Acoustic over-exposure triggers burst firing in dorsal cochlear nucleus fusiform cells

Hearing Research

Volumn 283, Issue 1-2, 2012, Pages 98-106

  Pilati, Nadia ^a   Large, Charles ^b   Forsythe, Ian D ^a   Hamann, Martine ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

^b GSK   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

VOLTAGE GATED POTASSIUM CHANNEL;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUDITORY DISCRIMINATION; AUDITORY STIMULATION; AUDITORY THRESHOLD SHIFT; CONTROLLED STUDY; DISEASE PREDISPOSITION; DORSAL COCHLEAR NUCLEUS; EVOKED BRAIN STEM AUDITORY RESPONSE; HEARING LOSS; LONG TERM EXPOSURE; MODULATION TRANSFER FUNCTION; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE POTENTIAL; NOISE INJURY; NONHUMAN; POTASSIUM CURRENT; PRIORITY JOURNAL; RAT; RISK FACTOR; SOUND INTENSITY; SPIKE WAVE; SPINDLE CELL; VOLTAGE CLAMP;

ACOUSTIC STIMULATION; ANIMALS; AUDITORY THRESHOLD; COCHLEAR NUCLEUS; DISEASE MODELS, ANIMAL; EVOKED POTENTIALS, AUDITORY, BRAIN STEM; HEARING LOSS, NOISE-INDUCED; MEMBRANE POTENTIALS; NOISE; PATCH-CLAMP TECHNIQUES; POTASSIUM; POTASSIUM CHANNELS, VOLTAGE-GATED; RATS; RATS, WISTAR; TIME FACTORS; TINNITUS;

EID: 84856612556     PISSN: 03785955     EISSN: 18785891     Source Type: Journal    
DOI: 10.1016/j.heares.2011.10.008     Document Type: Article

References (72)

