Direct and Transcutaneous Vagus Nerve Stimulation for Treatment of Tinnitus: A Scoping Review

Natalia Yakunina, Eui-Cheol Nam, Natalia Yakunina, Eui-Cheol Nam

Abstract

Recent animal research has shown that vagus nerve stimulation (VNS) paired with sound stimuli can induce neural plasticity in the auditory cortex in a controlled manner. VNS paired with tones excluding the tinnitus frequency eliminated physiological and behavioral characteristics of tinnitus in noise-exposed rats. Several clinical trials followed and explored the effectiveness of VNS paired with sound stimuli for alleviating tinnitus in human subjects. Transcutaneous VNS (tVNS) has received increasing attention as a non-invasive alternative approach to tinnitus treatment. Several studies have also explored tVNS alone (not paired with sound stimuli) as a potential therapy for tinnitus. In this review, we discuss existing knowledge about direct and tVNS in terms of applicability, safety, and effectiveness in diminishing tinnitus symptoms in human subjects. This review includes all existing clinical and neuroimaging studies of tVNS alone or paired with acoustic stimulation in tinnitus patients and outlines the present limitations that must be overcome to maximize the potential of (t)VNS as a therapy for tinnitus.

Keywords: auricular branch of vagus nerve; neuromodulation; tinnitus; transcutaneous vagus nerve stimulation; vagus nerve stimulation.

Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Copyright © 2021 Yakunina and Nam.

Figures

FIGURE 1
FIGURE 1
(A) Acustom-built MRI-compatible tVNS stimulator used in the tVNS fMRI studies by Yakunina et al., 2017, (B) Six silver electrodes (four active, two reference electrodes). (C) tVNS stimulation locations: inner surface of the tragus (A), inferoposterior wall of the external acoustic meatus (B), cymba conchae (C), and earlobe (sham; D).
FIGURE 2
FIGURE 2
Activation maps induced by tVNS in the tragus (A), inferoposterior wall of the external acoustic meatus (B), concha (C), and earlobe (D). tVNS at the tragus and concha activated the locus coeruleus (LC) and nucleus of the solitary tract (NTS), while tVNS at the ear canal and earlobe did not activate either brain center.
FIGURE 3
FIGURE 3
Activations (red) and deactivations (blue) induced by tVNS at the tragus and cymba conchae in tinnitus patients. tVNS resulted in deactivation of the auditory and limbic systems, as well as a number of other cortical areas. ACC/MCC/PCC, anterior/middle/posterior cingulate cortex; Amyg, amygdala; AnG, angular gyrus; CC, corpus callosum; CBLL, cerebellum; FuG, fusiform gyrus; Hip, hippocampus; LiG, lingual gyrus; MOG, middle orbital gyrus; MTG/STG, middle/superior temporal gyrus; PCu, precuneus; PoG/PrG, postcentral/precentral gyrus; SFG, superior frontal gyrus; TMP, temporal pole.

References

    1. Adcock K. S., Chandler C., Buell E. P., Solorzano B. R., Loerwald K. W., Borland M. S., et al. (2020). Vagus nerve stimulation paired with tones restores auditory processing in a rat model of Rett syndrome. Brain Stimul. 13 1494–1503. 10.1016/j.brs.2020.08.006
    1. Al Omari A. I., Alzoubi F. Q., Alsalem M. M., Aburahma S. K., Mardini D. T., Castellanos P. F. (2017). The vagal nerve stimulation outcome, and laryngeal effect: otolaryngologists roles and perspective. Am. J. Otolaryngol. 38 408–413. 10.1016/j.amjoto.2017.03.011
    1. Badran B. W., Dowdle L. T., Mithoefer O. J., LaBate N. T., Coatsworth J., Brown J. C., et al. (2018). Neurophysiologic effects of transcutaneous auricular vagus nerve stimulation (taVNS) via electrical stimulation of the tragus: a concurrent taVNS/fMRI study and review. Brain Stimul. 11 492–500. 10.1016/j.brs.2017.12.009
    1. Baguley D., McFerran D., Hall D. (2013). Tinnitus. Lancet 382 1600–1607.
    1. Bajbouj M., Merkl A., Schlaepfer T. E., Frick C., Zobel A., Maier W., et al. (2010). Two-year outcome of vagus nerve stimulation in treatment-resistant depression. J. Clin. Psychopharmacol. 30 273–281.
