Evidence for tinnitus-related plasticity in the auditory and limbic system, demonstrated by arg3.1 and c-fos immunocytochemistry

Hearing Research

Volumn 195, Issue 1-2, 2004, Pages 17-34

  Mahlke, C ^a   Wallhausser Franke E ^a  

^a DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

AAF, anterior auditory field; AC, auditory cortex; AI, primary auditory field; AVCN, anterior part of the ventral cochlear nucleus; BLA, basolateral nucleus of the amygdala; CeA, central nucleus of the amygdala

Indexed keywords

ARGININE DERIVATIVE; SALICYLIC ACID; SODIUM CHLORIDE;

AMYGDALOID NUCLEUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUDITORY CORTEX; AUDITORY STIMULATION; AUDITORY SYSTEM; BODY WEIGHT; BRAIN; COMPARATIVE STUDY; CONTROLLED STUDY; DRUG ACCUMULATION; FEMALE; GERBIL; HEARING LOSS; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; INFERIOR COLLICULUS; LIMBIC SYSTEM; MALE; NONHUMAN; ONCOGENE C FOS; PLASTICITY; PRIORITY JOURNAL; PROTEIN DOMAIN; TINNITUS;

ACOUSTIC STIMULATION; AMYGDALA; ANIMALS; AUDITORY CORTEX; AUDITORY PATHWAYS; CELL COUNT; COCHLEAR NUCLEUS; CYTOSKELETAL PROTEINS; FEMALE; GERBILLINAE; IMMUNOHISTOCHEMISTRY; INFERIOR COLLICULUS; INJECTIONS; MALE; NERVE TISSUE PROTEINS; NEURONAL PLASTICITY; NEURONS; PROTO-ONCOGENE PROTEINS C-FOS; SALICYLATES; SODIUM CHLORIDE; TINNITUS;

EID: 4444369792     PISSN: 03785955     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.heares.2004.03.005     Document Type: Article

References (128)

