Auditory nerve synapses persist in ventral cochlear nucleus long after loss of acoustic input in mice with early-onset progressive hearing loss

Brain Research

Volumn 1605, Issue 1, 2015, Pages 22-30

  McGuire, Brian ^a   Fiorillo, Benjamin ^a   Ryugo, David K ^b,c   Lauer, Amanda M ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Auditory nerve; Deafness; Endbulb; Hearing loss; Ventral cochlear nucleus

Indexed keywords

VESICULAR GLUTAMATE TRANSPORTER 1;

ACOUSTICS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUDIOMETRY; BRAIN STEM RESPONSE; CELL BODY; COCHLEAR NERVE; CONTROLLED STUDY; FEMALE; MALE; MOUSE; NONHUMAN; PERCEPTION DEAFNESS; PRIORITY JOURNAL; SYNAPSE; TRANSMISSION ELECTRON MICROSCOPY; VENTRAL COCHLEAR NUCLEUS; ANIMAL; CBA MOUSE; COCHLEAR NUCLEUS; DBA MOUSE; EVOKED BRAIN STEM AUDITORY RESPONSE; HEARING IMPAIRMENT; PATHOLOGY; STARTLE REFLEX; SYNAPTIC TRANSMISSION; VESTIBULOCOCHLEAR NERVE DISEASE;

MUS;

ANIMALS; COCHLEAR NERVE; COCHLEAR NUCLEUS; DEAFNESS; EVOKED POTENTIALS, AUDITORY, BRAIN STEM; FEMALE; MALE; MICE; MICE, INBRED CBA; MICE, INBRED DBA; REFLEX, STARTLE; SYNAPSES; SYNAPTIC TRANSMISSION; VESTIBULOCOCHLEAR NERVE DISEASES;

EID: 84932613332     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2015.02.012     Document Type: Article

References (45)

