Efferent synapses return to inner hair cells in the aging cochlea

Neurobiology of Aging

Volumn 33, Issue 12, 2012, Pages 2892-2902

  Lauer, Amanda M ^a   Fuchs, Paul A ^a   Ryugo, David K ^a,b   Francis, Howard W ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

Age related hearing loss; Cochlear innervation; Efferent; Neural plasticity; Olivocochlear

Indexed keywords

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ULTRASTRUCTURE; COCHLEAR NERVE; CONTROLLED STUDY; EFFERENT NERVE; EVOKED BRAIN STEM AUDITORY RESPONSE; FEMALE; HAIR CELL; HEARING ACUITY; MOUSE; NERVE ENDING; NONHUMAN; POSTSYNAPTIC INHIBITION; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC INHIBITION; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; TRANSMISSION ELECTRON MICROSCOPY;

ACOUSTIC STIMULATION; AGING; ANIMALS; COCHLEA; EFFERENT PATHWAYS; FEMALE; HAIR CELLS, AUDITORY, INNER; MICE; MICE, INBRED C57BL; MICROSCOPY, ELECTRON, TRANSMISSION; MODELS, NEUROLOGICAL; SYNAPSES;

EID: 84866775219     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2012.02.007     Document Type: Article

References (65)

1. Bao J., Lei D., Du Y., Ohlemiller K.K., Beaudet A.L., Role L.W. Requirement of nicotinic acetylcholine receptor subunit beta2 in the maintenance of spiral ganglion neurons during aging. J. Neurosci 2005, 25:3041-3045.
2. Blanchet C., Eróstegui C., Sugasawa M., Dulon D. Acetylcholine-induced potassium current of guinea pig outer hair cells: Its dependence on a calcium influx through nicotinic-like receptors. J. Neurosci 1996, 16:2574-2584.
3. Brown M.C. Anatomy of olivocochlear neurons. Auditory and Vestibular Efferents 2011, 17-38. Springer, New York. D.K. Ryugo, R.R. Fay, A.N. Popper (Eds.).
4. Darrow K.N., Maison S.F., Liberman M.C. Cochlear efferent feedback balances interaural sensitivity. Nat. Neurosci 2006, 9:1474-1476.
5. Darrow K.N., Maison S.F., Liberman M.C. Selective removal of lateral olivocochlear efferents increases vulnerability to acute acoustic injury. J. Neurophysiol 2007, 97:1775-1785.
6. Dolan D.F., Nuttall A.L. Masked cochlear whole-nerve response intensity functions altered by electrical stimulation of the crossed olivocochlear bundle. J. Acoust. Soc. Am 1988, 83:1081-1086.
7. Evans M.G. Acetylcholine activates two currents in guinea-pig outer hair cells. J. Physiol 1996, 491:563-578.
8. Fiala J.C. Reconstruct: a free editor for serial section microscopy. J. Microsc. 2005, 218:52-61.
9. Fiala J.C., Harris K.M. Cylindrical diameters method for calibrating section thickness in serial electron microscopy. J. Microsc 2001, 202:468-472.
10. Ferrari R., Pedrazzi P., Algeri S., Agnati L.F., Zoli M. Subunit and region-specific decreases in nicotinic acetylcholine receptor mRNA in the aged rat brain. Neurobiol. Aging 1999, 20:37-46.
11. Francis H.W., Rivas A., Lehar M., Ryugo D.K. Two types of afferent terminals innervate cochlear inner hair cells in C57BL/6J mice. Brain Res 2004, 196:182-194.
12. Francis H.W., Ryugo D.K., Gorelikow M.J., Prosen C.A., May B.J. The functional age of hearing loss in a mouse model of presbycusis. II. Neuroanatomical correlates. Hear. Res 2003, 183:29-36.
13. Frisina R.D., Karcich K.J., Tracy T.C., Sullivan D.M., Walton J.P., Colombo J. Preservation of amplitude modulation coding in the presence of background noise by chinchilla auditory-nerve fibers. J. Acoust. Soc. Am 1996, 99:475-490.
14. Fu B., Le Prell C., Simmons D., Lei D., Schrader A., Chen A.B., Bao J. Age-related synaptic loss of the medial olivocochlear efferent innervation. Mol. Neurodegener 2010, 5:53.
15. Galambos R. Suppression of auditory activity by stimulation of efferent fibers to cochlea. J. Neurophysiol 1956, 19:424-437.
16. Glowatzki E., Fuchs P.A. Cholinergic synaptic inhibition of inner hair cells in the neonatal mammalian cochlea. Science 2000, 288:2366-2368.
17. Gómez-Casati M.E., Wedemeyer C., Taranda J., Lipovsek M., Dalamon V., Elgoyhen A.B., Katz E. Electrical properties and functional expression of ionic channels in cochlear inner hair cells of mice lacking the alpha10 nicotinic cholinergic receptor subunit. J. Assoc. Res. Otolaryngol 2009, 10:221-232.
18. Goutman J.D., Fuchs P.A., Glowatzki E. Facilitating efferent inhibition of inner hair cells in the cochlea of the neonatal rat. J. Physiol 2005, 566:49-59.
