Altered Neuronal Intrinsic Properties and Reduced Synaptic Transmission of the Rat's Medial Geniculate Body in Salicylate-Induced Tinnitus

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Su, Yan Yan ^a   Luo, Bin ^a   Jin, Yan ^a   Wu, Shu Hui ^b   Lobarinas, Edward ^c   Salvi, Richard J ^c   Chen, Lin ^a  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b CARLETON UNIVERSITY   (Canada)

^c UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SALICYLATE SODIUM; SALICYLIC ACID;

ANIMAL EXPERIMENT; ARTICLE; AUDITORY CORTEX; DRUG INDUCED DISEASE; EXCITATORY POSTSYNAPTIC POTENTIAL; INFERIOR COLLICULUS; INHIBITORY POSTSYNAPTIC POTENTIAL; MALE; MEDIAL GENICULATE BODY; MEMBRANE STEADY POTENTIAL; MIDDLE CEREBELLAR PEDUNCLE; NONHUMAN; PATCH CLAMP; PREPULSE INHIBITION; RAT; SALICYLATE INDUCED TINNITUS; SYNAPTIC TRANSMISSION; THALAMUS NUCLEUS;

ACOUSTIC STIMULATION; ACTION POTENTIALS; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; GENICULATE BODIES; INFERIOR COLLICULI; INHIBITORY POSTSYNAPTIC POTENTIALS; MALE; MEMBRANE POTENTIALS; NEURAL INHIBITION; NEURONS; PATCH-CLAMP TECHNIQUES; RATS; RATS, WISTAR; RECEPTORS, GABA-A; RECEPTORS, N-METHYL-D-ASPARTATE; SODIUM SALICYLATE; STARTLE REACTION; SYNAPTIC TRANSMISSION; TINNITUS;

EID: 84867363440     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0046969     Document Type: Article

References (54)

