Stimulus-timing-dependent modifications of rate-level functions in animals with and without tinnitus

Journal of Neurophysiology

Volumn 113, Issue 3, 2015, Pages 956-970

  Stefanescu, Roxana A ^a   Koehler, Seth D ^c   Shore, Susan E ^a,b  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c Johns Hopkins University   (United States)

Author keywords

Dorsal cochlear nucleus; Multisensory integration; Neural plasticity; Rate level functions; Tinnitus

Indexed keywords

AMPLITUDE MODULATION; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN FUNCTION; CONTROLLED STUDY; DORSAL COCHLEAR NUCLEUS; EVOKED AUDITORY RESPONSE; EVOKED BRAIN STEM RESPONSE; FEMALE; GUINEA PIG; IN VITRO STUDY; IN VIVO STUDY; LEARNING; NERVE CELL PLASTICITY; NOISE; NONHUMAN; PRIORITY JOURNAL; RATE LEVEL FUNCTION; SHAM PROCEDURE; SOUND; SPINDLE CELL; STIMULUS; TINNITUS; ANIMAL; AUDITORY EVOKED POTENTIAL; COCHLEAR NUCLEUS; CYTOLOGY; NERVE CELL; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; COCHLEAR NUCLEUS; EVOKED POTENTIALS, AUDITORY; FEMALE; GUINEA PIGS; NEURONAL PLASTICITY; NEURONS; NOISE; TINNITUS;

EID: 84922216807     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00457.2014     Document Type: Article

References (74)

