Coding deficits in noise-induced hidden hearing loss may stem from incomplete repair of ribbon synapses in the cochlea

Frontiers in Neuroscience

Volumn 10, Issue MAY, 2016, Pages

  Shi, Lijuan ^a   Chang, Yin ^a   Li, Xiaowei ^a   Aiken, Steven J ^b   Liu, Lijie ^a   Wang, Jian ^a,b  

^a MEDICAL SCHOOL OF SOUTHEAST UNIVERSITY   (China)

^b DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Auditory coding; Auditory nerve fibers; Hidden hearing loss; Noise; Ribbon synapse

Indexed keywords

ALBINO GUINEA PIG; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COCHLEA; COCHLEA INJURY; CODING; CODING DEFICIT; CONTROLLED STUDY; FEMALE; HEARING IMPAIRMENT; MALE; NOISE INDUCED HIDDEN HEARING LOSS; NOISE INDUCED SYNAPTIC DAMAGE; NONHUMAN; SYNAPSE; SYNAPTIC REPAIR;

EID: 84973531042     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2016.00231     Document Type: Article

References (56)

1. Altrock, W. D., Tom Dieck, S., Sokolov, M., Meyer, A. C., Sigler, A., Brakebusch, C., et al. (2003). Functional inactivation of a fraction of excitatory synapses in mice deficient for the active zone protein bassoon. Neuron 37, 787-800. doi: 10.1016/S0896-6273(03)00088-6
2. Bharadwaj, H. M., Verhulst, S., Shaheen, L., Liberman, M. C., and Shinn-Cunningham, B. G. (2014). Cochlear neuropathy and the coding of supra-threshold sound. Front. Syst. Neurosci. 8:26. doi: 10.3389/fnsys.2014.00026
3. Borg, E., Canlon, B., and Engstrom, B. (1995). Noise-induced hearing loss: literature review and experiments in rabbits. morphological and electrophysiological features, exposure parameters and temporal factors, variability and interactions. Scand. Audiol. Suppl. 40, 1-147.
4. Bulankina, A. V., and Moser, T. (2012). Neural circuit development in the mammalian cochlea. Physiology 27, 100-112. doi: 10.1152/physiol.00036.2011
5. Buran, B. N., Strenzke, N., Neef, A., Gundelfinger, E. D., Moser, T., and Liberman, M. C. (2010). Onset coding is degraded in auditory nerve fibers from mutant mice lacking synaptic ribbons. J. Neurosci. 30, 7587-7597. doi: 10.1523/JNEUROSCI.0389-10.2010
6. Chang, K. W., and Norton, S. J. (1996). The effects of continuous versus interrupted noise exposures on distortion product otoacoustic emissions in guinea pigs. Hear. Res. 96, 1-12. doi: 10.1016/0378-5955(95)00225-1
7. Chen, C., Nenov, A., and Bobbin, R. P. (1995). Noise exposure alters the response of outer hair cells to ATP. Hear. Res. 88, 215-221. doi: 10.1016/0378-5955(95)00115-K
8. Chen, G. D., and Liu, Y. (2005). Mechanisms of noise-induced hearing loss potentiation by hypoxia. Hear. Res. 200, 1-9. doi: 10.1016/j.heares.2004.08.016
9. Chen, G. D., and Zhao, H. B. (2007). Effects of intense noise exposure on the outer hair cell plasma membrane fluidity. Hear. Res. 226, 14-21. doi: 10.1016/j.heares.2006.06.007
10. Costalupes, J. A. (1985). Representation of tones in noise in the responses of auditory nerve fibers in cats. I. Comparison with detection thresholds. J. Neurosci. 5, 3261-3269.
11. Eggermont, J. J. (2015). Animal models of auditory temporal processing. Int. J. Psychophysiol. 95, 202-215. doi: 10.1016/j.ijpsycho.2014.03.011
12. Fuchs, P. A. (2005). Time and intensity coding at the hair cell's ribbon synapse. J. Physiol. 566, 7-12. doi: 10.1113/jphysiol.2004.082214
13. Furman, A. C., Kujawa, S. G., and Liberman, M. C. (2013). Noise-induced cochlear neuropathy is selective for fibers with low spontaneous rates. J. Neurophysiol. 110, 577-586. doi: 10.1152/jn.00164.2013
14. Heil, P., and Peterson, A. J. (2015). Basic response properties of auditory nerve fibers: a review. Cell Tissue Res. 361, 129-158. doi: 10.1007/s00441-015-2177-9
15. Henderson, D., and Subramaniam, M. (2011). Advances in our understanding of noise-induced hearing loss. Appl. Occup. Environ. Hyg. 11, 255-260. doi: 10.1080/1047322X.1996.10389319
16. Henry, W. R., and Mulroy, M. J. (1995). Afferent synaptic changes in auditory hair cells during noise-induced temporary threshold shift. Hear. Res. 84, 81-90. doi: 10.1016/0378-5955(95)00014-U