1. Adams J.C. Sound stimulation induces Fos-related antigens in cells with common morphological properties throughout the auditory brainstem. J. Comp. Neurol. 361:1995;645-668
2. Adolphs R., Tranel D., Damasio H., Damasio A.R. Fear and the human amygdala. J. Neurosci. 15:1995;5879-5891
3. Ahissar E., Abeles M., Ahissar M., Haidarliu S., Vaadia E. Hebbian-like functional plasticity in the auditory cortex of the behaving monkey. Neuropharmacology. 37:1998;633-655
4. Andersson G., Lyttkens L., Hirvela C., Furmark T., Tillfors M., Fredrikson M. Regional cerebral blood flow during tinnitus: a PET case study with lidocaine and auditory stimulation. Acta Otolaryngol. 120:2000;967-972
5. Arnold W., Bartenstein P., Oestreicher E., Romer W., Schwaiger M. Focal metabolic activation in the predominant left auditory cortex in patients suffering from tinnitus: a PET study with [18F]deoxyglucose. J. Otorhinolaryngol. 58:1996;195-199
6. Baudry M. Synaptic plasticity and learning and memory: 15 years of progress. Neurobiol. Learn. Mem. 70:1998;113-118
7. Bauer C.A., Brozoski T.J., Rojas R., Boley J., Wyder M. Behavioral model of chronic tinnitus in rats. Otolaryngol. Head Neck Surg. 121(4):1999;457-462
8. Bjordahl T.S., Dimyan M.A., Weinberger N.M. Induction of long-term receptive field plasticity in the auditory cortex of the waking guinea pig by stimulation of the nucleus basalis. Behav. Neurosci. 112:1998;467-479
9. Brennan J.F., Jastreboff P.J. Generalization of conditioned suppression during salicylate-induced phantom auditory perception in rats. Acta Neurobiol. Exp. 51:1991;15-27
10. Brown M.C., Liu T.S. Fos-like immunoreactivity in central auditory neurons of the mouse. J. Comp. Neurol. 357:1995;85-97
11. 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. 22:2002;2383-2390
12. Budinger E., Heil P., Scheich H. Functional organization of auditory cortex in the Mongolian gerbil (Meriones unguiculatus). III. Anatomical subdivisions and corticocortical connections. Eur. J. Neurosci. 12:2000;2425-2451
13. Budinger E., Heil P., Scheich H. Functional organization of auditory cortex in the Mongolian gerbil (Meriones unguiculatus). IV. Connections with anatomically characterized subcortical structures. Eur. J. Neurosci. 12:2000;2452-2474
14. Budinger, E., Scheich, H., 2003. Medial prefrontal cortex of the gerbil: anatomical subdivisions, thalamic connections, and auditory cortical afferents. In: Elsner, N., Zimmermann, H. (Eds.), Proccedings of the 29th Göttingen Neurobiology Conference, Thieme, Stuttgart, No. 687
15. Bush G., Luu P., Posner M.I. Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn. Sci. 4:2000;215-222
16. Buss E., Hall J.W. III, Grose J.H., Hatch D.R. Perceptual consequences of peripheral hearing loss: do edge effects exist for abrupt cochlear lesions? Hear. Res. 125:1998;98-108
17. Cain M.E., Kapp B.S., Puryear C.B. The contribution of the amygdala to conditioned thalamic arousal. J. Neurosci. 22:2002;11026-11034
18. Calverley R.K., Jones D.G. Contributions of dendritic spines and perforated synapses to synaptic plasticity. Brain Res. Rev. 15:1990;215-249
19. Cardinal R.N., Parkinson J.A., Hall J., Everitt B.J. Emotion and motivation: the role of the amygdala. ventral striatum, and prefrontal cortex. Neurosci. Biobehav. Rev. 26:2002;321-352
20. Cazals Y. Auditory sensori-neural alterations induced by salicylate. Progr. Neurobiol. 62:2000;583-631
21. Chen G.D., Jastreboff P.J. Salicylate-induced abnormal activity in the inferior colliculus of rats. Hear. Res. 82:1995;158-178
22. Chicurel M.E., Harris K.M. Three-dimensional analysis of the structure and composition of CA3 branched dendritic spines and their synaptic relationships with mossy fiber boutons in the rat hippocampus. J. Comp. Neurol. 325:1992;169-182
23. Comery T.A., Shah R., Greenough W.T. Differential rearing alters spine density on medium-sized spiny neurons in the rat corpus striatum: evidence for association of morphological plasticity with early response gene expression. Neurobiol. Learn. Mem. 63:1995;217-219
24. Cox C.L., Metherate R., Ashe J.H. Modulation of cellular excitability in neocortex: muscarinic receptor and second messenger-mediated actions of acetylcholine. Synapse. 16:1994;123-136
25. Devinsky O., Morrell M.J., Vogt B.A. Contributions of anterior cingulate cortex to behaviour. Brain. 118:1995;279-306