19. Hellström-Lindahl E., Court J.A. Nicotinic acetylcholine receptors during prenatal development and brain pathology in human aging. Behav. Brain Res. 2000, 113:159-168.
20. Jacobson M., Kim S., Romney J., Zhu X., Frisina R.D. Contralateral suppression of distortion-product otoacoustic emissions declines with age: A comparison of findings in CBA mice with human listeners. Laryngoscope 2003, 113:1707-1713.
21. Johnson S.L., Eckrich T., Kuhn S., Zampini V., Franz C., Ranatunga K.M., Roberts T.P., Masetto S., Knipper M., Kros C.J., Marcotti W. Position-dependent patterning of spontaneous action potentials in immature cochlear inner hair cells. Nat. Neurosci 2011, 14:711-717.
22. Katz E., Elgoyhen A.B., Gómez-Casati M.E., Knipper M., Vetter D.E., Fuchs P.A., Glowatzki E. Developmental regulation of nicotinic synapses on cochlear inner hair cells. J. Neurosci 2004, 24:7814-7820.
23. Kawase T., Delgutte B., Liberman M.C. Antimasking effects of the olivocochlear reflex. II. Enhancement of auditory-nerve response to masked tones. J. Neurophysiol 1993, 70:2533-2549.
24. Kawase T., Liberman M.C. Antimasking effects of the olivocochlear reflex. I. Enhancement of compound action potentials to masked tones. J. Neurophysiol 1993, 70:2519-2532.
25. Kong J., Adelman J.P., Fuchs P.A. Expression of the SK2 calcium-activated potassium channel is required for cholinergic function in mouse cochlear hair cells. J. Physiol 2008, 586:5471-5485.
26. Kujawa S., Liberman M.C. Conditioning-related protection from acoustic injury: effects of chronic deefferentation and sham surgery. J. Neurophysiol 1997, 78:3095-3106.
27. Lauder J.M. Neurotransmitters as growth regulatory signals: role of receptors and second messengers. Trends Neurosci 1993, 16:233-240.
28. Lauer A.M., May B.J. The medial olivocochlear system attenuates the developmental impact of early noise exposure. J. Assoc. Res. Otolaryngol 2011, 12:329-343.
29. Le Prell C.G., Halsey K., Hughes L.F., Dolan D.F., Bledsoe S.C. Disruption of lateral olivocochlear neurons via a dopaminergic neurotoxin depresses sound-evoked auditory nerve activity. J. Assoc. Res. Otolaryngol 2005, 6:48-62.
30. Le Prell C.G., Shore S.E., Hughes L.F., Bledsoe S.C. Disruption of lateral efferent pathways: Functional changes in auditory evoked responses. J. Assoc. Res. Otolaryngol 2003, 4:276-290.
31. Liberman M.C. Efferent synapses in the inner hair cell area of the cat cochlea: an electron microscopic study of serial sections. Hear. Res 1980, 3:189-204.
32. Liberman M.C. Effects of chronic cochlear de-efferentation on auditory-nerve response. Hear. Res 1990, 49:209-224.
33. Liberman M.C., Brown M.C. Physiology and anatomy of single olivocochlear neurons in the cat. Hear. Res 1986, 24:17-36.
34. Liberman M.C., Dodds L.W. Single-neuron labeling and chronic cochlear pathology. II. Stereocilia damage and alterations of spontaneous discharge rates. Hear. Res 1984, 16:43-53.
35. Lin F.R., Thorpe R., Gordon-Salant S., Ferrucci L. Hearing loss prevalence and risk factors among older adults in the United States. J. Gerontol. A Biol. Sci. Med. Sci 2011, 66:582-590.
36. Maison S.F., Luebke A.E., Liberman M.C., Zuo J. Efferent protection from acoustic injury is mediated via alpha9 nicotinic acetylcholine receptors on outer hair cells. J. Neurosci 2002, 22:10838-10846.
37. Maison S.F., Rosahl T.W., Homanics G.E., Liberman M.C. Functional role of GABAergic innervation of the cochlea: phenotypic analysis of mice lacking GABA(A) receptor subunits alpha 1, alpha 2, alpha 5, alpha 6, beta 2, beta 3, or delta. J. Neurosci 2006, 26:10315-10326.
38. Müller M., von Hünerbein K., Hoidis S., Smolders J.W. A physiological place-frequency map of the cochlea in the CBA/J mouse. Hear. Res 2005, 202:63-73.
39. Prosen C.A., Dore D.J., May B.J. The functional age of hearing loss in a mouse model of presbycusis. I. Behavioral assessments. Hear. Res 2003, 183:44-56.
40. Rajan R. Centrifugal pathways protect hearing sensitivity at the cochlea in noisy environments that exacerbate the damage induced by loud sound. J. Neurosci 2000, 20:6684-6693.
41. Reiss L.A., Ramachandran R., May B.J. Effects of signal level and background noise on spectral representations in the auditory nerve of the domestic cat. J. Assoc. Res. Otolaryngol 2011, 12:71-88.
