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Animal Models of Tinnitus Treatment: Cochlear and Brain Stimulation

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The Behavioral Neuroscience of Tinnitus

Part of the book series: Current Topics in Behavioral Neurosciences ((CTBN,volume 51))

Abstract

Neuromodulation, via stimulation of a variety of peripheral and central structures, is used to suppress tinnitus. However, investigative limitations in humans due to ethical reasons have made it difficult to decipher the mechanisms underlying treatment-induced tinnitus relief, so a number of animal models have arisen to address these unknowns. This chapter reviews animal models of cochlear and brain stimulation and assesses their modulatory effects on behavioral evidence of tinnitus and its related neural correlates. When a structure is stimulated, localized modulation, often presenting as downregulation of spontaneous neuronal spike firing rate, bursting and neurosynchrony, occurs within the brain area. Through anatomical projections and transmitter pathways, the interventions activate both auditory- and non-auditory structures by taking bottom-up ascending and top-down descending modes to influence their target brain structures. Furthermore, it is the brain oscillations that cochlear or brain stimulation evoke and connect the prefrontal cortex, striatal systems, and other limbic structures to refresh neural networks and relieve auditory, attentive, conscious, as well as emotional reactive aspects of tinnitus. This oscillatory neural network connectivity is achieved via the thalamocorticothalamic circuitry including the lemniscal and non-lemniscal auditory brain structures. Beyond existing technologies, the review also reveals opportunities for developing advanced animal models using new modalities to achieve precision neuromodulation and tinnitus abatement, such as optogenetic cochlear and/or brain stimulation.

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Abbreviations

ABI:

Auditory brainstem implant

AC:

Auditory cortex

ACC:

Anterior cingulate cortex

ACES:

Auditory cortex electrical stimulation

AMI:

Auditory midbrain implant

BDNF:

Brain derived neurotrophic factor

CBT:

Cognitive behavioral therapy

CES:

Cochlear electrical stimulation

CFC:

Cross-frequency coupling

CI:

Cochlear implant

CIC:

Central nucleus of the inferior colliculus

DBS:

Deep brain stimulation

DCIC:

Dorsal cortex of the inferior colliculus

DCN:

Dorsal cochlear nucleus

dlPFC:

Dorsolateral prefrontal cortex

dMGB:

Dorsal subdivision of the medial geniculate body

ECIC:

External cortex of the inferior colliculus

ECS:

Epi-cranial electrical stimulation

EEG:

Electroencephalogram

FLS:

Fronto-limbic-striatal

fMRI:

Functional magnetic resonance imaging

GAD:

Glutamate decarboxylase

GPIAS:

Gap-prepulse inhibition of the acoustic startle reflex

HPC:

Hippocampus

IC:

Inferior colliculus

LFP:

Local field potential

MDT:

Mediodorsal thalamus

MGB:

Medial geniculate body

mMGB:

Medial subdivision of the medial geniculate body

MRI:

Magnetic resonance imaging

NAc:

Nucleus accumbens

NF2:

Neurofibromatosis type II

PET:

Positron emission tomography

PFC:

Prefrontal cortex

rTMS:

Repetitive transcranial magnetic stimulation

SFR:

Spontaneous firing rate

SGN:

Spiral ganglion neuron

SR:

Stochastic resonance

STN:

Subthalamic nucleus

tACS:

Transcranial alternate current stimulation

TBI:

Traumatic brain injury

TCD:

Thalamocortical dysrhythmias

TCT:

Thalamocorticothalamic

tDCS:

Transcranial direct current stimulation

TES:

Transcranial electrical stimulation

TMS:

Transcranial magnetic stimulation

TRN:

Thalamic reticular nucleus

tRNS:

Random-noise stimulation

vMGB:

Ventral subdivision of the medial geniculate body

References

  • Adamchic I et al (2014) Abnormal cross-frequency coupling in the tinnitus network. Front Neurosci 8:284

    Article  PubMed  PubMed Central  Google Scholar 

  • Adjamian P et al (2012) Neuromagnetic indicators of tinnitus and tinnitus masking in patients with and without hearing loss. J Assoc Res Otolaryngol 13:715–731

    Article  PubMed  PubMed Central  Google Scholar 

  • Ahn MH, Hong SK, Min BK (2017) The absence of resting-state high-gamma cross-frequency coupling in patients with tinnitus. Hear Res 356:63–73

    Article  PubMed  Google Scholar 

  • Ahsan SF et al (2018) An animal model of deep brain stimulation for treating tinnitus: a proof of concept study. Laryngoscope 128:1213–1222

    Article  PubMed  Google Scholar 

  • Araneda R et al (2018) A key role of the prefrontal cortex in the maintenance of chronic tinnitus: an fMRI study using a Stroop task. Neuroimage Clin 17:325–334

    Article  PubMed  Google Scholar 

  • Argence M et al (2008) Stimulation by cochlear implant in unilaterally deaf rats reverses the decrease of inhibitory transmission in the inferior colliculus. Eur J Neurosci 28:1589–1602

    Article  PubMed  Google Scholar 

  • Arts RA et al (2012) Review: cochlear implants as a treatment of tinnitus in single-sided deafness. Curr Opin Otolaryngol Head Neck Surg 20:398–403

    Article  PubMed  Google Scholar 

  • Arts RA et al (2015) Tinnitus suppression by Intracochlear electrical stimulation in single-sided deafness: a prospective clinical trial – part I. Audiol Neurootol 20:294–313

    Article  PubMed  Google Scholar 

  • Atencio CA et al (2014) Primary auditory cortical responses to electrical stimulation of the thalamus. J Neurophysiol 111:1077–1087

    Article  PubMed  Google Scholar 

  • Axelsson A, Ringdahl A (1989) Tinnitus – a study of its prevalence and characteristics. Br J Audiol 23:53–62

    Article  CAS  PubMed  Google Scholar 

  • Baguley DM, Atlas MD (2007) Cochlear implants and tinnitus. Prog Brain Res 166:347–355

    Article  PubMed  Google Scholar 

  • Barry KM et al (2015) Modulation of medial geniculate nucleus neuronal activity by electrical stimulation of the nucleus accumbens. Neuroscience 308:1–10

    Article  CAS  PubMed  Google Scholar 

  • Barry KM, Robertson D, Mulders W (2019) Changes in auditory thalamus neural firing patterns after acoustic trauma in rats. Hear Res 379:89–97

    Article  CAS  PubMed  Google Scholar 

  • Basta D et al (2015) Bilateral changes of spontaneous activity within the central auditory pathway upon chronic unilateral intracochlear electrical stimulation. Otol Neurotol 36:1759–1765

