Dopaminergic signaling in the cochlea: Receptor expression patterns and deletion phenotypes

Journal of Neuroscience

Volumn 32, Issue 1, 2012, Pages 344-355

  Maison, Stéphane F ^a,b,c   Liu, Xiao Ping ^b,c   Eatock, Ruth Anne ^a,b,c   Sibley, David R ^d   Grandy, David K ^e   Charles Liberman, M ^a,b,c  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS EYE AND EAR INFIRMARY   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^e OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOPAMINE; DOPAMINE RECEPTOR;

129 MOUSE; ANIMAL; ARTICLE; C57BL MOUSE; CHEMISTRY; CLASSIFICATION; COCHLEA; CYTOLOGY; FEMALE; GENETICS; HAIR CELL; HEARING; MALE; MOUSE; MOUSE MUTANT; PHENOTYPE; PHYSIOLOGY; SIGNAL TRANSDUCTION; SPIRAL GANGLION;

ANIMALS; COCHLEA; DOPAMINE; FEMALE; HAIR CELLS, AUDITORY, INNER; HAIR CELLS, AUDITORY, OUTER; HEARING; MALE; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, MUTANT STRAINS; PHENOTYPE; RECEPTORS, DOPAMINE; SIGNAL TRANSDUCTION; SPIRAL GANGLION;

EID: 84855981927     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4720-11.2012     Document Type: Article

References (58)

