disord, 14(5):847–850. https://doi.org/10.1002/1531-8257(199909)14:5<847::AI D-MDS1021>3.0.CO;2-G

    Article  CAS  PubMed  Google Scholar 

  • Krack P, Batir A, van Blercom N, et al., 2003. Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson’s disease. N Engl J Med, 349(20):1925–1934. https://doi.org/10.1056/NEJMoa035275

    Article  CAS  PubMed  Google Scholar 

  • Kreuzer PM, Landgrebe M, Schecklmann M, et al., 2011. Can temporal repetitive transcranial magnetic stimulation be enhanced by targeting affective components of tinnitus with frontal rTMS? A randomized controlled pilot trial.Front Syst Neurosci, 5:88. https://doi.org/10.3389/fnsys.2011.00088

    Google Scholar 

  • Kreuzer PM, Landgrebe M, Husser O, et al., 2012. Transcutaneous vagus nerve stimulation: retrospective assessment of cardiac safety in a pilot study. Front Psychiatry, 3:70. https://doi.org/10.3389/fpsyt.2012.00070

    Article  PubMed  PubMed Central  Google Scholar 

  • Kreuzer PM, Landgrebe M, Resch M, et al., 2014. Feasibility, safety and efficacy of transcutaneous vagus nerve stimulation in chronic tinnitus: an open pilot study. Brain Stimul, 7(5):740–747. https://doi.org/10.1016/j.brs.2014.05.003

    Article  PubMed  Google Scholar 

  • Langguth B, Schecklmann M, Lehner A, et al., 2012. Neuroimaging and neuromodulation: complementary approaches for identifying the neuronal correlates of tinnitus. Front Syst Neurosci, 6:15. https://doi.org/10.3389/fnsys.2012.00015

    Article  PubMed  PubMed Central  Google Scholar 

  • Langguth B, Kreuzer PM, Kleinjung T, et al., 2013. Tinnitus: causes and clinical management. Lancet Neurol, 12(9): 920–930. https://doi.org/10.1016/S1474-4422(13)70160-1

    Article  PubMed  Google Scholar 

  • Langguth B, Landgrebe M, Frank E, et al., 2014. Efficacy of different protocols of transcranial magnetic stimulation for the treatment of tinnitus: pooled analysis of two randomized controlled studies. World J Biol Psychiatry, 15(4):276–285. https://doi.org/10.3109/15622975.2012.708438

    Article  CAS  PubMed  Google Scholar 

  • Lansbergen MM, van Dongen-Boomsma M, Buitelaar JK, et al., 2011. ADHD and EEG-neurofeedback: a doubleblind randomized placebo-controlled feasibility study. J Neural Transm, 118(2):275–284. https://doi.org/10.1007/s00702-010-0524-2

    Article  CAS  PubMed  Google Scholar 

  • Leaver AM, Renier L, Chevillet MA, et al., 2011. Dysregulation of limbic and auditory networks in tinnitus. Neuron, 69(1):33–43. https://doi.org/10.1016/j.neuron.2010.12.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leaver AM, Seydell-Greenwald A, Turesky TK, et al., 2012. Cortico-limbic morphology separates tinnitus from tinnitus distress. Front Syst Neurosci, 6:21. https://doi.org/10.3389/fnsys.2012.00021

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Leaver AM, Turesky TK, Seydell-Greenwald A, et al., 2016b. Intrinsic network activity in tinnitus investigated using functional MRI. Hum Brain Mapp, 37(8):2717–2735. https://doi.org/10.1002/hbm.23204

    Article  PubMed  PubMed Central  Google Scholar 

  • Lee HY, Yoo SD, Ryu EW, et al., 2013. Short term effects of repetitive transcranial magnetic stimulation in patients with catastrophic intractable tinnitus: preliminary report. Clin Exp Otorhinolaryngol, 6(2):63–67. https://doi.org/10.3342/ceo.2013.6.2.63

