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Neural mechanisms underlying tinnitus induced by sodium salicylate

  • Auditory Research Laboratory, University of Science and Technology of China, Hefei 230027, China

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  • Corresponding author: CHEN Lin, E-mail: linchen@ustc.edu.cn
  • Received Date: 15 June 2008
  • Rev Recd Date: 01 July 2008
  • Publish Date: 31 August 2008
    Abstract

  • Abstract

    Sodium salicylate (NaSal) is the metabolite and active component of aspirin. NaSal is often used for tinnitus research because it can reliably induce a tinnitus-like behavior in animals at a high dose. Given that NaSal can reach a high concentration in the cerebrospinal fluid, we propose that NaSal induces tinnitus by changing the balance between excitation and inhibition in the central auditory system. In order to test this hypothesis, a series of studies were conducted to investigate the effects of NaSal on the neuronal responses and synaptic transmissions in the central auditory region with whole-cell patch-clamp techniques. It has been found that NaSal significantly suppresses the functional activity of GABA neurons, suggesting that NalSal raises excitability in the central auditory system to induce tinnitus.

    Abstract

    Sodium salicylate (NaSal) is the metabolite and active component of aspirin. NaSal is often used for tinnitus research because it can reliably induce a tinnitus-like behavior in animals at a high dose. Given that NaSal can reach a high concentration in the cerebrospinal fluid, we propose that NaSal induces tinnitus by changing the balance between excitation and inhibition in the central auditory system. In order to test this hypothesis, a series of studies were conducted to investigate the effects of NaSal on the neuronal responses and synaptic transmissions in the central auditory region with whole-cell patch-clamp techniques. It has been found that NaSal significantly suppresses the functional activity of GABA neurons, suggesting that NalSal raises excitability in the central auditory system to induce tinnitus.
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    • References(63)
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    Yang G, Lobarinas E, Zhang L, et al. Salicylate induced tinnitus: behavioral measures and neural activity in auditory cortex of awake rats [J]. Hear Res, 2007, 226(1-2): 244-253.
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    Ramsden R T, Latif A, OMalley S. Electrocochleographic changes in acute salicylate overdosage [J]. J Laryngol Otol, 1985, 99(12): 1 269-1 273.
    [27]
    Silverstein H, Bernstein J M, Davies D G. Salicylate ototoxicity. A biochemical and electrophysiological study [J]. Ann Otol Rhinol Laryngol, 1967, 76(1): 118-128.
    [28]
    Tanaka Y, Brown P G. Action of metabolic inhibitors and energy-rich phosphate compounds on cochlear potentials [J]. Ann Otol Rhinol Laryngol, 1970, 79(2): 338-351.
    [29]
    Arruda J, Jung T T, McGann D G. Effect of leukotriene inhibitor on otoacoustic emissions in salicylate ototoxicity [J]. Am J Otol, 1996, 17(5): 787-792.
    [30]
    Ueda H, Yamamoto Y, Yanagita N. Effect of aspirin on transiently evoked otoacoustic emissions in guinea pigs [J]. ORL J Otorhinolaryngol Relat Spec, 1996, 58(2): 61-67.
    [31]
    Kurata K, Yamamoto M, Tsukuda R, et al. A characteristic of aspirin-induced hearing loss in auditory brainstem response of conscious rats [J]. J Vet Med Sci, 1997, 59(1): 9-15.
    [32]
    Ochi K, Eggermont J J. Effects of salicylate on neural activity in cat primary auditory cortex [J]. Hear Res, 1996, 95(1-2): 63-76.
    [33]
    Muller M, Klinke R, Arnold W, et al. Auditory nerve fibre responses to salicylate revisited [J]. Hear Res, 2003, 183(1-2): 37-43.
    [34]
    Stypulkowski P H. Mechanisms of salicylate ototoxicity [J]. Hear Res, 1990, 46(1-2): 113-145.