    1. Bakin J. S., Weinberger N. M. (1996). Induction of a physiological memory in the cerebral cortex by stimulation of the nucleus basalis. Proc. Natl. Acad. Sci. U S A 93 11219–11224. 10.1073/pnas.93.20.11219
    1. Bear M. F., Singer W. (1986). Modulation of visual cortical plasticity by acetylcholine and noradrenaline. Nature 320 172–176. 10.1038/320172a0
    1. Ben-Menachem E. (2001). Vagus nerve stimulation, side effects, and long-term safety. J. Clin. Neurophys. 18 415–418. 10.1097/00004691-200109000-00005
    1. Berntson G. G., Sarter M., Cacioppo J. T. (1998). Anxiety and cardiovascular reactivity: the basal forebrain cholinergic link. Behav. Brain Res. 94 225–248. 10.1016/s0166-4328(98)00041-2
    1. Berthoud H., Neuhuber W. L. (2000). Functional and chemical anatomy of the afferent vagal system. Autonom. Neurosci. 85 1–17. 10.1016/s1566-0702(00)00215-0
    1. Bohning D. E., Lomarev M. P., Denslow S., Nahas Z., Shastri A., George M. S. (2001). Feasibility of vagus nerve stimulation-synchronized blood oxygenation level-dependent functional MRI. Invest. Radiol. 36 470–479. 10.1097/00004424-200108000-00006
    1. Bramham C. R., Messaoudi E. B. D. N. F. (2005). function in adult synaptic plasticity: the synaptic consolidation hypothesis. Prog. Neurobiol. 76 99–125. 10.1016/j.pneurobio.2005.06.003
    1. Buell E. P., Borland M. S., Loerwald K. W., Chandler C., Hays S. A., Engineer C. T., et al. (2019). Vagus nerve stimulation rate and duration determine whether sensory pairing produces neural plasticity. Neuroscience 406 290–299. 10.1016/j.neuroscience.2019.03.019
    1. Butt M. F., Albusoda A., Farmer A. D., Aziz Q. (2020). The anatomical basis for transcutaneous auricular vagus nerve stimulation. J. Anat. 236 588–611. 10.1111/joa.13122
    1. Chae J., Nahas Z., Lomarev M., Denslow S., Lorberbaum J. P., Bohning D. E., et al. (2003). review of functional neuroimaging studies of vagus nerve stimulation (VNS). J. Psychiatr. Res. 37 443–455. 10.1016/s0022-3956(03)00074-8
    1. Chen Y. C., Xia W., Chen H., Feng Y., Xu J. J., Gu J. P., 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 2384–2397. 10.1002/hbm.23525
    1. Childs J. E., Alvarez-Dieppa A. C., McIntyre C. K., Kroener S. (2015). Vagus nerve stimulation as a tool to induce plasticity in pathways relevant for extinction learning. JoVE 102:e53032.
    1. Darrow M. J., Mian T. M., Torres M., Haider Z., Danaphongse T., Rennaker Jr RL, et al. (2020a). Restoration of somatosensory function by pairing vagus nerve stimulation with tactile rehabilitation. Ann. Neurol. 194–205. 10.1002/ana.25664
    1. Darrow M. J., Mian T. M., Torres M., Haider Z., Danaphongse T., Seyedahmadi A., et al. (2020b). The tactile experience paired with vagus nerve stimulation determines the degree of sensory recovery after chronic nerve damage. Behav. Brain Res. 396:112910. 10.1016/j.bbr.2020.112910
