Semin Hear 2008; 29(4): 313-325
DOI: 10.1055/s-0028-1095891
© Thieme Medical Publishers

Electrical Modulation of Tinnitus-Related Activity

Jinsheng Zhang1 , 2 , Zhenlong Guan1 , 6 , Virginia Ramachandran1 , 2 , Jonathan Dunford1 , Michael Hoa1 , Edward Pace1 , Johnny Mao1 , Michael Seidman4 , Kost Elisevich5 , Susan Bowyer1 , 3 , Quan Jiang3
  • 1Department of Otolaryngology-Head and Neck Surgery & Neurology, Wayne State University School of Medicine, Henry Ford Health System, Detroit, Michigan
  • 2Department of Communication Sciences & Disorders, Wayne State University College of Liberal Arts & Sciences, Henry Ford Health System, Detroit, Michigan
  • 3Department of Neurology, Henry Ford Health System, Detroit, Michigan
  • 4Department of Otolaryngology-Head and Neck Surgery, Henry Ford Health System, Detroit, Michigan
  • 5Department of Neurosurgery, Henry Ford Health System, Detroit, Michigan
  • 6Department of Zoology, Hebei Normal University College of Life Science, Shijiazhuang, Hebei, P.R. China
Further Information

Publication History

Publication Date:
24 October 2008 (online)

ABSTRACT

Tinnitus is the conscious experience of sound without an external acoustic source. Many years of research effort have contributed to a better understanding of the mechanisms underlying tinnitus, including the neural correlates of tinnitus. Our laboratory has been investigating the modulatory effects of somatosensory and cortical electrical stimulation on the neural correlates of tinnitus in auditory and nonauditory structures. These aspects of tinnitus suppression research are explored in an effort to stimulate further studies and to promote the development of effective strategies in the management of tinnitus through electrical stimulation.