1. Day RO, Graham GG, Bieri D, Brown M, Cairns D, et al. (1989) Concentration-response relationships for salicylate-induced ototoxicity in normal volunteers. Br J Clin Pharmacol 28: 695-702.
2. Mongan E, Kelly P, Nies K, Porter WW, Paulus HE, (1973) Tinnitus as an indication of therapeutic serum salicylate levels. JAMA 226: 142-145.
3. Guitton MJ, Caston J, Ruel J, Johnson RM, Pujol R, et al. (2003) Salicylate induces tinnitus through activation of cochlear NMDA receptors. J Neurosci 23: 3944-3952.
4. Jastreboff PJ, Brennan JF, Coleman JK, Sasaki CT, (1988) Phantom auditory sensation in rats: an animal model for tinnitus. Behav Neurosci 102: 811-822.
5. Kizawa K, Kitahara T, Horii A, Maekawa C, Kuramasu T, et al. (2010) Behavioral assessment and identification of a molecular marker in a salicylate-induced tinnitus in rats. Neuroscience 165: 1323-1332.
6. Yang G, Lobarinas E, Zhang L, Turner J, Stolzberg D, et al. (2007) Salicylate induced tinnitus: behavioral measures and neural activity in auditory cortex of awake rats. Hear Res 226: 244-253.
7. Liu XP, Chen L, (2012) Auditory brainstem response as a possible objective indicator for salicylate-induced tinnitus in rats. Brain Res In press.
8. Cazals Y, (2000) Auditory sensori-neural alterations induced by salicylate. Prog Neurobiol 62: 583-631.
9. Sun W, Lu J, Stolzberg D, Gray L, Deng A, et al. (2009) Salicylate increases the gain of the central auditory system. Neuroscience 159: 325-334.
10. Zhang X, Yang P, Cao Y, Qin L, Sato Y, (2011) Salicylate induced neural changes in the primary auditory cortex of awake cats. Neuroscience 172: 232-245.
11. Eggermont JJ, Kenmochi M, (1998) Salicylate and quinine selectively increase spontaneous firing rates in secondary auditory cortex. Hear Res 117: 149-160.
12. Paul AK, Lobarinas E, Simmons R, Wack D, Luisi JC, et al. (2009) Metabolic imaging of rat brain during pharmacologically-induced tinnitus. Neuroimage 44: 312-318.
13. Wallhausser-Franke E, Mahlke C, Oliva R, Braun S, Wenz G, et al. (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.
14. Wang HT, Luo B, Zhou KQ, Xu TL, Chen L, (2006) Sodium salicylate reduces inhibitory postsynaptic currents in neurons of rat auditory cortex. Hear Res 215: 77-83.
15. Su YY, Luo B, Wang HT, Chen L, (2009) Differential effects of sodium salicylate on current-evoked firing of pyramidal neurons and fast-spiking interneurons in slices of rat auditory cortex. Hear Res 253: 60-66.
16. Eggermont JJ, (2008) Role of auditory cortex in noise- and drug-induced tinnitus. Am J Audiol 17: S162-169.
17. Leaver AM, Renier L, Chevillet MA, Morgan S, Kim HJ, et al. (2011) Dysregulation of limbic and auditory networks in tinnitus. Neuron 69: 33-43.
18. Gong N, Zhang M, Zhang XB, Chen L, Sun GC, et al. (2008) The aspirin metabolite salicylate enhances neuronal excitation in rat hippocampal CA1 area through reducing GABAergic inhibition. Neuropharmacology 54: 454-463.
19. Landgrebe M, Langguth B, Rosengarth K, Braun S, Koch A, et al. (2009) Structural brain changes in tinnitus: grey matter decrease in auditory and non-auditory brain areas. Neuroimage 46: 213-218.
20. Lockwood AH, Salvi RJ, Coad ML, Towsley ML, Wack DS, et al. (1998) The functional neuroanatomy of tinnitus: evidence for limbic system links and neural plasticity. Neurology 50: 114-120.
21. 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.
22. Lanting CP, de Kleine E, van Dijk P, (2009) Neural activity underlying tinnitus generation: results from PET and fMRI. Hear Res 255: 1-13.
23. Malmierca MS, (2003) The structure and physiology of the rat auditory system: an overview. Int Rev Neurobiol 56: 147-211.
24. Basta D, Goetze R, Ernst A, (2008) Effects of salicylate application on the spontaneous activity in brain slices of the mouse cochlear nucleus, medial geniculate body and primary auditory cortex. Hear Res 240: 42-51.
25. Ralli M, Lobarinas E, Fetoni AR, Stolzberg D, Paludetti G, et al. (2010) Comparison of salicylate- and quinine-induced tinnitus in rats: development, time course, and evaluation of audiologic correlates. Otol Neurotol 31: 823-831.
26. Bartlett EL, Smith PH, (1999) Anatomic, intrinsic, and synaptic properties of dorsal and ventral division neurons in rat medial geniculate body. J Neurophysiol 81: 1999-2016.
27. Hu B, (1995) Cellular basis of temporal synaptic signalling: an in vitro electrophysiological study in rat auditory thalamus. J Physiol 483 (Pt 1):: 167-182.
28. Peruzzi D, Bartlett E, Smith PH, Oliver DL, (1997) A monosynaptic GABAergic input from the inferior colliculus to the medial geniculate body in rat. J Neurosci 17: 3766-3777.