26. Dietrich V., Nieschalk M., Stoll W., Rajan R., Pantev C. Cortical reorganization in patients with high frequency cochlear hearing loss. Hear. Res. 158:2001;95-101
27. Dragunow M., Faull R. The use of c-fos as a metabolic marker in neuronal pathway tracing. J. Neurosci. Methods. 29:1989;261-265
28. Eggermont J.J. Central tinnitus. Auris Nasus Larynx. 30(Suppl.):2003;7-12
29. Ehret G., Fischer R. Neuronal activity and tonotopy in the auditory system visualized by c-fos gene expression. Brain Res. 567:1991;350-354
30. Fleischmann A., Hvalby O., Jensen V., Strekalova T., Zacher C., Layer L.E., Kvello A., Reschke M., Spanagel R., Sprengel R., Wagner E.F., Gass P. Impaired long-term memory and NR2A-type NMDA receptor-dependent synaptic plasticity in mice lacking c-Fos in the CNS. J. Neurosci. 23:2003;9116-9122
31. Flor H., Elbert T., Knecht S., Wienbruch C., Pantev C., Birbaumer N., Larbig W., Taub E. Phantom-limb pain as a perceptual correlate of cortical reorganization following arm amputation. Nature. 375:1995;482-484
32. Forth, W., Henschler, D., Rummel, W., Starke, K., 1992. Allgemeine und spezielle Pharmakologie und Toxikologie, sixth ed. BI-Wiss-Verl., Mann-heim, pp. 217-219
33. Friauf E. Tonotopic order in the adult and developing auditory system of the rat as shown by c-fos immunocytochemistry. Eur. J. Neurosci. 4:1992;798-812
34. Fulwiler C.E., Saper C.B. Subnuclear organization of the efferent connections of the parabrachial nucleus in the rat. Brain Res. 319:1984;229-259
35. Gao E., Suga N. Experience-dependent plasticity in the auditory cortex and the inferior colliculus of bats: role of the corticofugal system. Poc. Natl. Acad. Sci. USA. 97:2000;8081-8086
36. Goldstein L.E., Rasmusson A.M., Bunney B.S., Roth R.H. Role of the amygdala in the coordination of behavioral neuroendocrine, and prefrontal cortical monoamine responses to psychological stress in the rat. J. Neurosci. 16:1996;4787-4798
37. Greenough W.T., Volkmar F.R. Pattern of dendritic branching in occipital cortex of rats reared in complex environments. Exp. Neurol. 40:1973;491-504
38. Greenough W.T., West R.W., DeVoogd T.J. Subsynaptic plate perforations: changes with age and experience in the rat. Science. 202:1978;1096-1098
39. Grimm R., Schicknick H., Riede I., Gundelfinger E.D., Herdegen T., Zuschratter W., Tischmeyer W. Suppression of c-fos induction in rat brain impairs retention of a brightness discrimination reaction. Learn. Mem. 3:1997;402-413
40. Gu Q. Neuromodulatory transmitter systems in the cortex and their role in cortical plasticity. Neuroscience. 111:2002;815-835
41. Guitton M.J., Caston J., Ruel J., Johnson R.M., Pujol R., Puel J.L. Salicylate induces tinnitus through activation of cochlear NMDA receptors. J. Neurosci. 23:2003;3944-3952
42. Guzowski J.F., Lyford G.L., Stevenson G.D., Houston F.P., McGaugh J.L., Worley P.F., Barnes C.A. Inhibition of activity-dependent arc protein expression in the rat hippocampus impairs the maintenance of long-term potentiation and the consolidation of long-term memory. J. Neurosci. 20:2000;3993-4001
43. Han J.S., Holland P.C., Gallagher M. Disconnection of the amygdala central nucleus and substantia innominata/nucleus basalis disrupts increments in conditioned stimulus processing in rats. Behav. Neurosci. 113:1999;143-151
44. Heller M.F., Bergman M. Tinnitus aurium in normally hearing persons. Ann. Otol. 62:1953;73-83
45. Herbert H., Aschoff A., Ostwald J. Topography of projections from the auditory cortex to the inferior colliculus in the rat. J. Comp. Neurol. 304:1991;103-122
46. Herbert H., Aschoff A., Ostwald J. Topography of projections from the auditory cortex to the inferior colliculus in the rat. J. Comp. Neurol. 304:1991;103-122
47. Hisanaga K., Sagar S.M., Sharp F.R. N-Methyl-D-aspartate antagonists block fos-like protein expression induced via multiple signaling pathways in cultured cortical neurons. J. Neurochem. 58:1992;1836-1844
48. Holland P.C., Gallagher M. Amygdala circuitry in attentional and representational processes. Trends Cogn. Sci. 1999;65-73
49. Holstege, J.C., Biesheuvel, K., Plath, N., Jaarsma, D., 2003. Arc induction in the spinal dorsal horn after peripheral nociceptive stimulation. In: Society for Neuroscience, 33rd Annual Meeting, New Orleans, LA, p. 13.9