    Article  PubMed  Google Scholar 

  • Bauer CA et al (2008) Tinnitus and inferior colliculus activity in chinchillas related to three distinct patterns of cochlear trauma. J Neurosci Res 86:2564–2578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blood AJ, Zatorre RJ (2001) Intensely pleasurable responses to music correlate with activity in brain regions implicated in reward and emotion. Proc Natl Acad Sci U S A 98:11818–11823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boyden ES et al (2005) Millisecond-timescale, genetically targeted optical control of neural activity. Nat Neurosci 8:1263–1268

    Article  CAS  PubMed  Google Scholar 

  • Calixto R et al (2013) Investigation of a new electrode array technology for a central auditory prosthesis. PLoS One 8:e82148

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Canolty RT, Knight RT (2010) The functional role of cross-frequency coupling. Trends Cogn Sci 14:506–515

    Article  PubMed  PubMed Central  Google Scholar 

  • Canolty RT et al (2006) High gamma power is phase-locked to theta oscillations in human neocortex. Science 313:1626–1628

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cardin JA et al (2009) Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 459:663–667

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Casquero-Veiga M et al (2016) Response to deep brain stimulation in three brain targets with implications in mental disorders: a PET study in rats. PLoS One 11:e0168689

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cavdar S et al (2018) Afferent projections of the subthalamic nucleus in the rat: emphasis on bilateral and interhemispheric connections. Acta Neurobiol Exp (Wars) 78:251–263

    Article  Google Scholar 

  • Chen YC et al (2017) Resting-state brain abnormalities in chronic subjective tinnitus: a meta-analysis. Front Hum Neurosci 11:22

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen YC et al (2018) Alterations of the default mode network and cognitive impairment in patients with unilateral chronic tinnitus. Quant Imaging Med Surg 8:1020–1029

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen JJ et al (2020) Association of central noninvasive brain stimulation interventions with efficacy and safety in tinnitus management: a meta-analysis. JAMA Otolaryngol Head Neck Surg 146:801–809

    Article  PubMed  Google Scholar 

  • Cheung SW, Larson PS (2010) Tinnitus modulation by deep brain stimulation in locus of caudate neurons (area LC). Neuroscience 169:1768–1778

    Article  CAS  PubMed  Google Scholar 

  • Cheung SW et al (2019) Phase I trial of caudate deep brain stimulation for treatment-resistant tinnitus. J Neurosurg:1–10

    Google Scholar 

  • Claes L et al (2014) Auditory cortex tACS and tRNS for tinnitus: single versus multiple sessions. Neural Plast 2014:436713

    Article  PubMed  PubMed Central  Google Scholar 

  • Coomes DL, Schofield RM, Schofield BR (2005) Unilateral and bilateral projections from cortical cells to the inferior colliculus in guinea pigs. Brain Res 1042:62–72

    Article  CAS  PubMed  Google Scholar 

  • Crandall SR, Cruikshank SJ, Connors BW (2015) A corticothalamic switch: controlling the thalamus with dynamic synapses. Neuron 86:768–782

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crocetti A et al (2009) Questionnaires to evaluate anxiety and depressive levels in tinnitus patients. Otolaryngol Head Neck Surg 140:403–405

    Article  PubMed  Google Scholar 

  • Daneshi A et al (2005) Auditory electrical tinnitus suppression in patients with and without implants. Int Tinnitus J 11:85–91

    PubMed  Google Scholar 

  • Darrow KN et al (2015) Optogenetic stimulation of the cochlear nucleus using channelrhodopsin-2 evokes activity in the central auditory pathways. Brain Res 1599:44–56

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • de Mena L, Rizk P, Rincon-Limas DE (2018) Bringing light to transcription: the optogenetics repertoire. Front Genet 9:518

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • De Ridder D, Vanneste S (2012) EEG driven tDCS versus bifrontal tDCS for tinnitus. Front Psych 3:84

    Google Scholar 

  • De Ridder D et al (2006) Primary and secondary auditory cortex stimulation for intractable tinnitus. ORL J Otorhinolaryngol Relat Spec 68:48–54

    Article  PubMed  Google Scholar 

  • De Ridder D et al (2007) Electrical stimulation of auditory and somatosensory cortices for treatment of tinnitus and pain. Prog Brain Res 166:377–388

    Article  PubMed  Google Scholar 

  • De Ridder D et al (2010) Burst stimulation of the auditory cortex: a new form of neurostimulation for noise-like tinnitus suppression. J Neurosurg 112:1289–1294

    Article  PubMed  Google Scholar 

  • De Ridder D et al (2011) Theta-gamma dysrhythmia and auditory phantom perception. J Neurosurg 114:912–921

    Article  PubMed  Google Scholar 

  • De Ridder D et al (2012) Dorsolateral prefrontal cortex transcranial magnetic stimulation and electrode implant for intractable tinnitus. World Neurosurg 77:778–784

    Article  PubMed  Google Scholar 

  • De Ridder D et al (2014a) Safety and efficacy of vagus nerve stimulation paired with tones for the treatment of tinnitus: a case series. Neuromodulation 17:170–179

    Article  PubMed  Google Scholar 

  • De Ridder D, Vanneste S, Freeman W (2014b) The Bayesian brain: phantom percepts resolve sensory uncertainty. Neurosci Biobehav Rev 44:4–15

    Article  PubMed  Google Scholar 

  • De Ridder D et al (2014c) An integrative model of auditory phantom perception: tinnitus as a unified percept of interacting separable subnetworks. Neurosci Biobehav Rev 44:16–32

    Article  PubMed  Google Scholar 

  • De Ridder D et al (2015) Thalamocortical dysrhythmia: a theoretical update in tinnitus. Front Neurol 6:124

    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 124:893–901

    Article  PubMed  Google Scholar 

  • Deklerck AN et al (2020) Invasive neuromodulation as a treatment for tinnitus: a systematic review. Neuromodulation 23:451–462

    Article  PubMed  Google Scholar 

  • Deschenes M, Veinante P, Zhang ZW (1998) The organization of corticothalamic projections: reciprocity versus parity. Brain Res Brain Res Rev 28:286–308

    Article  CAS  PubMed  Google Scholar 

  • Di NW et al (2009) Transtympanic electrical stimulation for immediate and long-term tinnitus suppression. Int Tinnitus J 15:100–106

    Google Scholar 

  • Dieter A et al (2019) Near physiological spectral selectivity of cochlear optogenetics. Nat Commun 10:1962