REFERENCES

  • 1 Dobie R A. Overview: Suffering from tinnitus. In: Snow JB Tinnitus: Theory and Management. Hamilton, Ontario, Canada; BC Decker 2004: 1-7
  • 2 Hoffman H J, Reed G W. Epidemiology of tinnitus. In: Snow JB Tinnitus: Theory and Management. Hamilton, Ontario, Canada; BC Decker 2004: 16-41
  • 3 Kaye V, Brandstater M E. Transcutaneous electrical nerve stimulation.  eMedicine J. 2002;  3(1)
  • 4 Owen S LF, Green A L, Stein J F, Aziz T Z. Deep brain stimulation for the alleviation of post-stroke neuropathic pain.  Pain. 2006;  120 202-206
  • 5 Sweetow R. Cognitive behavior modification. In: Tyler RS Tinnitus Handbook. San Diego; Singular 2000: 297-312
  • 6 Rubinstein J T, Tyler R S. Electrical suppression of tinnitus. In: Snow JB Tinnitus: Theory and Management. Lewison, NY; BC Decker 2004: 326-335
  • 7 Cazals Y, Rouanet J F, Negrevergne M, Lagourgue P. First results of chronic electrical stimulation with a round-window electrode in totally deaf patients.  Arch Otorhinolaryngol. 1984;  239 191-196
  • 8 Chouard C H, Meyer B, Maridat D. Transcutaneous electrotherapy for severe tinnitus.  Acta Otolaryngol. 1981;  91 415-422
  • 9 Engleberg M, Bauer W. Transcutaneous electrical stimulation for tinnitus.  Laryngoscope. 1985;  95(10) 1167-1172
  • 10 Shulman A. External electrical stimulation in tinnitus control.  Am J Otol. 1985;  6(1) 110-115
  • 11 Steenerson R L, Cronin G W. Treatment of tinnitus with electrical stimulation.  Otolaryngol Head Neck Surg. 1999;  121 1-4
  • 12 Brackmann D E. Reduction of tinnitus in cochlear-implant patients.  J Laryngol Otol Suppl. 1981;  4 163-165
  • 13 Dauman R, Tyler R S, Aran J M. Intracochlear electrical tinnitus reduction.  Acta Otolaryngol. 1993;  113 291-295
  • 14 Graham J M, Hazell J WP. Electrical stimulation of the human cochlea using a transtympanic electrode.  Br J Audiol. 1977;  11 59-62
  • 15 Hazell J WP, Jastreboff P J, Meerton L E, Conway M J. Electrical tinnitus suppression: frequency dependence of effects.  Audiology. 1993;  32 68-77
  • 16 Konopka W, Zalewski P, Olszewski J, Olszewska-Ziaber A, Pietkiewicz P. Tinnitus suppression by electrical promontory stimulation (EPS) in patients with sensorineural hearing loss.  Auris Nasus Larynx. 2001;  28 35-40
  • 17 Kuk F K, Tyler R S, Rustad N, Harker L A, Tye-Murray N. Alternating current at the eardrum for tinnitus reduction.  J Speech Hear Res. 1989;  32 393-400
  • 18 Matsushima J, Sakai N, Sakajiri M, Miyoshi S, Uemi N, Ifukube T. An experience of the usage of electrical tinnitus suppressor.  Artif Organs. 1996;  20(8) 955-958
  • 19 McKerrow W S, Schreiner C E, Snyder R L, Merzenich M M, Toner J G. Tinnitus suppression by cochlear implants.  Ann Otol Rhinol Laryngol. 1991;  100 552-558
  • 20 Okusa M, Shiraishi T, Kubo T, Matsunaga T. Tinnitus suppression by electrical promontory stimulation in sensorineural deaf patients.  Acta Otolaryngol Suppl. 1993;  501 54-58
  • 21 Portmann M, Negrevergne M, Aran J M, Cazals Y. Electrical stimulation of the ear: clinical applications.  Ann Otol Rhinol Laryngol. 1983;  92 621-622
  • 22 Rothera M, Conway M J, Brightwell A, Graham J. Evaluation of patients for cochlear implant by promontory stimulation.  Br J Audiol. 1986;  20 25-28
  • 23 Thedinger B, House W F, Edgerton B J. Cochlear implant for tinnitus.  Ann Otol Rhinol Laryngol. 1985;  94 10-13
  • 24 De Ridder D, De Mulder G, Walsh V, Muggleton N, Sunaert S, Moller A. Magnetic and electrical stimulation of the auditory cortex for intractable tinnitus.  J Neurosurg. 2004;  100 560-564
  • 25 Soussi T, Otto S R. Effects of electrical brainstem stimulation on tinnitus.  Acta Otolaryngol. 1994;  114 135-140
  • 26 Langguth B, Zowe M, Landgrebe M et al.. Transcranial magnetic stimulation for the treatment of tinnitus: a new coil positioning method and first results.  Brain Topogr. 2006;  18(4) 241-247
