Choline acetyltransferase activity in the hamster central auditory system and long-term effects of intense tone exposure

Journal of Neuroscience Research

Volumn 91, Issue 7, 2013, Pages 987-996

  Godfrey, Donald A ^a   Kaltenbach, James A ^b   Chen, Kejian ^c   Ilyas, Omer ^a  

^a MEDICAL COLLEGE OF OHIO   (United States)

^b LERNER RESEARCH INSTITUTE   (United States)

^c NAVAL MEDICAL CENTER SAN DIEGO   (United States)

Author keywords

Acetylcholine; Cochlear nucleus; Granular regions; Olivocochlear bundle; Tinnitus

Indexed keywords

ACETYLCHOLINE; CHOLINE ACETYLTRANSFERASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUDITORY NERVOUS SYSTEM; COCHLEAR NUCLEUS; CONTROLLED STUDY; ENZYME ACTIVITY; EXPOSURE; EXTERNAL CAPSULE; FACIAL NERVE; FACIAL NERVE NUCLEUS; HAMSTER; HEARING; IMMUNORADIOMETRIC ASSAY; INFERIOR COLLICULUS; INTENSE TONE EXPOSURE; MALE; MICRODISSECTION; NERVE FIBER; NERVE ROOT; NONHUMAN; PERIAQUEDUCTAL GRAY MATTER; PRIORITY JOURNAL; SUPERIOR OLIVARY NUCLEUS; UPREGULATION;

ACOUSTIC STIMULATION; ANIMALS; AUDITORY CORTEX; AUDITORY PATHWAYS; AUDITORY PERCEPTION; BRAIN; CHOLINE O-ACETYLTRANSFERASE; COCHLEAR NUCLEUS; CRICETINAE; MALE; MESOCRICETUS; PSYCHOACOUSTICS; SOUND; TIME;

EID: 84877924862     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.23227     Document Type: Article

References (76)