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dieter A, Keppeler D, Moser T (2020) Towards the optical cochlear implant: optogenetic approaches for hearing restoration. EMBO Mol Med 12:e11618

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • DiGuiseppi J, Zuo J (2019) The awesome power of optogenetics in hearing research. Neurosci Lett 701:175–179

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dong C et al (2020) Low-frequency repetitive transcranial magnetic stimulation for the treatment of chronic tinnitus: a systematic review and meta-analysis of randomized controlled trials. Biomed Res Int 2020:3141278

    Article  PubMed  PubMed Central  Google Scholar 

  • Eggermont JJ (2015) The auditory cortex and tinnitus – a review of animal and human studies. Eur J Neurosci 41:665–676

    Article  PubMed  Google Scholar 

  • Eggermont JJ, Roberts LE (2004) The neuroscience of tinnitus. Trends Neurosci 27:676–682

    Article  CAS  PubMed  Google Scholar 

  • Engelhardt J et al (2014) Effect of chronic cortical stimulation on chronic severe tinnitus: a prospective randomized double-blind cross-over trial and long-term follow up. Brain Stimul 7:694–700

    Article  PubMed  Google Scholar 

  • Engineer ND et al (2011) Reversing pathological neural activity using targeted plasticity. Nature 470:101–104

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Faber M et al (2012) Top down prefrontal affective modulation of tinnitus with multiple sessions of tDCS of dorsolateral prefrontal cortex. Brain Stimul 5:492–498

    Article  PubMed  Google Scholar 

  • Fallon JB, Irvine DR, Shepherd RK (2008) Cochlear implants and brain plasticity. Hear Res 238:110–117

    Article  PubMed  Google Scholar 

  • Fallon JB, Irvine DR, Shepherd RK (2009) Neural prostheses and brain plasticity. J Neural Eng 6:065008

    Article  PubMed  PubMed Central  Google Scholar 

  • Fallon JB, Shepherd RK, Irvine DR (2014) Effects of chronic cochlear electrical stimulation after an extended period of profound deafness on primary auditory cortex organization in cats. Eur J Neurosci 39:811–820

    Article  PubMed  Google Scholar 

  • Fernandes NF et al (2020) Auditory and language skills in children with auditory brainstem implants. Int J Pediatr Otorhinolaryngol 132:110010

    Article  PubMed  Google Scholar 

  • Firestone E, Luo H, Pace E, Liu B, Agabigum B, Zhu L, Zhang XG, Moran J, Zhang JS (2019) Pathology-specific brain oscillations serve as underpinnings of tinnitus and its modulation. Assoc Res Otolaryngol Abs 804:501

    Google Scholar 

  • Folmer RL et al (2006) Effects of repetitive transcranial magnetic stimulation (rTMS) on chronic tinnitus. Acta Otolaryngol Suppl:96–101

    Google Scholar 

  • Folmer RL et al (2015) Repetitive transcranial magnetic stimulation treatment for chronic tinnitus: a randomized clinical trial. JAMA Otolaryngol Head Neck Surg 141:716–722

    Article  PubMed  CAS  Google Scholar 

  • Friedland DR et al (2007) Feasibility of auditory cortical stimulation for the treatment of tinnitus. Otol Neurotol 28:1005–1012

    Article  PubMed  Google Scholar 

  • Fries P (2009) Neuronal gamma-band synchronization as a fundamental process in cortical computation. Annu Rev Neurosci 32:209–224

    Article  CAS  PubMed  Google Scholar 

  • Gault R, McGinnity TM, Coleman S (2018) A computational model of thalamocortical dysrhythmia in people with tinnitus. IEEE Trans Neural Syst Rehabil Eng 26:1845–1857

    Article  PubMed  Google Scholar 

  • Gerken GM, Saunders SS, Paul RE (1984) Hypersensitivity to electrical stimulation of auditory nuclei follows hearing loss in cats. Hear Res 13:249–259

    Article  CAS  PubMed  Google Scholar 

  • Ghafouri S et al (2019) Deep brain stimulation restores the glutamatergic and GABAergic synaptic transmission and plasticity to normal levels in kindled rats. PLoS One 14:e0224834

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gilles A et al (2020) Neural substrates of tinnitus in an auditory brainstem implant patient: a preliminary molecular imaging study using H2 15 O-PET including a 5-year follow-up of auditory performance and tinnitus perception. Otol Neurotol 41:e15–e20

    Article  PubMed  Google Scholar 

  • Godbehere J et al (2019) Treatment of tinnitus using theta burst based repetitive transcranial magnetic stimulation-a single blinded randomized control trial. Otol Neurotol 40:S38–S42

    Article  PubMed  Google Scholar 

  • Gray CM, Singer W (1989) Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. Proc Natl Acad Sci U S A 86:1698–1702

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gray CM et al (1989) Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature 338:334–337

    Article  CAS  PubMed  Google Scholar 

  • Halassa MM et al (2014) State-dependent architecture of thalamic reticular subnetworks. Cell 158:808–821

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hasson D et al (2011) Stress and prevalence of hearing problems in the Swedish working population. BMC Public Health 11:130

    Article  PubMed  PubMed Central  Google Scholar 

  • Henry KS et al (2016) Neural correlates of behavioral amplitude modulation sensitivity in the budgerigar midbrain. J Neurophysiol 115:1905–1916

    Article  PubMed  PubMed Central  Google Scholar 

  • Hitier M et al (2020) The effects of selective electrical stimulation of the rat cochlea on hippocampal field potentials. Hear Res 395:108023

    Article  PubMed  Google Scholar 

  • Holz EM et al (2010) Theta-gamma phase synchronization during memory matching in visual working memory. Neuroimage 52:326–335

    Article  PubMed  Google Scholar 

  • Hoover WB, Vertes RP (2007) Anatomical analysis of afferent projections to the medial prefrontal cortex in the rat. Brain Struct Funct 212:149–179

    Article  PubMed  Google Scholar 

  • House JW, Brackmann DE (1981) Tinnitus: surgical treatment. Ciba Found Symp 85:204–216

    CAS  PubMed  Google Scholar 

  • Hullfish J et al (2019) Frontostriatal network dysfunction as a domain-general mechanism underlying phantom perception. Hum Brain Mapp 40:2241–2251

    Article  PubMed  PubMed Central  Google Scholar 

  • Ito J, Sakakihara J (1994) Tinnitus suppression by electrical stimulation of the cochlear wall and by cochlear implantation. Laryngoscope 104:752–754

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Jacobs J, Kahana MJ (2010) Direct brain recordings fuel advances in cognitive electrophysiology. Trends Cogn Sci 14:162–171