    Article  PubMed  PubMed Central  Google Scholar 

  • Lefaucheur JP, Andre-Obadia N, Antal A, et al., 2014. Evidencebased guidelines on the therapeutic use of repetitive transcranial magnetic stimulation (rTMS). Clin Neurophysiol, 125(11):2150–2206. https://doi.org/10.1016/j.clinph.2014.05.021

    Article  PubMed  Google Scholar 

  • Lehner A, Schecklmann M, Kreuzer PM, et al., 2013a. Comparing single-site with multisite rTMS for the treatment of chronic tinnitus—clinical effects and neuroscientific insights: study protocol for a randomized controlled trial. Trials, 14(1):269. https://doi.org/10.1186/1745-6215-14-269

    Article  PubMed  PubMed Central  Google Scholar 

  • Lehner A, Schecklmann M, Poeppl TB, et al., 2013b. Multisite rTMS for the treatment of chronic tinnitus: stimulation of the cortical tinnitus network—a pilot study. Brain Topogr, 26(3):501–510. https://doi.org/10.1007/s10548-012-0268-4

    Article  PubMed  Google Scholar 

  • Lehner A, Schecklmann M, Poeppl TB, et al., 2015. Efficacy and safety of repeated courses of rTMS treatment in patients with chronic subjective tinnitus. BioMed Res Int, 2015:975808. https://doi.org/10.1155/2015/975808

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lehtimӓki J, Hyvӓrinen P, Ylikoski M, et al., 2013. Transcutaneous vagus nerve stimulation in tinnitus: a pilot study. Acta Oto-Laryngol, 133(4):378–382. https://doi.org/10.3109/00016489.2012.750736

    Article  Google Scholar 

  • Li TT, Wang ZJ, Yang SB, et al., 2015. Transcutaneous electrical stimulation at auricular acupoints innervated by auricular branch of vagus nerve pairing tone for tinnitus: study protocol for a randomized controlled clinical trial. Trials, 16(1):101. https://doi.org/10.1186/s13063-015-0630-4

    Article  PubMed  PubMed Central  Google Scholar 

  • Llinás RR, Ribary U, Jeanmonod D, et al., 1999. Thalamocortical dysrhythmia: a neurological and neuropsychiatric syndrome characterized by magnetoencephalography. Proc Natl Acad Sci USA, 96(26):15222–15227.

    Article  PubMed  Google Scholar 

  • Llinás R, Urbano FJ, Leznik E, et al., 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.2005.04.006

    Article  CAS  PubMed  Google Scholar 

  • Lorenz I, Muller N, Schlee W, et al., 2009. Loss of alpha power is related to increased gamma synchronization— a marker of reduced inhibition in tinnitus? Neurosci Lett, 453(3):225–228. https://doi.org/10.1016/j.neulet.2009.02.028

    Article  CAS  PubMed  Google Scholar 

  • Lubar JF, Bahler WW, 1976. Behavioral management of epileptic seizures following EEG biofeedback training of the sensorimotor rhythm. Biofeedback Self Regul, 1(1):77–104.

    Article  CAS  PubMed  Google Scholar 

  • Lubar JF, Shouse MN, 1976. EEG and behavioral changes in a hyperkinetic child concurrent with training of the sensorimotor rhythm (SMR): a preliminary report. Biofeedback Self Regul, 1(3):293–306.

    Article  CAS  PubMed  Google Scholar 

  • Marchand S, Kupers RC, Bushnell MC, et al., 2003. Analgesic and placebo effects of thalamic stimulation. Pain, 105(3): 481–488. https://doi.org/10.1016/S0304-3959(03)00265-3

    Article  PubMed  Google Scholar 

  • Marcondes RA, Sanchez TG, Kii MA, et al., 2010. Repetitive transcranial magnetic stimulation improve tinnitus in normal hearing patients: a double-blind controlled, clinicaland neuroimaging outcome study. Eur J Neurol, 17(1): 38–44. https://doi.org/10.1111/j.1468-1331.2009.02730.x

    Article  CAS  PubMed  Google Scholar 

  • Mennemeier M, Chelette KC, Allen S, et al., 2011. Variable changes in PET activity before and after rTMS treatment for tinnitus. Laryngoscope, 121(4):815–822. https://doi.org/10.1002/lary.21425