1. Ding, D., McFadden, S. L., Salvi, R. J., 2001. Cochlear hair cell densities and inner ear staining techniques. In: Willott, J. F. (Ed.), Handbook of Mouse Auditory Research: From Behavior to Molecular Biology. CRC Press, pp. 189.
2. Erway, L. C., Willott, J. F., Archer, J. R., Harrison, D. E., 1993. Genetics of age-related hearing loss in mice: I. Inbred and F1 hybrid strains. Hear. Res. 65, 125-132.
3. Furman, A. C., Kujawa, S. G., Liberman, M. C., 2013. Noise-induced cochlear neuropathy is selective for fibers with low spontaneous rates. J. Neurophysiol. 110, 577-586.
4. Fyk-Kolodziej, B., Shimano, T., Gong, T. W., Holt, A. G., 2011. Vesicular glutamate transporters: spatio-temporal plasticity following hearing loss. Neuroscience 178, 218-239.
5. Gentschev, T., Sotelo, C., 1973. Degenerative patterns in the ventral cochlear nucleus of the rat after primary deafferentation. An ultra-structural study. Brain Res. 62, 37-60.
6. Gómez-Nieto, R., Rubio, M. E., 2009. A bushy cell network in the rat ventral cochlear nucleus. J. Comp. Neurol. 516, 241-263.
7. Green, K. M., Bhatt, Y., Mawman, D. J., O'Driscoll, M. P., Saeed, S. R., Ramsden, R. T., Green, M. W., 2007. Predictors of audiological outcome following cochlear implantation in adults. Cochlear Implants Int. 8, 1-11.
8. Gundersen, H. J. G., Jensen, E. B., 1987. The efficiency of systematic sampling in stereology and its prediction. Journal of microscopy 147(Pt. 3), 229-263.
9. Hildebrandt, H., Hoffmann, N. A., Illing, R. B., 2011. Synaptic reorganization in the adult rat's ventral cochlear nucleus following its total sensory deafferentation. PLoS One 6, e23686.
10. Ison, J. R., 2001. The acoustic startle response: reflex elicitation and reflex modification by preliminary stimuli. In: Willott, J. F. (Ed.), The Handbook of Mouse Auditory Research: From Behavior to Molecular Biology. CRC Press, pp. 59.
11. Johnson, K. R., Longo-Guess, C., Gagnon, L. H., Yu, H., Zheng, Q. Y., 2008. A locus on distal chromosome 11 (ahl8) and its interaction with Cdh23 ahl underlie the early onset, agerelated hearing loss of DBA/2J mice. Genomics 92, 219-225.
12. Kim, J. J., Gross, J., Potashner, S. J., Morest, D. K., 2004. Fine structure of long-term changes in the cochlear nucleus after acoustic overstimulation: chronic degeneration and new growth of synaptic endings. J. Neurosci. Res. 77, 817-828.
13. Knipper, M., Da Penha Berzaghi, M., Blochl, A., Breer, H., Thoenen, H., Lindholm, D., 1994a. Positive feedback between acetylcholine and the neurotrophins nerve growth factor and brain-derived neurotrophic factor in the rat hippocampus. Eur. J. Neurosci. 6, 668-671.
14. Knipper, M., Leung, L. S., Zhao, D., Rylett, R. J., 1994b. Short-term modulation of glutamatergic synapses in adult rat hippocampus by NGF. NeuroReport 5, 2433-2436.
15. Kraus, K. S., Ding, D., Jiang, H., Lobarinas, E., Sun, W., Salvi, R. J., 2011. Relationship between noise-induced hearing-loss, persistent tinnitus and growth-associated protein-43 expression in the rat cochlear nucleus: does synaptic plasticity in ventral cochlear nucleus suppress tinnitus?. Neuroscience 194, 309-325.
16. Lang, H., Schulte, B. A., Schmiedt, R. A., 2002. Endocochlear potentials and compound action potential recovery: functions in the C57BL/6 J mouse. Hear. Res. 172, 118-126.
17. Lauer, A. M., May, B. J., 2011. The medial olivocochlear system attenuates the developmental impact of early noise exposure. J. Assoc. Res. Otolaryngol. 12, 329-343.
18. Lauer, A. M., Connelly, C. J., Graham, H., Ryugo, D. K., 2013. Morphological characterization of bushy cells and their inputs in the laboratory mouse (mus musculus) anteroventral cochlear nucleus. PLoS One 8, e73308.
19. Lauer, A. M., Fuchs, P. A., Ryugo, D. K., Francis, H. W., 2012. Efferent synapses return to inner hair cells in the aging cochlea. Neurobiol. Aging 33, 2892-2902.
20. Lauer, A. M., May, B. J., Hao, Z. J., Watson, J., 2009. Analysis of environmental sound levels in modern rodent housing rooms. Lab. Anim. (NY) 38, 154-160.
21. Lazard, D. S., Bordure, P., Lina-Granade, G., Magnan, J., Meller, R., Meyer, B., Radafy, E., Roux, P. E., Gnansia, D., Pean, V., Truy, E., 2010. Speech perception performance for 100 post-lingually deaf adults fitted with neurelec cochlear implants: comparison between digisonic (R) convex and digisonic (R) SP devices after a 1-year follow-up. Acta Otolaryngol. 130, 1267-1273.
22. Lee, D. J., Cahill, H. B., Ryugo, D. K., 2003. Effects of congenital deafness in the cochlear nuclei of shaker-2 mice: an ultrastructural analysis of synapse morphology in the endbulbs of held. J. Neurocytol. 32, 229-243.
23. Liberman, M. C., Dodds, L. W., 1984. Single-neuron labeling and chronic cochlear pathology. III. Stereocilia damage and alterations of threshold tuning curves. Hear. Res. 16, 55-74.