  • 27 Fregni F, Marcondes R, Boggio P S et al.. Transient tinnitus suppression induced by repetitive transcranial magnetic stimulation and transcranial direct current stimulation.  Eur J Neurol. 2006;  13(9) 996-1001
  • 28 De Ridder D, De Mulder G, Verstraeten E et al.. Auditory cortex stimulation for tinnitus.  Acta Neurochir Suppl. 2007;  97 451-462
  • 29 Cacace A T, Cousins J P, Parnes S M et al.. Cutaneous-evoked tinnitus. I. Phenomenology, psychophysics and functional imaging.  Audiol Neurootol. 1999;  4(5) 247-257
  • 30 Levine R A, Abel M D, Cheng H. CNS somatosensory-auditory interactions elicit or modulate tinnitus.  Exp Brain Res. 2003;  153(4) 643-648
  • 31 Cooper B C, Cooper D L, Lucente F E. Electromyography of masticatory muscles in craniomandibular disorders.  Laryngoscope. 1991;  101(2) 150-157
  • 32 Rubinstein B. Tinnitus and craniomandibular disorders—is there a link?.  Swed Dent J Suppl. 1993;  95 1-46
  • 33 Lockwood A H, Salvi R J, Coad M L, Towsley M L, Wack D S, Murphy B W. The functional neuroanatomy of tinnitus: evidence for limbic system links and neural plasticity.  Neurology. 1998;  50 114-120
  • 34 Levine R A. Somatic (craniocervical) tinnitus and the dorsal cochlear nucleus hypothesis.  Am J Otolaryngol. 1999;  20(6) 351-362
  • 35 Moller A R, Moller M B, Yokota M. Some forms of tinnitus may involve the extralemniscal auditory pathway.  Laryngoscope. 1992;  102 1165-1171
  • 36 Haenggeli A, Zhang J S, Vischer M W, Pelizzone M, Rouiller E M. Electrically evoked compound action potential (ECAP) of the cochlear nerve in response to pulsatile electrical stimulation of the cochlea in the rat: effects of stimulation at high rates.  Audiology. 1998;  37 353-371
  • 37 Salvinelli F, Casale M, Paparo F, Persico A M, Zin C MH. Subjective tinnitus, temporomandibular joint dysfunction, and serotonin modulation of neural plasticity: causal or casual triad?.  Med Hypotheses. 2003;  61(4) 446-448
  • 38 Brozoski T J, Bauer C A, Caspary D M. Elevated fusiform cell activity in the dorsal cochlear nucleus of chinchillas with psychophysical evidence of tinnitus.  J Neurosci. 2002;  22(6) 2383-2390
  • 39 Kaltenbach J A, Zacharek M A, Zhang J, Frederick S. Activity in the dorsal cochlear nucleus of hamsters previously tested for tinnitus following intense tone exposure.  Neurosci Lett. 2004;  355 121-125
  • 40 Kaltenbach J A, McCaslin D L. Increases in spontaneous activity in the dorsal cochlear nucleus following exposure to high intensity sound: a possible neural correlate of tinnitus.  Aud Neurosci. 1996;  3(1) 57-78
  • 41 Zhang J S, Kaltenbach J A. Increases in spontaneous activity in the dorsal cochlear nucleus of the rat following exposure to high-intensity sound.  Neurosci Lett. 1998;  250 197-200
  • 42 Heffner H E, Harrington I A. Tinnitus in hamsters following exposure to intense sound.  Hear Res. 2002;  170 83-95
  • 43 Brozoski T J, Bauer C A. The effect of dorsal cochlear nucleus ablation on tinnitus in rats.  Hear Res. 2005;  206 227-236
  • 44 Davis K A. Evidence of a functionally segregated pathway from dorsal cochlear nucleus to inferior colliculus.  J Neurophysiol. 2002;  87(4) 1824-1835
  • 45 Imig T J, Durham D. Effect of unilateral noise exposure on the tonotopic distribution of spontaneous activity in the cochlear nucleus and inferior colliculus in the cortically intact and decorticate rat.  J Comp Neurol. 2005;  490(4) 391-413
  • 46 Oliver D L, Beckius G E, Bishop D C, Kuwada S. Simultaneous anterograde labeling of axonal layers from lateral superior olive and dorsal cochlear nucleus in the inferior colliculus of cat.  J Comp Neurol. 1997;  382(2) 215-229
  • 47 Norena A J, Eggermont J J. Enriched acoustic environment after noise trauma abolishes neural signs of tinnitus.  Neuroreport. 2006;  17(6) 559-563