    1. Davis A., Rafaie E. A. (2000). Epidemiology of tinnitus. Tinnitus Handbook 1:23.
    1. Dawson J., Pierce D., Dixit A., Kimberley T. J., Robertson M., Tarver B., et al. (2016). Safety, feasibility, and efficacy of vagus nerve stimulation paired with upper-limb rehabilitation after ischemic stroke. Stroke 47 143–150. 10.1161/strokeaha.115.010477
    1. De Ridder D., Kilgard M., Engineer N., Vanneste S. (2015). Placebo-controlled vagus nerve stimulation paired with tones in a patient with refractory tinnitus: a case report. Otol. Neurotol. 36 575–580. 10.1097/mao.0000000000000704
    1. De Ridder D., Vanneste S., Engineer N. D., Kilgard M. P. (2014a). Safety and efficacy of vagus nerve stimulation paired with tones for the treatment of tinnitus: a case series. Neuromodulation 17 170–179. 10.1111/ner.12127
    1. De Ridder D., Vanneste S., Weisz N., Londero A., Schlee W., Elgoyhen A. B., et al. (2014b). An integrative model of auditory phantom perception: tinnitus as a unified percept of interacting separable subnetworks. Neurosci. Biobehav. Rev. 44 16–32. 10.1016/j.neubiorev.2013.03.021
    1. Detari L., Juhasz G., Kukorelli T. (1983). Effect of stimulation of vagal and radial nerves on neuronal activity in the basal forebrain area of anaesthetized cats. Acta Physiol. Hung. 61 147–154.
    1. Dietrich S., Smith J., Scherzinger C., Hofmann-Preiss K., Freitag T., Eisenkolb A., et al. (2008). novel transcutaneous vagus nerve stimulation leads to brainstem and cerebral activations measured by functional MRI. Biomed. Tech. 53 104–111. 10.1515/bmt.2008.022
    1. Eggermont J. J., Roberts L. E. (2004). The neuroscience of tinnitus. Trends Neurosci. 27 676–682.
    1. Engineer C. T., Engineer N. D., Riley J. R., Seale J. D., Kilgard M. P. (2015). Pairing speech sounds with vagus nerve stimulation drives stimulus-specific cortical plasticity. Brain Stimul. 8 637–644. 10.1016/j.brs.2015.01.408
    1. Engineer C. T., Shetake J. A., Engineer N. D., Vrana W. A., Wolf J. T., Kilgard M. P. (2017). Temporal plasticity in auditory cortex improves neural discrimination of speech sounds. Brain stimul. 10 543–552. 10.1016/j.brs.2017.01.007
    1. Engineer N. D., Riley J. R., Seale J. D., Vrana W. A., Shetake J. A., Sudanagunta S. P., et al. (2011). Reversing pathological neural activity using targeted plasticity. Nature 470 101–104. 10.1038/nature09656
    1. Follesa P., Biggio F., Gorini G., Caria S., Talani G., Dazzi L., et al. (2007). Vagus nerve stimulation increases norepinephrine concentration and the gene expression of BDNF and bFGF in the rat brain. Brain Res. 1179 28–34. 10.1016/j.brainres.2007.08.045
    1. Frangos E., Komisaruk B. R. (2017). Access to vagal projections via cutaneous electrical stimulation of the neck: fMRI evidence in healthy humans. Brain Stimul. 10 19–27. 10.1016/j.brs.2016.10.008
    1. Frangos E., Ellrich J., Komisaruk B. R. (2015). Non-invasive Access to the Vagus Nerve Central Projections via Electrical Stimulation of the External Ear: fMRI Evidence in Humans. Brain Stimul. 8 624–636. 10.1016/j.brs.2014.11.018
    1. Groves D. A., Brown V. J. (2005). Vagal nerve stimulation: a review of its applications and potential mechanisms that mediate its clinical effects. Neurosci. Biobehav. Rev. 29 493–500. 10.1016/j.neubiorev.2005.01.004
    1. Hassert D., Miyashita T., Williams C. (2004). The effects of peripheral vagal nerve stimulation at a memory-modulating intensity on norepinephrine output in the basolateral amygdala. Behav. Neurosci. 118:79. 10.1037/0735-7044.118.1.79
    1. Hays S. A., Rennaker R. L., Kilgard M. P. (2013). Targeting plasticity with vagus nerve stimulation to treat neurological disease. Prog. Brain Res. 207 275–299. 10.1016/b978-0-444-63327-9.00010-2
    1. Henry T. R. (2002). Therapeutic mechanisms of vagus nerve stimulation. Neurology 59(6 Suppl. 4), S3–S14.
    1. Hyvarinen P., Yrttiaho S., Lehtimaki J., Ilmoniemi R. J., Makitie A., Ylikoski J., et al. (2015). Transcutaneous vagus nerve stimulation modulates tinnitus-related beta- and gamma-band activity. Ear. Hear. 36 e76–e85.