    [35]
    Kakehata S, Santos-Sacchi J. Effects of salicylate and lanthanides on outer hair cell motility and associated gating charge [J]. J Neurosci, 1996, 16(16): 4 881-4 889.
    [36]
    Tunstall M J, Gale J E, Ashmore J F. Action of salicylate on membrane capacitance of outer hair cells from the guinea-pig cochlea [J]. J Physiol, 1995, 485(Pt 3): 739-752.
    [37]
    Oliver D, He D Z, Klocker N, et al. Intracellular anions as the voltage sensor of prestin, the outer hair cell motor protein [J]. Science, 2001, 292(5 525): 2 340-2 343.
    [38]
    Peng B G, Chen S, Lin X. Aspirin selectively augmented N-methyl-D-aspartate types of glutamate responses in cultured spiral ganglion neurons of mice [J]. Neurosci Lett, 2003, 343(1): 21-24.
    [39]
    Wallhausser-Franke E, Braun S, Langner G. Salicylate alters 2-DG uptake in the auditory system: a model for tinnitus? [J]. Neuroreport, 1996, 7(10): 1 585-1 588.
    [40]
    Wallhausser-Franke E. Salicylate evokes c-fos expression in the brain stem: implications for tinnitus [J]. Neuroreport, 1997, 8(3): 725-728.
    [41]
    Jastreboff P J, Hansen R, Sasaki P G, et al. Differential uptake of salicylate in serum, cerebrospinal fluid, and perilymph [J]. Arch Otolaryngol Head Neck Surg, 1986, 112(10): 1 050-1 053.
    [42]
    Chen G D, Jastreboff P J. Salicylate-induced abnormal activity in the inferior colliculus of rats [J]. Hear Res, 1995, 82(2): 158-178.
    [43]
    Manabe Y, Yoshida S, Saito H, et al. Effects of lidocaine on salicylate-induced discharge of neurons in the inferior colliculus of the guinea pig [J]. Hear Res, 1997, 103(1-2): 192-198.
    [44]
    Basta D, Ernst A. Effects of salicylate on spontaneous activity in inferior colliculus brain slices [J]. Neurosci Res, 2004, 50(2): 237-243.
    [45]
    Liu Y, Li X. Effects of salicylate on voltage-gated sodium channels in rat inferior colliculus neurons [J]. Hear Res, 2004, 193(1-2): 68-74.
    [46]
    Liu Y, Li X, Ma C, et al. Salicylate blocks L-type calcium channels in rat inferior colliculus neurons [J]. Hear Res, 2005, 205(1-2): 271-276.
    [47]
    Liu Y, Li X. Effects of salicylate on transient outward and delayed rectifier potassium channels in rat inferior colliculus neurons [J]. Neurosci Lett, 2004, 369(2): 115-120.
    [48]
    Liu Y X, Li X P, Liu J X, et al. Inhibition of salicylate on potassium channels in rat inferior colliculus neurons[J]. Zhonghua Er Bi Yan Hou Tou Jing Wai Ke Za Zhi, 2005, 40(11): 835-839.
    [49]
    Rudy B, McBain C J. Kv3 channels: voltage-gated K+ channels designed for high-frequency repetitive firing [J]. Trends Neurosci, 2001, 24(9): 517-526.
    [50]
    Joho R H, Ho C S, Marks G A. Increased gamma- and decreased delta-oscillations in a mouse deficient for a potassium channel expressed in fast-spiking interneurons [J]. J Neurophysiol, 1999, 82(4): 1 855-1 864.
    [51]
    Tateno T, Robinson H P. Quantifying noise-induced stability of a cortical fast-spiking cell model with Kv3-channel-like current [J]. Biosystems, 2007, 89(1-3): 110-116.
    [52]
    von Hehn C 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]. J Neurosci, 2004, 24(8): 1 936-1 940.
    [53]
    Song P, Yang Y, Barnes-Davies M, et al. Acoustic environment determines phosphorylation state of the Kv3.1 potassium channel in auditory neurons [J]. Nat Neurosci, 2005, 8(10): 1 335-1 342.
