Immediate and delayed cochlear neuropathy after noise exposure in pubescent mice

PLoS ONE

Volumn 10, Issue 5, 2015, Pages

  Jensen, Jane Bjerg ^a,b,c   Lysaght, Andrew C ^a,b,c   Liberman, M Charles ^a,b,c   Qvortrup, Klaus ^d   Stankovic, Konstantina M ^a,b,c  

^a MASSACHUSETTS EYE AND EAR INFIRMARY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

AMPLITUDE MODULATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUDITORY THRESHOLD SHIFT; CELL BODY; COCHLEAR NERVE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DELAYED COCHLEAR SYNAPTOPATHY; EVOKED BRAIN STEM AUDITORY RESPONSE; IMMEDIATE COCHLEAR SYNAPTOPATHY; LONG TERM EXPOSURE; MALE; MOUSE; NERVE CELL; NERVE DEGENERATION; NERVE FIBER; NEUROPATHY; NOISE; NONHUMAN; PUBERTY; SOUND PRESSURE; AGE; ANIMAL; AUDITORY THRESHOLD; CBA MOUSE; COCHLEA; NOISE INJURY; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SEXUAL MATURATION; SPIRAL GANGLION; SYNAPSE; TIME FACTOR;

AGE FACTORS; ANIMALS; AUDITORY THRESHOLD; COCHLEA; COCHLEAR NERVE; EVOKED POTENTIALS, AUDITORY, BRAIN STEM; HEARING LOSS, NOISE-INDUCED; MALE; MICE; MICE, INBRED CBA; NOISE; SEXUAL MATURATION; SPIRAL GANGLION; SYNAPSES; TIME FACTORS;

EID: 84957582513     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0125160     Document Type: Article

References (66)