    1. Jastreboff P. J. (1990). Phantom auditory perception (tinnitus): mechanisms of generation and perception. Neurosci. Res. 8 221–254. 10.1016/0168-0102(90)90031-9
    1. Khodaparast N., Hays S. A., Sloan A. M., Hulsey D. R., Ruiz A., Pantoja M., et al. (2013). Vagus nerve stimulation during rehabilitative training improves forelimb strength following ischemic stroke. Neurobiol. Dis. 60 80–88. 10.1016/j.nbd.2013.08.002
    1. Kilgard M. P., Merzenich M. M. (1998). Cortical map reorganization enabled by nucleus basalis activity. Science 279 1714–1718. 10.1126/science.279.5357.1714
    1. Kimberley T. J., Pierce D., Prudente C. N., Francisco G. E., Yozbatiran N., Smith P., et al. (2018). Vagus nerve stimulation paired with upper limb rehabilitation after chronic stroke: a blinded randomized pilot study. Stroke 49 2789–2792. 10.1161/strokeaha.118.022279
    1. Kirkwood A., Rozas C., Kirkwood J., Perez F., Bear M. F. (1999). Modulation of long-term synaptic depression in visual cortex by acetylcholine and norepinephrine. J. Neurosci. 19 1599–1609. 10.1523/jneurosci.19-05-01599.1999
    1. Kiyokawa J., Yamaguchi K., Okada R., Maehara T., Akita K. (2014). Origin, course and distribution of the nerves to the posterosuperior wall of the external acoustic meatus. Anat. Sci. Int. 89 238–245. 10.1007/s12565-014-0231-4
    1. Knipper M., Van Dijk P., Nunes I., Rüttiger L., Zimmermann U. (2013). Advances in the neurobiology of hearing disorders: recent developments regarding the basis of tinnitus and hyperacusis. Prog. Neurobiol. 111 17–33. 10.1016/j.pneurobio.2013.08.002
    1. Kochilas H. L., Cacace A. T., Arnold A., Seidman M. D., Tarver W. B. (2020). Vagus nerve stimulation paired with tones for tinnitus suppression: Effects on voice and hearing. Laryngoscope Investigat. Otolaryngol. 5 286–296. 10.1002/lio2.364
    1. Kraus T., Hosl K., Kiess O., Schanze A., Kornhuber J., Forster C. B. O. L. D. (2007). fMRI deactivation of limbic and temporal brain structures and mood enhancing effect by transcutaneous vagus nerve stimulation. J. Neural. Transm. 114 1485–1493. 10.1007/s00702-007-0755-z
    1. Kraus T., Kiess O., Hosl K., Terekhin P., Kornhuber J., Forster C. C. N. S. B. O. L. D. (2013). fMRI effects of sham-controlled transcutaneous electrical nerve stimulation in the left outer auditory canal - a pilot study. Brain Stimul. 6 798–804. 10.1016/j.brs.2013.01.011
    1. Kreuzer P. M., Landgrebe M., Husser O., Resch M., Schecklmann M., Geisreiter F., et al. (2012). Transcutaneous vagus nerve stimulation: retrospective assessment of cardiac safety in a pilot study. Front. Psychiatr. 3:70. 10.3389/fpsyt.2012.00070
    1. Kreuzer P. M., Landgrebe M., Resch M., Husser O., Schecklmann M., Geisreiter F., et al. (2014). Feasibility, safety and efficacy of transcutaneous vagus nerve stimulation in chronic tinnitus: an open pilot study. Brain Stimul. 7 740–747. 10.1016/j.brs.2014.05.003
    1. Lehtimaki J., Hyvarinen P., Ylikoski M., Bergholm M., Makela J. P., Aarnisalo A., et al. (2013). Transcutaneous vagus nerve stimulation in tinnitus: a pilot study. Acta Otolaryngol. 133 378–382. 10.3109/00016489.2012.750736
    1. Leslie R., Gwyn D., Hopkins D. (1982). The central distribution of the cervical vagus nerve and gastric afferent and efferent projections in the rat. Brain Res. Bull. 8 37–43. 10.1016/0361-9230(82)90025-9
    1. Llanos F., McHaney J. R., Schuerman W. L., Han G. Y., Leonard M. K., Chandrasekaran B. (2020). Non-invasive peripheral nerve stimulation selectively enhances speech category learning in adults. Npj Sci. Learn. 5 1–11.