50. Hunt S.P., Pini A., Evan G. Induction of c-fos-like protein in spinal cord neurons following sensory stimulation. Nature. 328:1987;632-634
51. Irvine D.R., Rajan R., McDermott H.J. Injury-induced reorganization in adult auditory cortex and its perceptual consequences. Hear. Res. 147:2000;188-199
52. Jastreboff P.J., Brennan J.F., Coleman J.K., Sasaki C.T. Phantom auditory sensation in rats: an animal model for tinnitus. Behav. Neurosci. 102:1988;811-822
53. Jastreboff P.J., Brennan J.F. Evaluating the loudness of phantom auditory perception (tinnitus) in rats. Audiology. 33:1994;202-217
54. Jastreboff, P.J., 1999. The neurophysiological model of tinnitus and hyperacusis. In: Hazell, J. (Ed.), Proceedings of the 6th International Tinnitus Seminar, Cambridge, pp. 32-38
55. Jastreboff P.J., Jastreboff M.M. Tinnitus retraining therapy for patients with tinnitus and decreased sound tolerance. Otolaryngol. Clin. N. Am. 36:2003;321
56. Jolkkonen E., Pitkänen A. Intrinsic connections of the rat amygdaloid complex: projections originating in the central nucleus. J. Comp. Neurol. 395:1998;53-72
57. Jolkkonen E., Miettinen R., Pikkarainen M., Pitkänen A. Projections from the amygdaloid complex to the magnocellular cholinergic basal forebrain in rat. Neuroscience. 111:2002;133-149
58. Kaltenbach J.A., Afman C.E. Hyperactivity in the dorsal cochlear nucleus after intense sound exposure and its resemblance to tone-evoked activity: a physiological model for tinnitus. Hear. Res. 140:2000;165-172
59. Kapp B.S., Whalen P.J., Supple W.F., Pascoe J.P. Amygdaloid contributions to conditioned arousal and sensory information processing. Aggleton J.P. The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction. 1992;229-254 Wiley-Liss., New York
60. Kapp B.S., Supple W.F. Jr., Whalen P.J. Effects of electrical stimulation of the amygdaloid central nucleus on neocortical arousal in the rabbit. Behav. Neurosci. 108:1994;81-93
61. Kilgard M.P., Merzenich M.M. Cortical map reorganization enabled by nucleus basalis activity. Science. 279:1998;1714-1718
62. Kleim J.A., Lussnig E., Schwarz E.R., Comery T.A., Greenough W.T. Synaptogenesis and Fos expression in the motor cortex of the adult rat after motor skill learning. J. Neurosci. 16:1996;4529-4535
63. Knecht S., Henningsen H., Elbert T., Flor H., Hohling C., Pantev C., Taub E. Reorganizational and perceptional changes after amputation. Brain. 119:1996;1213-1219
64. Kotak, V.C., Ter-Mikaelian, M., Lee, F.A., Sanes, D.H., 2003. Deaffening alters the balance between excitation and inhibition in the auditory cortex. In: Society for Neuroscience, 33rd Annual Meeting, New Orleans, LA, p. 181.2
65. Kuhl D. Learning about activity-dependent genes. Baudry M., Davis J.L., Thompson R.F. Advances in Synaptic Plasticity. 2000;1-31 MIT Press, Cambridge, MA
66. Lanahan A., Worley P. Immediate-early genes and synaptic function. Neurobiol. Learn. Mem. 70:1998;37-43
67. Langner, G., Braun, S., 1999. Orthogonal representation of periodicity pitch and frequency in the inferior colliculus of gerbil demonstrated by 2-deoxyglucose labeling. In: Proccedings of the 27th Göttingen Neurobiology Conference, No. 315
68. Langner, G., Wallh, E., 1999. Computer simulation of a tinnitus model based on labeling of tinnitus activity in the auditory cortex. In: Hazell, J. (Ed.), Proceedings of the 6th International Tinnitus Seminar, Cambridge, pp. 20-25
69. LeDoux J.E. Emotion memory and the brain. Sci. Am. 270(6):1994;32-39
70. LeDoux J. The emotional brain, fear, and the amygdala. Cell. Mol. Neurobiol. 3:2003;727-738
71. Link W., Konietzko U., Kauselmann G., Krug M., Schwanke B., Frey U., Kuhl D. Somatodendritic expression of an immediate early gene is regulated by synaptic activity. Proc. Natl. Acad. Sci. USA. 92:1995;5734-5738
72. 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. 50:1998;114-120
73. Long G.R., Tubis A. Modification of spontaneous and evoked otoacoustic emissions and associated psychoacoustic microstructure by aspirin consumption. J. Acoust. Soc. Am. 84:1988;1343-1353
74. Lyford G.L., Yamagata K., Kaufmann W.E., Barnes C.A., Sanders L.K., Copeland N.G., Gilbert D.J., Jenkins N.A., Lanahan A.A., Worley P.F. Arc a growth factor and activity-regulated gene, encodes a novel cytoskeleton- associated protein that is enriched in neuronal dendrites. Neuron. 14:1995;433-445