    Article  PubMed  PubMed Central  Google Scholar 

  • Meyer M, Neff P, Liem F, et al., 2016. Differential tinnitusrelated neuroplastic alterations of cortical thickness and surface area. Hear Res, 342:1–12. https://doi.org/10.1016/j.heares.2016.08.016

    Article  PubMed  Google Scholar 

  • Miranda PC, Lomarev M, Hallett M, 2006. Modeling the current distribution during transcranial direct current stimulation. Clin Neurophysiol, 117(7):1623–1629. https://doi.org/10.1016/j.clinph.2006.04.009

    Article  PubMed  Google Scholar 

  • Mühlau M, Rauschecker JP, Oestreicher E, et al., 2006. Structural brain changes in tinnitus. Cerebral Cortex, 16(9):1283–1288. https://doi.org/10.1093/cercor/bhj070

    Article  PubMed  Google Scholar 

  • Mühlnickel W, Elbert T, Taub E, et al., 1998. Reorganization of auditory cortex in tinnitus. Proc Natl Acad Sci USA, 95(17):10340–10343. https://doi.org/10.1073/pnas.95.17.10340

    Article  PubMed  Google Scholar 

  • Newman CW, Jacobson GP, Spitzer JB, 1996. Development of the Tinnitus Handicap Inventory. Arch Otolaryngol Head Neck Surg, 122(2):143–148. https://doi.org/10.1001/archotol.1996.01890140029007

    Article  CAS  PubMed  Google Scholar 

  • Nondahl DM, Cruickshanks KJ, Dalton DS, et al., 2007. The impact of tinnitus on quality of life in older adults. J Am Acad Audiol, 18(3):257–266. https://doi.org/10.3766/jaaa.18.3.7

    Article  PubMed  Google Scholar 

  • Owen SL, Green AL, Stein JF, et al., 2006. Deep brain stimulation for the alleviation of post-stroke neuropathic pain. Pain, 120(1–2): 202–206. https://doi.org/10.1016/j.pain.2005.09.035

    Article  PubMed  Google Scholar 

  • Pandya DN, Rosene DL, Doolittle AM, 1994. Corticothalamic connections of auditory-related areas of the temporal lobe in the rhesus monkey. J Comp Neurol, 345(3):447–471. https://doi.org/10.1002/cne.903450311

    Article  CAS  PubMed  Google Scholar 

  • Paulus W, 2011. Transcranial electrical stimulation (tES-tDCS; tRNS, tACS) methods. Neuropsychol Rehab, 21(5):602–617. https://doi.org/10.1080/09602011.2011.557292

    Article  Google Scholar 

  • Prestes R, Daniela G, 2009. Impact of tinnitus on quality of life, loudness and pitch match, and high-frequency audiometry. Int Tinnitus J, 15(2):134–138.

    PubMed  Google Scholar 

  • Punte AK, Vermeire K, Hofkens A, et al., 2011. Cochlear implantation as a durable tinnitus treatment in singlesided deafness. Cochlear Implants Int, 12(Suppl 1): S26-S29. https://doi.org/10.1179/146701011X13001035752336

    Google Scholar 

  • Ramos Á, Polo R, Masgoret E, et al., 2012. Cochlear implant in patients with sudden unilateral sensorineural hearing loss and associated tinnitus. Acta Otorrinolaringol Esp, 63(1):15–20. https://doi.org/10.1016/j.otorri.2011.07.004

    Article  PubMed  Google Scholar 

  • Rauschecker JP, Leaver AM, Mühlau M, 2010. Tuning out the noise: limbic-auditory interactions in tinnitus. Neuron, 66(6):819–826. https://doi.org/10.1016/j.neuron.2010.04.032

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rauschecker JP, May ES, Maudoux A, et al., 2015. Frontostriatal gating of tinnitus and chronic pain. Trends Cogn Sci, 19(10):567–578. https://doi.org/10.1016/j.tics.2015.08.002