1. Accili D, Fishburn CS, Drago J, Steiner H, Lachowicz JE, Park BH, Gauda EB, Lee EJ, Cool MH, Sibley DR, Gerfen CR, Westphal H, Fuchs S (1996) A targeted mutation of the D3 dopamine receptor gene is associated with hyperactivity in mice. Proc Natl Acad Sci U S A 93:1945-1949.
2. Beaulieu JM, Gainetdinov RR (2011) The physiology, signaling, and pharmacology of dopamine receptors. Pharmacol Rev 63:182-217.
3. d'Aldin C, Puel JL, Leducq R, Crambes O, Eybalin M, Pujol R (1995) Effects of a dopaminergic agonist in the guinea pig cochlea. Hear Res 90:202-211.
4. Darrow KN, Simons EJ, Dodds L, Liberman MC (2006a) Dopaminergic innervation of the mouse inner ear: evidence for a separate cytochemical group of cochlear efferent fibers. J Comp Neurol 498:403-414.
5. Darrow KN, Maison SF, Liberman MC (2006b) Cochlear efferent feedback balances interaural sensitivity. Nat Neurosci 9:1474-1476.
6. Darrow KN, Maison SF, Liberman MC (2007) Selective removal of lateral olivocochlear efferents increases vulnerability to acute acoustic injury. J Neurophysiol 97:1775-1785.
7. Dau J, Wenthold RJ (1989) Immunocytochemical localization of neurofilament subunits in the spiral ganglion of normal and neomycin-treated guinea pigs. Hear Res 42:253-263.
8. Drago J, Gerfen CR, Lachowicz JE, Steiner H, Hollon TR, Love PE, Ooi GT, Grinberg A, Lee EJ, Huang SP, Bartlettii PF, Jose PA, Sibley DR, Westphal H (1994) Altered striatal function in a mutant mouse lacking D1A dopamine receptors. Proc Natl Acad Sci U S A 91:12564-12568.
9. Elgoyhen AB, Vetter DE, Katz E, Rothlin CV, Heinemann SF, Boulter J. (2001) alpha10: a determinant of nicotinic cholinergic receptor function in mammalian vestibular and cochlear mechanosensory hair cells. Proc Natl Acad Sci U S A 98:3501-3506.
10. Eybalin M, Charachon G, Renard N (1993) Dopaminergic lateral efferent innervation of the guinea-pig cochlea: immunoelectron microscopy of catecholamine-synthesizing enzymes and effect of 6-hydroxydopamine. Neuroscience 54:133-142.
11. Gáborján A, Lendvai B, Vizi ES (1999) Neurochemical evidence of dopamine release by lateral olivocochlear efferents and its presynaptic modulation in guinea-pig cochlea. Neuroscience 90:131-138.
12. Gao J, Maison SF, Wu X, Hirose K, Jones SM, Bayazitov I, Tian Y, Mittleman G, Matthews DB, Zakharenko SS, Liberman MC, Zuo J (2007) Orphan glutamate receptor delta1 subunit required for high-frequency hearing. Mol Cell Biol 27:4500-4512.
13. Garrett AR, Robertson D, Sellick PM, Mulders WH (2011) The actions of dopamine receptors in the guinea pig cochlea. Audiol Neurootol 16:145-157.
14. Groff JA, Liberman MC (2003) Modulation of cochlear afferent response by the lateral olivocochlear system: activation via electrical stimulation of the inferior colliculus. J Neurophysiol 90:3178-3200.
15. Guinan JJ Jr (2006) Olivocochlear efferents: anatomy, physiology, function, and the measurement of efferent effects in humans. Ear Hear 27:589-607.
16. Halmos G, Doleviczényi Z, Répássy G, Kittel A, Vizi ES, Lendvai B, Zelles T (2005) D2 autoreceptor inhibition reveals oxygen-glucose deprivation-induced release of dopamine in guinea-pig cochlea. Neuroscience 132:801-809.
17. Hequembourg S, Liberman MC (2001) Spiral ligament pathology: a major aspect of age-related cochlear degeneration in C57BL/6J mice. J Assoc Res Otolaryngol 2:118-129.
18. Holmes A, Hollon TR, Gleason TC, Liu Z, Dreiling J, Sibley DR, Crawley JN (2001) Behavioral characterization of dopamine D5 receptor null mutant mice. Behav Neurosci 115:1129-1144.
19. Hossain WA, Antic SD, Yang Y, Rasband MN, Morest DK (2005) Where is the spike generator of the cochlear nerve? Voltage-gated sodium channels in the mouse cochlea. J Neurosci 25:6857-6868.
20. Inoue T, Matsubara A, Maruya S, Yamamoto Y, Namba A, Sasaki A, Shinkawa H (2006) Localization of dopamine receptor subtypes in the rat spiral ganglion. Neurosci Lett 399:226-229.
21. Jones N, Fex J, Altschuler RA (1987) Tyrosine hydroxylase immunoreactivity identifies possible catecholaminergic fibers in the organ of Corti. Hear Res 30:33-38.
22. Karadaghy AA, Lasak JM, Chomchai JS, Khan KM, Drescher MJ, Drescher DG (1997) Quantitative analysis of dopamine receptor messages in the mouse cochlea. Mol Brain Res 44:151-156.
23. Kelly MA, Rubinstein M, Asa SL, Zhang G, Saez C, Bunzow JR, Allen RG, Hnasko R, Ben-Jonathan N, Grandy DK, Low MJ (1997) Pituitary lactotroph hyperplasia and chronic hyperprolactinemia in dopamine D2 receptor-deficient mice. Neuron 19:103-113.
24. Kujawa SG, Liberman MC (2009) Adding insult to injury: cochlear nerve degeneration after "temporary" noise-induced hearing loss. J Neurosci 29:14077-14085.
25. Lendvai B, Halmos GB, Polony G, Kapocsi J, Horváth T, Aller M, Sylvester Vizi E, Zelles T (2011) Chemical neuroprotection in the cochlea: the modulation of dopamine release from lateral olivocochlear efferents. Neurochem Int 59:150-158.
26. 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.
27. Liberman MC (1980a) Morphological differences among radial afferent fibers in the cat cochlea: An electron-microscopic study of serial sections. Hear Res 3:45-63.
28. Liberman MC (1980b) Efferent synapses in the inner hair cell area of the cat cochlea: An electron microscopic study of serial sections. Hear Res 3:189-204.
