Stimulus timing-dependent plasticity in dorsal cochlear nucleus is altered in tinnitus

Journal of Neuroscience

Volumn 33, Issue 50, 2013, Pages 19647-19656

  Koehler, Seth D ^a,b   Shore, Susan E ^a,b  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Bimodal; Cochlear damage; Noise damage; Plasticity; Somatosensory; Tinnitus

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; AUDITORY STIMULATION; AUDITORY THRESHOLD SHIFT; CONTROLLED STUDY; DORSAL COCHLEAR NUCLEUS; EVOKED BRAIN STEM AUDITORY RESPONSE; FEMALE; GUINEA PIG; HYPERACTIVITY; NERVE CELL PLASTICITY; NERVE CONDUCTION; NONHUMAN; PRIORITY JOURNAL; SOMATOSENSORY STIMULATION; SURGICAL APPROACH; TINNITUS;

BIMODAL; COCHLEAR DAMAGE; NOISE DAMAGE; PLASTICITY; SOMATOSENSORY; TINNITUS;

ACOUSTIC STIMULATION; ANIMALS; AUDITORY PERCEPTION; COCHLEAR NUCLEUS; DISEASE MODELS, ANIMAL; EVOKED POTENTIALS, AUDITORY, BRAIN STEM; GUINEA PIGS; NEURONAL PLASTICITY; NEURONS; TINNITUS;

EID: 84889775536     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2788-13.2013     Document Type: Article

References (55)