    Article  PubMed  PubMed Central  Google Scholar 

  • Jahnsen H, Llinas R (1984a) Ionic basis for the electro-responsiveness and oscillatory properties of Guinea-pig thalamic neurones in vitro. J Physiol 349:227–247

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jahnsen H, Llinas R (1984b) Electrophysiological properties of guinea-pig thalamic neurones: an in vitro study. J Physiol 349:205–226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jakobs M, Lozano AM (2019) Editorial. Deep brain stimulation for tinnitus: exploring the frontier between sensory perception and awareness. J Neurosurg:1–4

    Google Scholar 

  • Jang SH, Yeo SS (2014) Thalamocortical connections between the mediodorsal nucleus of the thalamus and prefrontal cortex in the human brain: a diffusion tensor tractographic study. Yonsei Med J 55:709–714

    Article  PubMed  PubMed Central  Google Scholar 

  • Jastreboff PJ, Jastreboff MM (2000) Tinnitus retraining therapy (TRT) as a method for treatment of tinnitus and hyperacusis patients. J Am Acad Audiol 11:162–177

    Article  CAS  PubMed  Google Scholar 

  • Johansen-Berg H et al (2008) Anatomical connectivity of the subgenual cingulate region targeted with deep brain stimulation for treatment-resistant depression. Cereb Cortex 18:1374–1383

    Article  CAS  PubMed  Google Scholar 

  • Kahlbrock N, Weisz N (2008) Transient reduction of tinnitus intensity is marked by concomitant reductions of delta band power. BMC Biol 6:4

    Article  PubMed  PubMed Central  Google Scholar 

  • Kalappa BI et al (2014) Single unit hyperactivity and bursting in the auditory thalamus of awake rats directly correlates with behavioural evidence of tinnitus. J Physiol 592:5065–5078

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keppeler D et al (2018) Ultrafast optogenetic stimulation of the auditory pathway by targeting-optimized chronos. EMBO J:37

    Google Scholar 

  • Khatoun A, Asamoah B, Mc Laughlin M (2019) Investigating the feasibility of epicranial cortical stimulation using concentric-ring electrodes: a novel minimally invasive neuromodulation method. Front Neurosci 13:773

    Article  PubMed  PubMed Central  Google Scholar 

  • Kiang NY, Liberman MC, Levine RA (1976) Auditory-nerve activity in cats exposed to ototoxic drugs and high-intensity sounds. Ann Otol Rhinol Laryngol 85:752–768

    Article  CAS  PubMed  Google Scholar 

  • Kim K et al (2015) A novel method for device-related electroencephalography artifact suppression to explore cochlear implant-related cortical changes in single-sided deafness. J Neurosci Methods 255:22–28

    Article  PubMed  Google Scholar 

  • Klinke R et al (1999) Recruitment of the auditory cortex in congenitally deaf cats by long-term cochlear electrostimulation. Science 285:1729–1733

    Article  CAS  PubMed  Google Scholar 

  • Komiya H, Eggermont JJ (2000) Spontaneous firing activity of cortical neurons in adult cats with reorganized tonotopic map following pure-tone trauma. Acta Otolaryngol 120:750–756

    Article  CAS  PubMed  Google Scholar 

  • Konig O et al (2006) Course of hearing loss and occurrence of tinnitus. Hear Res 221:59–64

    Article  PubMed  Google Scholar 

  • Kral A et al (1998) Spatial resolution of cochlear implants: the electrical field and excitation of auditory afferents. Hear Res 121:11–28

    Article  CAS  PubMed  Google Scholar 

  • Krauss P et al (2016) Stochastic resonance controlled upregulation of internal noise after hearing loss as a putative cause of tinnitus-related neuronal hyperactivity. Front Neurosci 10:597

    Article  PubMed  PubMed Central  Google Scholar 

  • Krauss P et al (2017) Adaptive stochastic resonance for unknown and variable input signals. Sci Rep 7:2450

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kreuzer PM et al (2017) Individualized repetitive transcranial magnetic stimulation treatment in chronic tinnitus? Front Neurol 8:126

    Article  PubMed  PubMed Central  Google Scholar 

  • Kreuzer PM et al (2019) Daily high-frequency transcranial random noise stimulation of bilateral temporal cortex in chronic tinnitus – a pilot study. Sci Rep 9:12274

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lachowska M et al (2020) Detailed insight in intraoperative eABR measurements to assist auditory brainstem implantation in a patient with neurofibromatosis type 2. Acta Neurol Belg 120:1371–1378

    Article  PubMed  Google Scholar 

  • Langguth B (2020) Non-invasive neuromodulation for tinnitus. J Audiol Otol 24:113–118

    Article  PubMed  PubMed Central  Google Scholar 

  • Langguth B, Elgoyhen AB (2012) Current pharmacological treatments for tinnitus. Expert Opin Pharmacother 13:2495–2509

    Article  CAS  PubMed  Google Scholar 

  • Lavin A, Grace AA (1996) Physiological properties of rat ventral pallidal neurons recorded intracellularly in vivo. J Neurophysiol 75:1432–1443

    Article  CAS  PubMed  Google Scholar 

  • Leaver AM et al (2011) Dysregulation of limbic and auditory networks in tinnitus. Neuron 69:33–43

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ledoux JE, Farb C, Ruggiero DA (1990) Topographic organization of neurons in the acoustic thalamus that project to the amygdala. Hear Res 10:1043–1054

    CAS  Google Scholar 

  • Lee DJ et al (2019) Current and future directions of deep brain stimulation for neurological and psychiatric disorders. J Neurosurg 131:333–342

    Article  CAS  PubMed  Google Scholar 

  • Li LP et al (2019) Steady-state auditory evoked fields reflect long-term effects of repetitive transcranial magnetic stimulation in tinnitus. Clin Neurophysiol 130:1665–1672

    Article  PubMed  Google Scholar 

  • Liberman T, Velluti RA, Pedemonte M (2009) Temporal correlation between auditory neurons and the hippocampal theta rhythm induced by novel stimulations in awake guinea pigs. Brain Res 1298:70–77

    Article  CAS  PubMed  Google Scholar 

  • Lim HH, Lenarz T (2015) Auditory midbrain implant: research and development towards a second clinical trial. Hear Res 322:212–223

    Article  PubMed  PubMed Central  Google Scholar 

  • Lin X et al (2020) Altered topological patterns of Gray matter networks in tinnitus: a graph-theoretical-based study. Front Neurosci 14:541