1. Anari M, Axelsson A, Eliasson A, Magnusson L. Hypersensitivity to sound: questionnaire data, audiometry and classification. Scand Audiol 28: 219–230, 1999.
2. Bartnik G, Fabijanska A, Rogowski M. Our experience in treatment of patients with tinnitus and/or hyperacusis using the habituation method. In: Proceedings of the Sixth International Tinnitus Seminar. London: The Tinnitus and Hyperacusis Centre, 1999, p. 415–417.
3. Bauer CA, Turner JG, Caspary DM, Myers KS, Brozoski TJ. Tinnitus and inferior colliculus activity in chinchillas related to three distinct patterns of cochlear trauma. J Neurosci Res 86: 2564–2578, 2008.
4. Bell CC, Han VZ, Sugawara Y, Grant K. Synaptic plasticity in a cerebellum- like structure depends on temporal order. Nature 387: 278–281, 1997.
5. Brozoski TJ, Bauer CA, Caspary DM. Elevated fusiform cell activity in the dorsal cochlear nucleus of chinchillas with psychophysical evidence of tinnitus. J Neurosci 22: 2383–2390, 2002.
6. Cai S, Ma WL, Young ED. Encoding intensity in ventral cochlear nucleus following acoustic trauma: implications for loudness recruitment. J Assoc Res Otolaryngol 10: 5–22, 2009.
7. Campagnola L, Manis PB. A map of functional synaptic connectivity in the mouse anteroventral cochlear nucleus. J Neurosci 34: 2214–2230, 2014.
8. Chance FS, Abbott LF, Reyes AD. Gain modulation from background synaptic input. Neuron 35: 773–782, 2002.
9. Chen G, Lee C, Sandridge SA, Butler HM, Manzoor NF, Kaltenbach JA. Behavioral evidence for possible simultaneous induction of hyperacusis and tinnitus following intense sound exposure. J Assoc Res Otolaryngol 14: 413–424, 2013.
10. Cho KK, Khibnik L, Philpot BD, Bear MF. The ratio of NR2A/B NMDA receptor subunits determines the qualities of ocular dominance plasticity in visual cortex. Proc Natl Acad Sci USA 106: 5377–5382, 2009.
11. Dalton GL, Wu DC, Wang YT, Floresco SB, Phillips AG. NMDA GluN2A and GluN2B receptors play separate roles in the induction of LTP and LTD in the amygdala and in the acquisition and extinction of conditioned fear. Neuropharmacology 62: 797–806, 2012.
12. Daoudal G, Debanne D. Long-term plasticity of intrinsic excitability: learning rules and mechanisms. Learn Mem 10: 456–465, 2003.
13. Dauman R, Bouscau-Faure F. Assessment and amelioration of hyperacusis in tinnitus patients. Acta Otolaryngol (Stockh) 125: 503–509, 2005.
14. Davis KA, Young ED. Pharmacological evidence of inhibitory and disinhibitory neuronal circuits in dorsal cochlear nucleus. J Neurophysiol 83: 926–940, 2000.
15. de la Rocha J, Marchetti C, Schiff M, Reyes AD. Linking the response properties of cells in auditory cortex with network architecture: cotuning versus lateral inhibition. J Neurosci 28: 9151–9163, 2008.
16. Dean I, Harper NS, McAlpine D. Neural population coding of sound level adapts to stimulus statistics. Nat Neurosci 8: 1684–1689, 2005.
17. Debanne D, Poo MM. Spike-timing dependent plasticity beyond synapse–preand post-synaptic plasticity of intrinsic neuronal excitability. Front Synaptic Neurosci 2: 21, 2010.
18. Dehmel S, Eisinger D, Shore SE. Gap prepulse inhibition and auditory brainstem-evoked potentials as objective measures for tinnitus in guinea pigs. Front Syst Neurosci 6: 42, 2012a.
19. Dehmel S, Pradhan S, Koehler S, Bledsoe S, Shore S. Noise overexposure alters long-term somatosensory-auditory processing in the dorsal cochlear nucleus–possible basis for tinnitus-related hyperactivity? J Neurosci 32: 1660–1671, 2012b.
20. Ding J, Voigt HF. Intracellular response properties of units in the dorsal cochlear nucleus of unanesthetized decerebrate gerbil. J Neurophysiol 77: 2549–2572, 1997.
21. Doiron B, Zhao Y, Tzounopoulos T. Combined LTP and LTD of modulatory inputs controls neuronal processing of primary sensory inputs. J Neurosci 31: 10579–10592, 2011.
22. Evans EF, Nelson PG. The responses of single neurones in the cochlear nucleus of the cat as a function of their location and the anaesthetic state. Exp Brain Res 17: 402–427, 1973.
23. Gu JW, Halpin CF, Nam EC, Levine RA, Melcher JR. Tinnitus, diminished sound-level tolerance, and elevated auditory activity in humans with clinically normal hearing sensitivity. J Neurophysiol 104: 3361–3370, 2010.