1. Barnes-Davies M., Barker M.C., Osmani F., Forsythe I.D. Kv1 currents mediate a gradient of principal neuron excitability across the tonotopic axis in the rat lateral superior olive. Eur. J. Neurosci. 2004, 19:325-333.
2. Barrs D.M., Brackmann D.E., Hitselberger W.E. Facial nerve anastomosis in the cerebellopontine angle: a review of 24 cases. Am. J. Otol. 1984, 5:269-272.
3. Brew H., Forsythe I. Two voltage-dependent K+ conductances with complementary functions in postsynaptic integration at a central auditory synapse. J.Neurosci. 1995, 15:8011-8022.
4. 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, 22:2383-2390.
5. Buzsaki G., Csicsvari J., Dragoi G., Harris K., Henze D., Hirase H. Homeostatic maintenance of neuronal excitability by burst discharges invivo. Cereb. Cortex 2002, 12:893-899.
6. Calvin W.H., Stevens C.F. Synaptic noise and other sources of randomness in motoneuron interspike intervals. J.Neurophysiol. 1968, 31:574-587.
7. Chance F.S., Abbott L.F., Reyes A.D. Gain modulation from background synaptic input. Neuron 2002, 35:773-782.
8. Chang H., Chen K., Kaltenbach J.A., Zhang J., Godfrey D.A. Effects of acoustic trauma on dorsal cochlear nucleus neuron activity in slices. Hear Res. 2002, 164:59-68.
9. Chen K., Waller H.J., Godfrey D.A. Effects of endogenous acetylcholine on spontaneous activity in rat dorsal cochlear nucleus slices. Brain Res. 1998, 783:219-226.
10. Chen K., Waller H.J., Godfrey T.G., Godfrey D.A. Glutamatergic transmission of neuronal responses to carbachol in rat dorsal cochlear nucleus slices. Neuroscience 1999, 90:1043-1049.
11. Dallos P., Harris D. Properties of auditory nerve responses in absence of outer hair cells. J.Neurophysiol. 1978, 41:365-383.
12. Davies E., Knox E., Donaldson I. The usefulness of nimodipine, an L-calcium channel antagonist, in the treatment of tinnitus. Br. J. Audiol. 1994, 28:125-129.
13. Ding J., Benson T.E., Voigt H.F. Acoustic and current-pulse responses of identified neurons in the dorsal cochlear nucleus of unanesthetized, decerebrate gerbils. J.Neurophysiol. 1999, 82:3434-3457.
14. Eggermont J.J., Roberts L.E. The neuroscience of tinnitus. Trends Neurosci. 2004, 27:676-682.
15. Ehrenberger K. Topical administration of caroverine in somatic tinnitus treatment: proof-of-concept study. Int. Tinnitus J. 2005, 11:34-37.
16. Finlayson P.G., Kaltenbach J.A. Alterations in the spontaneous discharge patterns of single units in the dorsal cochlear nucleus following intense sound exposure. Hear Res. 2009, 256:104-117.
17. Friedland D.R., Eernisse R., Popper P. Potassium channel gene expression in the rat cochlear nucleus. Hear Res. 2007, 228:31-43.
18. Geal-Dor M., Freeman S., Li G., Sohmer H. Development of hearing in neonatal rats: air and bone conducted ABR thresholds. Hear Res. 1993, 69:236-242.
19. + channels, types Kv1.1, 1.2, 1.3, 1.5, and 3.1, stably expressed in mammalian cell lines. Mol. Pharmacol. 1994, 45:1227-1234.
20. Hancock K.E., Voigt H.F. Intracellularly labeled fusiform cells in dorsal cochlear nucleus of the gerbil. I. Physiological response properties. J. Neurophysiol. 2002, 87:2505-2519.
21. Hirsch J.A., Oertel D. Intrinsic properties of neurones in the dorsal cochlear nucleus of mice, invitro. J.Physiol. 1988, 396:535-548.
22. Holt G.R., Koch C. Shunting inhibition does not have a divisive effect on firing rates. Neural Comput. 1997, 9:1001-1013.
23. Hopkins W.F. Toxin and subunit specificity of blocking affinity of three peptide toxins for heteromultimeric, voltage-gated potassium channels expressed in Xenopus oocytes. J.Pharmacol. Exp. Ther. 1998, 285:1051-1060.
24. Johnston J., Forsythe I.D., Kopp-Scheinpflug C. Going native: voltage-gated potassium channels controlling neuronal excitability. J.Physiol. 2010, 588:3187-3200.
25. Kaltenbach J.A. The dorsal cochlear nucleus as a contributor to tinnitus: mechanisms underlying the induction of hyperactivity. Progress in Brain Research 2007, vol. 166:89-106. Elsevier. B. Langguth, G. Hajak, T. Kleinjung, A. Cacace, A.R. Møller (Eds.).
