Origin of hyperactivity in the hamster dorsal cochlear nucleus following intense sound exposure

Journal of Neuroscience Research

Volumn 84, Issue 4, 2006, Pages 819-831

  Zhang, J S ^a   Kaltenbach, J A ^a   Godfrey, D A ^b   Wang, J ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MEDICAL COLLEGE OF OHIO   (United States)

Author keywords

Auditory; Descending pathways; Plasticity; Spontaneous activity; Tinnitus

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN STEM; COCHLEAR NERVE; COCHLEAR NUCLEUS; HISTOLOGY; HYPERACTIVITY; MALE; NERVE CELL PLASTICITY; NERVE FIBER TRANSECTION; NONHUMAN; PRIORITY JOURNAL; SOUND INTENSITY;

ACOUSTIC STIMULATION; ANALYSIS OF VARIANCE; ANIMALS; AUDITORY PATHWAYS; BRAIN MAPPING; COCHLEAR NUCLEUS; CRICETINAE; ELECTROPHYSIOLOGY; EVOKED POTENTIALS, AUDITORY, BRAIN STEM; FUNCTIONAL LATERALITY; MALE; MESOCRICETUS; SOUND;

EID: 33748538400     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.20985     Document Type: Article

References (90)

1. Adams JC. 1983. Cytology of periolivary cells and the organization of their projections in cat. J Comp Neurol 215:275-289.
2. Adams JC, Warr WB. 1976. Origins of axons in the cat's acoustic striae determined by injection of horseradish peroxidase into severed tracts. J Comp Neurol 170:107-121.
3. Alibardi L. 2000. Cytology, synaptology and immunocytochemistry of commissural neurons and their putative axonal terminals in the dorsal cochlear nucleus of the rat. Ann Anat 182:207-220.
4. Arnott RH, Wallace MN, Shackleton TM, Palmer AR. 2004. Onset neurones in the anteroventral cochlear nucleus project to the dorsal cochlear nucleus. J Assoc Res Otolaryngol 5:153-170.
5. Benson CG, Gross JS, Suneja SK, Potashner SJ. 1997. Synaptophysin immunoreactivity in the cochlear nucleus after unilateral cochlear or os-sicular removal. Synapse 25:243-257.
6. Bilak MM, Bilak SR, Morest DK. 1996. Differential expression of N-methyl-D-aspartate receptor in the cochlear nucleus of the mouse. Neuroscience 75:1075-1097.
7. Bilak M, Kim J, Potashner SJ, Bohne BA, Morest DK. 1997. New growth of axons in the cochlear nucleus of adult chinchillas after acoustic trauma. Exp Neurol 147:256-268.
8. Brown MC, Liberman MC, Benson TE, Ryugo DK. 1988. Brainstem branches from olivocochlear axons in cats and rodents. J Comp Neurol 278:591-603.
9. Brozoski TJ, Bauer CA, Caspary DM. 2002. Elevated fusiform cell activity in the dorsal cochlear nucleus of chinchillas with psychophysical evidence of tinnitus. J Neurosci 22:2383-2390.
10. Cacace AT, Cousins JP, Parnes SM, Semenoff D, Holmes T, McFarland DJ, Davenport C, Stegbauer K, Lovely TJ. 1999. Cutaneous-evoked tinnitus. I. Phenomenology, psychophysics and functional imaging. Audiol Neurootol 4:247-257.
11. Caicedo A, Herbert H. 1993. Topography of descending projections from the inferior colliculus to auditory brainstem nuclei in the rat. J Comp Neurol 328:377-392.
12. Cant NB, Gaston KC. 1982. Pathways connecting the right and left cochlear nuclei. J Comp Neurol 212:313-326.
13. Chang H, Chen K, Kaltenbach JA, Zhang JS, Godfrey DA. 2002. Effects of acoustic trauma on dorsal cochlear nucleus neuron activity in slices. Hear Res 164:59-68.
14. Chen K, Waller HJ, Godfrey DA. 1998. Effects of endogenous acetylcholine on spontaneous activity in rat dorsal cochlear nucleus slices. Brain Res 783:219-226.
15. Chouard CH, Meyer B, Mandat D. 1981. Transcutaneous electrotherapy for severe tinnitus. Acta Otolaryngol 91:415-422.
16. Conlee JW and Kane ES. 1982. Descending projections from the inferior colliculus to the dorsal cochlear nucleus in the cat: an autoradiographic study. Neuroscience 7:161-178.
17. Doucet JR, Ryugo DK. 1997. Projections from the ventral cochlear nucleus to the dorsal cochlear nucleus in rats. J Comp Neurol 385:245-264.
18. Ebert U. 1996. Noradrenalin enhances the activity of cochlear nucleus neurons in the rat. Eur J Neurosci 8:1306-1314.