1. Leigh J, Macaskill P, Kuosma E, Mandryk J (1999) Global burden of disease and injury due to occupational factors. Epidemiology 10: 626-631. PMID: 10468442
2. Kujawa SG, Liberman MC (2009) Adding insult to injury: Cochlear nerve degeneration after "temporary" noise-induced hearing loss. J Neurosci 29: 14077-14085. doi: 10.1523/JNEUROSCI.2845-09.2009 PMID: 19906956
3. Lin HW, Furman AC, Kujawa SG, Liberman MC (2011) Primary neural degeneration in the Guinea pig cochlea after reversible noise-induced threshold shift. J Assoc Res Otolaryngol 12: 605-616. doi: 10. 1007/s10162-011-0277-0 PMID: 21688060
4. Robertson D (1982) Effects of acoustic trauma on stereocilia structure and spiral ganglion cell tuning properties in the guinea pig cochlea. Hear Res 7: 55-74. PMID: 7096217
5. Liberman MC, Dodds LW (1984) Single-neuron labeling and chronic cochlear pathology. III. Stereocilia damage and alterations of threshold tuning curves. Hear Res 16: 55-74. PMID: 6511673
6. Wang Y, Hirose K, Liberman MC (2002) Dynamics of noise-induced cellular injury and repair in the mouse cochlea. J Assoc Res Otolaryngol 3: 248-268. PMID: 12382101
7. Liberman MC, Kujawa SG (2014) Hot Topics-Hidden hearing loss: Permanent cochlear-nerve degeneration after temporary noise-induced threshold shift. J Acoust Soc Am 135: 2311.
8. Furman AC, Kujawa SG, Liberman MC (2013) Noise-induced cochlear neuropathy is selective for fibers with low spontaneous rates. J Neurophysiol 110: 577-586. doi: 10.1152/jn.00164.2013 PMID: 23596328
9. Han SK, Gottsch ML, Lee KJ, Popa SM, Smith JT, Jakawich SK, et al. (2005) Activation of gonadotropin- releasing hormone neurons by kisspeptin as a neuroendocrine switch for the onset of puberty. J Neurosci 25: 11349-11356. PMID: 16339030
10. Henry KR (1984) Noise and the young mouse: Genotype modifies the sensitive period for effects on cochlear physiology and audiogenic seizures. Behav Neurosci 98: 1073-1082. PMID: 6508912
11. Ohlemiller KK, Wright JS, Heidbreder AF (2000) Vulnerability to noise-induced hearing loss in 'middleaged' and young adult mice: A dose-response approach in CBA, C57BL, and BALB inbred strains. Hear Res 149: 239-247. PMID: 11033262
12. Kujawa SG, Liberman MC (2006) Acceleration of age-related hearing loss by early noise exposure: Evidence of a misspent youth. J Neurosci 26: 2115-2123. PMID: 16481444
13. Henry KR (1982) Influence of genotype and age on noise-induced auditory losses. Behav Genet 12: 563-573. PMID: 7183323
14. Falk SA, Cook RO, Haseman JK, Sanders GM (1974) Noise-induced inner ear damage in newborn and adult guinea pigs. Laryngoscope 84: 444-453. PMID: 4592286
15. Price GR (1976) Age as a factor in susceptibility to hearing loss: Young versus adult ears. J Acoust Soc Am 60: 886-892. PMID: 993475
16. Saunders JC, Chen CS (1982) Sensitive periods of susceptibility to auditory trauma in mammals. Environ Health Perspect 44: 63-66. PMID: 7044777
17. Morata TC (2007) Young people: Their noise and music exposures and the risk of hearing loss. Int J Audiol 46: 111-112. PMID: 17365063
18. Henry KR, Chole RA (1980) Genotypic differences in behavioral, physiological and anatomical expressions of age-related hearing loss in the laboratory mouse. Audiology 19: 369-383. PMID: 7436856
19. Khimich D, Nouvian R, Pujol R, Tom Dieck S, Egner A, Gundelfinger ED, et al. (2005) Hair cell synaptic ribbons are essential for synchronous auditory signalling. Nature 434: 889-894. PMID: 15829963
20. Larsen JO (1998) Stereology of nerve cross sections. J Neurosci Methods 85: 107-118. PMID: 9874147
21. West MJ, Slomianka L, Gundersen HJ (1991) Unbiased stereological estimation of the total number of neurons in thesubdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231: 482-497. PMID: 1793176
22. Sergeyenko Y, Lall K, Liberman MC, Kujawa SG (2013) Age-related cochlear synaptopathy: An earlyonset contributor to auditory functional decline. J Neurosci 33: 13686-13694. doi: 10.1523/ JNEUROSCI.1783-13.2013 PMID: 23966690
23. Varghese GI, Zhu X, Frisina RD (2005) Age-related declines in distortion product otoacoustic emissions utilizing pure tone contralateral stimulation in CBA/CaJ mice. Hear Res 209: 60-67. PMID: 16061336