24. Hebb DO. The Organization of Behavior. NewYork: Wiley & Sons, 1949.
25. Hebert S, Fournier P, Norena A. The auditory sensitivity is increased in tinnitus ears. J Neurosci 33: 2356–2364, 2013.
26. Jastreboff PJ, Jastreboff MM. Tinnitus retraining therapy (TRT) as a method for treatment of tinnitus and hyperacusis patients. J Am Acad Audiol 11: 162–177, 2000.
27. Kaltenbach JA, Zacharek MA, Zhang J, Frederick S. Activity in the dorsal cochlear nucleus of hamsters previously tested for tinnitus following intense tone exposure. Neurosci Lett 355: 121–125, 2004.
28. Kanold PO, Manis PB. A physiologically based model of discharge pattern regulation by transient K_ currents in cochlear nucleus pyramidal cells. J Neurophysiol 85: 523–538, 2001.
29. Kanold PO, Young ED. Proprioceptive information from the pinna provides somatosensory input to cat dorsal cochlear nucleus. J Neurosci 21: 7848–7858, 2001.
30. Koehler S, Shore S. Stimulus Timing-dependent plasticity in dorsal cochlear nucleus is altered in tinnitus. J Neurosci 33: 19647–19656, 2013a.
31. Koehler SD, Shore SE. Stimulus-timing dependent multisensory plasticity in the guinea pig dorsal cochlear nucleus. PLoS One 8: e59828, 2013b.
32. Li S, Choi V, Tzounopoulos T. Pathogenic plasticity of Kv7.2/3 channel activity is essential for the induction of tinnitus. Proc Natl Acad Sci USA 110: 9980–9985, 2013.
33. Magee JC, Johnston D. A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science 275: 209–213, 1997.
34. Marianowski R, Liao WH, Van Den Abbeele T, Fillit P, Herman P, Frachet B, Huy PT. Expression of NMDA, AMPA and GABA(A) receptor subunit mRNAs in the rat auditory brainstem. I. Influence of early auditory deprivation. Hear Res 150: 1–11, 2000.
35. Markram H, Lubke J, Frotscher M, Sakmann B. Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275: 213–215, 1997.
36. Moore JK, Osen KK. The cochlear nuclei in man. Am J Anat 154: 393–418, 1979.
37. Muller M, Robertson D, Yates GK. Rate-versus-level functions of primary auditory nerve fibres: evidence for square law behaviour of all fibre categories in the guinea pig. Hear Res 55: 50–56, 1991.
38. Norena AJ. An integrative model of tinnitus based on a central gain controlling neural sensitivity. Neurosci Biobehav Rev 35: 1089–1109, 2011.
39. Oertel D, Wright S, Cao XJ, Ferragamo M, Bal R. The multiple functions of T stellate/multipolar/chopper cells in the ventral cochlear nucleus. Hear Res 276: 61–69, 2011.
40. Paul AK, Lobarinas E, Simmons R, Wack D, Luisi JC, Spernyak J, Mazurchuk R, Abdel-Nabi H, Salvi R. Metabolic imaging of rat brain during pharmacologically-induced tinnitus. Neuroimage 44: 312–318, 2009.
41. Peng Y, Zhao J, Gu QH, Chen RQ, Xu Z, Yan JZ, Wang SH, Liu SY, Chen Z, Lu W. Distinct trafficking and expression mechanisms underlie LTP and LTD of NMDA receptor-mediated synaptic responses. Hippocampus 20: 646–658, 2010.
42. Pilati N, Ison MJ, Barker M, Mulheran M, Large CH, Forsythe ID, Matthias J, Hamann M. Mechanisms contributing to central excitability changes during hearing loss. Proc Natl Acad Sci USA 109: 8292–8297, 2012a.
43. Pilati N, Large C, Forsythe ID, Hamann M. Acoustic over-exposure triggers burst firing in dorsal cochlear nucleus fusiform cells. Hear Res 283: 98–106, 2012b.
44. Rhode WS, Roth GL, Recio-Spinoso A. Response properties of cochlear nucleus neurons in monkeys. Hear Res 259: 1–15, 2010.
45. Rhode WS, Smith PH, Oertel D. Physiological response properties of cells labeled intracellularly with horseradish peroxidase in cat dorsal cochlear nucleus. J Comp Neurol 213: 426–447, 1983.
46. Rubio ME, Gudsnuk KA, Smith Y, Ryugo DK. Revealing the molecular layer of the primate dorsal cochlear nucleus. Neuroscience 154: 99–113, 2008.
47. Sachs MB, Abbas PJ. Rate versus level functions for auditory-nerve fibers in cats: tone-burst stimuli. J Acoust Soc Am 56: 1835–1847, 1974.
48. Sato K, Shiraishi S, Nakagawa H, Kuriyama H, Altschuler RA. Diversity and plasticity in amino acid receptor subunits in the rat auditory brain stem. Hear Res 147: 137–144, 2000.
49. Schaette R, Kempter R. Computational models of neurophysiological correlates of tinnitus. Front Syst Neurosci 6: 34, 2012.