    Article  PubMed  PubMed Central  Google Scholar 

  • Rehncrona S, Johnels B, Widner H, et al., 2003. Long-term efficacy of thalamic deep brain stimulation for tremor: double-blind assessments. Mov Disord, 18(2):163–170. https://doi.org/10.1002/mds.10309

    Article  PubMed  Google Scholar 

  • Rossi S, de Capua A, Ulivelli M, et al., 2007. Effects of repetitive transcranial magnetic stimulation on chronic tinnitus: a randomised, crossover, double blind, placebo controlled study. J Neurol Neurosurg Psychiatry, 78(8): 857–863. https://doi.org/10.1136/jnnp.2006.105007

    Article  PubMed  PubMed Central  Google Scholar 

  • Saiote C, Polanía R, Rosenberger K, et al., 2013. Highfrequency TRNS reduces BOLD activity during visuomotor learning. PLoS ONE, 8(3):e59669. https://doi.org/10.1371/journal.pone.0059669

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salvi RJ, Wang J, Ding D, 2000. Auditory plasticity and hyperactivity following cochlear damage. Hear Res, 147(1-2): 261–274. https://doi.org/10.1016/S0378-5955(00)00136-2

    Article  CAS  PubMed  Google Scholar 

  • Schenk S, Lamm K, Gündel H, et al., 2005. Neurofeedbackbased EEG alpha and EEG beta training. Effectiveness in patients with chronically decompensated tinnitus. HNO, 53(1):29–37 (in German). https://doi.org/10.1007/s00106-004-1066-4

    CAS  PubMed  Google Scholar 

  • Schlee W, Weisz N, Bertrand O, et al., 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.0003720

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schlee W, Mueller N, Hartmann T, et al., 2009. Mapping cortical hubs in tinnitus. BMC Biol, 7:80. https://doi.org/10.1186/1741-7007-7-80

    Article  PubMed  PubMed Central  Google Scholar 

  • Sedley W, Gander PE, Kumar S, et al., 2015. Intracranial mapping of a cortical tinnitus system using residual inhibition. Curr Biol, 25(9):1208–1214. https://doi.org/10.1016/j.cub.2015.02.075

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seidman MD, de Ridder D, Elisevich K, et al., 2008. Direct electrical stimulation of Heschl’s gyrus for tinnitus treatment. Laryngoscope, 118(3):491–500. https://doi.org/10.1097/MLG.0b013e31815daf5a

    Article  CAS  PubMed  Google Scholar 

  • Seydell-Greenwald A, Leaver AM, Turesky TK, et al., 2012. Functional MRI evidence for a role of ventral prefrontal cortex in tinnitus. Brain Res, 1485:22–39. https://doi.org/10.1016/j.brainres.2012.08.052

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seydell-Greenwald A, Raven EP, Leaver AM, et al., 2014. Diffusion imaging of auditory and auditory-limbic connectivity in tinnitus: preliminary evidence and methodological challenges. Neural Plast, 2014:145943. https://doi.org/10.1155/2014/145943

    Article  PubMed  PubMed Central  Google Scholar 

  • Shekhawat GS, Stinear CM, Searchfield GD, 2013. Transcranial direct current stimulation intensity and duration effects on tinnitus suppression. Neurorehab Neural Rep, 27(2):164–172. https://doi.org/10.1177/1545968312459908

    Article  Google Scholar 

  • Shekhawat GS, Sundram F, Bikson M, et al., 2016. Intensity, duration, and location of high-definition transcranial direct current stimulation for tinnitus relief. Neurorehabil Neural Repair, 30(4):349–359. https://doi.org/10.1177/1545968315595286

    Article  PubMed  Google Scholar 

  • Shi Y, Burchiel KJ, Anderson VC, et al., 2009. Deep brain stimulation effects in patients with tinnitus. Otolaryngol Head Neck Surg, 141(2):285–287. https://doi.org/10.1016/j.otohns.2009.05.020

    Article  PubMed  Google Scholar 

  • Siebner HR, Filipovic SR, Rowe JB, et al., 2003. Patients with focal arm dystonia have increased sensitivity to slowfrequency repetitive TMS of the dorsal premotor cortex. Brain, 126(12):2710–2725. https://doi.org/10.1093/brain/awg282