75. Ma X., Suga N. Augmentation of plasticity of the central auditory system by the basal forebrain and/or somatosensory cortex. J. Neurophysiol. 89(1):2003;90-103
76. Mirz F., Pedersen B., Ishizu K., Johannsen P., Ovesen T., Stodkilde-Jorgensen H., Gjedde A. Positron emission tomography of cortical centers of tinnitus. Hear. Res. 134:1999;133-144
77. McDonald A.J. Cortical pathways to the mammalian amygdala. Progr. Neurobiol. 55:1998;257-332
78. McFadden D., Plattsmier H.S. Aspirin abolishes spontaneous oto-acoustic emissions. J. Acoust. Soc. Am. 76:1984;443-448
79. McGaugh J.L., McIntyre C.K., Power A.E. Amygdala modulation of memory consolidation: interaction with other brain systems. Neurobiol. Learn. Mem. 78:2002;539-552
80. Metherate R., Ashe J.H. Basal forebrain stimulation modifies auditory cortex responsiveness by an action at muscarinic receptors. Brain Res. 559:1991;163-167
81. Møller A.R. Pathophysiology of tinnitus. Otolaryngol. Clin. N. Am. 36:2003;249
82. Montag-Sallaz M., Welzl H., Kuhl D., Montag D., Schachner M. Novelty-induced increased expression of immediate-early genes c-fos and arg 3.1 in the mouse brain. J. Neurobiol. 38:1999;234-246
83. Morgan M.A., Romanski L.M., LeDoux J.E. Extinction of emotional learning: contribution of medial prefrontal cortex. Neurosci. Lett. 163:1993;109-113
84. Müller M., Klinke R., Arnold W., Oestreicher E. Auditory nerve fibre responses to salicylate revisited. Hear. Res. 183:2003;37-43
85. Mühlnickel W., Elbert T., Taub E., Flor H. Reorganization of auditory cortex in tinnitus. Proc. Natl. Acad. Sci. USA. 95:1998;10340-10343
86. Oliver D., He D.Z., Klocker N., Ludwig J., Schulte U., Waldegger S., Ruppersberg J.P., Dallos P., Fakler B. Intracellular anions as the voltage sensor of prestin the outer hair cell motor protein. Science. 292:2001;2340-2343
87. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates. 1986;Academic Press, New York
88. Pinaud R., Penner M.R., Robertson H.A., Currie R.W. Upregulation of the immediate early gene arc in the brains of rats exposed to environmental enrichment: implications for molecular plasticity. Brain Res. Mol. Brain Res. 91:2001;50-56
89. Pitkänen A., Savander V., LeDoux J.E. Organization of intra-amygdaloid circuitries in the rat: an emerging framework for understanding functions of the amygdala. Trends Neurosci. 20:1997;517-523
90. Platenik J., Kuramoto N., Yoneda Y. Molecular mechanisms associated with long-term consolidation of the NMDA signals. Life Sci. 67:2000;335-364
91. Posner M.I., Rothbart M.K. Attention, self-regulation and consciousness. Philos. Trans. R. Soc. Lond B. Biol. Sci. 353:1998;1915-1927
92. Quirk G.J., Armony J.L., LeDoux J.E. Fear conditioning enhances different temporal components of tone-evoked spike trains in auditory cortex and lateral amygdala. Neuron. 19:1997;613-624
93. Rajan R., Irvine D.R. Neuronal responses across cortical field A1 in plasticity induced by peripheral auditory organ damage. Audiol. Neurootol. 3:1998;123-144
94. Rajan R. Receptor organ damage causes loss of cortical surround inhibition without topographic map plasticity. Nat. Neurosci. 1:1998;138-143
95. Reimer K. Simultaneous demonstration of fos-like immunoreactivity and 2-deoxy-glucose uptake in the inferior colliculus of the mouse. Brain Res. 616:1993;339-343
96. Rial Verde, E.M., Worley, P., Malinow, R., Cline, H.T, 2003 The immediate-early gene arc regulates ampa-receptor trafficking. In: Society for Neuroscience, 33rd Annual Meeting, New Orleans, LA, No. 55.7
97. Roozendaal B., Koolhaas J.M., Bohus B. The role of the central amygdala in stress and adaption. Acta Physiol. Scand. Suppl. 640:1997;51-54
98. Rüttiger L., Ciuffani J., Zenner H.P., Knipper M. A behavioral paradigm to judge acute sodium salicylate-induced sound experience in rats: a new approach for an animal model on tinnitus. Hear. Res. 180:2003;39-50
99. Sagar S.M., Sharp F.R., Curran T. Expression of c-fos protein in brain: metabolic mapping at the cellular level. Science. 240:1988;1328-1331
100. Sah P., Faber E.S., Lopez D.A., Power J. The amygdaloid complex: anatomy and physiology. Physiol. Rev. 83:2003;803-834