50. Shore SE. Multisensory integration in the dorsal cochlear nucleus: unit responses to acoustic and trigeminal ganglion stimulation. Eur J Neurosci 21: 3334–3348, 2005.
51. Shore SE, Koehler S, Oldakowski M, Hughes LF, Syed S. Dorsal cochlear nucleus responses to somatosensory stimulation are enhanced after noiseinduced hearing loss. Eur J Neurosci 27: 155–168, 2008.
52. Shore SE, Vass Z, Wys NL, Altschuler RA. Trigeminal ganglion innervates the auditory brainstem. J Comp Neurol 419: 271–285, 2000.
53. Stabler SE, Palmer AR, Winter IM. Temporal and mean rate discharge patterns of single units in the dorsal cochlear nucleus of the anesthetized guinea pig. J Neurophysiol 76: 1667–1688, 1996.
54. Suneja SK, Benson CG, Potashner SJ. Glycine receptors in adult guinea pig brain stem auditory nuclei: regulation after unilateral cochlear ablation. Exp Neurol 154: 473–488, 1998.
55. Turner JG, Brozoski TJ, Bauer CA, Parrish JL, Myers K, Hughes LF, Caspary DM. Gap detection deficits in rats with tinnitus: a potential novel screening tool. Behav Neurosci 120: 188–195, 2006.
56. Tzounopoulos T, Kim Y, Oertel D, Trussell LO. Cell-specific, spike timingdependent plasticities in the dorsal cochlear nucleus. Nat Neurosci 7: 719–725, 2004.
57. Tzounopoulos T, Rubio ME, Keen JE, Trussell LO. Coactivation of preand postsynaptic signaling mechanisms determines cell-specific spike-timing- dependent plasticity. Neuron 54: 291–301, 2007.
58. Wang H, Brozoski TJ, Turner JG, Ling L, Parrish JL, Hughes LF, Caspary DM. Plasticity at glycinergic synapses in dorsal cochlear nucleus of rats with behavioral evidence of tinnitus. Neuroscience 164: 747–759, 2009.
59. Watkins PV, Barbour DL. Level-tuned neurons in primary auditory cortex adapt differently to loud versus soft sounds. Cereb Cortex 21: 178–190, 2011a.
60. Watkins PV, Barbour DL. Rate-level responses in awake marmoset auditory cortex. Hear Res 275: 30–42, 2011b.
61. Whiting B, Moiseff A, Rubio ME. Cochlear nucleus neurons redistribute synaptic AMPA and glycine receptors in response to monaural conductive hearing loss. Neuroscience 163: 1264–1276, 2009.
62. Xu J, Kang N, Jiang L, Nedergaard M, Kang J. Activity-dependent long-term potentiation of intrinsic excitability in hippocampal CA1 pyramidal neurons. J Neurosci 25: 1750–1760, 2005.
63. Yang G, Lobarinas E, Zhang L, Turner J, Stolzberg D, Salvi R, Sun W. Salicylate induced tinnitus: behavioral measures and neural activity in auditory cortex of awake rats. Hear Res 226: 244–253, 2007.
64. Yates GK, Winter IM, Robertson D. Basilar membrane nonlinearity determines auditory nerve rate-intensity functions and cochlear dynamic range. Hear Res 45: 203–219, 1990.
65. Young ED. Identification of response properties of ascending axons from dorsal cochlear nucleus. Brain Res 200: 23–37, 1980.
66. Young ED, Brownell WE. Responses to tones and noise of single cells in dorsal cochlear nucleus of unanesthetized cats. J Neurophysiol 39: 282–300, 1976.
67. Zeng C, Nannapaneni N, Zhou J, Hughes LF, Shore S. Cochlear damage changes the distribution of vesicular glutamate transporters associated with auditory and nonauditory inputs to the cochlear nucleus. J Neurosci 29: 4210–4217, 2009.
68. Zeng C, Yang Z, Shreve L, Bledsoe S, Shore S. Somatosensory projections to cochlear nucleus are upregulated after unilateral deafness. J Neurosci 32: 15791–15801, 2012.
69. Zeng FG. An active loudness model suggesting tinnitus as increased central noise and hyperacusis as increased nonlinear gain. Hear Res 295: 172–179, 2013.
70. Zhan X, Ryugo DK. Projections of the lateral reticular nucleus to the cochlear nucleus in rats. J Comp Neurol 504: 583–598, 2007.
71. Zhang JS, Kaltenbach JA. Modulation of spontaneous activity by acetylcholine receptors in the rat dorsal cochlear nucleus in vivo. Hear Res 140: 7–17, 2000.
72. Zhao Y, Tzounopoulos T. Physiological activation of cholinergic inputs controls associative synaptic plasticity via modulation of endocannabinoid signaling. J Neurosci 31: 3158–3168, 2011.
73. Zhou J, Shore S. 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, 2004.
74. Zhou M, Tao HW, Zhang LI. Generation of intensity selectivity by differential synaptic tuning: fast-saturating excitation but slow-saturating inhibition. J Neurosci 32: 18068–18078, 2012.