    [54]
    Wang H T, Luo B, Huang Y N, et al. Sodium salicylate suppresses serotonin-induced enhancement of GABAergic spontaneous inhibitory postsynaptic currents in rat inferior colliculus in vitro [J]. Hear Res, 2008, 236(1-2): 42-51.
    [55]
    Eggermont J J. Central tinnitus [J]. Auris Nasus Larynx, 2003, 30 Suppl: S7-12.
    [56]
    Xu H, Gong N, Chen L, et al. Sodium salicylate reduces gamma aminobutyric acid-induced current in rat spinal dorsal horn neurons [J]. Neuroreport, 2005, 16(8): 813-816.
    [57]
    Smiley J F, Goldman-Rakic P S. Serotonergic axons in monkey prefrontal cerebral cortex synapse predominantly on interneurons as demonstrated by serial section electron microscopy [J]. J Comp Neurol, 1996, 367(3): 431-443.
    [58]
    Zhou F M, Hablitz J J. Activation of serotonin receptors modulates synaptic transmission in rat cerebral cortex [J]. J Neurophysiol, 1999, 82(6): 2 989-2 999.
    [59]
    Bennett B D, Huguenard J R, Prince D A. Adrenergic modulation of GABAA receptor-mediated inhibition in rat sensorimotor cortex [J]. J Neurophysiol, 1998, 79(2): 937-946.
    [60]
    Gorelova N, Seamans J K, Yang C R. Mechanisms of dopamine activation of fast-spiking interneurons that exert inhibition in rat prefrontal cortex [J]. J Neurophysiol, 2002, 88(6): 3 150-3 166.
    [61]
    Christophe E, Roebuck A, Staiger J F, et al. Two types of nicotinic receptors mediate an excitation of neocortical layer I interneurons [J]. J Neurophysiol, 2002, 88(3): 1 318-1 327.
    [62]
    Peruzzi D, Dut A. GABA, serotonin and serotonin receptors in the rat inferior colliculus [J]. Brain Res, 2004, 998(2): 247-250.
    [63]
    Liu J, Li X, Wang L, et al. Effects of salicylate on serotoninergic activities in rat inferior colliculus and auditory cortex [J]. Hear Res, 2003, 175(1-2): 45-53.
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    [1]
    Flor H, Elbert T, Knecht S, et al. Phantom-limb pain as a perceptual correlate of cortical reorganization following arm amputation [J]. Nature, 1995, 375(6 531): 482-484.
    [2]
    Saunders J C. The role of central nervous system plasticity in tinnitus [J]. J Commun Disord, 2007, 40(4): 313-334.
    [3]
    Eggermont J J, Komiya H. Moderate noise trauma in juvenile cats results in profound cortical topographic map changes in adulthood [J]. Hear Res, 2000, 142(1-2): 89-101.
    [4]
    Seki S, Eggermont J J. Changes in spontaneous firing rate and neural synchrony in cat primary auditory cortex after localized tone-induced hearing loss [J]. Hear Res, 2003, 180(1-2): 28-38.
    [5]
    Eggermont J J. Tinnitus: neurobiological substrates [J]. Drug Discov Today, 2005, 10(19): 1 283-1 290.
    [6]
    Eggermont J J, Roberts L E. The neuroscience of tinnitus [J]. Trends Neurosci, 2004, 27(11): 676-682.
    [7]
    Cazals Y, Horner K C, Huang Z W. Alterations in average spectrum of cochleoneural activity by long-term salicylate treatment in the guinea pig: a plausible index of tinnitus [J]. J Neurophysiol, 1998, 80(4): 2 113-2 120.
    [8]
    Eggermont J J, Kenmochi M. Salicylate and quinine selectively increase spontaneous firing rates in secondary auditory cortex [J]. Hear Res, 1998, 117(1-2): 149-160.
    [9]
    Guitton M J, Caston J, Ruel J, et al. Salicylate induces tinnitus through activation of cochlear NMDA receptors [J]. J Neurosci, 2003, 23(9): 3 944-3 952.