24. Liberman, M. C., Kiang, N. Y., 1978. Acoustic trauma in cats. Cochlear pathology and auditory-nerve activity. Acta Otolaryngol. Suppl. 358, 1-63.
25. Lina, I. A., Lauer, A. M., 2013. Rapid measurement of auditory filter shape in mice using the auditory brainstem response and notched noise. Hear. Res. 298, 73-79.
26. Meidinger, M. A., Hildebrandt-Schoenfeld, H., Illing, R. B., 2006. Cochlear damage induces GAP-43 expression in cholinergic synapses of the cochlear nucleus in the adult rat: a light and electron microscopic study. Eur. J. Neurosci. 23, 3187-3199.
27. Mikuriya, T., Sugahara, K., Sugimoto, K., Fujimoto, M., Takemoto, T., Hashimoto, M., Hirose, Y., Shimogori, H., Hayashida, N., Inouye, S., Nakai, A., Yamashita, H., 2008. Attenuation of progressive hearing loss in a model of age-related hearing loss by a heat shock protein inducer, geranylgeranylacetone. Brain Res. 1212, 9-17.
28. Miller, J. M., Chi, D. H., O'Keeffe, L. J., Kruszka, P., Raphael, Y., Altschuler, R. A., 1997. Neurotrophins can enhance spiral ganglion cell survival after inner hair cell loss. Int. J. Dev. Neurosci. 15, 631-643.
29. Mulders, W., Rodger, J., Albertsen, M., Yates, C., Robertson, D., 2014. Effects of cochlear trauma on BDNF expression in guinea pig cochlear nucleus and inferior colliculus. Otolaryngology S3 6, 2.
30. Noben-Trauth, K., Zheng, Q. Y., Johnson, K. R., 2003. Association of cadherin 23 with polygenic inheritance and genetic modification of sensorineural hearing loss. Nat. Genet. 35, 21-23.
31. Schettino, A. E., Lauer, A. M., 2013. The efficiency of design-based stereology in estimating spiral ganglion populations in mice. Hear. Res. 304, 153-158.
32. Shin, J. B., Longo-Guess, C. M., Gagnon, L. H., Saylor, K. W., Dumont, R. A., Spinelli, K. J., Pagana, J. M., Wilmarth, P. A., David, L. L., Gillespie, P. G., Johnson, K. R., 2010. The R109H variant of fascin-2, a developmentally regulated actin crosslinker in hair-cell stereocilia, underlies early-onset hearing loss of DBA/2J mice. J. Neurosci. 30, 9683-9694.
33. Someya, S., Yamasoba, T., Prolla, T. A., Tanokura, M., 2007. Genes encoding mitochondrial respiratory chain components are profoundly down-regulated with aging in the cochlea of DBA/2J mice. Brain Res. 1182, 26-33.
34. Suneja, S. K., Yan, L., Potashner, S. J., 2005. Regulation of NT-3 and BDNF levels in guinea pig auditory brain stem nuclei after unilateral cochlear ablation. J. Neurosci. Res. 80, 381-390.
35. Taberner, A. M., Liberman, M. C., 2005. Response properties of single auditory nerve fibers in the mouse. J. Neurophysiol. 93, 557-569.
36. Turner, J. G., Willott, J. F., 1998. Exposure to an augmented acoustic environment alters auditory function in hearing-impaired DBA/2J mice. Hear. Res. 118, 101-113.
37. Wang, Y., Manis, P. B., 2006. Temporal coding by cochlear nucleus bushy cells in DBA/2J mice with early onset hearing loss. J. Assoc. Res. Otolaryngol. 7, 412-424.
38. Wang, Y., Manis, P. B., 2005. Synaptic transmission at the cochlear nucleus endbulb synapse during age-related hearing loss in mice. J. Neurophysiol. 94, 1814-1824.
39. Willott, J. F., Bross, L. S., McFadden, S., 2005. Ameliorative effects of exposing DBA/2J mice to an augmented acoustic environment on histological changes in the cochlea and anteroventral cochlear nucleus. J. Assoc. Res. Otolaryngol. 6, 234-243.
40. Willott, J. F., Erway, L. C., 1998. Genetics of age-related hearing loss in mice. IV. Cochlear pathology and hearing loss in 25 BXD recombinant inbred mouse strains. Hear. Res. 119, 27-36.
41. Willott, J. F., 1981. Comparison of response properties of inferior colliculus neurons of two inbred mouse strains differing in susceptibility to audiogenic seizures. J. Neurophysiol. 45, 35-47.
42. Xie, R., Manis, P. B., 2013. Glycinergic synaptic transmission in the cochlear nucleus of mice with normal hearing and age-related hearing loss. J. Neurophysiol. 110, 1848-1859.
43. Yuan, Y., Shi, F., Yin, Y., Tong, M., Lang, H., Polley, D. B., Liberman, M. C., Edge, A. S., 2014. Ouabain-induced cochlear nerve degeneration: synaptic loss and plasticity in a mouse model of auditory neuropathy. J. Assoc. Res. Otolaryngol. 15, 31-43.
44. Zeng, C., Nannapaneni, N., Zhou, J., Hughes, L. F., Shore, S., 2009a. Cochlear damage changes the distribution of vesicular glutamate transporters associated with auditory and nonauditory inputs to the cochlear nucleus. J. Neurosci. 29, 4210-4217.
45. Zeng, C., Nannapaneni, N., Zhou, J., Hughes, L. F., Shore, S., 2009b. Cochlear damage changes the distribution of vesicular glutamate transporters associated with auditory and nonauditory inputs to the cochlear nucleus. J. Neurosci. 29, 4210-4217.