    1. Lomarev M., Denslow S., Nahas Z., Chae J. H., George M. S., Bohning D. E. (2002). Vagus nerve stimulation (VNS) synchronized BOLD fMRI suggests that VNS in depressed adults has frequency/dose dependent effects. J. Psychiatr. Res. 36 219–227. 10.1016/s0022-3956(02)00013-4
    1. Lulic D., Ahmadian A., Baaj A. A., Benbadis S. R., Vale F. L. (2009). Vagus nerve stimulation. Neurosurg. Focus 27:E5.
    1. Lv H., Zhao Y., Chen J., Wang D., Chen H. (2019). Vagus nerve stimulation for depression: a systematic review. Front. Psychol. 10:64. 10.3389/fpsyg.2019.00064
    1. Manta S., Dong J., Debonnel G., Blier P. (2009). Enhancement of the function of rat serotonin and norepinephrine neurons by sustained vagus nerve stimulation. J. Psychiatr. Neurosci. 34 272–280.
    1. Martins A. R. O., Froemke R. C. (2015). Coordinated forms of noradrenergic plasticity in the locus coeruleus and primary auditory cortex. Nat. Neurosci. 18 1483–1492. 10.1038/nn.4090
    1. Mega M. S., Cummings J. L., Salloway S., Malloy P. (1997). The limbic system: an anatomic, phylogenetic, and clinical perspective. J. Neuropsychiatr. Clin. Neurosci. 9 315–330. 10.1176/jnp.9.3.315
    1. Meyers E. C., Kasliwal N., Solorzano B. R., Lai E., Bendale G., Berry A., et al. (2019). Enhancing plasticity in central networks improves motor and sensory recovery after nerve damage. Nat. Comm. 10 1–14. 10.1155/2020/9484298
    1. Milby A. H., Halpern C. H., Baltuch G. H. (2008). Vagus nerve stimulation for epilepsy and depression. Neurotherapeutics 5 75–85.
    1. Muhlnickel W., Elbert T., Taub E., Flor H. (1998). Reorganization of auditory cortex in tinnitus. Proc. Natl. Acad. Sci. U S A 95 10340–10343. 10.1073/pnas.95.17.10340
    1. Nahas Z., Marangell L. B., Husain M. M., Rush A. J., Sackeim H. A., Lisanby S. H., et al. (2005). Two-year outcome of vagus nerve stimulation (VNS) for treatment of major depressive episodes. J. Clin. Psychiatr. 66 1097–1104. 10.4088/jcp.v66n0902
    1. Narayanan J. T., Watts R., Haddad N., Labar D. R., Li P. M., Filippi C. G. (2002). Cerebral activation during vagus nerve stimulation: a functional MR study. Epilepsia 43 1509–1514. 10.1046/j.1528-1157.2002.16102.x
    1. Nemeroff C. B., Mayberg H. S., Krahl S. E., McNamara J., Frazer A., Henry T. R., et al. (2006). therapy in treatment-resistant depression: clinical evidence and putative neurobiological mechanisms. Neuropsychopharmacology 31 1345–1355. 10.1038/sj.npp.1301082
    1. Noble L. J., Souza R. R., McIntyre C. K. (2019). Vagus nerve stimulation as a tool for enhancing extinction in exposure-based therapies. Psychopharmacology 236 355–367. 10.1007/s00213-018-4994-5
    1. Norena A. J., Eggermont J. J. (2003). Changes in spontaneous neural activity immediately after an acoustic trauma: implications for neural correlates of tinnitus. Hear Res. 183 137–153. 10.1016/s0378-5955(03)00225-9