    [10]
    Jastreboff P J, Brennan J F, Coleman J K, et al. Phantom auditory sensation in rats: an animal model for tinnitus [J]. Behav Neurosci, 1988,102(6): 811-822.
    [11]
    Lobarinas E, Yang G, Sun W, et al. Salicylate- and quinine-induced tinnitus and effects of memantine [J]. Acta Otolaryngol Suppl, 2006,(556): 13-19.
    [12]
    Yang G, Lobarinas E, Zhang L, et al. Salicylate induced tinnitus: behavioral measures and neural activity in auditory cortex of awake rats [J]. Hear Res, 2007, 226(1-2): 244-253.
    [13]
    Elattar T M, Lin H S, Tira D E. The effect of non-steroidal anti-inflammatory drugs on the metabolism of 14C-arachidonic acid by human gingival tissue in vitro [J]. J Dent Res, 1983, 62(9): 975-979.
    [14]
    Siegel M I. Effect of non-steroidal anti-inflammatory drugs on arachidonic acid metabolism [J]. Headache, 1981, 21(6): 264-271.
    [15]
    Siesjo B K, Agardh C D, Bengtsson F, et al. Arachidonic acid metabolism in seizures [J]. Ann N Y Acad Sci, 1989, 559: 323-339.
    [16]
    Didier A, Miller J M, Nuttall A L. The vascular component of sodium salicylate ototoxicity in the guinea pig [J]. Hear Res, 1993, 69(1-2): 199-206.
    [17]
    Barbour B, Szatkowski M, Ingledew N, et al. Arachidonic acid induces a prolonged inhibition of glutamate uptake into glial cells [J]. Nature, 1989, 342(6 252): 918-920.
    [18]
    Pearlman R J, Aubrey K R, Vandenberg R J. Arachidonic acid and anandamide have opposite modulatory actions at the glycine transporter, GLYT1a [J]. J Neurochem, 2003, 84(3): 592-601.
    [19]
    Saxena N C. Inhibition of GABA(A) receptor (GABAR) currents by arachidonic acid in HEK 293 cells stably transfected with alpha1beta2gamma2 GABAR subunits [J]. Pflugers Arch, 2000, 440(3): 380-392.
    [20]
    Mahlke C, Wallhausser-Franke E. Evidence for tinnitus-related plasticity in the auditory and limbic system, demonstrated by arg3.1 and c-fos immunocytochemistry [J]. Hear Res, 2004, 195(1-2): 17-34.
    [21]
    Wallhausser-Franke E, Cuautle-Heck B, Wenz G, et al. Scopolamine attenuates tinnitus-related plasticity in the auditory cortex [J]. Neuroreport, 2006, 17(14): 1 487-1 491.
    [22]
    Zheng Y, Seung Lee H, Smith P F, et al. Neuronal nitric oxide synthase expression in the cochlear nucleus in a salicylate model of tinnitus [J]. Brain Res, 2006, 1 123(1): 201-206.
    [23]
    Akaneya Y, Tsumoto T. Bidirectional trafficking of prostaglandin E2 receptors involved in long-term potentiation in visual cortex [J]. J Neurosci, 2006, 26(40): 10 209-10 221.
    [24]
    Douek E E, Dodson H C, Bannister L H. The effects of sodium salicylate on the cochlea of guinea pigs [J]. J Laryngol Otol, 1983, 97(9): 793-799.
    [25]
    Puel J L, Bobbin R P, Fallon M. Salicylate, mefenamate, meclofenamate, and quinine on cochlear potentials [J]. Otolaryngol Head Neck Surg, 1990, 102(1): 66-73.
    [26]
    Ramsden R T, Latif A, OMalley S. Electrocochleographic changes in acute salicylate overdosage [J]. J Laryngol Otol, 1985, 99(12): 1 269-1 273.
