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.
KEYWORDS
Tinnitus - electrical stimulation - dorsal cochlear nucleus - inferior colliculus
- amygdala
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 [14 C]-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