19. Evans EF, Nelson PG. 1973. On the functional relationship between the dorsal and ventral divisions of the cochlear nucleus of the cat. Exp Brain Res 17:428-442.
20. Faye-Lund H. 1988. Inferior colliculus and related descending pathways in rat. Upsala J Med Sci 93:1-17.
21. Francis HW, Manis PB. 2000. Effects of deafferentation on the electrophysiology of ventral cochlear nucleus neurons. Hear Res 149:91-105.
22. Gacek RR. 1973. A cerebellocochlear nucleus pathway in the cat. Exp Neurol 41:101-112.
23. Godfrey DA, Park-Hellendall JL, Dunn JD, Ross CD. 1987a. Effects of trapezoid body and superior olive lesions on choline acetyltransferase activity in the rat cochlear nucleus. Hear Res 28:253-270.
24. Godfrey DA, Park-Hellendall JL, Dunn JD, Ross CD. 1987b. Effect of olivocochlear bundle transection on choline acetyltransferase activity in the rat cochlear nucleus. Hear Res 28:237-251.
25. Gonzalez-Lima F, Scheich H. 1984. Functional activation in the auditory system of the rat produced by arousing reticular stimulation: a 2-deoxyglucose study. Brain Res 299:201-214.
26. Heffner HE, Harrington IA. 2002. Tinnitus in hamsters following exposure to intense sound. Hear Res 170:83-95.
27. Imig TJ, Durham D. 2005. 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 490:391-413.
28. Ito J, Sakakihara J. 1994. Tinnitus suppression by electrical stimulation of the cochlear wall and by cochlear implantation. Laryngoscope 104:752-754.
29. Itoh K, Kamiya H, Mitani A, Yasui Y, Takada M, Mizuno N. 1987. Direct projections from the dorsal column nuclei and the spinal trigeminal nuclei to the cochlear nuclei in the cat. Brain Res 400:145-150.
30. Jin YM, Godfrey DA, Wang J, Kaltenbach JA. 2006. Effects of intense tone exposure on choline acetyltransferase activity in the hamster cochlear nucleus. Hear Res [E-pub ahead of print].
31. Kaltenbach JA, McCaslin DL. 1996. Increases in spontaneous activity in the dorsal cochlear nucleus following exposure to high intensity sound: a possible neural correlate of tinnitus. Audit Neurosci 3:57-78.
32. Kaltenbach JA, Zhang JS. 2006. Intense sound induced plasticity in the dorsal cochlear nucleus of rats: evidence for cholinergic receptor up-regulation. Hear Res (in press).
33. Kaltenbach JA, Zacharek MA, Zhang JS, Frederick S. 2004. Recordings of activity in the dorsal cochlear nucleus of hamsters previously tested for tinnitus following intense sound exposure. Neurosci Lett 355:121-125.
34. Kaltenbach JA, Zhang JS, Finlayson P. 2005. Tinnitus as a plastic phenomenon and its possible neural underpinnings in the dorsal cochlear nucleus. Hear Res 206:200-226.
35. Kane ES. 1977 Descending inputs to the cat dorsal cochlear nucleus: an electron microscopic study. J Neurocytol 6:583-605.
36. Kim DS, Choi JO, Rim HD, Cho HJ. 2002. Down-regulation of voltage-gated potassium channel alpha gene expression in dorsal root ganglia following chronic constriction injury of the rat sciatic nerve. Brain Res Mol Brain Res 105:146-152.
37. Kim JJ, Gross J, Morest DK, Potashner SJ. 2004a. Quantitative study of degeneration and new growth of axons and synaptic endings in the chinchilla cochlear nucleus after acoustic overstimulation. J Neurosci Res 77:829-842.
38. Kim JJ, Gross J, Potashner SJ, Morest DK. 2004b. Fine structure of long-term changes in the cochlear nucleus after acoustic overstimulation: chronic degeneration and new growth of synaptic endings. J Neurosci Res 77:817-828.
39. Koerber KC, Pfeiffer RR, Warr WB, Kiang NYS. 1966. Spontaneous spike discharges from single units in the cochlear nucleus after destruction of the cochlea. Exp Neurol 16:119-130.
40. Komiya H, Eggermont JJ. 2000. Spontaneous firing activity of cortical neurons in adult cats with reorganized tonotopic map following puretone trauma. Acta Otolaryngol 6:750-756.
41. Kromer LF, Moore RY. 1980. Norepinephrine innervation of the cochlear nuclei by locus coeruleus neurons in the rat. Anat Embryol 158:227-244.