  • 48 Seki S, Eggermont J J. Changes in spontaneous firing rate and neural synchrony in cat primary auditory cortex after localized tone-induced hearing loss.  Hear Res. 2003;  180 28-38
  • 49 Komiya H, Eggermont J J. Spontaneous firing activity of cortical neurons in adult cats with reorganized tonotopic map following pure-tone trauma.  Acta Otolaryngol. 2000;  120(6) 750-756
  • 50 Zhang J S, Kaltenbach J A, Godfrey D A, Wang J. Origin of hyperactivity in the hamster dorsal cochlear nucleus following intense sound exposure.  J Neurosci Res. 2006;  84(4) 819-831
  • 51 Shore S E, Vass Z, Wys N L, Altschuler R A. Trigeminal ganglion innervates the auditory brainstem.  J Comp Neurol. 2000;  419(3) 271-285
  • 52 Zhou J, Shore S. Projections from the trigeminal nuclear complex to the cochlear nuclei: A retrograde and anterograde tracing study in the guinea pig.  J Neurosci Res. 2004;  78(6) 901-907
  • 53 Wolff A, Kunzle H. Cortical and medullary somatosensory projections to the cochlear nuclear complex in the hedgehog tenrec.  Neurosci Lett. 1997;  221(2–3) 125-128
  • 54 Itoh K, Kamiya H, Mitani A, Yasui Y, Takada M, Mizuno N. Direct projections from the dorsal column nuclei and the spinal trigeminal nuclei to the cochlear nuclei in the cat.  Brain Res. 1987;  400 145-150
  • 55 Li H, Mizuno N. Single neurons in the spinal trigeminal and dorsal column nuclei project to both the cochlear nucleus and the inferior colliculus by way of axon collaterals: A fluorescent retrograde double-labeling study in the rat.  Neurosci Res. 1997;  29 135-142
  • 56 Weinberg R J, Rustioni A. Brainstem projections to the rat cuneate nucleus.  J Comp Neurol. 1989;  282 142-156
  • 57 Wright D D, Ryugo D K. Mossy fiber projections from the cuneate nucleus to the cochlear nucleus in the rat.  J Comp Neurol. 1996;  365 159-172
  • 58 Davis K A, Miller R L, Young E D. Effects of somatosensory and parallel-fiber stimulation on neurons in dorsal cochlear nucleus.  J Neurophysiol. 1996;  76(5) 3012-3024
  • 59 Manis P B. Responses to parallel fiber stimulation in the guinea pig dorsal cochlear nucleus in vitro.  J Neurophysiol. 1989;  61(1) 149-161
  • 60 Shore S E. Multisensory integration in the dorsal cochlear nucleus: unit responses to acoustic and trigeminal ganglion stimulation.  Eur J Neurosci. 2005;  21(12) 3334-3348
  • 61 Young E D, Nelken I, Conley R A. Somatosensory effects on neurons in dorsal cochlear nucleus.  J Neurophysiol. 1995;  73(2) 743-765
  • 62 Kanold P O, Young E D. Proprioceptive information from the pinna provides somatosensory input to cat dorsal cochlear nucleus.  J Neurosci. 2001;  21(19) 7848-7858
  • 63 Zhang J S, Guan Z L. Suppressive effects of somatosensory electrical stimulation on spontaneous activity in the dorsal cochlear nucleus of anesthetized hamsters.  J Neurosci Res. 2007;  , Nov 1 [Epub ahead of print]
  • 64 Zhang J S, Guan Z L. Pathways involved in somatosensory electrical modulation of dorsal cochlear nucleus activity.  Brain Res. 2007;  1184 121-131
  • 65 Ehret G, Fischer R. Neuronal activity and tonotopy in the auditory system visualized by c-fos gene expression.  Brain Res. 1991;  567(2) 350-354
  • 66 Rouiller E M, Wan X S, Moret V, Liang F. Mapping of c-fos expression elicited by pure tones stimulation in the auditory pathways of the rat, with emphasis on the cochlear nucleus.  Neurosci Lett. 1992;  144(1–2) 19-24
  • 67 Zhang J S, Haenggeli C A, Tempini A, Vischer M W, Moret V, Rouiller E M. Electrically induced fos-like immunoreactivity in the auditory pathway of the rat: effects of survival time, duration, and intensity of stimulation.  Brain Res Bull. 1996;  39(2) 75-82
  • 68 Alibardi L. Ultrastructural immunocytochemistry for glycine in neurons of the dorsal cochlear nucleus of the guinea pig.  J Submicrosc Cytol Pathol. 2003;  35(4) 373-387
  • 69 Golding N L, Oertel D. Context-dependent synaptic action of glycinergic and GABAergic inputs in the dorsal cochlear nucleus.  J Neurosci. 1996;  16(7) 2208-2219