    [27]
    Silverstein H, Bernstein J M, Davies D G. Salicylate ototoxicity. A biochemical and electrophysiological study [J]. Ann Otol Rhinol Laryngol, 1967, 76(1): 118-128.
    [28]
    Tanaka Y, Brown P G. Action of metabolic inhibitors and energy-rich phosphate compounds on cochlear potentials [J]. Ann Otol Rhinol Laryngol, 1970, 79(2): 338-351.
    [29]
    Arruda J, Jung T T, McGann D G. Effect of leukotriene inhibitor on otoacoustic emissions in salicylate ototoxicity [J]. Am J Otol, 1996, 17(5): 787-792.
    [30]
    Ueda H, Yamamoto Y, Yanagita N. Effect of aspirin on transiently evoked otoacoustic emissions in guinea pigs [J]. ORL J Otorhinolaryngol Relat Spec, 1996, 58(2): 61-67.
    [31]
    Kurata K, Yamamoto M, Tsukuda R, et al. A characteristic of aspirin-induced hearing loss in auditory brainstem response of conscious rats [J]. J Vet Med Sci, 1997, 59(1): 9-15.
    [32]
    Ochi K, Eggermont J J. Effects of salicylate on neural activity in cat primary auditory cortex [J]. Hear Res, 1996, 95(1-2): 63-76.
    [33]
    Muller M, Klinke R, Arnold W, et al. Auditory nerve fibre responses to salicylate revisited [J]. Hear Res, 2003, 183(1-2): 37-43.
    [34]
    Stypulkowski P H. Mechanisms of salicylate ototoxicity [J]. Hear Res, 1990, 46(1-2): 113-145.
    [35]
    Kakehata S, Santos-Sacchi J. Effects of salicylate and lanthanides on outer hair cell motility and associated gating charge [J]. J Neurosci, 1996, 16(16): 4 881-4 889.
    [36]
    Tunstall M J, Gale J E, Ashmore J F. Action of salicylate on membrane capacitance of outer hair cells from the guinea-pig cochlea [J]. J Physiol, 1995, 485(Pt 3): 739-752.
    [37]
    Oliver D, He D Z, Klocker N, et al. Intracellular anions as the voltage sensor of prestin, the outer hair cell motor protein [J]. Science, 2001, 292(5 525): 2 340-2 343.
    [38]
    Peng B G, Chen S, Lin X. Aspirin selectively augmented N-methyl-D-aspartate types of glutamate responses in cultured spiral ganglion neurons of mice [J]. Neurosci Lett, 2003, 343(1): 21-24.
    [39]
    Wallhausser-Franke E, Braun S, Langner G. Salicylate alters 2-DG uptake in the auditory system: a model for tinnitus? [J]. Neuroreport, 1996, 7(10): 1 585-1 588.
    [40]
    Wallhausser-Franke E. Salicylate evokes c-fos expression in the brain stem: implications for tinnitus [J]. Neuroreport, 1997, 8(3): 725-728.
    [41]
    Jastreboff P J, Hansen R, Sasaki P G, et al. Differential uptake of salicylate in serum, cerebrospinal fluid, and perilymph [J]. Arch Otolaryngol Head Neck Surg, 1986, 112(10): 1 050-1 053.
    [42]
    Chen G D, Jastreboff P J. Salicylate-induced abnormal activity in the inferior colliculus of rats [J]. Hear Res, 1995, 82(2): 158-178.
    [43]
    Manabe Y, Yoshida S, Saito H, et al. Effects of lidocaine on salicylate-induced discharge of neurons in the inferior colliculus of the guinea pig [J]. Hear Res, 1997, 103(1-2): 192-198.
    [44]
    Basta D, Ernst A. Effects of salicylate on spontaneous activity in inferior colliculus brain slices [J]. Neurosci Res, 2004, 50(2): 237-243.
    [45]
    Liu Y, Li X. Effects of salicylate on voltage-gated sodium channels in rat inferior colliculus neurons [J]. Hear Res, 2004, 193(1-2): 68-74.