42. Levine RA, Abel M, Cheng H. 2003. CNS somatosensory-auditory interactions elicit or modulate tinnitus. Exp Brain Res 153:643-648.
43. Lenhardt ML, Goldstein BA, Shulman A, Guinta R. 2003. Use of high-frequency and muscle vibration in the treatment of tinnitus. Int Tinnitus J 9:32-36.
44. Li H, Mizuno N. 1997. 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 29:135-142.
45. Mahlke C, Wallhausser-Franke E. 2004. Evidence for tinnitus-related plasticity in the auditory and limbic system, demonstrated by arg3.1 and c-fos immunocytochemistry. Hear Res 195:17-34.
46. Manis PB. 1990. Membrane properties and discharge characteristics of guinea pig dorsal cochlear nucleus neurons studied in vitro. J Neurosci 10:2338-2351.
47. Manis PB, Spirou GA, Wright DD, Paydar S, Ryugo DK. 1994. Physiology and morphology of complex spiking neurons in the guinea pig dorsal cochlear nucleus. J Comp Neurol 348:261-276.
48. Morest DK, Kim J, Bohne BA. 1997. Neuronal and transneuronal degeneration of auditory axons in the brainstem after cochlear lesions in the chinchilla: cochleotopic and non-cochleotopic patterns. Hear Res 103:151-168.
49. Muly SM, Gross JS, Morest DK, Potashner SJ. 2002. Synaptophysin in the cochlear nucleus following acoustic trauma. Exp Neurol 177:202-221.
50. 3H]aspartate release and AMPA binding in chinchilla cochlear nucleus. J Neurosci Res 75:585-596.
51. Oertel D, Wu SH, Garb MW, Dizack C. 1990. Morphology and physiology of cells in slice preparations of the posteroventral cochlear nucleus of mice. J Comp Neurol 295:136-154.
52. Osen KK, Mugnaini E, Dahl AL, Christiansen AH. 1984. Histochemical localization of acetylcholinesterase in the cochlear and superior olivary nuclei. A reappraisal with emphasis on the cochlear granule cell system. Arch Ital Biol 122:169-212.
53. Ostapoff EM, Benson CG, Saint Marie RL. 1997. GABA- and glycine-immunoreactive projections from the superior olivary complex to the cochlear nucleus in guinea pig. J Comp Neurol 381:500-512.
54. Parham K, Kim DO. 1995. Spontaneous and sound-evoked discharge characteristics of complex-spiking neurons in the dorsal cochlear nucleus of the unanesthetized decerebrate cat. J Neurophysiol 73:550-561.
55. Petralia RS, Wang YX, Zhao HM, Wenthold RJ. 1996. Ionotropic and metabotropic glutamate receptors show unique postsynaptic, presynaptic, and glial localizations in the dorsal cochlear nucleus. J Comp Neurol 372:356-383.
56. Petralia RS, Rubio ME, Wang YX, Wenthold RJ. 2000. Differential distribution of glutamate receptors in the cochlear nuclei. Hear Res 147:59-69.
57. Potashner SJ, Suneja SK, Benson CG. 1997. Regulation of D-aspartate release and uptake in adult brain stem auditory nuclei after unilateral middle ear ossicle removal and cochlear ablation. Exp Neurol 148:222-235.
58. Rasmussen GL. 1960. Efferent fibers of the cochlear nerve and cochlear nucleus. In: Rasmussen GL, Windle EF, editors. Neural mechanisms of the auditory and vesribular systems. Springfield, IL: Thomas, p 105-115.
59. Rasmussen GL. 1967. Efferent connections of the cochlear nucleus. In: Graham AB, editor. Sensorineural hearing processes and disorders. Boston: Little, Brown and Co. p 61-75.
60. Rossi G, Cortesina G, Robecchi MG. 1967. Cerebellifugal fibres to the cochlear nuclei and superior olivary complex. Acta Otolaryngol 63:166-171.
61. Rubinstein JT, Tyler RS, Johnson A, Brown CT. 2003. Electrical suppression of tinnitus with high-rate pulse trains. Oto Neurotol 24:478-485.
62. Ruckenstein MJ, Hedgepeth C, Rafter KO, Montes ML, Bigelow DC. 2001. Tinnitus suppression in patients with cochlear implants. Otol Neurotol 22:200-204.
63. Sato K, Shiraishi S, Nakagawa H, Kuriyama H, Altschuler RA. 2000. Diversity and plasticity in amino acid receptor subunits in the rat auditory brain stem. Hear Res 147:137-144.
64. Schaette R, Gollisch T, Herz AV. 2005. Spike-train variability of auditory neurons in vivo: dynamic responses follow predictions from constant stimuli. J Neurophysiol 93:3270-3281.