  • 70 Juiz J M, Helfert R H, Bonneau J M, Wenthold R J, Altschuler R A. Three classes of inhibitory amino acid terminals in the cochlear nucleus of the guinea pig.  J Comp Neurol. 1996;  373(1) 11-26
  • 71 Guan Z L, Zhang J S. Effects of sectioning of parallel fibers on somatosensory electrical stimulation induced-effects on neural activity of the dorsal cochlear nucleus of hamsters. Assoc Res Otolaryngol Meeting, 2007
  • 72 Kleinjung J, Romein J, Lin K, Heringa J. Contact-based sequence alignment.  Nucleic Acids Res. 2004;  32(8) 2464-2473
  • 73 De Ridder D, Verstraeten E, Van der Kelen K et al.. Transcranial magnetic stimulation for tinnitus: influence of tinnitus duration on stimulation parameter choice and maximal tinnitus suppression.  Otol Neurotol. 2005;  26(4) 616-619
  • 74 Plewnia C, Reimold M, Najib A, Reischl G, Plontke S K, Gerloff C. Moderate therapeutic efficacy of positron emission tomography-navigated repetitive transcranial magnetic stimulation for chronic tinnitus: a randomised, controlled pilot study.  J Neurol Neurosurg Psychiatry. 2007;  78(2) 152-156
  • 75 Seidman M D, De Ridder D, Elisevich K et al.. Direct electrical stimulation of Heschl's gyrus for tinnitus treatment.  Laryngoscope. 2008;  118 491-500
  • 76 Zhang J S, Kaltenbach J A, Wang J, Bronchti G. Changes in [14C]-2-deoxyglucose uptake in the auditory pathway of hamsters previously exposed to intense sound.  Hear Res. 2003;  185 13-21
  • 77 Manabe Y, Yoshida S, Saito H, Oka H. Effects of lidocaine on salicylate-induced discharge of neurons in the inferior colliculus of the guinea pig.  Hear Res. 1997;  103(1–2) 192-198
  • 78 Chen G-D, Jastreboff P J. Salicylate-induced abnormal activity in the inferior colliculus of rats.  Hear Res. 1995;  82 158-178
  • 79 Wallhausser-Franke E. Salicylate evokes c-fos expression in the brain stem: implications for tinnitus.  Neuroreport. 1997;  8 725-728
  • 80 Ma W L, Hidaka H, May B J. Spontaneous activity in the inferior colliculus of CBA/J mice after manipulations that induce tinnitus.  Hear Res. 2006;  212 9-21
  • 81 Jastreboff P J, Sasaki C T. Salicylate-induced changes in spontaneous activity of single units in the inferior colliculus of the guinea pig.  J Acoust Soc Am. 1986;  80(5) 1384-1391
  • 82 Wu J L, Chiu T W, Poon P W. Differential changes in fos-immunoreactivity at the auditory brainstem after chronic injections of salicylate in rats.  Hear Res. 2003;  176(1–2) 80-93
  • 83 Harrison J M, Howe M E. Anatomy of the afferent auditory nervous system of mammals. In: Keidel WD, Neff WD Handbook of Sensory Physiology. Berlin, Germany; Springer 1974
  • 84 Faye-Lund H. The neocortical projection to the inferior colliculus in the albino rat.  Anat Embryol (Berl). 1985;  173(1) 53-70
  • 85 Faye-Lund H. Projection from the inferior colliculus to the superior olivary complex in the albino rat.  Anat Embryol (Berl). 1986;  175(1) 35-52
  • 86 Huffman R F, Henson Jr O W. The descending auditory pathway and acousticomotor systems: connections with the inferior colliculus.  Brain Res. 1990;  15(3) 295-323
  • 87 Spangler K M, Warr W B. The descending auditory system. In: Altschuler RA, Bobbin RP, Clopton BM, Hoffman DW Neurobiology of Hearing: The Central Auditory System. New York, NY; Raven Press 1991: 27-45
  • 88 Saldaña E. Descending projections from the inferior colliculus to the cochlear nuclei in mammals. In: Merchan M, Juiz JS, Godfrey DA, Mugniani E The Mammalian Cochlear Nuclei: Organization and Function. New York, NY; Plenum Press 1993: 153-165
  • 89 Suga N, Gao E, Zhang Y, Ma X, Olsen J F. The corticofugal system for hearing: Recent progress.  Proc Natl Acad Sci U S A. 2000;  97(22) 11807-11814
  • 90 Rouiller E M. Mapping activity in the auditory pathway with c-fos. In: Syka J Acoustical Signal Processing in the Central Auditory System. New York, NY; Plenum Press 1997: 33-48