101. Scheich H., Heil P., Langner G. Functional organization of auditory cortex in the mongolian gerbil (Meriones unguiculatus). II. Tonotopic 2-deoxyglucose. Eur. J. Neurosci. 5:1993;898-914
102. Sharp F.R., Hisanaga K., Sagar S.M. NMDA receptor blockade prevents translation, but not transcription, of the c-fos gene following stimulation with multiple extracellular signals in cultured cortical neurons: implications for plasticity and molecular memory. NIDA Res. Monogr. 125:1993;172-180
103. Sheng M., Greenberg M.E. The regulation and function of c-fos and other immediate early genes in the nervous system. Neuron. 4:1990;477-485
104. Shulz D.E., Cohen S., Haidarliu S., Ahissar E. Differential effects of acetylcholine on neuronal activity and interactions in the auditory cortex of the guinea-pig. Eur. J. Neurosci. 9:1997;396-409
105. Steward O., Falk P.M., Torre E.R. Ultrastructural basis for gene expression at the synapse: synapse-associated polyribosome complexes. J. Neurocytol. 25:1996;717-734
106. Steward O., Worley P.F. Selective targeting of newly synthesized Arc mRNA to active synapses requires NMDA receptor activation. Neuron. 30:2001;227-240
107. Steward O., Worley P.F. A cellular mechanism for targeting newly synthesized mRNAs to synaptic sites on dendrites. Proc. Natl. Acad. Sci. USA. 98:2001;7062-7068
108. Steward O., Worley P. Local synthesis of proteins at synaptic sites on dendrites: role in synaptic plasticity and memory consolidation? Neurobiol. Learn. Mem. 78:2002;508-527
109. Stork O., Welzl H. Memory formation and the regulation of gene expression. Cell. Mol. Life Sci. 55:1999;575-592
110. Syka J. Plastic changes in the central auditory system after hearing loss, restoration of function, and during learning. Physiol. Rev. 82:2002;601-636
111. Thomas H., Tillein J., Heil P., Scheich H. Functional organization of auditory cortex in the mongolian gerbil (Meriones unguiculatus). I. Electrophysiological mapping of frequency representation and distinction of fields. Eur. J. Neurosci. 5:1993;882-897
112. Tiedge H., Brosius J. Translational machinery in dendrites of hippocampal neurons in culture. J. Neurosci. 16:1996;7171-7181
113. Tischmeyer W., Grimm R. Activation of immediate early genes and memory formation. Cell. Mol. Life Sci. 55:1999;564-574
114. Touma J.B. Controversies in noise-induced hearing loss (NIHL). Ann. Occup. Hyg. 36:1992;199-209
115. Wallhäusser-Franke E., Braun S., Langner G. Salicylate alters 2-DG uptake in the auditory system: a model for tinnitus? NeuroReport. 7:1996;1585-1588
116. Wallhäusser-Franke E. Salicylate evokes c-fos expression in the brain stem: implications for tinnitus. NeuroReport. 8:1997;725-728
117. Wallhäusser-Franke E., Langner G. Phantom sounds: mechanisms of tinnitus in the central nervous system. NeuroReport. 1/01:2001;21-27
118. Wallhäusser-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. 153:2003;649-654
119. Weinberger N.M., Bakin J.S. Research on auditory cortex plasticity. Science. 280:1998;1174
120. Weinberger N.M. The nucleus basalis and memory codes: auditory cortical plasticity and the induction of specific, associative behavioral memory. Neurobiol. Learn. Mem. 80:2003;268-284
121. Woodson W., Farb C.R., LeDoux J.E. Afferents from the auditory thalamus synapse on inhibitory interneurons in the lateral nucleus of the amygdala. Synapse. 38:2000;124-137
122. Worley P.F., Cole A.J., Murphy T.H., Christy B.A., Nakabeppu Y., Baraban J.M. Synaptic regulation of immediate-early genes in brain. Cold Spring Harb. Symp. Quant. Biol. 55:1990;213-223
123. 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. 176:2003;80-93
124. 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. 250:1998;197-200
125. Zhang J.S., Kaltenbach J.A., Wang J., Kim S.A. Fos-like immunoreactivity in auditory and nonauditory brain structures of hamsters previously exposed to intense sound. Exp. Brain Res. 153:2003;655-660
126. Zhang P.C., Keleshian A.M., Sachs F. Voltage-induced membrane movement. Nature. 413:2001;428-432
127. Zheng J., Shen W., He D.Z., Long K.B., Madison L.D., Dallos P. Prestin is the motor protein of cochlear outer hair cells. Nature. 405:2000;149-155
128. Zuschratter W., Gass P., Herdegen T., Scheich H. Comparison of frequency-specific c-Fos expression and fluoro-2- deoxyglucose uptake in auditory cortex of gerbils (Meriones unguiculatus). Eur. J. Neurosci. 7:1995;1614-1626