Development of tinnitus-related neuronal hyperactivity through homeostatic plasticity after hearing loss: A computational model

European Journal of Neuroscience

Volumn 23, Issue 11, 2006, Pages 3124-3138

  Schaette, Roland ^a   Kempter, Richard ^a,b,c  

^a HUMBOLDT UNIVERSITY   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c BERNSTEIN CENTER FOR COMPUTATIONAL NEUROSCIENCE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACOUSTIC NERVE FIBER; ANIMAL CELL; ARTICLE; AUDITORY STIMULATION; COCHLEAR NERVE; CONTROLLED STUDY; DOWNSTREAM PROCESSING; HAIR CELL; HEARING LOSS; HOMEOSTASIS; HUMAN; HUMAN CELL; HYPERACTIVITY; MATHEMATICAL MODEL; NERVE CELL PLASTICITY; NERVE CONDUCTION; NONHUMAN; PRIORITY JOURNAL; STEREOCILIUM; TINNITUS;

ACOUSTIC STIMULATION; ANIMALS; AUDITORY PATHWAYS; COMPUTER SIMULATION; DOSE-RESPONSE RELATIONSHIP, RADIATION; HEARING LOSS; HUMANS; MODELS, BIOLOGICAL; NEURONS; PROBABILITY; TINNITUS;

EID: 33745087777     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2006.04774.x     Document Type: Article

References (74)