26. Kaltenbach J.A., Godfrey D.A. Dorsal cochlear nucleus hyperactivity and tinnitus: are they related?. Am. J. Audiol. 2008, 17:S148-S161.
27. Kaltenbach J.A., Godfrey D.A., Neumann J.B., McCaslin D.L., Afman C.E., Zhang J. Changes in spontaneous neural activity in the dorsal cochlear nucleus following exposure to intense sound: relation to threshold shift. Hear Res. 1998, 124:78-84.
28. Kaltenbach J.A., Falzarano P.R. DCN hyperactivity induced by previous intense sound exposure: origin with respect to cell layer. Abs. Assoc. Res. Otolaryngol. 2002, 25:208.
29. Kiang N.Y., Pfeiffer R.R., Warr W.B., Backus A.S. Stimulus coding in the cochlear nucleus. Ann. Otol. Rhinol. Laryngol. 1965, 74:463-485.
30. Koch C. Biophysics of Computation: Information Processing in Single Neurons 1999.
31. 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, 120:750-756.
32. Lau D., de Miera E.V.-S., Contreras D., Ozaita A., Harvey M., Chow A., Noebels J.L., Paylor R., Morgan J.I., Leonard C.S., Rudy B. Impaired fast-spiking, suppressed cortical inhibition, and increased susceptibility to seizures in mice lacking Kv3.2 K+ channel proteins. J.Neurosci. 2000, 20:9071-9085.
33. + currents in mouse auditory brainstem neurons. Eur. J. Neurosci. 2010, 32:1658-1667.
34. Leao R.N., Sun H., Svahn K., Berntson A., Youssoufian M., Paolini A.G., Fyffe R.E.W., Walmsley B. Topographic organization in the auditory brainstem of juvenile mice is disrupted in congenital deafness. J.Physiol. 2006, 571:563-578.
35. Lien C.-C., Jonas P. Kv3 potassium conductance is necessary and kinetically optimized for high-frequency action potential generation in hippocampal interneurons. J.Neurosci. 2003, 23:2058-2068.
36. Loeb M., Smith R.P. Relation of induced tinnitus to physical characteristics of the inducing stimuli. J.Acoust. Soc. Am. 1967, 42:453-455.
37. Ma W.-L.D., 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.
38. Manis P. Membrane properties and discharge characteristics of guinea pig dorsal cochlear nucleus neurons studied invitro. J.Neurosci. 1990, 10:2338-2351.
39. Manis P.B., Spirou G.A., Wright D.D., Paydar S., Ryugo D.K. Physiology and morphology of complex spiking neurons in the guinea pig dorsal cochlear nucleus. J.Comp. Neurol. 1994, 348:261-276.
40. Middleton J.W., Kiritani T., Pedersen C., Turner J.G., Shepherd G.M.G., Tzounopoulos T. Mice with behavioral evidence of tinnitus exhibit dorsal cochlear nucleus hyperactivity because of decreased GABAergic inhibition. PNAS 2011, 108:7601-7606.
41. Murashita H., Tabuchi K., Hoshino T., Tsuji S., Hara A. The effects of tempol, 3-aminobenzamide and nitric oxide synthase inhibitors on acoustic injury of the mouse cochlea. Hear Res. 2006, 214:1-6.
42. Nicolas-Puel C., Faulconbridge R.L., Guitton M., Puel J.L., Mondain M., Uziel A. Characteristics of tinnitus and etiology of associated hearing loss: a study of 123 patients. Int. Tinnitus J. 2002, 8:37-44.
43. Norena A.J., Eggermont J.J. Changes in spontaneous neural activity immediately after an acoustic trauma: implications for neural correlates of tinnitus. Hear Res. 2003, 183:137-153.
44. Oertel D., Wu S.H. Morphology and physiology of cells in slice preparations of the dorsal cochlear nucleus of mice. J.Comp. Neurol. 1989, 283:228-247.
45. Oertel D., Young E.D. What's a cerebellar circuit doing in the auditory system?. Trends Neurosci. 2004, 27:104-110.
46. Pierson M., Liebmann S.L. Noise exposure-induced audiogenic seizure susceptibility in Sprague-Dawley rats. Epilepsy Res. 1992, 13:35-42.
47. Pilati N., Barker M., Panteleimonitis S., Donga R., Hamann M. Arapid method combining Golgi and Nissl staining to study neuronal morphology and cytoarchitecture. J.Histochem. Cytochem. 2008, 56:539-550.
48. Roberts L.E., Eggermont J.J., Caspary D.M., Shore S.E., Melcher J.R., Kaltenbach J.A. Ringing ears: the neuroscience of tinnitus. J.Neurosci. 2010, 30:14972-14979.