29. Sun H, Wu SH, (2008) Physiological characteristics of postinhibitory rebound depolarization in neurons of the rat's dorsal cortex of the inferior colliculus studied in vitro. Brain Res 1226: 70-81.
30. Lobarinas E, Sun W, Cushing R, Salvi R, (2004) A novel behavioral paradigm for assessing tinnitus using schedule-induced polydipsia avoidance conditioning (SIP-AC). Hear Res 190: 109-114.
31. Ruttiger L, Ciuffani J, Zenner HP, Knipper M, (2003) 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: 39-50.
32. Smith PH, Bartlett EL, Kowalkowski A, (2006) Unique combination of anatomy and physiology in cells of the rat paralaminar thalamic nuclei adjacent to the medial geniculate body. J Comp Neurol 496: 314-334.
33. Goldstein SA, Bockenhauer D, O'Kelly I, Zilberberg N, (2001) Potassium leak channels and the KCNK family of two-P-domain subunits. Nat Rev Neurosci 2: 175-184.
34. Meuth SG, Kanyshkova T, Meuth P, Landgraf P, Munsch T, et al. (2006) Membrane resting potential of thalamocortical relay neurons is shaped by the interaction among TASK3 and HCN2 channels. J Neurophysiol 96: 1517-1529.
35. Liu Y, Li X, (2004) Effects of salicylate on voltage-gated sodium channels in rat inferior colliculus neurons. Hear Res 193: 68-74.
36. Hodgkin AL, Huxley AF, (1952) Currents carried by sodium and potassium ions through the membrane of the giant axon of Loligo. J Physiol 116: 449-472.
37. Jung HY, Mickus T, Spruston N, (1997) Prolonged sodium channel inactivation contributes to dendritic action potential attenuation in hippocampal pyramidal neurons. J Neurosci 17: 6639-6646.
38. Cong D, Tang Z, Li L, Huang Y, Wang J, et al. (2011) Cross-talk between NMDA and GABA(A) receptors in cultured neurons of the rat inferior colliculus. Sci China Life Sci 54: 560-566.
39. Surges R, Sarvari M, Steffens M, Els T, (2006) Characterization of rebound depolarization in hippocampal neurons. Biochem Biophys Res Commun 348: 1343-1349.
40. Winer JA, Larue DT, (1988) Anatomy of glutamic acid decarboxylase immunoreactive neurons and axons in the rat medial geniculate body. J Comp Neurol 278: 47-68.
41. Winer JA, Larue DT, (1996) Evolution of GABAergic circuitry in the mammalian medial geniculate body. Proc Natl Acad Sci U S A 93: 3083-3087.
42. Clerici WJ, Coleman JR, (1990) Anatomy of the rat medial geniculate body: I. Cytoarchitecture, myeloarchitecture, and neocortical connectivity. J Comp Neurol 297: 14-31.
43. Clerici WJ, McDonald AJ, Thompson R, Coleman JR, (1990) Anatomy of the rat medial geniculate body: II. Dendritic morphology. J Comp Neurol 297: 32-54.
44. Silverstein H, Bernstein JM, Davies DG, (1967) Salicylate ototoxicity. A biochemical and electrophysiological study. Ann Otol Rhinol Laryngol 76: 118-128.
45. Basta D, Ernst A, (2004) Effects of salicylate on spontaneous activity in inferior colliculus brain slices. Neurosci Res 50: 237-243.
46. Chen GD, Jastreboff PJ, (1995) Salicylate-induced abnormal activity in the inferior colliculus of rats. Hear Res 82: 158-178.
47. Wei L, Ding D, Sun W, Xu-Friedman MA, Salvi R, (2010) Effects of sodium salicylate on spontaneous and evoked spike rate in the dorsal cochlear nucleus. Hear Res 267: 54-60.
48. Cruikshank SJ, Lewis TJ, Connors BW, (2007) Synaptic basis for intense thalamocortical activation of feedforward inhibitory cells in neocortex. Nat Neurosci 10: 462-468.
49. Tennigkeit F, Schwarz DW, Puil E, (1998) Postnatal development of signal generation in auditory thalamic neurons. Brain Res Dev Brain Res 109: 255-263.
50. Hsieh CY, Chen Y, Leslie FM, Metherate R, (2002) Postnatal development of NR2A and NR2B mRNA expression in rat auditory cortex and thalamus. J Assoc Res Otolaryngol 3: 479-487.
51. Luo B, Wang HT, Su YY, Wu SH, Chen L, (2011) Activation of presynaptic GABA(B) receptors modulates GABAergic and glutamatergic inputs to the medial geniculate body. Hear Res 280: 157-165.
52. Deer BC, Hunter-Duvar I, (1982) Salicylate ototoxicity in the chinchilla: a behavioral and electron microscope study. J Otolaryngol 11: 260-264.
53. Jastreboff PJ, Hansen R, Sasaki PG, Sasaki CT, (1986) Differential uptake of salicylate in serum, cerebrospinal fluid, and perilymph. Arch Otolaryngol Head Neck Surg 112: 1050-1053.
54. Sun H, Wu SH, (2009) The physiological role of pre- and postsynaptic GABA(B) receptors in membrane excitability and synaptic transmission of neurons in the rat's dorsal cortex of the inferior colliculus. Neuroscience 160: 198-211.