29. Liberman MC (1990) Effects of chronic cochlear de-efferentation on auditory-nerve response. Hear Res 49:209-224.
30. Liberman MC, Mulroy MJ (1982) Acute and chronic effects of acoustic trauma: Cochlear pathology and auditory nerve pathophysiology. In: New perspectives on noise-induced hearing loss (Hamernik RP, Henderson D, Salvi R, eds), pp 105-136. New York: Raven.
31. 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.
32. 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.
33. Maison SF, Luebke AE, Liberman MC, Zuo J (2002) Efferent protection from acoustic injury is mediated via alpha9 nicotinic acetylcholine receptors on outer hair cells. J Neurosci 22:10838-10846.
34. Maison SF, Adams JC, Liberman MC (2003) Olivocochlear innervation in mouse: immunocytochemical maps, crossed vs. uncrossed contributions and colocalization of ACh, GABA, and CGRP. J Comp Neurol 455:406-416.
35. Maison SF, Rosahl TW, Homanics GE, Liberman MC (2006) 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 26:10315-10326.
36. Maison SF, Vetter DE, Liberman MC (2007) A novel effect of cochlear efferents: in vivo response enhancement does not require alpha9 cholinergic receptors. J Neurophysiol 97:3269-3278.
37. Maison SF, Liu XP, Vetter DE, Eatock RA, Nathanson NM, Wess J, Liberman MC (2010) Muscarinic signaling in the cochlea: presynaptic and postsynaptic effects on efferent feedback and afferent excitability. J Neurosci 30:6751-6762.
38. Matsubara A, Laake JH, Davanger S, Usami S, Ottersen OP (1996) Organization of AMPA receptor subunits at a glutamate synapse: quantitative immunogold analysis of hair cell synapses in the rat organ of Corti. J Neurosci 16:4457-4467.
39. McLean WJ, Smith KA, Glowatzki E, Pyott SJ (2009) Distribution of the Na,K-ATPase alpha subunit in the rat spiral ganglion and organ of corti. J Assoc Res Otolaryngol 10:37-49.
40. Mulders WH, Robertson D (2004) Dopaminergic olivocochlear neurons originate in the high frequency region of the lateral superior olive of guinea pigs. Hear Res 187:122-130.
41. Niu X, Canlon B (2002) Activation of tyrosine hydroxylase in the lateral efferent terminals by sound conditioning. Hear Res 174:124-132.
42. Niu X, Canlon B (2006) The signal transduction pathway for the dopamine D1 receptor in the guinea-pig cochlea. Neuroscience 137:981-990.
43. 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.
44. Robertson D (1983) Functional significance of dendritic swelling after loud sounds in the guinea pig cochlea. Hear Res 9:263-278.
45. Roux I, Safieddine S, Nouvian R, Grati M, Simmler MC, Bahloul A, Perfettini I, Le Gall M, Rostaing P, Hamard G, Triller A, Avan P, Moser T, Petit C (2006) Otoferlin, defective in a human deafness form, is essential for exocytosis at the auditory ribbon synapse. Cell 127:277-289.
46. Rubinstein M, Phillips TJ, Bunzow JR, Falzone TL, Dziewczapolski G, Zhang G, Fang Y, Larson JL, McDougall JA, Chester JA, Saez C, Pugsley TA, Gershanik O, Low MJ, Grandy DK (1997) Mice lacking dopamine D4 receptors are supersensitive to ethanol, cocaine, and methamphetamine. Cell 90:991-1001.
47. Ruel J, Nouvian R, Gervais d'Aldin C, Pujol R, Eybalin M, Puel JL (2001) Dopamine inhibition of auditory nerve activity in the adult mammalian cochlea. Eur J Neurosci 14:977-986.
48. Ruel J, Wang J, Demêmes D, Gobaille S, Puel JL, Rebillard G (2006) Dopamine transporter is essential for the maintenance of spontaneous activity of auditory nerve neurones and their responsiveness to sound stimulation. J Neurochem 97:190-200.
49. Simmons DD, Moulding HD, Zee D (1996) Olivocochlear innervation of inner and outer hair cells during postnatal maturation: an immunocytochemical study. Brain Res Dev Brain Res 95:213-226.
50. Stankovic KM, Corfas G (2003) Real-time quantitative RT-PCR for lowabundance transcripts in the inner ear: analysis of neurotrophic factor expression. Hear Res 185:97-108.
51. Vetter DE, Liberman MC, Mann J, Barhanin J, Boulter J, Brown MC, Saffiote-Kolman J, Heinemann SF, Elgoyhen AB (1999) Role of alpha9 nicotinic ACh receptor subunits in the development and function of cochlear efferent innervation. Neuron 23:93-103.
52. Vetter DE, Li C, Zhao L, Contarino A, Liberman MC, Smith GW, Marchuk Y, Koob GF, Heinemann SF, Vale W, Lee KF (2002) Urocortin-deficient mice show hearing impairment and increased anxiety-like behavior. Nat Genet 31:363-369.
53. Vetter DE, Katz E, Maison SF, Taranda J, Turcan S, Ballestero J, Liberman MC, Elgoyhen AB, Boulter J (2007) The alpha10 nicotinic acetylcholine receptor subunit is required for normal synaptic function and integrity of the olivocochlear system. Proc Natl Acad Sci U S A 104:20594-20599.
54. Vizi ES, Lábos E (1991) Non-synaptic interactions at presynaptic level. Prog Neurobiol 37:145-163.
55. Walsh EJ, McGee J, McFadden SL, Liberman MC (1998) Long-term effects of sectioning the olivocochlear bundle in neonatal cats. J Neurosci 18:3859-3869.
56. 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.
57. Wiederhold ML, Kiang NY (1970) Effects of electric stimulation of the crossed olivocochlear bundle on single auditory-nerve fibers in the cat. J Acoust Soc Am 48:950-965.
58. Winter IM, Robertson D, Yates GK (1990) Diversity of characteristic frequency rate-intensity functions in guinea pig auditory nerve fibres. Hear Res 45:191-202.