24. Parham K, Sun XM, Kim DO (1999) Distortion product otoacoustic emissions in the CBA/J mouse model of presbycusis. Hear Res 134: 29-38. PMID: 10452373
25. Meyer AC, Frank T, Khimich D, Hoch G, Riedel D, Chapochnikov NM, et al. (2009) Tuning of synapse number, structure and function in the cochlea. Nat Neurosci 12: 444-453. doi: 10.1038/nn.2293 PMID: 19270686
26. Zhang SY, Robertson D, Yates G, Everett A (1999) Role of L-type Ca(2+) channels in transmitter release from mammalian inner hair cells I. Gross sound-evoked potentials. J Neurophysiol 82: 3307-3315. PMID: 10601462
27. Skinner LJ, Enee V, Beurg M, Jung HH, Ryan AF, Hafidi A, et al. (2003) Contribution of BK Ca2+-activated K+ channels to auditory neurotransmission in the Guinea pig cochlea. J Neurophysiol 90: 320-332. PMID: 12611976
28. Subramanian J, Morozov A (2011) Erk1/2 inhibit synaptic vesicle exocytosis through L-type calcium channels. J Neurosci 31: 4755-4764. doi: 10.1523/JNEUROSCI.6594-10.2011 PMID: 21430174
29. Moser T, Neef A, Khimich D (2006) Mechanisms underlying the temporal precision of sound coding at the inner hair cell ribbon synapse. J Physiol 576: 55-62. PMID: 16901948
30. Glowatzki E, Fuchs PA (2002) Transmitter release at the hair cell ribbon synapse. Nat Neurosci 5: 147-154. PMID: 11802170
31. Goutman JD, Glowatzki E (2007) Time course and calcium dependence of transmitter release at a single ribbon synapse. Proc Natl Acad Sci U S A 104: 16341-16346. PMID: 17911259
32. Brandt A, Khimich D, Moser T (2005) Few CaV1.3 channels regulate the exocytosis of a synaptic vesicle at the hair cell ribbon synapse. J Neurosci 25: 11577-11585. PMID: 16354915
33. Liberman MC (1980) Morphological differences among radial afferent fibers in the cat cochlea: An electron- microscopic study of serial sections. Hear Res 3: 45-63. PMID: 7400048
34. Liberman MC, Dodds LW, Pierce S (1990) Afferent and efferent innervation of the cat cochlea: Quantitative analysis with light and electron microscopy. J Comp Neurol 301: 443-460. PMID: 2262601
35. Le Prell CG, Dell S, Hensley B, Hall JW 3rd, Campbell KC, Antonelli PJ, et al. (2012) Digital music exposure reliably induces temporary threshold shift in normal-hearing human subjects. Ear Hear 33: E44- 58. doi: 10.1097/AUD.0b013e31825f9d89 PMID: 22885407
36. Puel JL, Ruel J, Gervais d'Aldin C, Pujol R (1998) Excitotoxicity and repair of cochlear synapses after noise-trauma induced hearing loss. Neuroreport 9: 2109-2114. PMID: 9674603
37. Pujol R, Puel JL, Gervais d'Aldin C, Eybalin M (1993) Pathophysiology of the glutamatergic synapses in the cochlea. Acta Otolaryngol 113: 330-334. PMID: 8100108
38. Spoendlin H (1971) Primary structural changes in the organ of Corti after acoustic overstimulation. Acta Otolaryngol 71: 166-176. PMID: 5577011
39. Robertson D (1983) Functional significance of dendritic swelling after loud sounds in the guinea pig cochlea. Hear Res 9: 263-278. PMID: 6841283
40. Pujol R, Lenoir M, Robertson D, Eybalin M, Johnstone BM (1985) Kainic acid selectively alters auditory dendrites connected with cochlear inner hair cells. Hear Res 18: 145-151. PMID: 2864329
41. Puel JL, Pujol R, Ladrech S, Eybalin M (1991) Alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid electrophysiological and neurotoxic effects in the guinea-pig cochlea. Neuroscience 45: 63-72. PMID: 1684414
42. Puel JL, Pujol R, Tribillac F, Ladrech S, Eybalin M (1994) Excitatory amino acid antagonists protect cochlear auditory neurons from excitotoxicity. J Comp Neurol 341: 241-256. PMID: 7512999
43. Castellano-Munoz M, Ricci AJ (2014) Role of intracellular calcium stores in hair-cell ribbon synapse. Front Cell Neurosci 8: 162. doi: 10.3389/fncel.2014.00162 PMID: 24971053
44. Choi DW (1987) Ionic dependence of glutamate neurotoxicity. J Neurosci 7: 369-379. PMID: 2880938
45. Randall RD, Thayer SA (1992) Glutamate-induced calcium transient triggers delayed calcium overload and neurotoxicity in rat hippocampal neurons. J Neurosci 12: 1882-1895. PMID: 1349638