1. Blum J.J. Reed M.C. ( 1998) Effects of wide band inhibitors in the dorsal cochlear nucleus. II. Model calculations of the responses to complex sounds. J. Acoust. Soc. Am., 103, 2000 2009.
2. Brozoski T.J. Bauer C.A. ( 2005) The effect of dorsal cochlear nucleus ablation on tinnitus in rats. Hear. Res., 206, 227 236.
3. Brozoski T.J. Bauer C.A. Caspary D.M. ( 2002) Elevated fusiform cell activity in the dorsal cochlear nucleus of chinchillas with psychophysical evidence of tinnitus. J. Neurosci., 22, 2383 2390.
4. Burrone J. Murthy V.N. ( 2003) Synaptic gain control and homeostasis. Curr. Opin. Neurobiol., 13, 560 567.
5. Cant N.B. Gaston K.C. ( 1982) Pathways connecting the right and left cochlear nuclei. J. Comp. Neurol., 212, 313 326.
6. Caspary D.M. Schatteman T.A. Hughes L.F. ( 2005) Age-related changes in the inhibitory response properties of dorsal cochlear nucleus output neurons: role of inhibitory inputs. J. Neurosci., 25, 10952 10959.
7. Chen G.D. Fechter L.D. ( 2003) The relationship between noise-induced hearing loss and hair cell loss in rats. Hear. Res., 177, 81 90.
8. Dallos P. Harris D. ( 1978) Properties of auditory nerve responses in absence of outer hair cells. J. Neurophysiol., 41, 365 383.
9. Desai N.S. Rutherford L.C. Turrigiano G.G. ( 1999) Plasticity in the intrinsic excitability of cortical pyramidal neurons. Nature Neurosci., 2, 515 520.
10. Escabi M.A. Miller L.M. Read H.L. Schreiner C.E. ( 2003) Naturalistic auditory contrast improves spectrotemporal coding in the cat inferior colliculus. J. Neurosci., 23, 11489 11504.
11. Formby C. Sherlock L. Gold S.L. ( 2003) Adaptive plasticity of loudness induced by chronic attenuation and enhancement of the acoustic background. J. Acoust. Soc. Am., 114, 55 58.
12. Franosch J.-M.P. Kempter R. Fastl H. van Hemmen J.L. ( 2003) Zwicker tone illusion and noise reduction in the auditory system. Phys. Rev. Lett., 90, 178103.
13. Geisler C.D. ( 1998) From Sound to Synapse. Oxford University Press, New York.
14. Harrison R.V. ( 1981) Rate-versus-intensity functions and related AP responses in normal and pathological guinea pig and human cochleas. J. Acoust. Soc. Am., 70, 1036 1044.
15. Hazell J.W.P. ( 1999) The TRT method in practice. In Hazell J.W.P., (Ed) Proceedings of the Sixth International Tinnitus Seminar. The Tinnitus and Hyperacusis Centre, London, pp. 92 98.
16. Heffner H.E. Harrington I.A. ( 2002) Tinnitus in hamsters following exposure to intense sound. Hear. Res., 170, 83 95.
17. Heinz M.G. Young E.D. ( 2004) Response growth with sound level in auditory nerve fibers after noise-induced hearing loss. J. Neurophysiol., 91, 784 794.
18. Henry J.A. Meikle M. Gilbert A. ( 1999) Audiometric correlates of tinnitus pitch: insights from the Tinnitus Data Registry. In Hazell J.W.P., (Ed), Proceedings of the Sixth International Tinnitus Seminar. The Tinnitus and Hyperacusis Centre, London, pp. 51 57.
19. Houweling A.R. Bazhenov M. Timofeev I. Steriade M. Sejnowski T.J. ( 2005) Homeostatic synaptic plasticity can explain post-traumatic epileptogenesis in chronically isolated neocortex. Cereb. Cortex, 15, 834 845.
20. Ito J. Sakakihara J. ( 1994) Suppression of tinnitus by cochlear implantation. Am. J. Otolaryngol., 15, 145 148.
21. Jacomme A.V. Nodal F.R. Bajo V.M. Manunta Y. Edeline J.M. Babalian A. Rouiller E.M. ( 2003) The projection from auditory cortex to cochlear nucleus in guinea pigs: an in vivo anatomical and in vitro electrophysiological study. Exp. Brain Res., 153, 467 476.
22. Jastreboff P.J. ( 1999) The neurophysiological model of tinnitus and hyperacusis. In Hazell J.W.P., (Ed), Proceedings of the Sixth International Tinnitus Seminar. The Tinnitus and Hyperacusis Centre, London, pp. 32 38.
23. Jastreboff M.M. Jastreboff P.J. ( 1999) How TRT derives from the neurophysiological model. In Hazell J.W.P. (Ed), Proceedings of the Sixth International Tinnitus Seminar. The Tinnitus and Hyperacusis Centre, London, pp. 87 91.
24. Kaltenbach J.A. Afman C.E. ( 2000) Hyperactivity in the dorsal cochlear nucleus after intense sound exposure and its resemblance to tone-evoked activity: a physiological model for tinnitus. Hear. Res., 140, 165 172.
25. Kaltenbach J.A. Godfrey D.A. Neumann J.B. McCaslin D.L. Afman C.E. Zhang J. ( 1998) Changes in spontaneous neural activity in the dorsal cochlear nucleus following exposure to intense sound: relation to threshold shift. Hear. Res., 124, 78 84.
26. Kaltenbach J.A. Rachel J.D. Mathog T.A. Zhang J. Falzarano P.R. Lewandowski M. ( 2002) Cisplatin-induced hyperactivity in the dorsal cochlear nucleus and its relation to outer hair cell loss: relevance to tinnitus. J. Neurophysiol., 88, 699 714.