1. Aosaki T, Miura M, Suzuki T, Nishimura K, Masuda M (2010) Acetylcholine-dopamine balance hypothesis in the striatum: an update. Geriatr Gerontol Int 10 [Suppl 1]:S148-S157.
2. Basura GJ, Koehler SD, Shore SE (2012) Multi-sensory integration in brainstem and auditory cortex. Brain Res 1485:95-107. CrossRef Medline
3. Bauer CA, Turner JG, Caspary DM, Myers KS, Brozoski TJ (2008) Tinnitus and inferior colliculus activity in chinchillas related to three distinct patterns of cochlear trauma. J Neurosci Res 86:2564-2578. CrossRef Medline
4. Brozoski TJ, Bauer CA, CasparyDM (2002) Elevated fusiform cell activity in the dorsal cochlear nucleus of chinchillas with psychophysical evidence of tinnitus. J Neurosci 22:2383-2390. Medline
5. Brozoski TJ, Wisner KW, Sybert LT, Bauer CA (2012) Bilateral dorsal cochlear nucleus lesions prevent acoustic-trauma induced tinnitus in an animal model. J Assoc Res Otolaryngol 13:55-66. CrossRef Medline
6. Dahmen JC, Hartley DE, King AJ (2008) Stimulus timing-dependent plasticity of cortical frequency representation. J Neurosci 28:13629-13639. CrossRef Medline
7. Davis KA, Miller RL, Young ED (1996) Effects of somatosensory and parallel-fiber stimulation on neurons in dorsal cochlear nucleus. J Neurophysiol 76:3012-3024. Medline
8. Dehmel S, Eisinger D, Shore SE (2012a) Gap prepulse inhibition and auditory brainstem-evoked potentials as objective measures for tinnitus in guinea pigs. Front Syst Neurosci 6:42. CrossRef Medline
9. Dehmel S, Pradhan S, Koehler S, Bledsoe S, Shore S (2012b) Noise overexposure alters long-term somatosensory-auditory processing in the dorsal cochlear nucleus: possible basis for tinnitus-related hyperactivity? J Neurosci 32:1660-1671. CrossRef Medline
10. Doiron B, Zhao Y, Tzounopoulos T (2011) Combined LTP and LTD of modulatory inputs controls neuronal processing of primary sensory inputs. J Neurosci 31:10579-10592. CrossRef Medline
11. Engineer ND, Møller AR, Kilgard MP (2013) Directing neural plasticity to understand and treat tinnitus. Hear Res 295:58-66. CrossRef Medline
12. Gambino F, Holtmaat A (2012) Spike timing-dependent potentiation of sensory surround in the somatosensory cortex is facilitated by deprivation-mediated disinhibition. Neuron 75:490-502. CrossRef Medline
13. Garcia MM, Edward R, Brennan GB, Harlan RE (2000) Deafferentationinduced changes in protein kinase C expression in the rat cochlear nucleus. Hear Res 147:113-124. CrossRef Medline
14. Guo Y, Huang S, de Pasquale R, McGehrin K, Lee HK, Zhao K, Kirkwood A (2012) Dark exposure extends the integration window for spike timingdependent plasticity. J Neurosci 32:15027-15035. CrossRef Medline
15. Haenggeli CA, Pongstaporn T, Doucet JR, Ryugo DK (2005) Projections from the spinal trigeminal nucleus to the cochlear nucleus in the rat. J Comp Neurol 484:191-205. CrossRef Medline
16. Heller AJ (2003) Classification and epidemiology of tinnitus. Otolaryngol Clin North Am 36:239-248. CrossRef Medline
17. Jin YM, Godfrey DA, Wang J, Kaltenbach JA (2006) Effects of intense tone exposure on choline acetyltransferase activity in the hamster cochlear nucleus. Hear Res 216:168-175. CrossRef Medline
18. Kaltenbach JA, McCaslin DL (1996) Increases in spontaneous activity in the dorsal cochlear nucleus following exposure to high intensity sound: a possible neural correlate of tinnitus. Auditory Neurosci 3:57-78.
19. Kaltenbach JA, Zacharek MA, Zhang J, Frederick S (2004) Activity in the dorsal cochlear nucleus of hamsters previously tested for tinnitus following intense tone exposure. Neurosci Lett 355:121-125. CrossRef Medline
20. Kanold PO, Young ED (2001) Proprioceptive information from the pinna provides somatosensory input to cat dorsal cochlear nucleus. J Neurosci 21:7848-7858. Medline
21. Kanold PO, Davis KA, Young ED (2011) Somatosensory context alters auditory responses in the cochlear nucleus. J Neurophysiol 105:1063-1070. CrossRef Medline
22. Koehler SD, Shore SE (2013) Stimulus timing-dependent multisensory plasticity in the guinea pig dorsal cochlear nucleus. PLoS One 8:e59828. CrossRef Medline
23. Koehler SD, Pradhan S, Manis PB, Shore SE (2011) Somatosensory inputs modify auditory spike timing in dorsal cochlear nucleus principal cells. Eur J Neurosci 33:409-420. CrossRef Medline
24. Komiya H, Eggermont JJ (2000) Spontaneous firing activity of cortical neurons in adult cats with reorganized tonotopic map following pure-tone trauma. Acta Otolaryngol 120:750-756. CrossRef Medline
25. Kujawa SG, Liberman MC (2009) Adding insult to injury: cochlear nerve degeneration after "temporary" noise-induced hearing loss. J Neurosci 29:14077-14085. CrossRef Medline
26. Levine RA (1999) Somatic (craniocervical) tinnitus and the dorsal cochlear nucleus hypothesis. Am J Otolaryngol 20:351-362. CrossRef Medline
27. Lindblad AC, Hagerman B, Rosenhall U (2011) Noise-induced tinnitus: a comparison between four clinical groups without apparent hearing loss. Noise Health 13:423-431. CrossRef Medline
28. Ma WL, Young ED (2006) Dorsal cochlear nucleus response properties following acoustic trauma: response maps and spontaneous activity. Hear Res 216:176-188. CrossRef Medline