    1. Ogbonnaya S., Kaliaperumal C. (2013). Vagal nerve stimulator: Evolving trends. J. Nat. Sci. Biol. Med. 4 8–13. 10.4103/0976-9668.107254
    1. Okamoto H., Stracke H., Stoll W., Pantev C. (2010). Listening to tailor-made notched music reduces tinnitus loudness and tinnitus-related auditory cortex activity. Proc. Natl. Acad. Sci. U S A 107 1207–1210. 10.1073/pnas.0911268107
    1. Pantev C., Okamoto H., Teismann H. (2012). Music-induced cortical plasticity and lateral inhibition in the human auditory cortex as foundations for tonal tinnitus treatment. Front. Syst. Neurosci. 6:50. 10.3389/fnsys.2012.00050
    1. Pantev C., Okamoto H., Ross B., Stoll W., Ciurlia−Guy E., Kakigi R., et al. (2004). Lateral inhibition and habituation of the human auditory cortex. Eur. J. Neurosci. 19 2337–2344. 10.1111/j.0953-816x.2004.03296.x
    1. Peña D. F., Childs J. E., Willett S., Vital A., McIntyre C. K., Kroener S. (2014). Vagus nerve stimulation enhances extinction of conditioned fear and modulates plasticity in the pathway from the ventromedial prefrontal cortex to the amygdala. Front. Behav. Neurosci. 8:327. 10.3389/fnbeh.2014.00327
    1. Peuker E. T., Filler T. J. (2002). The nerve supply of the human auricle. Clin. Anat. 15 35–37. 10.1002/ca.1089
    1. Polak T., Markulin F., Ehlis A., Langer J. B., Ringel T. M., Fallgatter A. J. (2009). Far field potentials from brain stem after transcutaneous vagus nerve stimulation: optimization of stimulation and recording parameters. J. Neural. Transm. 116 1237–1242. 10.1007/s00702-009-0282-1
    1. Porter B. A., Khodaparast N., Fayyaz T., Cheung R. J., Ahmed S. S., Vrana W. A., et al. (2012). Repeatedly pairing vagus nerve stimulation with a movement reorganizes primary motor cortex. Cereb. Cortex 22 2365–2374. 10.1093/cercor/bhr316
    1. Pruitt D. T., Schmid A. N., Kim L. J., Abe C. M., Trieu J. L., Choua C., et al. (2016). Vagus nerve stimulation delivered with motor training enhances recovery of function after traumatic brain injury. J. Neurotrauma. 33 871–879. 10.1089/neu.2015.3972
    1. Raedt R., Clinckers R., Mollet L., Vonck K., El Tahry R., Wyckhuys T., et al. (2011). Increased hippocampal noradrenaline is a biomarker for efficacy of vagus nerve stimulation in a limbic seizure model. J. Neurochem. 117 461–469. 10.1111/j.1471-4159.2011.07214.x
    1. Rajmohan V., Mohandas E. (2007). The limbic system. Indian J. Psychiatr. 49 132–139.
    1. Rong P., Liu J., Wang L., Liu R., Fang J., Zhao J., et al. (2016). Effect of transcutaneous auricular vagus nerve stimulation on major depressive disorder: a nonrandomized controlled pilot study. J. Affect Disord. 195 172–179. 10.1016/j.jad.2016.02.031
    1. Schachter S. C., Saper C. B. (1998). Vagus nerve stimulation. Epilepsia 39 677–686.
    1. Schulz K. F., Altman D. G., Moher D. C. O. N. S. O. R. T. (2010). 2010 statement: updated guidelines for reporting parallel group randomised trials. Trials 11 1–8.