27. Kaltenbach J.A. Zacharek M.A. Zhang J. Frederick S. ( 2004) Activity in the dorsal cochlear nucleus of hamsters previously tested for tinnitus following intense tone exposure. Neurosci. Lett., 355, 121 125.
28. Kaltenbach J.A. Zhang J. Afman C.E. ( 2000) Plasticity of spontaneous neural activity in the dorsal cochlear nucleus after intense sound exposure. Hear. Res., 147, 282 292.
29. Kanold P.O. Manis P.B. ( 2001) A physiologically based model of discharge pattern regulation by transient K+ currents in cochlear nucleus pyramidal cells. J. Neurophysiol., 85, 523 538.
30. Kanold P.O. Young E.D. ( 2001) Proprioceptive information from the pinna provides somatosensory input to cat dorsal cochlear nucleus. J. Neurosci., 21, 7848 7858.
31. Kilman V. van Rossum M.C.W. Turrigiano G.G. ( 2002) Activity deprivation reduces miniature IPSC amplitude by decreasing the number of postsynaptic GABAA receptors clustered at neocortical synapses. J. Neurosci., 22, 1328 1337.
32. Kotak V.C. Fujisawa S. Lee F.A. Karthikeyan O. Aoki C. Sanes D.H. ( 2005) Hearing loss raises excitability in the auditory cortex. J. Neurosci., 25, 3908 3918.
33. Laughlin S. ( 1981) A simple coding procedure enhances a neuron's information capacity. Z. Naturforsch., 36, 910 912.
34. Liberman M.C. ( 1978) Auditory-nerve response from cats raised in a low-noise chamber. J. Acoust. Soc. Am., 63, 442 455.
35. Liberman M.C. ( 1984) Single-neuron labeling and chronic cochlear pathology. I. Threshold shift and characteristic-frequency shift. Hear. Res., 16, 33 41.
36. Liberman M.C. Dodds L.W. ( 1984) Single-neuron labeling and chronic cochlear pathology. II. Stereocilia damage and alterations of spontaneous discharge rates. Hear. Res., 16, 43 53.
37. Liberman M.C. Kiang N.Y. ( 1984) Single-neuron labeling and chronic cochlear pathology. IV. Stereocilia damage and alterations in rate- and phase-level functions. Hear. Res., 16, 75 90.
38. Maffei A. Nelson S.B. Turrigiano G.G. ( 2004) Selective reconfiguration of layer 4 visual cortical circuitry by visual deprivation. Nature Neurosci., 7, 1353 1359.
39. Meleca R.J. Kaltenbach J.A. Falzarano P.R. ( 1997) Changes in the tonotopic map of the dorsal cochlear nucleus in hamsters with hair cell loss and radial nerve bundle degeneration. Brain Res., 750, 201 213.
40. Muly S.M. Gross J.S. Potashner S.J. ( 2004) Noise trauma alters d-[3H]aspartate release and AMPA binding in chinchilla cochlear nucleus. J. Neurosci. Res., 75, 585 596.
41. Noreña A.J. Eggermont J.J. ( 2003) Changes in spontaneous neural activity immediately after an acoustic trauma: implications for neural correlates of tinnitus. Hear. Res., 183, 137 153.
42. Norena A. Micheyl C. Chery-Croze S. Collet L. ( 2002) Psychoacoustic characterization of the tinnitus spectrum: implications for the underlying mechanisms of tinnitus. Audiol. Neurootol., 7, 358 369.
43. Oleskevich S. Walmsley B. ( 2002) Synaptic transmission in the auditory brainstem of normal and congenitally deaf mice. J. Physiol., 540, 447 455.
44. Pilgramm M. Rychlik R. Siedentrop H. Goebel G. Kirchhoff D. ( 1999) Tinnitus in the Federal Republic of Germany: a representative epidemological study. In Hazell J.W.P., (Ed), Proceedings of the Sixth International Tinnitus Seminar. The Tinnitus and Hyperacusis Centre, London, pp. 64 67.
45. Quaranta N. Wagstaff S. Baguley D.M. ( 2004) Tinnitus and cochlear implantation. Int. J. Audiol., 43, 245 251.
46. Reed M.C. Blum J.J. ( 1995) A computational model for signal processing by the dorsal cochlear nucleus. I. Responses to pure tones. J. Acoust. Soc. Am., 97, 425 438.
47. Rhode W.S. Greenberg S. ( 1992) Physiology of the cochlear nuclei. In Oertel D. Fay R.R. Popper A.N., (Eds), The Mammalian Auditory Pathway: Neurophysiology 2 of Springer Handbook of Auditory Research. Springer, New York, pp. 94 152.
48. van Ruijven M.W. de Groot J.C. Klis S.F. Smoorenburg G.F. ( 2005) The cochlear targets of cisplatin: an electrophysiological and morphological time-sequence study. Hear. Res., 205, 241 248.
49. van Ruijven M.W. de Groot J.C. Smoorenburg G. ( 2004) Time sequence of degeneration pattern in the guinea pig cochlea during cisplatin administration. A quantitative histological study. Hear. Res., 197, 44 54.
50. Ryugo D.K. ( 1992) The auditory nerve: peripheral innervation, cell body morphology, and central projections. In Webster D. Popper A. Fay R., (Eds), The Mammalian Auditory Pathway, Neuroanatomy. Springer, New York, pp. 23 65.