    Article  PubMed  PubMed Central  Google Scholar 

  • Llinas RR et al (1999) Thalamocortical dysrhythmia: a neurological and neuropsychiatric syndrome characterized by magnetoencephalography. Proc Natl Acad Sci U S A 96:15222–15227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Llinas R et al (2005) Rhythmic and dysrhythmic thalamocortical dynamics: GABA systems and the edge effect. Trends Neurosci 28:325–333

    Article  CAS  PubMed  Google Scholar 

  • Luo H et al (2012) Tinnitus suppression by electrical stimulation of the rat dorsal cochlear nucleus. Neurosci Lett 522:16–20

    Article  CAS  PubMed  Google Scholar 

  • Lv H et al (2020) Altered functional connectivity of the thalamus in tinnitus patients is correlated with symptom alleviation after sound therapy. Brain Imaging Behav 14:2668–2678

    Article  PubMed  Google Scholar 

  • Mager T et al (2018) High frequency neural spiking and auditory signaling by ultrafast red-shifted optogenetics. Nat Commun 9:1750

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Malmierca MS et al (2002) Direct projections from cochlear nuclear complex to auditory thalamus in the rat. J Neurosci 22:10891–10897

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marcondes RA et al (2010) Repetitive transcranial magnetic stimulation improve tinnitus in normal hearing patients: a double-blind controlled, clinical and neuroimaging outcome study. Eur J Neurol 17:38–44

    Article  CAS  PubMed  Google Scholar 

  • Marks KL et al (2018) Auditory-somatosensory bimodal stimulation desynchronizes brain circuitry to reduce tinnitus in guinea pigs and humans. Sci Transl Med 10

    Google Scholar 

  • Martel DT, Pardo-Garcia TR, Shore SE (2019) Dorsal Cochlear nucleus fusiform-cell plasticity is altered in salicylate-induced tinnitus. Neuroscience 407:170–181

    Article  CAS  PubMed  Google Scholar 

  • Mauger SJ et al (2012) An in vivo investigation of inferior colliculus single neuron responses to cochlear nucleus pulse train stimulation. J Neurophysiol 108:2999–3008

    Article  PubMed  Google Scholar 

  • McCreery D, Han M, Pikov V (2010) Neuronal activity evoked in the inferior colliculus of the cat by surface macroelectrodes and penetrating microelectrodes implanted in the cochlear nucleus. IEEE Trans Biomed Eng 57:1765–1773

    Article  PubMed  Google Scholar 

  • McCreery D et al (2013) Encoding of the amplitude modulation of pulsatile electrical stimulation in the feline cochlear nucleus by neurons in the inferior colliculus; effects of stimulus pulse rate. J Neural Eng 10:056010

    Article  PubMed  Google Scholar 

  • McCreery D, Yadev K, Han M (2018) Responses of neurons in the feline inferior colliculus to modulated electrical stimuli applied on and within the ventral cochlear nucleus; implications for an advanced auditory brainstem implant. Hear Res 363:85–97

    Article  PubMed  PubMed Central  Google Scholar 

  • McCullough LD, Sokolowski JD, Salamone JD (1993) A neurochemical and behavioral investigation of the involvement of nucleus accumbens dopamine in instrumental avoidance. Neuroscience 52:919–925

    Article  CAS  PubMed  Google Scholar 

  • McFerran DJ et al (2019) Why is there no cure for tinnitus? Front Neurosci 13:802

    Article  PubMed  PubMed Central  Google Scholar 

  • Melloni L et al (2007) Synchronization of neural activity across cortical areas correlates with conscious perception. J Neurosci 27:2858–2865

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meltzer NE, Ryugo DK (2006) Projections from auditory cortex to cochlear nucleus: a comparative analysis of rat and mouse. Anat Rec A Discov Mol Cell Evol Biol 288:397–408

    Article  PubMed  PubMed Central  Google Scholar 

  • Mertens G, De Bodt M, Van de Heyning P (2016) Cochlear implantation as a long-term treatment for ipsilateral incapacitating tinnitus in subjects with unilateral hearing loss up to 10 years. Hear Res 331:1–6

    Article  PubMed  Google Scholar 

  • Min HK et al (2016) Dopamine release in the nonhuman primate caudate and putamen depends upon site of stimulation in the subthalamic nucleus. J Neurosci 36:6022–6029

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Minami SB et al (2015) Auditory resting-state functional connectivity in tinnitus and modulation with transcranial direct current stimulation. Acta Otolaryngol 135:1286–1292

    Article  PubMed  Google Scholar 

  • Mitchell AS (2015) The mediodorsal thalamus as a higher order thalamic relay nucleus important for learning and decision-making. Neurosci Biobehav Rev 54:76–88

    Article  PubMed  Google Scholar 

  • Miyakawa A et al (2019) Tinnitus correlates with downregulation of cortical glutamate decarboxylase 65 expression but not auditory cortical map reorganization. J Neurosci 39:9989–10001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mogenson GJ et al (1987) Ventral pallidum projections to mediodorsal nucleus of the thalamus: an anatomical and electrophysiological investigation in the rat. Brain Res 404:221–230

    Article  CAS  PubMed  Google Scholar 

  • Mohsen S et al (2019) Multisite transcranial random noise stimulation (tRNS) modulates the distress network activity and oscillatory powers in subjects with chronic tinnitus. J Clin Neurosci 67:178–184

    Article  PubMed  Google Scholar 

  • Møller AR (2011) Anatomy and physiology of the auditory system. Springer, New York

    Book  Google Scholar 

  • Mulders WH, Spencer TC, Robertson D (2016a) Effects of pulsatile electrical stimulation of the round window on central hyperactivity after cochlear trauma in guinea pig. Hear Res 335:128–137

    Article  CAS  PubMed  Google Scholar 

  • Mulders WH et al (2016b) The effects of repetitive transcranial magnetic stimulation in an animal model of tinnitus. Sci Rep 6:38234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mulders W et al (2019) Low-intensity repetitive transcranial magnetic stimulation over prefrontal cortex in an animal model alters activity in the auditory thalamus but does not affect behavioural measures of tinnitus. Exp Brain Res 237:883–896

    Article  CAS  PubMed  Google Scholar 

  • Neuheiser A et al (2010) Effects of pulse phase duration and location of stimulation within the inferior colliculus on auditory cortical evoked potentials in a guinea pig model. J Assoc Res Otolaryngol 11:689–708

    Article  PubMed  PubMed Central  Google Scholar 

  • Norena AJ, Mulders WH, Robertson D (2015) Suppression of putative tinnitus-related activity by extra-cochlear electrical stimulation. J Neurophysiol 113:132–143