    Article  PubMed  Google Scholar 

  • Smit JV, Janssen ML, Engelhard M, et al., 2016. The impact of deep brain stimulation on tinnitus. Surg Neurol Int, 7(Suppl 35): S848-S854. https://doi.org/10.4103/2152-7806.194156

    Book  Google Scholar 

  • Soleimani R, Jalali MM, Hasandokht T, 2016. Therapeutic impact of repetitive transcranial magnetic stimulation (rTMS) on tinnitus: a systematic review and meta-analysis. Eur Arch Oto-Rhino-Laryngol, 273(7):1663–1675. https://doi.org/10.1007/s00405-015-3642-5

    Article  Google Scholar 

  • Song JJ, Vanneste S, van de Heyning P, et al., 2012. Transcranial direct current stimulation in tinnitus patients: a systemic review and meta-analysis. Sci World J, 2012: 427941. https://doi.org/10.1100/2012/427941

    Google Scholar 

  • Tanibuchi I, Goldman-Rakic PS, 2003. Dissociation of spatial-, object-, and sound-coding neurons in the mediodorsal nucleus of the primate thalamus. J Neurophysiol, 89(2): 1067–1077. https://doi.org/10.1152/jn.00207.2002

    Article  PubMed  Google Scholar 

  • Terney D, Chaieb L, Moliadze V, et al., 2008. Increasing human brain excitability by transcranial high-frequency random noise stimulation. J Neurosci, 28(52):14147–14155. https://doi.org/10.1523/JNEUROSCI.4248-08.2008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Theodoroff SM, Folmer RL, 2013. Repetitive transcranial magnetic stimulation as a treatment for chronic tinnitus: a critical review. Otol Neurotol, 34(2):199–208.

    Article  PubMed  Google Scholar 

  • To WT, Ost J, Hart Jr J, et al., 2017. The added value of auditory cortex transcranial random noise stimulation (tRNS) after bifrontal transcranial direct current stimulation (tDCS) for tinnitus. J Neural Transm, 124(1):79–88. https://doi.org/10.1007/s00702-016-1634-2

    Article  PubMed  Google Scholar 

  • van de Heyning P, Vermeire K, Diebl M, et al., 2008. Incapacitating unilateral tinnitus in single-sided deafness treated by cochlear implantation. Ann Otol Rhinol Laryngol, 117(9):645–652. https://doi.org/10.1177/000348940811700903

    Article  PubMed  Google Scholar 

  • van Doren J, Langguth B, Schecklmann M, 2014. Electroencephalographic effects of transcranial random noise stimulation in the auditory cortex. Brain Stimul, 7(6): 807–812. https://doi.org/10.1016/j.brs.2014.08.007

    Article  PubMed  Google Scholar 

  • Vanneste S, de Ridder D, 2011. Bifrontal transcranial direct current stimulation modulates tinnitus intensity and tinnitusdistress-related brain activity. Eur J Neurosci, 34(4):605–614. https://doi.org/10.1111/j.1460-9568.2011.07778.x

    Article  PubMed  Google Scholar 

  • Vanneste S, de Ridder D, 2012. Noninvasive and invasive neuromodulation for the treatment of tinnitus: an overview. Neuromodulation, 15(4):350–360. https://doi.org/10.1111/j.1525-1403.2012.00447.x

    Article  PubMed  Google Scholar 

  • Vanneste S, de Ridder D, 2013. Differences between a single session and repeated sessions of 1Hz TMS by doublecone coil prefrontal stimulation for the improvement of tinnitus. Brain Stimul, 6(2):155–159. https://doi.org/10.1016/j.brs.2012.03.019

    Article  PubMed  Google Scholar 

  • Vanneste S, Plazier M, Ost J, et al., 2010a. Bilateral dorsolateral prefrontal cortex modulation for tinnitus by transcranial direct current stimulation: a preliminary clinical study. Exp Brain Res, 202(4):779–785. https://doi.org/10.1007/s00221-010-2183-9