51. Sachs M.B. Abbas P.J. ( 1974) Rate versus level functions for auditory-nerve fibers in cats: tone-burst stimuli. J. Acoust. Soc. Am., 56, 1835 1847.
52. Salvi R.J. Wang J. Ding D. ( 2000) Auditory plasticity and hyperactivity following cochlear damage. Hear. Res., 147, 261 274.
53. Schmiedt R.A. Zwislocki J.J. ( 1980) Effects of hair cell lesions on responses of cochlear nerve fibers. II. Single- and two-tone intensity functions in relation to tuning curves. J. Neurophysiol., 43, 1390 1405.
54. Schneider E. Hocker K.M. Lebisch H. Pilgramm M. ( 1999) Does systematic noise stimulation improve tinnitus habituation? Hazell J.W.P. (Ed), Proceedings of the Sixth International Tinnitus Seminar. The Tinnitus and Hyperacusis Centre, London, pp. 391 393.
55. Seki S. Eggermont J.J. ( 2002) Changes in cat primary auditory cortex after minor-to-moderate pure-tone induced hearing loss. Hear. Res., 173, 172 186.
56. Seki S. Eggermont J.J. ( 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.
57. Shore S.E. Godfrey D.A. Helfert R.H. Altschuler R.A. Bledsoe S.C.J. ( 1992) Connections between the cochlear nuclei in guinea pig. Hear. Res., 62, 16 26.
58. Spirou G.A. Young E.D. ( 1991) Organization of dorsal cochlear nucleus type IV unit response maps and their relationship to activation by bandlimited noise. J. Neurophysiol., 66, 1750 1768.
59. Sumner C.J. O'Mard L.P. Lopez-Poveda E.A. Meddis R. ( 2003) A nonlinear filter-bank model of the guinea-pig cochlear nerve: rate responses. J. Acoust. Soc. Am., 113, 3264 3274.
60. Suneja S.K. Benson C.G. Potashner S.J. ( 1998a) Glycine receptors in adult guinea pig brain stem auditory nuclei: regulation after unilateral cochlear ablation. Exp. Neurol., 154, 473 488.
61. Suneja S.K. Potashner S.J. Benson C.G. ( 1998b) Plastic changes in glycine and GABA release and uptake in adult brain stem auditory nuclei after unilateral middle ear ossicle removal and cochlear ablation. Exp. Neurol., 151, 273 288.
62. Surr R.K. Kolb J.A. Cord M.T. Garrus N.P. ( 1999) Tinnitus handicap inventory (THI) as a hearing aid outcome measure. J. Am. Acad. Audiol., 10, 489 495.
63. Turrigiano G.G. ( 1999) Homeostatic plasticity in neuronal networks: the more things change, the more they stay the same. Trends Neurosci., 22, 221 227.
64. Turrigiano G.G. Leslie K.R. Desai N.S. Rutherford L.C. Nelson S.B. ( 1998) Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature, 391, 892 896.
65. Vale C. Sanes D.H. ( 2002) The effect of bilateral deafness on excitatory and inhibitory synaptic strength in the inferior colliculus. Eur. J. Neurosci., 16, 2394 2404.
66. Wang J. Ding D. Salvi R.J. ( 2002a) Functional reorganization in chinchilla inferior colliculus associated with chronic and acute cochlear damage. Hear. Res., 168, 238 249.
67. Wang Y. Hirose K. Liberman M.C. ( 2002b) Dynamics of noise-induced cellular injury and repair in the mouse cochlea. J. Assoc. Res. Otolaryngol., 3, 248 268.
68. Wang J. Powers N.L. Hofstetter P. Trautwein P. Ding R. Salvi R. ( 1997) Effects of selective inner hair cell loss on auditory nerve fiber threshold, tuning and spontaneous and driven discharge rate. Hear. Res., 107, 67 82.
69. Weedman D.L. Ryugo D. ( 1996) Pyramidal cells in primary auditory cortex project to cochlear nucleus in rat. Brain Res., 706, 97 102.
70. Weisz N. Hartmann T. Dohrmann K. Schlee N. Norena A. ( 2005) Psychoacoustic evidence for deafferentiation in tinnitus subjects with normal audiograms. In Dauman R. Bouscau-Faure F., (Eds), Proceedings of the VIIIth International Tinnitus Seminar, Pau France, September 2005. The French Society for Audiology, Paris, France 76.
71. Young E.D. Davis K.A. ( 2002) Circuitry and function of the dorsal cochlear nucleus. In Oertel D. Fay R.R. Popper A.N., (Eds), Integrative Functions in the Mammalian Auditory Pathway 15 of Springer Handbook of Auditory Research. Springer, New York, pp. 121 157.
72. Zacharek M.A. Kaltenbach J.A. Mathog T.A. Zhang J. ( 2002) Effects of cochlear ablation on noise induced hyperactivity in the hamster dorsal cochlear nucleus: implications for the origin of noise induced tinnitus. Hear. Res., 172, 137 144.
73. Zhang X. Heinz M.G. Bruce I.C. Carney L.H. ( 2001) A phenomenological model for the responses of auditory nerve fibers: I. Non-linear tuning with compression and suppression. J. Acoust. Soc. Am., 109, 648 670.
74. Zhou J. Shore S. ( 2004) Projections from the trigeminal nuclear complex to the cochlear nuclei: a retrograde and anterograde tracing study in the guinea pig. J. Neurosci. Res., 78, 901 907.