1. Abbott SD, Hughes LF, Bauer CA, Salvi R, Caspary DM. 1999. Detection of glutamate decarboxylase isoforms in rat inferior colliculus following acoustic exposure. Neuroscience 93:1375-1381.
2. Adams JC, Wenthold RJ. 1979. Distribution of putative amino acid transmitters, choline acetyltransferase and glutamate decarboxylase in the inferior colliculus. Neuroscience 4:1947-1951.
3. Benson TE, Brown MC. 2004. Postsynaptic targets of type II auditory nerve fibers in the cochlear nucleus. J Assoc Res Otolaryngol 5:111-125.
4. 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.
5. Brown MC. 1993. Anatomical and physiological studies of type I and type II spiral ganglion neurons. In: Merchan MA, Juiz JM, Godfrey DA, Mugnaini E, editors. The mammalian cochlear nuclei: organization and function. New York: Plenum Press. p 43-54.
6. Brown MC, Liberman MC, Benson TE, Ryugo DK. 1988. Brainstem branches from olivocochlear axons in cats and rodents. J Comp Neurol 278:591-603.
7. 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.
8. Chang H, Chen K, Kaltenbach JA, Zhang J, Godfrey DA. 2002. Effects of acoustic trauma on dorsal cochlear nucleus neuron activity in slices. Hear Res 164:59-68.
9. Chen K, Waller HJ, Godfrey TG, Godfrey DA. 1999. Glutamatergic transmission of neuronal responses to carbachol in rat dorsal cochlear nucleus slices. Neuroscience 90:1043-1049.
10. Collinge C, Schweitzer L. 1991. Details of the central projections of the cochlear nerve in the hamster revealed by the fluorescent tracer DiI. Hear Res 53:159-172.
11. Contreras NEIR, Bachelard HS. 1979. Some neurochemical studies on auditory regions of mouse brain. Exp Brain Res 36:573-584.
12. Dehmel S, Pradhan S, Koehler S, Bledsoe S, Shore S. 2012. Noise overexposure alters long-term somatosensory-auditory processing in the dorsal cochlear nucleus-possible basis for tinnitus-related hyperactivity? J Neurosci 32:1660-1671.
13. Dong S, Mulders WH, Rodger J, Woo S, Robertson D. 2010. Acoustic trauma evokes hyperactivity and changes in gene expression in guinea-pig auditory brainstem. Eur J Neurosci 31:1616-1628.
14. Du X, Chen K, Choi C-H, Li W, Cheng W, Stewart C, Hu N, Floyd RA, Kopke RD. 2012. Selective degeneration of synapses in the dorsal cochlear nucleus of chinchilla following acoustic trauma and effects of antioxidant treatment. Hear Res 283:1-13.
15. Eggermont JJ. 2012. The neuroscience of tinnitus. Oxford: Oxford University Press.
16. Feng J, Bendiske J, Morest DK. 2011. Degeneration in the ventral cochlear nucleus after severe noise damage in mice. J Neurosci Res 90:831-841.
17. Finlayson PG, Kaltenbach JA. 2009. Alterations in the spontaneous discharge patterns of single units in the dorsal cochlear nucleus following intense sound exposure. Hear Res 256:104-117.
18. Fonnum F. 1969. Radiochemical micro assays for the determination of choline acetyltransferase and acetylcholinesterase activities. Biochem J 115:465-472.
19. Fonnum F. 1970. Topographical and subcellular localization of choline acetyltransferase in rat hippocampal region. J Neurochem 17:1029-1037.
20. Fonnum F. 1975. Radiochemical assays for choline acetyltransferase and acetylcholinesterase. In: Marks N, Rodnight R, editors. Research methods in neurochemistry, vol 3. New York: Plenum Press. p 253-275.
21. Friauf E. 1992. Tonotopic order in the adult and developing auditory system of the rat as shown by c-fos immunocytochemistry. Eur J Neurosci 4:798-812.
22. Games KD, Winer JA. 1988. Layer V in rat auditory cortex: projections to the inferior colliculus and contralateral cortex. Hear Res 34:1-26.
23. Godfrey DA, Matschinsky FM. 1976. Approach to three-dimensional mapping of quantitative histochemical measurements applied to studies of the cochlear nucleus. J Histochem Cytochem 24:697-712.
24. Godfrey DA, Ross CD. 1990. Acetylcholine chemistry in the inferior colliculus. Otolaryngol Head Neck Surg 103:230.
25. Godfrey DA, Williams AD, Matschinsky FM. 1977. Quantitative histochemical mapping of enzymes of the cholinergic system in cat cochlear nucleus. J Histochem Cytochem 25:397-416.
26. Godfrey DA, Park JL, Rabe JR, Dunn JD, Ross CD. 1983. Effects of large brain stem lesions on the cholinergic system in the rat cochlear nucleus. Hear Res 11:133-156.