    1. Sclocco R., Garcia R. G., Kettner N. W., Isenburg K., Fisher H. P., Hubbard C. S., et al. (2019). The influence of respiration on brainstem and cardiovagal response to auricular vagus nerve stimulation: A multimodal ultrahigh-field (7T) fMRI study. Brain Stimul. 12 911–921. 10.1016/j.brs.2019.02.003
    1. Seol G. H., Ziburkus J., Huang S., Song L., Kim I. T., Takamiya K., et al. (2007). Neuromodulators control the polarity of spike-timing-dependent synaptic plasticity. Neuron 55 919–929. 10.1016/j.neuron.2007.08.013
    1. Shetake J. A., Engineer N. D., Vrana W. A., Wolf J. T., Kilgard M. P. (2012). Pairing tone trains with vagus nerve stimulation induces temporal plasticity in auditory cortex. Exp. Neurol. 233 342–349. 10.1016/j.expneurol.2011.10.026
    1. Shim H. J., Kwak M. Y., An Y. H., Kim D. H., Kim Y. J., Kim H. J. (2015). Feasibility and Safety of Transcutaneous Vagus Nerve Stimulation Paired with Notched Music Therapy for the Treatment of Chronic Tinnitus. J. Audiol. Otol. 19 159–167. 10.7874/jao.2015.19.3.159
    1. Shore S. E., Roberts L. E., Langguth B. (2016). Maladaptive plasticity in tinnitus–triggers, mechanisms and treatment. Nat. Rev. Neurol. 12 150–160. 10.1038/nrneurol.2016.12
    1. Stegeman I., Velde H., Robe P., Stokroos R., Smit A. (2021). Tinnitus treatment by vagus nerve stimulation: A systematic review. PLoS One 16:e0247221. 10.1371/journal.pone.0247221
    1. Suk W. C., Kim S. J., Chang D. S., Lee H. Y. (2018). Characteristics of stimulus intensity in transcutaneous vagus nerve stimulation for chronic tinnitus. J. Internat. Adv. Otol. 14:267.
    1. Sumal K. K., Blessing W., Joh T. H., Reis D. J., Pickel V. M. (1983). Synaptic interaction of vagal afferents and catecholaminergic neurons in the rat nucleus tractus solitarius. Brain Res. 277 31–40. 10.1016/0006-8993(83)90904-6
    1. Tekdemir I., Aslan A., Elhan A. A. (1998). clinico-anatomic study of the auricular branch of the vagus nerve and Arnold’s ear-cough reflex. Surg. Radiol. Anat. 20 253–257. 10.1007/s00276-998-0253-5
    1. Tyler R. S., Aran J., Dauman R. (1992). Recent advances in tinnitus. Am. J. Audiol. 1 36–44. 10.1044/1059-0889.0104.36
    1. Tyler R. S., Noble W., Coelho C. (2006). Considerations for the design of clinical trials for tinnitus. Acta Otolaryngol. 126 44–49. 10.1080/03655230600895424
    1. Tyler R. S., Oleson J., Noble W., Coelho C., Ji H. (2007). Clinical trials for tinnitus: study populations, designs, measurement variables, and data analysis. Prog. Brain Res. 166 499–509. 10.1016/s0079-6123(07)66048-8
    1. Tyler R., Cacace A., Stocking C., Tarver B., Engineer N., Martin J., et al. (2017). Vagus Nerve Stimulation Paired with Tones for the Treatment of Tinnitus: A Prospective Randomized Double-blind Controlled Pilot Study in Humans. Sci. Rep. 7:11960.
    1. Tyler R., Coelho C., Tao P., Ji H., Noble W., Gehringer A., et al. (2008). Identifying tinnitus subgroups with cluster analysis. Age 1:3.
    1. Van Der Loo E., Gais S., Congedo M., Vanneste S., Plazier M., Menovsky T., et al. (2009). Tinnitus intensity dependent gamma oscillations of the contralateral auditory cortex. PLoS One 4:e7396. 10.1371/journal.pone.0007396
    1. Vanneste S., Martin J., Rennaker R. L., Kilgard M. P. (2017). Pairing sound with vagus nerve stimulation modulates cortical synchrony and phase coherence in tinnitus: An exploratory retrospective study. Sci. Rep. 7 1–11.