    Article  CAS  PubMed  Google Scholar 

  • Nozaradan S et al (2017) Intracerebral evidence of rhythm transform in the human auditory cortex. Brain Struct Funct 222:2389–2404

    Article  PubMed  Google Scholar 

  • O’Donnell P, Grace AA (1995) Synaptic interactions among excitatory afferents to nucleus accumbens neurons: hippocampal gating of prefrontal cortical input. J Neurosci 15:3622–3639

    Article  PubMed  PubMed Central  Google Scholar 

  • O’Donnell P et al (1997) Interconnected parallel circuits between rat nucleus accumbens and thalamus revealed by retrograde transynaptic transport of pseudorabies virus. J Neurosci 17:2143–2167

    Article  PubMed  PubMed Central  Google Scholar 

  • O'Driscoll M, El-Deredy W, Ramsden RT (2011) Brain stem responses evoked by stimulation of the mature cochlear nucleus with an auditory brain stem implant. Ear Hear 32:286–299

    Article  PubMed  Google Scholar 

  • Offutt SJ et al (2014) Suppression and facilitation of auditory neurons through coordinated acoustic and midbrain stimulation: investigating a deep brain stimulator for tinnitus. J Neural Eng 11:066001

    Article  PubMed  PubMed Central  Google Scholar 

  • Ongur D, Price JL (2000) The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cereb Cortex 10:206–219

    Article  CAS  PubMed  Google Scholar 

  • Pages DS et al (2016) Effects of electrical stimulation in the inferior colliculus on frequency discrimination by rhesus monkeys and implications for the auditory midbrain implant. J Neurosci 36:5071–5083

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perreau A, Tyler R, Mancini PC (2020) Programming a Cochlear implant for tinnitus suppression. J Am Acad Audiol 31:302–308

    Article  PubMed  Google Scholar 

  • Pinault D (2004) The thalamic reticular nucleus: structure, function and concept. Brain Res Brain Res Rev 46:1–31

    Article  PubMed  Google Scholar 

  • Plewnia C (2018) Transcranial brain stimulation for the treatment of tinnitus: positive lessons from a negative trial. Brain Stimul 11:1–2

    Article  PubMed  Google Scholar 

  • Plewnia C et al (2012) Treatment of chronic tinnitus with theta burst stimulation: a randomized controlled trial. Neurology 78:1628–1634

    Article  CAS  PubMed  Google Scholar 

  • Poncet-Wallet C et al (2020) Prospective multicentric follow-up study of Cochlear implantation in adults with single-sided deafness: tinnitus and audiological outcomes. Otol Neurotol 41:458–466

    Article  PubMed  Google Scholar 

  • Quass GL et al (2018) Electrical stimulation of the midbrain excites the auditory cortex asymmetrically. Brain Stimul 11:1161–1174

    Article  PubMed  Google Scholar 

  • Rauschecker JP, Leaver AM, Muhlau M (2010) Tuning out the noise: limbic-auditory interactions in tinnitus. Neuron 66:819–826

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rauschecker JP et al (2015) Frontostriatal gating of tinnitus and chronic pain. Trends Cogn Sci 19:567–578

    Article  PubMed  PubMed Central  Google Scholar 

  • Roberts LE, Moffat G, Bosnyak DJ (2006) Residual inhibition functions in relation to tinnitus spectra and auditory threshold shift. Acta Otolaryngol Suppl:27–33

    Google Scholar 

  • Roberts DS et al (2017) Tinnitus suppression after auditory brainstem implantation in patients with neurofibromatosis type-2. Otol Neurotol 38:118–122

    Article  PubMed  Google Scholar 

  • Rode T et al (2013) Neural representation in the auditory midbrain of the envelope of vocalizations based on a peripheral ear model. Front Neural Circuits 7:166

    Article  PubMed  PubMed Central  Google Scholar 

  • Rotge JY et al (2012) The associative and limbic thalamus in the pathophysiology of obsessive-compulsive disorder: an experimental study in the monkey. Transl Psychiatry 2:e161

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rubinstein JT et al (2003) Electrical suppression of tinnitus with high-rate pulse trains. Otol Neurotol 24:478–485

    Article  PubMed  Google Scholar 

  • Ryugo DK et al (2010) Synaptic plasticity after chemical deafening and electrical stimulation of the auditory nerve in cats. J Comp Neurol 518:1046–1063

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sadeghi M et al (2019) A neural ensemble correlation code for sound category identification. PLoS Biol 17:e3000449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sahlsten H et al (2019) Neuronavigated versus non-navigated repetitive transcranial magnetic stimulation for chronic tinnitus: a randomized study. Trends Hear 23:2331216518822198

    PubMed  PubMed Central  Google Scholar 

  • Sametsky EA et al (2015) Enhanced GABAA-mediated tonic inhibition in auditory thalamus of rats with behavioral evidence of tinnitus. J Neurosci 35:9369–9380

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sasso V et al (2016) Repetitive transcranial magnetic stimulation reduces remote apoptotic cell death and inflammation after focal brain injury. J Neuroinflammation 13:150

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schecklmann M et al (2016) Neuronavigated left temporal continuous theta burst stimulation in chronic tinnitus. Restor Neurol Neurosci 34:165–175

    PubMed  Google Scholar 

  • Schierholz I et al (2017) Auditory and audio-visual processing in patients with cochlear, auditory brainstem, and auditory midbrain implants: an EEG study. Hum Brain Mapp 38:2206–2225

    Article  PubMed  PubMed Central  Google Scholar 

  • Schwippel T et al (2019) Clinical review: the therapeutic use of theta-burst stimulation in mental disorders and tinnitus. Prog Neuropsychopharmacol Biol Psychiatry 92:285–300

    Article  PubMed  Google Scholar 

  • Sedley W et al (2012) Single-subject oscillatory gamma responses in tinnitus. Brain 135:3089–3100

    Article  PubMed  PubMed Central  Google Scholar 

  • Sedley W et al (2015a) Intracranial mapping of a cortical tinnitus system using residual inhibition. Curr Biol 25:1208–1214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sedley W et al (2015b) Human auditory cortex neurochemistry reflects the presence and severity of tinnitus. J Neurosci 35:14822–14828

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seeley WW et al (2007) Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci 27:2349–2356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seidman MD et al (2008) Direct electrical stimulation of Heschl’s gyrus for tinnitus treatment. Laryngoscope 118:491–500