    [46]
    Liu Y, Li X, Ma C, et al. Salicylate blocks L-type calcium channels in rat inferior colliculus neurons [J]. Hear Res, 2005, 205(1-2): 271-276.
    [47]
    Liu Y, Li X. Effects of salicylate on transient outward and delayed rectifier potassium channels in rat inferior colliculus neurons [J]. Neurosci Lett, 2004, 369(2): 115-120.
    [48]
    Liu Y X, Li X P, Liu J X, et al. Inhibition of salicylate on potassium channels in rat inferior colliculus neurons[J]. Zhonghua Er Bi Yan Hou Tou Jing Wai Ke Za Zhi, 2005, 40(11): 835-839.
    [49]
    Rudy B, McBain C J. Kv3 channels: voltage-gated K+ channels designed for high-frequency repetitive firing [J]. Trends Neurosci, 2001, 24(9): 517-526.
    [50]
    Joho R H, Ho C S, Marks G A. Increased gamma- and decreased delta-oscillations in a mouse deficient for a potassium channel expressed in fast-spiking interneurons [J]. J Neurophysiol, 1999, 82(4): 1 855-1 864.
    [51]
    Tateno T, Robinson H P. Quantifying noise-induced stability of a cortical fast-spiking cell model with Kv3-channel-like current [J]. Biosystems, 2007, 89(1-3): 110-116.
    [52]
    von Hehn C 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]. J Neurosci, 2004, 24(8): 1 936-1 940.
    [53]
    Song P, Yang Y, Barnes-Davies M, et al. Acoustic environment determines phosphorylation state of the Kv3.1 potassium channel in auditory neurons [J]. Nat Neurosci, 2005, 8(10): 1 335-1 342.
    [54]
    Wang H T, Luo B, Huang Y N, et al. Sodium salicylate suppresses serotonin-induced enhancement of GABAergic spontaneous inhibitory postsynaptic currents in rat inferior colliculus in vitro [J]. Hear Res, 2008, 236(1-2): 42-51.
    [55]
    Eggermont J J. Central tinnitus [J]. Auris Nasus Larynx, 2003, 30 Suppl: S7-12.
    [56]
    Xu H, Gong N, Chen L, et al. Sodium salicylate reduces gamma aminobutyric acid-induced current in rat spinal dorsal horn neurons [J]. Neuroreport, 2005, 16(8): 813-816.
    [57]
    Smiley J F, Goldman-Rakic P S. Serotonergic axons in monkey prefrontal cerebral cortex synapse predominantly on interneurons as demonstrated by serial section electron microscopy [J]. J Comp Neurol, 1996, 367(3): 431-443.
    [58]
    Zhou F M, Hablitz J J. Activation of serotonin receptors modulates synaptic transmission in rat cerebral cortex [J]. J Neurophysiol, 1999, 82(6): 2 989-2 999.
    [59]
    Bennett B D, Huguenard J R, Prince D A. Adrenergic modulation of GABAA receptor-mediated inhibition in rat sensorimotor cortex [J]. J Neurophysiol, 1998, 79(2): 937-946.
    [60]
    Gorelova N, Seamans J K, Yang C R. Mechanisms of dopamine activation of fast-spiking interneurons that exert inhibition in rat prefrontal cortex [J]. J Neurophysiol, 2002, 88(6): 3 150-3 166.
    [61]
    Christophe E, Roebuck A, Staiger J F, et al. Two types of nicotinic receptors mediate an excitation of neocortical layer I interneurons [J]. J Neurophysiol, 2002, 88(3): 1 318-1 327.
    [62]
    Peruzzi D, Dut A. GABA, serotonin and serotonin receptors in the rat inferior colliculus [J]. Brain Res, 2004, 998(2): 247-250.
    [63]
    Liu J, Li X, Wang L, et al. Effects of salicylate on serotoninergic activities in rat inferior colliculus and auditory cortex [J]. Hear Res, 2003, 175(1-2): 45-53.
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