65. 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.
66. Sherriff FE, Henderson Z. 1994. Cholinergic neurons in the ventral trapezoid nucleus project to the cochlear nuclei in the rat. Neuroscience 58:627-633.
67. Shofner WP, Young ED. 1987. Inhibitory connections between AVCN and DCN: evidence from lidocaine injection in AVCN. Hear Res 29:45-53.
68. Shore SE. 2005. Multisensory integration in the dorsal cochlear nucleus: unit responses to acoustic and trigeminal ganglion stimulation. Eur J Neurosci 21:3334-3348.
69. Shore SE, Helfert RH, Bledsoe SC Jr, Altschuler RA, Godfrey DA. 1991. Descending projections to the dorsal and ventral divisions of the cochlear nucleus in guinea pig. Hear Res 52:255-268.
70. Shore SE, Godfrey DA, Helfert RH, Altschuler RA, Bledsoe SC Jr. 1992. Connections between the cochlear nuclei in guinea pig. Hear Res 62:16-26.
71. Snyder RL, Leake PA. 1988. Intrinsic connections within and between cochlear nucleus subdivisions in cat. J Comp Neurol 278:209-225.
72. Starr A, Wernick JS. 1968. Olivocochlear bundle: effects on spontaneous and tone-evoked activities of single units in cat cochlear nucleus. J Neurophysiol 31:549-564.
73. Suneja SK, Potashner SJ. 2002. TrkB levels in the cochlear nucleus after unilateral cochlear ablation: correlations with postlesion plasticity. Brain Res 957:366-368.
74. Suneja SK, Potashner SJ, Benson CG. 1998. 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.
75. Thompson AM, Thompson GC. 2001. Serotonin projection patterns to the cochlear nucleus. Brain Res 907:195-207.
76. Tyler RS. 1995. Tinnitus in the profoundly hearing-impaired and the effects of cochlear implants. Ann Otol Rhinol Laryngol Suppl 165:25-30.
77. Vernon JA, Fenwick JA. 1985. Attempts to suppress tinnitus with transcutaneous electrical stimulation. Otolaryngol Head Neck Surg 93:385-389.
78. Waller HJ, Godfrey DA. 1994. Functional characteristics of spontaneously active neurons in rat dorsal cochlear nucleus in vitro. J Neurophysiol 71:467-478.
79. Waller HJ, Godfrey DA, Chen K. 1996. Effects of parallel fiber stimulation on neurons of rat dorsal cochlear nucleus. Hear Res 98:169-179.
80. Wallhausser-Franke E, Mahlke C, Oliva R, Braun S, Wenz G, Langner G. 2003. Expression of c-fos in auditory and non-auditory brain regions of the gerbil after manipulations that induce tinnitus. Exp Brain Res 153:649-654.
81. Weedman DL, Ryugo DK. 1996. Projections from auditory cortex to the cochlear nucleus in rats: synapses on granule cell dendrites. J Comp Neurol 371:311-324.
82. Weinberg RJ, Rustioni A. 1987. A cuneocochlear pathway in the rat. Neuroscience 20:209-219.
83. Wenthold RJ. 1987. Evidence for a glycinergic pathway connecting the two cochlear nuclei: an immunocytochemical and retrograde transport study. Brain Res 415:183-187.
84. Wright DD, Ryugo DK. 1996. Mossy fiber projections from the cuneate nucleus to the dorsal cochlear nucleus. J Comp Neurol 365:159-172.
85. Ye Y, Kim DO. 2001. Connections between the dorsal raphe nucleus and a hindbrain region consisting of the cochlear nucleus and neighboring structures. Acta Otolaryngol 121:284-288.
86. Zacharek MA, Kaltenbach JA, Mathog TA, Zhang JS. 2002. Effects of cochlear ablation on noise induced hyperactivity in the hamster dorsal cochlear nucleus: implications on the origin of noise-induced tinnitus. Hear Res 172:137-144.
87. Zhang JS, Kaltenbach JA. 1998. Increases in spontaneous activity in the dorsal cochlear nucleus of the rat following to high intensity sound. Neurosci Lett 250:197-200.
88. Zhang JS, Kaltenbach JA, Wang J, Kim SA. 2003. Fos-like immunoreactivity in auditory and nonauditory brain structures of hamsters previously exposed to intense sound. Exp Brain Res 153:655-660.
89. Zhang S, Oertel D. 1993. Cartwheel and superficial stellate cells of the dorsal cochlear nucleus of mice: intracellular recordings in slices. J Neurophysiol 69:1384-1397.
90. 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.