46. Stamataki S, Francis HW, Lehar M, May BJ, Ryugo DK (2006) Synaptic alterations at inner hair cells precede spiral ganglion cell loss in aging C57BL/6J mice. Hear Res 221: 104-118. PMID: 17005343
47. Merchan-Perez A, Liberman MC (1996) Ultrastructural differences among afferent synapses on cochlear hair cells: Correlations with spontaneous discharge rate. J Comp Neurol 371: 208-221. PMID: 8835727
48. Cho Y, Gong TW, Kanicki A, Altschuler RA, Lomax MI (2004) Noise overstimulation induces immediate early genes in the rat cochlea. Brain Res Mol Brain Res 130: 134-148. PMID: 15519684
49. Han Y, Hong L, Zhong C, Chen Y, Wang Y, Mao X, et al. (2012) Identification of new altered genes in rat cochleae with noise-induced hearing loss. Gene 499: 318-322. doi: 10.1016/j.gene.2012.02.042 PMID: 22426293
50. Patel M, Hu Z, Bard J, Jamison J, Cai Q, Hu BH, et al. (2013) Transcriptome characterization by RNASeq reveals the involvement of the complement components in noise-traumatized rat cochleae. Neuroscience 248C: 1-16.
51. Hickox AE, Liberman MC (2014) Is noise-induced cochlear neuropathy key to the generation of hyperacusis or tinnitus? J Neurophysiol 111: 552-564. doi: 10.1152/jn.00184.2013 PMID: 24198321
52. Puel JL, Saffiedine S, Gervais d'Aldin C, Eybalin M, Pujol R (1995) Synaptic regeneration and functional recovery after excitotoxic injury in the guinea pig cochlea. C R Acad Sci III 318: 67-75. PMID: 7538893
53. Chen Z, Peppi M, Kujawa SG, Sewell WF (2009) Regulated expression of surface AMPA receptors reduces excitotoxicity in auditory neurons. J Neurophysiol 102: 1152-1159. doi: 10.1152/jn.00288.2009 PMID: 19515954
54. Gates GA, Schmid P, Kujawa SG, Nam B, D'Agostino R (2000) Longitudinal threshold changes in older men with audiometric notches. Hear Res 141: 220-228. PMID: 10713509
55. Nadol JB Jr (1990) Degeneration of cochlear neurons as seen in the spiral ganglion of man. Hear Res 49: 141-154. PMID: 2292494
56. Ota CY, Kimura RS (1980) Ultrastructural study of the human spiral ganglion. Acta Otolaryngol 89: 53-62. PMID: 7405577
57. Rattay F, Potrusil T, Wenger C, Wise AK, Glueckert R, Schrott-Fischer A, et al. (2013) Impact of morphometry, myelinization and synaptic current strength on spike conduction in human and cat spiral ganglion neurons. PLoS One 8: E79256. doi: 10.1371/journal.pone.0079256 PMID: 24260179
58. Stamper GC, Johnson TA (2015) Auditory function in normal-hearing, noise-exposed human ears. Ear Hear 36: 172-184. doi: 10.1097/AUD.0000000000000107 PMID: 25350405
59. Schaette R, McAlpine D (2011) Tinnitus with a normal audiogram: Physiological evidence for hidden hearing loss and computational model. J Neurosci 31: 13452-13457. doi: 10.1523/JNEUROSCI.2156- 11.2011 PMID: 21940438
60. Gu JW, Herrmann BS, Levine RA, Melcher JR (2012) Brainstem auditory evoked potentials suggest a role for the ventral cochlear nucleus in tinnitus. J Assoc Res Otolaryngol 13: 819-833. doi: 10.1007/ s10162-012-0344-1 PMID: 22869301
61. Epp B, Hots J, Verhey JL, Schaette R (2012) Increased intensity discrimination thresholds in tinnitus subjects with a normal audiogram. J Acoust Soc Am 132: EL196-201. doi: 10.1121/1.4740462 PMID: 22979832
62. Konrad-Martin D, Dille MF, McMillan G, Griest S, McDermott D, Fausti SA, et al. (2012) Age-related changes in the auditory brainstem response. J Am Acad Audiol 23: 18-35; quiz 74-15. doi: 10.3766/ jaaa.23.1.3 PMID: 22284838
63. Yang X, Pu Y, Hsieh CL, Ong CA, Psaltis D, Stankovic KM, et al. (2013) Two-photon microscopy of the mouse cochlea in situ for cellular diagnosis. J Biomed Opt 18: 31104. doi: 10.1117/1.JBO.18.3.031104 PMID: 23165736
64. Plack CJ, Barker D, Prendergast G (2014) Perceptual consequences of "hidden" hearing loss. Trends Hear 18. doi: 10.1177/2331216514560442 PMID: 25492094
65. Verbeek JH, Kateman E, Morata TC, Dreschler WA, Mischke C (2012) Interventions to prevent occupational noise-induced hearing loss. Cochrane Database Syst Rev 10: CD006396.
66. Portnuff CD, Fligor BJ, Arehart KH (2011) Teenage use of portable listening devices: A hazard to hearing? J Am Acad Audiol 22: 663-677. doi: 10.3766/jaaa.22.10.5 PMID: 22212766