42. Roux I., Wersinger E., McIntosh J.M., Fuchs P.A., Glowatzki E. Onset of cholinergic efferent synaptic function in sensory hair cells of the rat cochlea. J. Neurosci 2011, 31:15092-15101.
43. Ruel J., Nouvian R., Gervais, d'Aldin C., Pujol R., Eyebalin M., Puel J.L. Dopamine inhibition of auditory nerve activity in the adult mammalian cochlea. Eur. J. Neurosci 2001, 14:977-986.
44. Ruel J., Wang J., Rebillard G., Eybalin M., Lloyd R., Pujol R., Puel J.L. Physiology, pharmacology and plasticity at the inner hair cell synaptic complex. Hear. Res 2007, 227:19-27.
45. Russell I.J., Murugasu E. Medial efferent inhibition suppresses basilar membrane responses to near characteristic frequency tones of moderate to high intensities. J. Acoust. Soc. Am 1997, 102:1734-1738.
46. Ryugo D.K., Rosenbaum B.T., Kim P.J., Niparko J.K., Saada A.A. Single unit recordings in the auditory nerve of congenitally deaf white cats: morphological correlates in the cochlea and cochlear nucleus. J. Comp. Neurol 1998, 397:532-548.
47. Schmiedt R.A., Mills J.H., Boettcher F.A. Age-related loss of activity of auditory-nerve fibers. J. Neurophysiol 1996, 76:2799-2803.
48. Shnerson A., Devigne C., Pujol R. Age-related changes in the C57BL/6J mouse cochlea. II. Ultrastructural findings. Dev. Brain Res 1982, 2:77-88.
49. Silkes S.M., Geisler C.D. Responses of "lower-spontaneous-rate" auditory-nerve fibers to speech syllables presented in noise: I. General characteristics. J. Acous. Soc. Am 1991, 90:3122-3139.
50. Simmons D., Duncan J., Crapon de Caprona D., Fritzsch B. Development of the inner ear efferent system. Auditory and Vestibular Efferents 2011, 187-216. Springer, New York. D.K. Ryugo, R.R. Fay, A.N. Popper (Eds.).
51. Sobkowicz H.M., Slapnick S.M. The efferents interconnecting auditory inner hair cells. Hear. Res 1994, 75:81-92.
52. Sobkowicz H.M., Slapnick S.M., August B.K. Differentiation of spinous synapses in the mouse organ of corti. Synapse 2002, 45:10-24.
53. Sobkowicz H.M., Slapnick S.M., Nitecka L.M., August B.K. Compound synapses within the GABAergic innervation of the auditory inner hair cells in the adolescent mouse. J. Comp. Neurol 1997, 377:423-442.
54. Spoendlin H. Anatomy of cochlear innervation. Am. J. Otolaryngol 1985, 6:453-467.
55. Sprinzl G.M., Riechelmann H. Current trends in treating hearing loss in elderly people: a review of the technology and treatment options-a mini-review. Gerontologist 2010, 56:351-358.
56. Stamataki S., Francis H.W., Lehar M., May B.J., Ryugo D.K. Synaptic alterations at inner hair cells precede spiral ganglion cell loss in aging C57BL/6J mice. Hear. Res 2006, 221:104-118.
57. Sullivan R.K.P., WoldeMussie E., Pow D.V. Dendritic and synaptic plasticity of neurons in the human age-related macular degeneneration retina. Invest. Opthalmol. Vis. Sci 2007, 48:2782-2791.
58. Taranda J., Maison S.F., Ballestero J.A., Katz E., Savino J., Vetter D.E., Boulter J., Liberman M.C., Fuchs P.A., Elgoyhen A.B. A point mutation in the hair cell nicotinic cholinergic receptor prolongs cochlear inhibition and enhances noise protection. PLoS Biol 2009, 7:e18.
59. Walsh E.J., McGee J., McFadden S.L., Liberman M.C. Long-term effects of sectioning the olivocochlear bundle in neonatal cats. J. Neurosci 1998, 18:3859-3869.
60. Wersinger E., McLean W.J., Fuchs P.A., Pyott S.J. BK channels mediate cholinergic inhibition of high frequency cochlear hair cells. PLoS One 2010, 5:e13836.
61. Winslow R.L., Sachs M.B. Effect of electrical stimulation of the crossed olivocochlear bundle on auditory nerve response to tones in noise. J. Neurophysiol 1987, 57:1002-1021.
62. Young E.D., Barta P.E. Rate responses of auditory nerve fibers to tones in noise near masked threshold. J. Acoust. Soc. Am 1986, 79:426-442.
63. Zeng F.G., Turner C.W., Relkin E.M. Recovery from prior stimulation II: effects on intensity discrimination. Hear. Res 1991, 55:223-230.
64. Zettel M.L., Zhu X., O'Neill W.E., Frisina R.D. Age-related decline in Kv3.1b expression in the mouse auditory brainstem correlates with functional deficits in the medial olivocochlear efferent system. J. Assoc. Res. Otolaryngol 2007, 8:280-293.
65. Zheng X.Y., Henderson D., McFadden S.L., Ding D.L., Salvi R.J. Auditory nerve fiber responses following chronic cochlear de-efferentation. J. Comp. Neurol 1999, 406:72-86.