    Article  PubMed  Google Scholar 

  • Vanneste S, Plazier M, van der Loo E, et al., 2010b. The neural correlates of tinnitus-related distress. NeuroImage, 52(2): 470–480. https://doi.org/10.1016/j.neuroimage.2010.04.029

    Article  PubMed  Google Scholar 

  • Vanneste S, Focquaert F, van de Heyning P, et al., 2011a. Different resting state brain activity and functional connectivity in patients who respond and not respond to bifrontal tDCS for tinnitus suppression. Exp Brain Res, 210(2):217–227. https://doi.org/10.1007/s00221-011-2617-z

    Article  PubMed  Google Scholar 

  • Vanneste S, van de Heyning P, de Ridder D, 2011b. 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.x

    Article  PubMed  Google Scholar 

  • Vanneste S, Walsh V, van de Heyning P, et al., 2013a. Comparing immediate transient tinnitus suppression using tACS and tDCS: a placebo-controlled study. Exp Brain Res, 226(1):25–31. https://doi.org/10.1007/s00221-013-3406-7

    Article  PubMed  Google Scholar 

  • Vanneste S, Fregni F, de Ridder D, 2013b. Head-to-head comparison of transcranial random noise stimulation, transcranial AC stimulation, and transcranial DC stimulation for Tinnitus. Front Psychiatry, 4:158. https://doi.org/10.3389/fpsyt.2013.00158

    Article  PubMed  PubMed Central  Google Scholar 

  • Vidailhet M, Yelnik J, Lagrange C, et al., 2009. Bilateral pallidal deep brain stimulation for the treatment of patients with dystonia-choreoathetosis cerebral palsy: a prospective pilot study. Lancet Neurol, 8(8):709–717. https://doi.org/10.1016/S1474-4422(09)70151-6

    Article  PubMed  Google Scholar 

  • Weidt S, Delsignore A, Meyer M, et al., 2016. Which tinnitusrelated characteristics affect current health-related quality of life and depression? A cross-sectional cohort study. Psychiatry Res, 237:114–121. https://doi.org/10.1016/j.psychres.2016.01.065

    Article  PubMed  Google Scholar 

  • Weisz N, Moratti S, Meinzer M, et al., 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.0020153

    Article  PubMed  PubMed Central  Google Scholar 

  • Weisz N, Dohrmann K, Elbert T, 2007. The relevance of spontaneous activity for the coding of the tinnitus sensation. Prog Brain Res, 166:61–70. https://doi.org/10.1016/S0079-6123(07)66006-3

    Article  PubMed  Google Scholar 

  • Zaehle T, Lenz D, Ohl FW, et al., 2010a. Resonance phenomena in the human auditory cortex: individual resonance frequencies of the cerebral cortex determine electrophysiological responses. Exp Brain Res, 203(3):629–635. https://doi.org/10.1007/s00221-010-2265-8

    Article  CAS  PubMed  Google Scholar 

  • Zaehle T, Rach S, Herrmann CS, 2010b. Transcranial alternating current stimulation enhances individual alpha activity in human EEG. PLoS ONE, 5(11):e13766. https://doi.org/10.1371/journal.pone.0013766

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zaghi S, de Freitas Rezende L, de Oliveira LM, et al., 2010a. Inhibition of motor cortex excitability with 15Hz transcranial alternating current stimulation (tACS). Neurosci Lett, 479(3):211–214. https://doi.org/10.1016/j.neulet.2010.05.060

    Article  CAS  PubMed  Google Scholar 

  • Zaghi S, Acar M, Hultgren B, et al., 2010b. Noninvasive brain stimulation with low-intensity electrical currents: putative mechanisms of action for direct and alternating current stimulation. Neuroscientist, 16(3):285–307. https://doi.org/10.1177/1073858409336227

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nicole Peter.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Peter, N., Kleinjung, T. Neuromodulation for tinnitus treatment: an overview of invasive and non-invasive techniques. J. Zhejiang Univ. Sci. B 20, 116–130 (2019). https://doi.org/10.1631/jzus.B1700117

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1631/jzus.B1700117

Key words

关键词

CLC number

Navigation