49. Rudy B., McBain C.J. Kv3 channels: voltage-gated K+ channels designed for high-frequency repetitive firing. Trends Neurosci. 2001, 24:517-526.
50. Rybalko N., Bures Z., Burianova J., Popelar J., Grecova J., Syka J. Noise exposure during early development influences the acoustic startle reflex in adult rats. Physiol. Behav. 2011, 102:453-458.
51. Salvi R.J., Hamernik R.P., Henderson D. Response patterns of auditory nerve fibers during temporary threshold shift. Hear Res. 1983, 10:37-67.
52. Sanes D.H., Kotak V.C. Developmental plasticity of auditory cortical inhibitory synapses. Hear Res. 2011, 279:140-148.
53. Schaette R., Kempter R. Predicting tinnitus pitch from patients' audiograms with a computational model for the development of neuronal hyperactivity. J.Neurophysiol. 2009, 101:3042-3052.
54. 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.
55. Shore S.E., Koehler S., Oldakowski M., Hughes L.F., Syed S. Dorsal cochlear nucleus responses to somatosensory stimulation are enhanced after noise-induced hearing loss. Eur. J. Neurosci. 2008, 27:155-168.
56. Smith R.L., Brachman M.L. Response modulation of auditory-nerve fibers by AM stimuli: effects of average intensity. Hear. Res. 1980, 2:123-133.
57. Song P., Yang Y., Barnes-Davies M., Bhattacharjee A., Hamann M., Forsythe I.D., Oliver D.L., Kaczmarek L.K. Acoustic environment determines phosphorylation state of the Kv3.1 potassium channel in auditory neurons. Nat. Neurosci. 2005, 8:1335-1342.
58. Steinert J.R., Robinson S.W., Tong H., Haustein M.D., Kopp-Scheinpflug C., Forsythe I.D. Nitric oxide is an activity-dependent regulator of target neuron intrinsic excitability. Neuron 2011, 71:291-305.
59. Theopold H.M. Nimodipine (Bay e 9736) a new therapy concept in diseases of the inner ear?. Laryngol. Rhinol. Otol. (Stuttg) 1985, 64:609-613.
60. Timofeev I., Bazhenov M., Avramescu S., Nita D.A. Posttraumatic epilepsy: the roles of synaptic plasticity. Neuroscientist 2010, 16:19-27.
61. Topolnik L., Steriade M., Timofeev I. Hyperexcitability of intact neurons underlies acute development of trauma-related electrographic seizures in cats invivo. Eur. J. Neurosci. 2003, 18:486-496.
62. Trellakis S., Lautermann J., Lehnerdt G. Lidocaine: neurobiological targets and effects on the auditory system. Progress in Brain Research 2007, vol. 166:303-322. Elsevier. B. Langguth, G. Hajak, T. Kleinjung, A. Cacace, A.R. Møller (Eds.).
63. Turrigiano G., LeMasson G., Marder E. Selective regulation of current densities underlies spontaneous changes in the activity of cultured neurons. J.Neurosci. 1995, 15:3640-3652.
64. Turrigiano G.G. Homeostatic plasticity in neuronal networks: the more things change, the more they stay the same. Trends Neurosci. 1999, 22:221-227.
65. Von Hehn C.A.A., Bhattacharjee A., Kaczmarek L.K. Loss of Kv3.1 tonotopicity and altErations in cAMP response element-binding protein signaling in central auditory neurons of hearing impaired mice. J.Neurosci. 2004, 24:1936-1940.
66. Waller H.J., Godfrey D.A., Chen K. Effects of parallel fiber stimulation on neurons of rat dorsal cochlear nucleus. Hear Res. 1996, 98:169-179.
67. Wang L.-Y., Gan L., Forsythe I.D., Kaczmarek L.K. Contribution of the Kv3.1 potassium channel to high-frequency firing in mouse auditory neurones. J.Physiol. 1998, 509:183-194.
68. Witsell D.L., Hannley M.T., Stinnet S., Tucci D.L. Treatment of tinnitus with gabapentin: a pilot study. Otol. Neurotol. 2007, 28:11-15.
69. Yajima Y., Hayashi Y. Response properties and tonotopical organization in the dorsal cochlear nucleus in rats. Exp. Brain Res. 1989, 75:381-389.
70. Zacharek M.A., Kaltenbach J.A., Mathog T.A., Zhang J. Effects of cochlear ablation on noise induced hyperactivity in the hamster dorsal cochlear nucleus: implications for the origin of noise induced tinnitus. Hear Res. 2002, 172:137-143.
71. 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.
72. Zhang S., Oertel D. Neuronal circuits associated with the output of the dorsal cochlear nucleus through fusiform cells. J.Neurophysiol. 1994, 71:914-930.