Mechanisms of efferent-mediated responses in the turtle posterior crista

Journal of Neuroscience

Volumn 26, Issue 51, 2006, Pages 13180-13193

  Holt, Joseph C ^a,c   Lysakowski, Anna ^b   Goldberg, Jay M ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^c University of Texas Medical Branch School of Medicine   (United States)

Author keywords

9; Hair cell; Nicotinic; Pharmacology; Vestibular afferent; Vestibular efferent

Indexed keywords

CALCIUM; NEUROTRANSMITTER RECEPTOR; NICOTINIC RECEPTOR BLOCKING AGENT; SMALL CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ULTRASTRUCTURE; CONTROLLED STUDY; DEPOLARIZATION; EFFERENT NERVE; ELECTROSTIMULATION; HAIR CELL; HYPERPOLARIZATION; MOTOR SYSTEM; NERVE STIMULATION; NEUROEPITHELIUM; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; SENSORY NERVE; SIGNAL TRANSDUCTION; SPIKE WAVE; TURTLE; VESTIBULAR NERVE;

ANIMALS; ELECTRIC STIMULATION; FEMALE; HAIR CELLS, VESTIBULAR; MALE; NEURONS, EFFERENT; PRESYNAPTIC TERMINALS; TURTLES; VESTIBULE;

EID: 33845799132     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3539-06.2006     Document Type: Article

References (68)

1. Allbritton NL, Meyer T, Stryer L (1992) Range of messenger action of calcium ion and inositol 1, 4, 5-trisphosphate. Science 258:1812-1815.
2. Anderson AD, Troyanovskaya M, Wackym PA (1997) Differential expression of α2-7, α9 and β2-4 nicotinic acetylcholine receptor subunit mRNA in the vestibular end-organs and Scarpa's ganglia of the rat. Brain Res 778:409-413.
3. Art JJ, Crawford AC, Fettiplace R, Fuchs PA (1985) Efferent modulation of hair cell tuning in the cochlea of the turtle. J Physiol (Lond) 360:397-421.
4. Bao H, Wong WH, Goldberg JM, Eatock RA (2003) Voltage-gated calcium channel currents in type I and type II hair cells isolated from the rat crista. J Neurophysiol 90:155-164.
5. Bernard C, Cochran SL, Precht W (1985) Presynaptic actions of cholinergic agents upon the hair cell-afferent fiber synapses in the vestibular labyrinth of the frog. Brain Res 338:225-236.
6. Boyle R, Highstein SM (1990) Efferent vestibular system in the toadfish: action upon horizontal semicircular canal afferents. J Neurosci 10:1570-1582.
7. Brichta AM, Goldberg JM (2000a) Morphological identification of physiologically characterized afferents innervating the turtle posterior crista. J Neurophysiol 83:1202-1223.
8. Brichta AM, Goldberg JM (2000b) Responses to efferent activation and excitatory response-intensity relations of turtle posterior-crista afferents. J Neurophysiol 83:1224-1242.
9. Brichta AM, Peterson EH (1994) Functional architecture of vestibular primary afferents from the posterior semicircular canal of a turtle, Pseudemys (Trachemys) scripta elegans. J Comp Neurol 344:481-507.
10. Brichta AM, Aubert A, Eatock RA, Goldberg JM (2002) Regional analysis of whole cell currents from hair cells of the turtle posterior crista. J Neurophysiol 88:3259-3278.
11. Crank J (1975) The mathematics of diffusion, Ed 2. Oxford: Oxford UP.
12. Cristobal R, Wackym PA, Cioffi JA, Erbe CB, Roche JP, Popper P (2005) Assessment of differential gene expression in vestibular epithelial cell types using microarray analysis. Brain Res Mol Brain Res 133:19-36.
13. Dailey SH, Wackym PA, Brichta AM, Gannon PJ, Popper P (2000) Topographic distribution of nicotinic acetylcholine receptors in the cristae of a turtle. Hear Res 141:51-56.
14. Dawkins R, Keller SL, Sewell WF (2005) Pharmacology of acetylcholine-mediated cell signaling in the lateral line organ following efferent stimulation. J Neurophysiol 93:2541-2551.
15. Dickman JD, Correia MJ (1993) Bilateral communication between vestibular labyrinths in pigeons. Neuroscience 57:1097-1108.
16. Dulon D, Luo L, Zhang C, Ryan AF (1998) Expression of small-conductance calcium-activated potassium channels (SK) in outer hair cells of the rat cochlea. Eur J Neurosci 10:907-915.
17. Elgoyhen AB, Johnson DS, Boulter J, Vetter DE, Heinemann S (1994) α9: an acetylcholine receptor with novel pharmacological properties expressed in rat cochlear hair cells. Cell 79:705-715.
18. Elgoyhen AB, Vetter DE, Katz E, Rothlin CV, Heinemann SF, Boulter J (2001) α10: a determinant of nicotinic cholinergic receptor function in mammalian vestibular and cochlear mechanosensory hair cells. Proc Natl Acad Sci USA 98:3501-3506.
19. Fayyazuddin A, Brichta AM, Art JJ (1991) Organization of eighth nerve efferents in the turtle, Pseudemys scripta. Soc Neurosci Abstr 17:312.
20. Fuchs PA, Murrow BW (1992) Cholinergic inhibition of short (outer) hair cells of the chick's cochlea. J Neurosci 12:800-809.
21. Furukawa T (1981) Effects of efferent stimulation on the saccule of goldfish. J Physiol (Lond) 315:203-215.
22. Glowatzki E, Fuchs PA (2000) Cholinergic synaptic inhibition of inner hair cells in the neonatal mammalian cochlea. Science 288:2366-2368.
23. Goldberg JM, Fernandez C (1980) Efferent vestibular system in the squirrel monkey: anatomical location and influence on afferent activity. J Neurophysiol 43:986-1025.
24. Goldberg JM, Brichta AM, Wackym PW (1999) Efferent vestibular system: anatomy, physiology and neurochemistry. In: Neurochemistry of the vestibular system (Anderson JH, Beitz AJ, eds), pp 61-94. Boca Raton, FL: CRC.
25. Gomez-Casati ME, Fuchs PA, Elgoyhen AB, Katz E (2005) Biophysical and pharmacological characterization of nicotinic cholinergic receptors in rat cochlear inner hair cells. J Physiol (Lond) 566:103-118.
26. Guth PS, Perin P, Norris CH, Valli P (1998) The vestibular hair cells: posttransductional signal processing. Prog Neurobiol 54:193-247.
27. Hiel H, Elgoyhen AB, Drescher DG, Morley BJ (1996) