Aging after noise exposure: Acceleration of cochlear synaptopathy in “recovered” ears

Journal of Neuroscience

Volumn 35, Issue 19, 2015, Pages 7509-7520

  Fernandez, Katharine A ^a,b   Jeffers, Penelope W C ^b   Lall, Kumud ^a,b   Liberman, M Charles ^a,b   Kujawa, Sharon G ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS EYE AND EAR INFIRMARY   (United States)

Author keywords

Age related hearing loss; Auditory nerve; Cochlear neuropathy; Cochlear synaptopathy; Noise induced hearing loss; Temporary threshold shift

Indexed keywords

ADULT; AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUDITORY STIMULATION; AUDITORY THRESHOLD; CELL COUNT; CELL LOSS; COCHLEAR SYNAPTOPATHY; CONTROLLED STUDY; EVOKED BRAIN STEM AUDITORY RESPONSE; FREQUENCY MODULATION; HAIR CELL; HEARING IMPAIRMENT; HISTOLOGY; IMAGE PROCESSING; INNER EAR DISEASE; MALE; MOUSE; NONHUMAN; OTOACOUSTIC EMISSION; PRIORITY JOURNAL; SPIRAL GANGLION; SYNAPTIC TRANSMISSION; ADVERSE EFFECTS; ANIMAL; CBA MOUSE; CELL DEATH; COCHLEA; COCHLEAR HAIR CELL; CYTOLOGY; METABOLISM; NOISE; NOISE INJURY; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SPONTANEOUS OTOACOUSTIC EMISSION; SYNAPSE; TIME FACTOR; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE; WAKEFULNESS;

AMPA RECEPTOR; CTBP2 PROTEIN, MOUSE; DNA BINDING PROTEIN; GLUTAMATE RECEPTOR IONOTROPIC, AMPA 2; PHOSPHOPROTEIN;

ACOUSTIC STIMULATION; AGING; ANIMALS; AUDITORY THRESHOLD; CELL DEATH; COCHLEA; DNA-BINDING PROTEINS; EVOKED POTENTIALS, AUDITORY, BRAIN STEM; HAIR CELLS, AUDITORY; HEARING LOSS, NOISE-INDUCED; MICE; MICE, INBRED CBA; MICROSCOPY, ELECTRON, TRANSMISSION; NOISE; OTOACOUSTIC EMISSIONS, SPONTANEOUS; PHOSPHOPROTEINS; RECEPTORS, AMPA; SPIRAL GANGLION; SYNAPSES; TIME FACTORS; WAKEFULNESS;

EID: 84929353520     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5138-14.2015     Document Type: Article

References (54)

1. ACOEM Task Force on Occupational Hearing Loss, Kirchner DB, Evenson E, Dobie RA, Rabinowitz P, Crawford J, Kopke R, Hudson TW (2012) Occupational noise-induced hearing loss: ACOEM Task Force on Occupational Hearing Loss. J Occup Environ Med 54:106-108. CrossRef Medline
2. Bharadwaj HM, Verhulst S, Shaheen L, Liberman MC, Shinn-Cunningham BG (2014) Cochlear neuropathy and the coding of supra-threshold sound. Front Syst Neurosci 8:26. Medline
3. Bohne BA, Harding GW (2000) Degeneration in the cochlea after noise damage: primary versus secondary events. Am J Otol 21:505-509. Medline
4. Bourien J, Tang Y, Batrel C, Huet A, Lenoir M, Ladrech S, Desmadryl G, Nouvian R, Puel JL, Wang J (2014) Contribution of auditory nerve fibers to compound action potential of the auditory nerve. J Neurophysiol 112:1025-1039. CrossRef Medline
5. Canlon B, Meltser I, Johnsson P, Tahera Y (2007) Glucocorticoid receptors modulate auditory sensitivity to acoustic trauma. Hear Res 226(1-2): 61-69.
6. Chen Z, Kujawa SG, Sewell WF (2007) Auditory sensitivity regulation via rapid changes in expression of surface AMPA receptors. Nat Neurosci 10:1238-1240. CrossRef Medline
7. 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. CrossRef Medline
8. Cruickshanks KJ, Nondahl DM, Tweed TS, Wiley TL, Klein BE, Klein R, Chappell R, Dalton DS, Nash SD (2010) Education, occupation, noise exposure history and the 10-yr cumulative incidence of hearing impairment in older adults. Hear Res 264(1-2):3-9.
9. Furman AC, Kujawa SG, Liberman MC (2013) Noise-induced cochlear neuropathy is selective for fibers with low spontaneous rates. J Neurophysiol 110:577-586. CrossRef Medline
10. Furness DN, Lawton DM (2003) Comparative distribution of glutamate transporters and receptors in relation to afferent innervation density in the mammalian cochlea. J Neurosci 23:11296-11304. Medline
11. Gates GA, Schmid P, Kujawa SG, Nam B, D’Agostino R (2000) Longitudinal threshold changes in people with audiometric notches. Hear Res 141: 220-228. CrossRef Medline
12. Grant L, Yi E, Glowatzki E (2010) Two modes of release shape the postsynaptic response at the inner hair cell ribbon synapse. J Neurosci 30:4210-4220. CrossRef Medline
13. Grose JH, Hall JW 3rd, Buss E (2006) Temporal processing deficits in the pre-senescent auditory system. J Acoust Soc Am 119:2305-2315. CrossRef Medline
14. Institute of Medicine (2005) Noise and military service: implications for hearing loss and tinnitus (Humes L, Joellenbeck L, Durch J, eds). Washington, DC: National Academies.
15. Khimich D, Nouvian R, Pujol R, Tom Dieck S, Egner A, Gundelfinger ED, Moser T (2005) Hair cell synaptic ribbons are essential for synchronous auditory signalling. Nature 434:889-894. CrossRef Medline
16. Knipper M, Van Dijk P, Nunes I, Rüttiger L, Zimmermann U (2013) Advances in the neurobiology of hearing disorders: recent developments regarding the basis of tinnitus and hyperacusis. Prog Neurobiol 111:17-33. CrossRef Medline
17. 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. CrossRef Medline
18. 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
19. Lee FS, Matthews LJ, Dubno JR, Mills JH (2005) Longitudinal study of pure-tone thresholds in older persons. Ear Hear 26:1-11. Medline
20. Liberman LD, Wang H, Liberman MC (2011) Opposing gradients of ribbon size and AMPA receptor expression underlie sensitivity differences among cochlear-nerve/hair-cell synapses. J Neurosci 31:801-808. CrossRef Medline
21. Liberman MC (1978) Auditory-nerve response from cats raised in a low-noise chamber. J Acoust Soc Am 63:442-455. CrossRef Medline
22. 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. CrossRef Medline
23. Liberman MC (1982) Single-neuron labeling in the cat auditory nerve. Science 216:1239-1241. CrossRef Medline
24. Liberman MC, Kiang NY (1978) Acoustic trauma in cats: cochlear pathology and auditory-nerve activity. Acta Otolaryngol Suppl 358:1-63. Medline
25. 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. CrossRef Medline
26. Liberman MC, Chesney CP, Kujawa SG (1997) Effects of selective inner hair cell loss on DPOAEs in carboplatin-treated chinchillas. Auditory Neuroscience 3:255-268.
27. 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. CrossRef Medline
28. Lobarinas E, Salvi R, Ding D (2013) Insensitivity of the audiogram to carboplatin induced inner hair cell loss in chinchillas. Hear Res 302:113-120. CrossRef Medline
29. Makary CA, Shin J, Kujawa SG, Liberman MC, Merchant SN (2011) Age-related primary cochlear neuronal degeneration in human temporal bones. J Assoc Res Otolaryngol 12:711-717. CrossRef Medline
30. Matsubara A, Laake JH, Davanger S, Usami S, Ottersen OP (1996) Organization of AMPA receptor subunits at a glutamate synapse: a quantitative immunogold analysis of hair cell synapses in the rat organ of Corti. J Neurosci 16:4457-4467. Medline
31. Meyer AC, Frank T, Khimich D, Hoch G, Riedel D, ChapochnikovNM, Yarin YM, Harke B, Hell SW, Egner A, Moser T (2009) Tuning of synapse number, structure and function in the cochlea. Nat Neurosci 12:444-453. CrossRef Medline
32. Müller M, von Hünerbein K, Hoidis S, Smolders JW (2005) A physiological place-frequency map of the cochlea in the CBA/J mouse. Hear Res 202: 63-73. CrossRef Medline
33. National Institute for Occupational Safety and Health (1998) Criteria for a recommended standard: occupational noise exposure, revised criteria 1998. U.S. Department of Health and Human Services, Centers for Disease Control and Prevention, National Institute for Occupational Safety and Health Publication No. 98-126. Cincinnati: NIOSH.
34. National Institute for Occupational Safety and Health (2013) Noise and hearing loss prevention. Available from: http://www.cdc.gov/niosh/ topics/noise/stats.html. Accessed Oct. 28, 2014.
35. Occupational Safety and Health Association (1981) Occupational noise exposure: hearing conservation amendment. U.S. Department of Labor, Occupational Safety and Health Administration Publication 46 Fed. Reg. 4078-4179. Washington, DC: U.S. Department of Labor.
36. Peppi M, Kujawa SG, Sewell WF (2011) A corticosteroid-responsive transcription factor, promyelocytic leukemia zinc finger protein, mediates protection of the cochlea from acoustic trauma. J Neurosci 31:735-741. CrossRef Medline
37. Plack CJ, Barker D, Prendergast G (2014) Perceptual consequences of “hidden” hearing loss. Trends Hear 18:pii:2331216514550621. CrossRef Medline
38. Pujol R, Puel JL, Gervais d’Aldin C, Eybalin M (1993) Pathophysiology of the glutamatergic synapses in the cochlea. Acta Otolaryngol 113:330-334. Medline
39. Rabinowitz PM (2012) The public health significance of noise-induced hearing loss. In: Noise-induced hearing loss: scientific advances (Le Prell CG, Henderson D, Fay RR, Popper AN, eds), pp 13-25. New York: Springer.
40. Robertson D (1983) Functional significance of dendritic swelling after loud sounds in the guinea pig cochlea. Hear Res 9:263-278. CrossRef Medline
41. Robertson D, Johnstone BM (1980) Acoustic trauma in the guinea pig cochlea: early changes in ultrastructure and neural threshold. Hear Res 3:167-179. CrossRef Medline
42. Rosenhall U (2003) The influence of ageing on noise-induced hearing loss. Noise Health 5:47-53. Medline
43. Ruel J, Wang J, Rebillard G, Eybalin M, Lloyd R, Pujol R, Puel JL (2007) Physiology, pharmacology and plasticity at the inner hair cell synaptic complex. Hear Res 227:19-27. CrossRef Medline
44. Saunders JC, Cohen YE, Szymko YM (1991) The structural and functional consequences of acoustic injury in the cochlea and peripheral auditory system: A five year update. J Acoust Soc Am 90:136-146. CrossRef Medline
45. Schaette R, McAlpine D (2011) Tinnitus with a normal audiogram: physiological evidence for hidden hearing loss and computational model. J Neurosci 31:13452-13457. CrossRef Medline
46. Schmiedt RA, Mills JH, Boettcher FA (1996) Age-related loss of activity of auditory-nerve fibers. J Neurophysiol 76:2799-2803. Medline
47. Schuknecht HF, Woellner RC (1955) An experimental and clinical study of deafness from lesions of the cochlear nerve. J Laryngol Otol 69:75-97. CrossRef Medline
48. Sergeyenko Y, Lall K, Liberman MC, Kujawa SG (2013) Age-related cochlear synaptopathy: an early-onset contributor to auditory functional decline. J Neurosci 33:13686-13694. CrossRef Medline
49. Snell KB, Frisina DR (2000) Relationships among age-related differences in gap detection and word recognition. J Acoust Soc Am 107:1615-1626. CrossRef Medline
50. Spoendlin H (1972) Innervation densities of the cochlea. Acta Otolaryngol 73:235-248. CrossRef Medline
51. Spongr VP, Flood DG, Frisina RD, Salvi RJ (1997) Quantitative measures of hair cell loss in CBA and C57BL/6 mice throughout their lifespans. J Acoust Soc Am 101:3546-3553. CrossRef Medline
52. Szydlowska K, Tymianski M (2010) Calcium, ischemia and excitotoxicity. Cell Calcium 47:122-129. CrossRef Medline
53. Tsuji J, Liberman MC (1997) Intracellular labeling of auditory nerve fibers in guinea pig: Central and peripheral projections. J Comp Neurol 381: 188-202. Medline
54. Xia A, Song Y, Wang R, Gao SS, Clifton W, Raphael P, Chao SI, Pereira FA, Groves AK, Oghalai JS (2013) Prestin regulation and function in residual outer hair cells after noise-induced hearing loss. PLoS One 8:e82602. CrossRef Medline