    1. Vonck K., De Herdt V., Bosman T., Dedeurwaerdere S., Van Laere K., Boon P. (2008). Thalamic and limbic involvement in the mechanism of action of vagus nerve stimulation, a SPECT study. Seizure 17 699–706. 10.1016/j.seizure.2008.05.001
    1. Wang Z., Fang J., Liu J., Rong P., Jorgenson K., Park J., et al. (2018). Frequency-dependent functional connectivity of the nucleus accumbens during continuous transcutaneous vagus nerve stimulation in major depressive disorder. J. Psychiatr. Res. 102 123–131. 10.1016/j.jpsychires.2017.12.018
    1. Watanabe K., Tubbs R. S., Satoh S., Zomorodi A. R., Liedtke W., Labidi M., et al. (2016). Isolated deep ear canal pain: possible role of auricular branch of vagus nerve—case illustrations with cadaveric correlation. World Neurosurg. 96 293–301. 10.1016/j.wneu.2016.08.102
    1. Wichova H., Alvi S. A., Shew M., Lin J., Sale K., Larsen C., et al. (2018). Tinnitus perception in patients after vagal nerve stimulator implantation for epilepsy. Am. J. Otolaryngol. 39 599–602. 10.1016/j.amjoto.2018.07.009
    1. Wu K., Wang Z., Zhang Y., Yao J., Zhang Z. (2020). Transcutaneous vagus nerve stimulation for the treatment of drug-resistant epilepsy: a meta-analysis and systematic review. ANZ J Surg. 90 467–471. 10.1111/ans.15681
    1. Yakunina N., Nam E. (2021). Does the tinnitus pitch correlate with the frequency of hearing loss? Acta Otolaryngol. 141 163–170. 10.1080/00016489.2020.1837394
    1. Yakunina N., Kim S. S., Nam E. B. O. L. D. (2018). fMRI effects of transcutaneous vagus nerve stimulation in patients with chronic tinnitus. PLoS One 13:e0207281. 10.1371/journal.pone.0207281
    1. Yakunina N., Kim S. S., Nam E. C. (2017). Optimization of Transcutaneous Vagus Nerve Stimulation Using Functional MRI. Neuromodulation 20 290–300. 10.1111/ner.12541
    1. Yap J. Y., Keatch C., Lambert E., Woods W., Stoddart P. R., Kameneva T. (2020). Critical review of transcutaneous vagus nerve stimulation: Challenges for translation to clinical practice. Front. Neurosci. 2020:14. 10.3389/fnins.2020.00284
    1. Ylikoski J., Lehtimaki J., Pirvola U., Makitie A., Aarnisalo A., Hyvarinen P., et al. (2017). Non-invasive vagus nerve stimulation reduces sympathetic preponderance in patients with tinnitus. Acta Otolaryngol. 137 426–431. 10.1080/00016489.2016.1269197
    1. Ylikoski J., Markkanen M., Pirvola U., Lehtimäki J. A., Ylikoski M., Jing Z., et al. (2020). Stress and Tinnitus; Transcutaneous Auricular Vagal Nerve Stimulation Attenuates Tinnitus-Triggered Stress Reaction. Front. Psychol. 11:2442. 10.3389/fpsyg.2020.570196
    1. Young E. D, Nelken I., Conley R. A. (1995). Somatosensory effects on neurons in dorsal cochlear nucleus. J. Neurophysiol. 73 743–765. 10.1152/jn.1995.73.2.743
    1. Yuan H., Silberstein S. D. (2016). Vagus Nerve and Vagus Nerve Stimulation, a Comprehensive Review: Part II. Headache 56 259–266. 10.1111/head.12650
    1. Zobel A., Joe A., Freymann N., Clusmann H., Schramm J., Reinhardt M., et al. (2005). Changes in regional cerebral blood flow by therapeutic vagus nerve stimulation in depression: an exploratory approach. Psychiatr. Res. 139 165–179. 10.1016/j.pscychresns.2005.02.010

Source: PubMed

3
Sottoscrivi