  • 91 Zhang J S, Vischer M W, Haenggeli C A, Rouiller E M. Responses of the auditory nerve to high rate pulsatile electrical stimulation: comparison between normal and deafened rats. In: Syka J Acoustical Signal Processing in the Central Auditory System. New York, NY; Plenum Press 1997: 577-583
  • 92 Saldaña E, Feliciano M, Mugniani E. Distribution of descending projections from primary auditory neocortex to inferior colliculus mimics the topography of intracollicular projections.  J Comp Neurol. 1996;  371(1) 15-40
  • 93 Weedman D L, Pongstaporn T, Ryugo D K. Ultrastructural study of the granule cell domain of the cochlear nucleus in rats: mossy fiber endings and their targets.  J Comp Neurol. 1996;  369 345-360
  • 94 Feliciano M, Potashner S J. Evidence for a glutamatergic pathway from the guinea pig auditory cortex to the inferior colliculus.  J Neurochem. 1995;  65(3) 1348-1357
  • 95 Schofield B R. Origins of projections from the inferior colliculus to the cochlear nucleus in guinea pigs.  J Comp Neurol. 2001;  429(2) 206-220
  • 96 Schofield B R, Coomes D L. Auditory cortical projections to the cochlear nucleus in guinea pigs.  Hear Res. 2005;  199(1–2) 89-102
  • 97 Jacomme A V, Nodal F R, Bajo V M et al.. The projection from auditory cortex to cochlear nucleus in guinea pigs: an in vivo anatomical and in vitro electrophysiological study.  Exp Brain Res. 2003;  153(4) 467-476
  • 98 Doucet J R, Rose L, Ryugo D K. The cellular origin of corticofugal projections to the superior olivary complex in the rat.  Brain Res. 2002;  925(1) 28-41
  • 99 Bajo V M, Moore D R. Descending projections from the auditory cortex to the inferior colliculus in the gerbil, Meriones unguiculatus .  J Comp Neurol. 2005;  486(2) 101-116
  • 100 Schofield B R, Coomes D L. Pathways from auditory cortex to the cochlear nucleus in guinea pigs.  Hear Res. 2006;  216–217 81-89
  • 101 Zhang J S, Guan Z L, Ramachandran V et al.. Mechanisms of auditory cortex stimulation. The 2nd Tinnitus Research Initiative Meeting 2007 Monaco;
  • 102 Mahlke C, Wallhausser-Franke E. Evidence for tinnitus-related plasticity in the auditory and limbic system, demonstrated by arg3.1 and c-fos immunocytochemistry.  Hear Res. 2004;  195 17-34
  • 103 Wallhausser-Franke E, Mahlke C, Oliva R, Braun S, Wenz G, Langner G. Expression of c-fos in auditory and non-auditory brain regions of the gerbil after manipulations that induce tinnitus.  Exp Brain Res. 2003;  153(4) 649-654
  • 104 Jastreboff P J, Hazell J WP. Tinnitus retraining therapy.  Br J Audiol. 1999;  33(1) 68-69
  • 105 Jastreboff P J, Jastreboff M M. Tinnitus retraining therapy for patients with tinnitus and decreased sound tolerance.  Otolaryngol Clin North Am. 2003;  36(2) 321-336
  • 106 Kaltenbach J A. The dorsal cochlear nucleus as a participant in the auditory, attentional and emotional components of tinnitus.  Hear Res. 2006;  216–217 224-234
  • 107 Holland P C, Gallagher M. Amygdala circuitry in attentional and representational processes.  Trends Cogn Sci. 1999;  3(2) 65-73
  • 108 Cardinal R N, Parkinson J A, Lachenal G et al.. Effects of selective excitotoxic lesions of the nucleus accumbens core, anterior cingulate cortex, and central nucleus of the amygdala on autoshaping performance in rats.  Behav Neurosci. 2002;  116(4) 553-567
  • 109 McGaugh J L, McIntyre C K, Power A E. Amygdala modulation of memory consolidation: interaction with other brain systems.  Neurobiol Learn Mem. 2002;  78(3) 539-553
  • 110 LeDoux J. The emotional brain, fear, and the amygdala.  Cell Mol Neurobiol. 2003;  23(4–5) 727-738

Dr. Jinsheng S ZhangPh.D. 

DLaboratory of Auditory Prostheses Research, Department of Otolaryngology-Head and Neck Surgery

5E-UHC, Wayne State University School of Medicine, 4201 Saint Antoine, Detroit, MI 48201

Email: jinzhang@med.wayne.edu

    >