17. Hudspeth, A. (1997). Mechanical amplification of stimuli by hair cells. Curr. Opin. Neurobiol. 7, 480-486. doi: 10.1016/S0959-4388(97)80026-8
18. Ivory, R., Kane, R., and Diaz, R. C. (2014). Noise-induced hearing loss: a recreational noise perspective. Curr. Opin. Otolaryngol. Head Neck Surg. 22, 394-398. doi: 10.1097/MOO.0000000000000085
19. Jing, Z., Rutherford, M. A., Takago, H., Frank, T., Fejtova, A., Khimich, D., et al. (2013). Disruption of the presynaptic cytomatrix protein bassoon degrades ribbon anchorage, multiquantal release, and sound encoding at the hair cell afferent synapse. J. Neurosci. 33, 4456-4467. doi: 10.1523/JNEUROSCI.3491-12.2013
20. Khimich, D., Nouvian, R., Pujol, R., Tom Dieck, S., Egner, A., Gundelfinger, E. D., et al. (2005). Hair cell synaptic ribbons are essential for synchronous auditory signalling. Nature 434, 889-894. doi: 10.1038/nature03418
21. Kiang, N. Y., Rho, J. M., Northrop, C. C., Liberman, M. C., and Ryugo, D. K. (1982). Hair-cell innervation by spiral ganglion cells in adult cats. Science 217, 175-177. doi: 10.1126/science.7089553
22. Kujawa, S. G., and Liberman, M. C. (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
23. Kujawa, S. G., and Liberman, M. C. (2015). Synaptopathy in the noise-exposed and aging cochlea: primary neural degeneration in acquired sensorineural hearing loss. Hear. Res. 330, 191-199. doi: 10.1016/j.heares.2015.02.009
24. Liberman, L. D., Suzuki, J., and Liberman, M. C. (2015). Dynamics of cochlear synaptopathy after acoustic overexposure. J. Assoc. Res. Otolaryngol. 16, 205-219. doi: 10.1007/s10162-015-0510-3
25. Liberman, M. C. (1978). Auditory-nerve response from cats raised in a low-noise chamber. J. Acoust. Soc. Am. 63, 442-455. doi: 10.1121/1.381736
26. Liberman, M. C. (1982). Single-neuron labeling in the cat auditory nerve. Science 216, 1239-1241. doi: 10.1126/science.7079757
27. Liberman, M. C., and Mulroy, M. J. (1982). "Acute and chronic effects of acoustic trauma: cochlear pathology and auditory nerve pathophysiology, "in New Perspectives on Noise-Induced Hearing Loss, eds R. P. Hamernik, D. Henderson, and R. Salvi (New York, NY: Raven Press), 105-135.
28. Lin, H. W., Furman, A. C., Kujawa, S. G., and Liberman, M. C. (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
29. Liu, L., Wang, H., Shi, L., Almuklass, A., He, T., Aiken, S., et al. (2012). Silent damage of noise on cochlear afferent innervation in guinea pigs and the impact on temporal processing. PLoS ONE 7:e49550. doi: 10.1371/journal.pone.0049550
30. Merchan-Perez, A., and Liberman, M. C. (1996). Ultrastructural differences among afferent synapses on cochlear hair cells: correlations with spontaneous discharge rate. J. Comp. Neurol. 371, 208-221.
31. Moser, T., Brandt, A., and Lysakowski, A. (2006). Hair cell ribbon synapses. Cell Tissue Res. 326, 347-359. doi: 10.1007/s00441-006-0276-3
32. Moser, T., Predoehl, F., and Starr, A. (2013). Review of hair cell synapse defects in sensorineural hearing impairment. Otol. Neurotol. 34, 995-1004. doi: 10.1097/MAO.0b013e3182814d4a
33. Mulroy, M. J., Fromm, R. F., and Curtis, S. (1990). Changes in the synaptic region of auditory hair cells during noise-induced temporary threshold shift. Hear. Res. 49, 79-87. doi: 10.1016/0378-5955(90)90096-8
34. Nemzou, N. R., Bulankina, A. V., Khimich, D., Giese, A., and Moser, T. (2006). Synaptic organization in cochlear inner hair cells deficient for the CaV1.3 (alpha1D) subunit of L-type Ca2+ channels. Neuroscience 141, 1849-1860. doi: 10.1016/j.neuroscience.2006.05.057
35. Nouvian, R., Beutner, D., Parsons, T. D., and Moser, T. (2006). Structure and function of the hair cell ribbon synapse. J. Membr. Biol. 209, 153-165. doi: 10.1007/s00232-005-0854-4
36. Plack, C. J., Barker, D., and Prendergast, G. (2014). Perceptual consequences of "hidden" hearing loss. Trends hear. 18, 1-11. doi: 10.1177/2331216514550621
37. Puel, J. L., d'Aldin, C., Ruel, J., Ladrech, S., and Pujol, R. (1997). Synaptic repair mechanisms responsible for functional recovery in various cochlear pathologies. Acta Otolaryngol. 117, 214-218. doi: 10.3109/00016489709117773