27. Godfrey DA, Park JL, Ross CD. 1984. Choline acetyltransferase and acetylcholinesterase in centrifugal labyrinthine bundles of rats. Hear Res 14:93-106.
28. Godfrey DA, Park JL, Dunn JD, Ross CD. 1985. Cholinergic neurotransmission in the cochlear nucleus. In: Drescher DG, editor. Auditory biochemistry. Springfield, IL: Charles C. Thomas. p 163-183.
29. Godfrey DA, Park-Hellendall JL, Dunn JD, Ross CD. 1987. Effects of trapezoid body and superior olive lesions on choline acetyltransferase activity in the rat cochlear nucleus. Hear Res 28:253-270.
30. Godfrey DA, Beranek KL, Carlson L, Parli JA, Dunn JD, Ross CD. 1990. Contribution of centrifugal innervation to choline acetyltransferase activity in the cat cochlear nucleus. Hear Res 49:259-280.
31. Godfrey DA, Godfrey TG, Mikesell NL, Waller HJ, Yao W, Chen K, Kaltenbach JA. 1997. Chemistry of granular and closely related regions of the cochlear nucleus. In: Syka J, editor. Acoustical signal processing in the central auditory system. New York: Plenum Press. p 139-153.
32. Godfrey DA, Mikesell NL, Godfrey TG, Fulcomer AB, Kong W, Godfrey MA, Kaltenbach JA, Zhang J. 2008. Effects of high-intensity sound exposure on neurotransmitter chemistry in the central auditory system. Semin Hear 29:259-269.
33. Godfrey DA, Kaltenbach JA, Chen K, Ilyas O, Liu X, Sacks J, McKnight D. 2012. Amino acid concentrations in the hamster central auditory system and long-term effects of intense tone exposure. J Neurosci Res 90:2214-2224.
34. Gu JW, Herrmann BS, Levine RA, Melcher JR. 2012. Brainstem auditory evoked potentials suggest a role for the ventral cochlear nucleus in tinnitus. J Assoc Res Otolaryngol 13:819-833.
35. Henry JA, Dennis KC, Schechter MA. 2005. General review of tinnitus: prevalence, mechanisms, effects, and management. J Speech Lang Hear Res 48:1204-1235.
36. Jin Y-M, Godfrey DA, Sun Y. 2005. Effects of cochlear ablation on choline acetyltransferase activity in the rat cochlear nucleus and superior olive. J Neurosci Res 81:91-101.
37. Jin Y-M, Godfrey DA, Wang J, Kaltenbach JA. 2006. Effects of intense tone exposure on choline acetyltransferase activity in the hamster cochlear nucleus. Hear Res 216/217:168-175.
38. Kaltenbach JA. 2011. Tinnitus: models and mechanisms. Hear Res 276:52-60.
39. Kaltenbach JA, Godfrey DA. 2008. Dorsal cochlear nucleus hyperactivity and tinnitus: are they related? Am J Audiol 17:S148-S161.
40. Kaltenbach JA, Zhang J. 2007. Intense sound-induced plasticity in the dorsal cochlear nucleus of rats: evidence for cholinergic receptor upregulation. Hear Res 226:232-243.
41. Kaltenbach JA, Czaja JM, Kaplan CR. 1992. Changes in the tonotopic map of the dorsal cochlear nucleus following induction of cochlear lesions by exposure to intense sound. Hear Res 59:213-223.
42. Kaltenbach JA, Zhang J, Afman CE. 2000. Plasticity of spontaneous neural activity in the dorsal cochlear nucleus after intense sound exposure. Hear Res 147:282-292.
43. Kim JJ, Gross J, Morest DK, Potashner SJ. 2004. 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.
44. Kraus KS, Ding D, Jiang H, Lobarinas E, Sun W, Salvi RJ. 2011. Relationship between noise-induced hearing-loss, persistent tinnitus and growth-associated protein-43 expression in the rat cochlear nucleus: does synaptic plasticity in ventral cochlear nucleus suppress tinnitus? Neuroscience 194:309-325.
45. Liberman MC, Dodds LW. 1984. Single-neuron labeling and chronic cochlear pathology. III. Stereocilia damage and alterations of threshold tuning curves. Hear Res 16:55-74.
46. Loftus WC, Malmierca MS, Bishop DC, Oliver DL. 2008. The cytoarchitecture of the inferior colliculus revisited: a common organization of the lateral cortex in rat and cat. Neuroscience 154:196-205.
47. Lowry OH, Passonneau JV. 1972. A flexible system of enzymatic analysis. New York: Academic Press.
48. Lyon MJ. 1978. The central location of the motor neurons to the stapedius muscle in the cat. Brain Res 143:437-444.
49. Mellott JG, Motts SD, Schofield BR. 2011. Multiple origins of cholinergic innervation of the cochlear nucleus. Neuroscience 180:138-147.