    Article  CAS  PubMed  Google Scholar 

  • Seki S, Eggermont JJ (2003) Changes in spontaneous firing rate and neural synchrony in cat primary auditory cortex after localized tone-induced hearing loss. Hear.Res. 180:28–38

    Article  PubMed  Google Scholar 

  • Shaaya M, Fauser J, Karginov AV (2021) Optogenetics: the art of illuminating complex signaling pathways. Physiology (Bethesda) 36:52–60

    CAS  Google Scholar 

  • Shekhawat GS et al (2016) Intensity, duration, and location of high-definition transcranial direct current stimulation for tinnitus relief. Neurorehabil Neural Repair 30:349–359

    Article  PubMed  Google Scholar 

  • Shi Y et al (2009) Deep brain stimulation effects in patients with tinnitus. Otolaryngol Head Neck Surg 141:285–287

    Article  PubMed  Google Scholar 

  • Shore SE, Roberts LE, Langguth B (2016) Maladaptive plasticity in tinnitus – triggers, mechanisms and treatment. Nat Rev Neurol 12:150–160

    Article  PubMed  PubMed Central  Google Scholar 

  • Singer W (1999) Neuronal synchrony: a versatile code for the definition of relations? Neuron 24(49–65):111–125

    Google Scholar 

  • Smit JV et al (2016a) The impact of deep brain stimulation on tinnitus. Surg Neurol Int 7:S848–S854

    Article  PubMed  PubMed Central  Google Scholar 

  • Smit JV et al (2016b) Deep brain stimulation of the inferior colliculus in the rodent suppresses tinnitus. Brain Res 1650:118–124

    Article  CAS  PubMed  Google Scholar 

  • Smit JV et al (2017) Hearing assessment during deep brain stimulation of the central nucleus of the inferior colliculus and dentate cerebellar nucleus in rat. PeerJ 5:e3892

    Article  PubMed  PubMed Central  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 Otorhinolaryngol 273:1663–1675

    Article  PubMed  Google Scholar 

  • Song JJ et al (2017) A quantitative electroencephalography study on Cochlear implant-induced cortical changes in single-sided deafness with tinnitus. Front Hum Neurosci 11:210

    Article  PubMed  PubMed Central  Google Scholar 

  • Soussi T, Otto SR (1994) Effects of electrical brainstem stimulation on tinnitus. Acta Otolaryngol 114:135–140

    Article  CAS  PubMed  Google Scholar 

  • Souza DDS et al (2020) Transcranial direct current stimulation improves tinnitus perception and modulates cortical electrical activity in patients with tinnitus: a randomized clinical trial. Neurophysiol Clin 50:289–300

    Article  PubMed  Google Scholar 

  • Spitzer B, Haegens S (2017) Beyond the status quo: a role for beta oscillations in endogenous content (re)activation. eNeuro 4

    Google Scholar 

  • Steriade M et al (1991) Fast oscillations (20-40 Hz) in thalamocortical systems and their potentiation by mesopontine cholinergic nuclei in the cat. Proc Natl Acad Sci U S A 88:4396–4400

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stevens C et al (2007) Severe tinnitus and its effect on selective and divided attention. Int J Audiol 46:208–216

    Article  PubMed  Google Scholar 

  • Suga N et al (2000) The corticofugal system for hearing: recent progress. Proc Natl Acad Sci U S A 97:11807–11814

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tae WS et al (2018) Changes in the regional shape and volume of subcortical nuclei in patients with tinnitus comorbid with mild hearing loss. Neuroradiology 60:1203–1211

    Article  PubMed  Google Scholar 

  • Tort AB et al (2008) Dynamic cross-frequency couplings of local field potential oscillations in rat striatum and hippocampus during performance of a T-maze task. Proc Natl Acad Sci U S A 105:20517–20522

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tunkel DE et al (2014) Clinical practice guideline: tinnitus executive summary. Otolaryngol Head Neck Surg 151:533–541

    Article  PubMed  Google Scholar 

  • Ueyama T et al (2013) Brain regions responsible for tinnitus distress and loudness: a resting-state FMRI study. PLoS One 8:e67778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vachicouras N et al (2019) Microstructured thin-film electrode technology enables proof of concept of scalable, soft auditory brainstem implants. Sci Transl Med 11(514):eaax9487

    Article  PubMed  Google Scholar 

  • van der Loo E et al (2009) Tinnitus intensity dependent gamma oscillations of the contralateral auditory cortex. PLoS One 4:e7396

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • van Zwieten G et al (2019) Inhibition of experimental tinnitus with high frequency stimulation of the rat medial geniculate body. Neuromodulation 22:416–424

    Article  PubMed  Google Scholar 

  • Vanneste S, De Ridder D (2011) Bifrontal transcranial direct current stimulation modulates tinnitus intensity and tinnitus-distress-related brain activity. Eur J Neurosci 34:605–614

    Article  PubMed  Google Scholar 

  • Vanneste S et al (2010) The neural correlates of tinnitus-related distress. Neuroimage 52:470–480

    Article  PubMed  Google Scholar 

  • Vanneste S, Langguth B, De Ridder D (2011a) Do tDCS and TMS influence tinnitus transiently via a direct cortical and indirect somatosensory modulating effect? A combined TMS-tDCS and TENS study. Brain Stimul 4:242–252

    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 34:718–731

    Article  PubMed  Google Scholar 

  • Vanneste S, Fregni F, De Ridder D (2013a) Head-to-head comparison of transcranial random noise stimulation, transcranial AC stimulation, and transcranial DC stimulation for tinnitus. Front Psych 4:158

    Google Scholar 

  • Vanneste S et al (2013b) Comparing immediate transient tinnitus suppression using tACS and tDCS: a placebo-controlled study. Exp Brain Res 226:25–31

    Article  PubMed  Google Scholar 

  • Vanneste S et al (2017) Pairing sound with vagus nerve stimulation modulates cortical synchrony and phase coherence in tinnitus: an exploratory retrospective study. Sci Rep 7:17345

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Verma R, Jha A, Singh S (2019) Functional near-infrared spectroscopy to probe tDCS-induced cortical functioning changes in tinnitus. J Int Adv Otol 15:321–325

    Article  PubMed  PubMed Central  Google Scholar 

  • Vianney-Rodrigues P, Iancu OD, Welsh JP (2011) Gamma oscillations in the auditory cortex of awake rats. Eur J Neurosci 33(1):119–129

    Article  PubMed  Google Scholar 

  • Vianney-Rodrigues P, Auerbach BD, Salvi R (2019) Aberrant thalamocortical coherence in an animal model of tinnitus. J Neurophysiol 121:893–907