29. Masquelier T, Guyonneau R, Thorpe SJ (2008) Spike timing dependent plasticity finds the start of repeating patterns in continuous spike trains. PLoS One 3:e1377. Medline
30. Meredith RM, Mansvelder HD (2010) STDP and mental retardation: dysregulation of dendritic excitability in fragile X syndrome. Front Synaptic Neurosci 2:10. CrossRef Medline
31. Mühlnickel W, Elbert T, Taub E, Flor H (1998) Reorganization of auditory cortex in tinnitus. Proc Natl Acad Sci U S A 95:10340-10343. CrossRef Medline
32. Pawlak V, Wickens JR, Kirkwood A, Kerr JN (2010) Timing is not everything: neuromodulation opens the STDP gate. Front Synaptic Neurosci 2:146. CrossRef Medline
33. Pilati N, Ison MJ, Barker M, Mulheran M, Large CH, Forsythe ID, Matthias J, Hamann M (2012) Mechanisms contributing to central excitability changes during hearing loss. Proc Natl Acad Sci U S A 109:8292-8297. CrossRef Medline
34. Pinchoff RJ, Burkard RF, Salvi RJ, Coad ML, Lockwood AH (1998) Modulation of tinnitus by voluntary jaw movements. Am J Otol 19:785-789. Medline
35. Roberts PD, Portfors CV (2008) Design principles of sensory processing in cerebellum-like structures: early stage processing of electrosensory and auditory objects. Biol Cybern 98:491-507. CrossRef Medline
36. Sanchez TG, da Silva Lima A, Brandão AL, Lorenzi MC, Bento RF (2007) Somatic modulation of tinnitus: test reliability and results after repetitive muscle contraction training. Ann Otol Rhinol Laryngol 116:30-35. Medline
37. Sato K, Shiraishi S, Nakagawa H, Kuriyama H, Altschuler RA (2000) Diversity and plasticity in amino acid receptor subunits in the rat auditory brain stem. Hear Res 147:137-144. CrossRef Medline
38. Sawtell NB (2010) Multimodal integration in granule cells as a basis for associative plasticity and sensory prediction in a cerebellum-like circuit. Neuron 66:573-584. CrossRef Medline
39. Shore SE (2005) Multisensory integration in the dorsal cochlear nucleus: unit responses to acoustic and trigeminal ganglion stimulation. Eur J Neurosci 21:3334-3348. CrossRef Medline
40. Shore SE, Koehler S, Oldakowski M, Hughes LF, Syed S (2008) Dorsal cochlear nucleus responses to somatosensory stimulation are enhanced after noise-induced hearing loss. Eur J Neurosci 27:155-168. CrossRef Medline
41. Suneja SK, Benson CG, Potashner SJ (1998a) Glycine receptors in adult guinea pig brain stem auditory nuclei: regulation after unilateral cochlear ablation. Exp Neurol 154:473-488. CrossRef Medline
42. Suneja SK, Potashner SJ, Benson CG (1998b) Plastic changes in glycine and GABA release and uptake in adult brain stem auditory nuclei after unilateral middle ear ossicle removal and cochlear ablation. Exp Neurol 151: 273-288. CrossRef Medline
43. Turner JG, Brozoski TJ, Bauer CA, Parrish JL, Myers K, Hughes LF, Caspary DM (2006) Gap detection deficits in rats with tinnitus: a potential novel screening tool. Behav Neurosci 120:188-195. CrossRef Medline
44. Turner J, Larsen D, Hughes L, Moechars D, Shore S (2012) Time course of tinnitus development following noise exposure in mice. J Neurosci Res 90:1480-1488. CrossRef Medline
45. Tzounopoulos T, Kim Y, Oertel D, Trussell LO (2004) Cell-specific, spike timing-dependent plasticities in the dorsal cochlear nucleus. Nat Neurosci 7:719-725. CrossRef Medline
46. Tzounopoulos T, Rubio ME, Keen JE, Trussell LO (2007) Coactivation of pre-and postsynaptic signaling mechanisms determines cell-specific spike timing-dependent plasticity. Neuron 54:291-301. CrossRef Medline
47. Wang H, Brozoski TJ, Turner JG, Ling L, Parrish JL, Hughes LF, CasparyDM (2009) Plasticity at glycinergic synapses in dorsal cochlear nucleus of rats with behavioral evidence of tinnitus. Neuroscience 164:747-759. CrossRef Medline
48. Young ED, Nelken I, Conley RA (1995) Somatosensory effects on neurons in dorsal cochlear nucleus. J Neurophysiol 73:743-765. Medline
49. Zeng C, Nannapaneni N, Zhou J, Hughes LF, Shore S (2009) Cochlear damage changes the distribution of vesicular glutamate transporters associated with auditory and nonauditory inputs to the cochlear nucleus. J Neurosci 29:4210-4217. CrossRef Medline
50. Zeng C, Yang Z, Shreve L, Bledsoe S, Shore S (2012) Somatosensory projections to cochlear nucleus are upregulated after unilateral deafness. J Neurosci 32:15791-15801. CrossRef Medline
51. Zhang J, Guan Z (2008) Modulatory effects of somatosensory electrical stimulation on neural activity of the dorsal cochlear nucleus of hamsters. J Neurosci Res 86:1178-1187. CrossRef Medline
52. Zhang JS, Kaltenbach JA (2000) Modulation of spontaneous activity by acetylcholine receptors in the rat dorsal cochlear nucleus in vivo. Hear Res 140:7-17. CrossRef Medline
53. Zhao Y, Tzounopoulos T (2011) Physiological activation of cholinergic inputs controls associative synaptic plasticity via modulation of endocannabinoid signaling. J Neurosci 31:3158-3168. CrossRef Medline
54. Zhou J, Shore S (2004) 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. CrossRef Medline
55. Zhou J, Nannapaneni N, Shore S (2007) Vessicular glutamate transporters 1 and 2 are differentially associated with auditory nerve and spinal trigeminal inputs to the cochlear nucleus. J Comp Neurol 500:777-787. CrossRef Medline