50. Michler SA, Illing RB. 2003. Molecular plasticity in the rat auditory brainstem: modulation of expression and distribution of phosphoserine, phosphor-CREB and TrkB after noise trauma. Audiol Neurootol 8:190-206.
51. Milbrandt JC, Holder TM, Wilson MC, Salvi RJ, Caspary DM. 2000. GAD levels and muscimol binding in rat inferior colliculus following acoustic trauma. Hear Res 147:251-260.
52. Morin LP, Wood RI. 2001. A stereotaxic atlas of the golden hamster brain. San Diego: Academic Press.
53. Mugnaini E, Warr WB, Osen KK. 1980. Distribution and light microscopic features of granule cells in the cochlear nuclei of cat, rat, and mouse. J Comp Neurol 191:581-606.
54. Mulders WH, Robertson D. 2011. Progressive centralization of midbrain hyperactivity after acoustic trauma. Neuroscience 192:753-760.
55. Osen KK, Mugnaini E, Dahl A-L, 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.
56. Paxinos G, Watson C. 1998. The rat brain in stereotaxic coordinates, 4th ed. San Diego: Academic Press.
57. Pilati N, Large C, Forsythe ID, Hamann M. 2012. Acoustic over-exposure triggers burst firing in dorsal cochlear nucleus fusiform cells. Hear Res 283:98-106.
58. Raji-Kubba J, Micevych PE, Simmons DD. 2002. The superior olivary complex of the hamster has multiple periods of cholinergic neuron development. J Chem Neuroanat 24:75-93.
59. Roberts LE, Eggermont JJ, Caspary DM, Shore SE, Melcher JR, Kaltenbach JA. 2010. Ringing ears: the neuroscience of tinnitus. J Neurosci 30:14972-14979.
60. Ross CD, Godfrey DA, Parli JA. 1995. Amino acid concentrations and selected enzyme activities in rat auditory, olfactory, and visual systems. Neurochem Res 20:1483-1490.
61. Ryan AF, Axelsson GA, Woolf NK. 1992. Central auditory metabolic activity induced by intense noise exposure. Hear Res 61:24-30.
62. Sánchez-González MA, Warr WB, López DE. 2003. Anatomy of olivocochlear neurons in the hamster studied with FluoroGold. Hear Res 185:65-76.
63. 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.
64. Sherriff FE, Henderson E. 1994. Cholinergic neurons in the ventral trapezoid nucleus project to the cochlear nuclei in the rat. Neuroscience 58:627-633.
65. Travers JB. 1995. Oromotor nuclei. In: Paxinos G, editor. The rat nervous system, 2nd ed. New York: Academic Press. p 239-255.
66. Tsuchitani C, Boudreau JC. 1966. Single unit analysis of cat superior olive S-segment with tonal stimuli. J Neurophysiol 29:684-697.
67. Vetter DE, Cozzari C, Hartman BK, Mugnaini E. 1993. Choline acetyltransferase in the rat cochlear nuclei: immunolocalization with a monoclonal antibody. In: Merchan MA, Juiz JM, Godfrey DA, Mugnaini E, editors. The mammalian cochlear nuclei: organization and function. New York: Plenum Press. p 279-290.
68. Vogler DP, Robertson D, Mulders WHAM. 2011. Hyperactivity in the ventral cochlear nucleus after cochlear trauma. J Neurosci 31:6639-6645.
69. Wang H, Brozoski TJ, Turner JG, Ling L, Parrish JL, Hughes LF, Caspary DM. 2009. Plasticity at glycinergic synapses in dorsal cochlear nucleus of rats with behavioral evidence of tinnitus. Neuroscience 164:747-759.
70. Wang H, Brozoski TJ, Caspary DM. 2011. Inhibitory neurotransmission in animal models of tinnitus: maladaptive plasticity. Hear Res 279:111-117.
71. Warr WB. 1992. Organization of olivocochlear efferent systems in mammals. In: Webster DB, Popper AN, Fay RR, editors. Mammalian auditory pathway: neuroanatomy. New York: Springer-Verlag. p 410-448.
72. Wenk H, Bigl V, Meyer U. 1980. Cholinergic projections from magnocellular nuclei of the basal forebrain to cortical areas in rats. Brain Res Rev 2:295-316.
73. Yao W, Godfrey DA. 1998. Immunohistochemical evaluation of cholinergic neurons in the rat superior olivary complex. Microsc Res Techniq 41:270-283.
74. Zar JH. 1984. Biostatistical analysis, 2nd ed. Englewood Cliffs, NJ: Prentice-Hall.
75. Zhang JS, Kaltenbach JA, Wang J, Bronchti G. 2003a. Changes in [14C]-2-deoxyglucose uptake in the auditory pathway of hamsters previously exposed to intense sound. Hear Res 185:13-21.
76. Zhang JS, Kaltenbach JA, Wang J, Kim SA. 2003b. Fos-like immunoreactivity in auditory and nonauditory brain structures of hamsters previously exposed to intense sound. Exp Brain Res 153:655-660.