38. Puel, J. L., Ruel, J., Guitton, M., and Pujol, R. (2002). The inner hair cell afferent/efferent synapses revisited: a basis for new therapeutic strategies. Adv. Otorhinolaryngol. 59, 124-130. doi: 10.1159/000059250
39. Pujol, R., and Puel, J. L. (1999). Excitotoxicity, synaptic repair, and functional recovery in the mammalian cochlea: a review of recent findings. Ann. N.Y. Acad. Sci. 884, 249-254. doi: 10.1111/j.1749-6632.1999.tb08646.x
40. Pujol, R., Puel, J. L., Gervais d'Aldin, C., and Eybalin, M. (1993). Pathophysiology of the glutamatergic synapses in the cochlea. Acta Otolaryngol. 113, 330-334. doi: 10.3109/00016489309135819
41. Robertson, D. (1983). Functional significance of dendritic swelling after loud sounds in th eguinea pig cochlea. Hear. Res. 9, 263-278. doi: 10.1016/0378-5955(83)90031-X
42. Ruel, J., Wang, J., Rebillard, G., Eybalin, M., Lloyd, R., Pujol, R., et al. (2007). Physiology, pharmacology and plasticity at the inner hair cell synaptic complex. Hear. Res. 227, 19-27. doi: 10.1016/j.heares.2006.08.017
43. Schnee, M. E., Lawton, D. M., Furness, D. N., Benke, T. A., and Ricci, A. J. (2005). Auditory hair cell-afferent fiber synapses are specialized to operate at their best frequencies. Neuron 47, 243-254. doi: 10.1016/j.neuron.2005.06.004
44. Shi, L., Liu, K., Wang, H., Zhang, Y., Hong, Z., Wang, M., et al. (2015). Noise induced reversible changes of cochlear ribbon synapses contribute to temporary hearing loss in mice. Acta Otolaryngol. 135, 1093-1102. doi: 10.3109/00016489.2015.1061699
45. Shi, L., Liu, L., He, T., Guo, X., Yu, Z., Yin, S., et al. (2013). Ribbon synapse plasticity in the cochleae of Guinea pigs after noise-induced silent damage. PLoS ONE 8:e81566. doi: 10.1371/journal.pone.0081566
46. Sohmer, H. (1997). Pathophysiological mechanisms of hearing loss. J. Basic Clin. Physiol. Pharmacol. 8, 113-125. doi: 10.1515/JBCPP.1997.8.3.113
47. Spoendlin, H. (1971). Primary structural changes in the organ of Corti after acoustic overstimulation. Acta Otolaryngol. 71, 166-176. doi: 10.3109/00016487109125346
48. Subramaniam, M., Henderson, D., and Spongr, V. (1994). The relationship among distortion product otoacoustic emissions, evoked potential thresholds and outer hair cells following interrupted noise exposures. Ear Hear. 15, 299-309. doi: 10.1097/00003446-199408000-00004
49. Szalai, R., Tsaneva-Atanasova, K., Homer, M. E., Champneys, A. R., Kennedy, H. J., and Cooper, N. P. (2011). Nonlinear models of development, amplification and compression in the mammalian cochlea. Philos. Trans. A. Math. Phys. Eng. Sci. 369, 4183-4204. doi: 10.1098/rsta.2011.0192
50. Tom Dieck, S., Altrock, W. D., Kessels, M. M., Qualmann, B., Regus, H., Brauner, D., et al. (2005). Molecular dissection of the photoreceptor ribbon synapse: physical interaction of Bassoon and RIBEYE is essential for the assembly of the ribbon complex. J. Cell Biol. 168, 825-836. doi: 10.1083/jcb.200408157
51. Tom Dieck, S., and Brandstätter, J. H. (2006). Ribbon synapses of the retina. Cell Tiss. Res. 326, 339-346. doi: 10.1007/s00441-006-0234-0
52. Uthaiah, R. C., and Hudspeth, A. J. (2010). Molecular anatomy of the hair cell's ribbon synapse. J. Neurosci. 30, 12387-12399. doi: 10.1523/JNEUROSCI.1014-10.2010
53. Wang, H., Yin, S., Yu, Z., Huang, Y., and Wang, J. (2011). Dynamic changes in hair cell stereocilia and cochlear transduction after noise exposure. Biochem. Biophys. Res. Commun. 409, 616-621. doi: 10.1016/j.bbrc.2011.05.049
54. Wang, J., Li, Q., Dong, J., and Chen, J. (1992). Effects of various noise exposures on endocochlear potentials correlated with cochlear gross reponses. Hear. Res. 59, 31-38. doi: 10.1016/0378-5955(92)90099-9
55. Wang, Y., Hirose, K., and Liberman, M. C. (2002). Dynamics of noise-induced cellular injury and repair in the mouse cochlea. J. Assoc. Res. Otolaryngol. 3, 248-268. doi: 10.1007/s101620020028
56. Young, E. D., and Barta, P. E. (1986). Rate responses of auditory nerve fibers to tones in noise near masked threshold. J. Acoust. Soc. Am. 79, 426-442. doi: 10.1121/1.393530