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang ZM et al (2015) Auditory rehabilitation in rhesus macaque monkeys (Macaca mulatta) with auditory brainstem implants. Chin Med J (Engl) 128:1363–1369

    Article  Google Scholar 

  • Wang TC et al (2018a) Effect of transcranial direct current stimulation in patients with tinnitus: a meta-analysis and systematic review. Ann Otol Rhinol Laryngol 127:79–88

    Article  PubMed  Google Scholar 

  • Wang W et al (2018b) Blocking tumor necrosis factor-alpha expression prevents blast-induced excitatory/inhibitory synaptic imbalance and parvalbumin-positive interneuron loss in the hippocampus. J Neurotrauma 35:2306–2316

    Article  PubMed  Google Scholar 

  • Wang W et al (2019) Neuroinflammation mediates noise-induced synaptic imbalance and tinnitus in rodent models. PLoS Biol 17:e3000307

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wegger M, Ovesen T, Larsen DG (2017) Acoustic coordinated reset neuromodulation: a systematic review of a novel therapy for tinnitus. Front Neurol 8:36

    Article  PubMed  PubMed Central  Google Scholar 

  • Weiss RS, Voss A, Hemmert W (2016) Optogenetic stimulation of the cochlea-a review of mechanisms, measurements, and first models. Network 27:212–236

    Article  PubMed  Google Scholar 

  • Weisz N et al (2005) Tinnitus perception and distress is related to abnormal spontaneous brain activity as measured by magnetoencephalography. PLoS Med 2:e153

    Article  PubMed  PubMed Central  Google Scholar 

  • Weisz N et al (2007) The neural code of auditory phantom perception. J Neurosci 27:1479–1484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wenzel GI et al (2014) Non-penetrating round window electrode stimulation for tinnitus therapy followed by cochlear implantation. Eur Arch Otorhinolaryngol 272 (11):3283–3293

    Google Scholar 

  • Wienbruch C et al (2006) Frequency organization of the 40-Hz auditory steady-state response in normal hearing and in tinnitus. Neuroimage 33:180–194

    Article  PubMed  Google Scholar 

  • Winne J et al (2019) Salicylate induces anxiety-like behavior and slow theta oscillation and abolishes the relationship between running speed and fast theta oscillation frequency. Hippocampus 29:15–25

    Article  CAS  PubMed  Google Scholar 

  • Wu C, Martel DT, Shore SE (2016) Increased synchrony and bursting of dorsal Cochlear nucleus fusiform cells correlate with tinnitus. J Neurosci 36:2068–2073

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang S et al (2011) Homeostatic plasticity drives tinnitus perception in an animal model. Proc Natl Acad Sci U S A 108:14974–14979

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang H et al (2016) Effect of repetitive transcranial magnetic stimulation on auditory function following acoustic trauma. Neurol Sci 37:1511–1516

    Article  PubMed  Google Scholar 

  • Yoon KJ, Lee YT, Han TR (2011) Mechanism of functional recovery after repetitive transcranial magnetic stimulation (rTMS) in the subacute cerebral ischemic rat model: neural plasticity or anti-apoptosis? Exp Brain Res 214:549–556

    Article  PubMed  Google Scholar 

  • Yuan T et al (2018) Transcranial direct current stimulation for the treatment of tinnitus: a review of clinical trials and mechanisms of action. BMC Neurosci 19:66

    Article  PubMed  PubMed Central  Google Scholar 

  • Zaehle T et al (2011) Excitability changes induced in the human auditory cortex by transcranial direct current stimulation: direct electrophysiological evidence. Exp Brain Res 215:135–140

    Article  PubMed  Google Scholar 

  • Zeng FG et al (2011) Tinnitus suppression by low-rate electric stimulation and its electrophysiological mechanisms. Hear Res 277:61–66

    Article  PubMed  PubMed Central  Google Scholar 

  • Zeng FG, Djalilian H, Lin H (2015) Tinnitus treatment with precise and optimal electric stimulation: opportunities and challenges. Curr Opin Otolaryngol Head Neck Surg 23:382–387

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang J (2013) Auditory cortex stimulation to suppress tinnitus: mechanisms and strategies. Hear Res 295:38–57

    Article  PubMed  Google Scholar 

  • Zhang J (2019) Blast-induced tinnitus: animal models. J Acoust Soc Am 146:3811

    Article  PubMed  Google Scholar 

  • Zhang JS, Kaltenbach JA (1998) Increases in spontaneous activity in the dorsal cochlear nucleus of the rat following exposure to high-intensity sound. Neurosci Lett 250:197–200

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Suga N (2000) Modulation of responses and frequency tuning of thalamic and collicular neurons by cortical activation in mustached bats. J Neurophysiol 84:325–333

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Zhang X (2010) Electrical stimulation of the dorsal cochlear nucleus induces hearing in rats. Brain Res 1311:37–50

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Zhang Y, Zhang X (2011) Auditory cortex electrical stimulation suppresses tinnitus in rats. J Assoc Res Otolaryngol 12:185–201

    Article  PubMed  Google Scholar 

  • Zhang L et al (2018) Remodeling of cholinergic input to the hippocampus after noise exposure and tinnitus induction in guinea pigs. Hippocampus 29 (8):669–682

    Google Scholar 

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Acknowledgements

This work was partially supported by the NIH/NIDCD R21DC014335-01, 1R21 DC010059-01.

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Authors and Affiliations

  1. Department of Otolaryngology-Head and Neck Surgery, Wayne State University School of Medicine, Detroit, MI, USA

    Jinsheng Zhang, Ethan Firestone & Ahmed Elattma

  2. Department of Communication Sciences and Disorders, Wayne State University College of Liberal Arts and Sciences, Detroit, MI, USA

    Jinsheng Zhang

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  1. Jinsheng Zhang
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  2. Ethan Firestone
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  3. Ahmed Elattma
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Correspondence to Jinsheng Zhang .

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Editors and Affiliations

  1. Medical and Health Sciences, University of Auckland, Auckland, New Zealand

    Grant D. Searchfield

  2. Department of Communication Sciences and Disorders, Department of Otolaryngology-Head Neck and Surgery, Wayne State University, Detroit, MI, USA

    Jinsheng Zhang

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Zhang, J., Firestone, E., Elattma, A. (2021). Animal Models of Tinnitus Treatment: Cochlear and Brain Stimulation. In: Searchfield, G.D., Zhang, J. (eds) The Behavioral Neuroscience of Tinnitus. Current Topics in Behavioral Neurosciences, vol 51. Springer, Cham. https://doi.org/10.1007/7854_2021_227

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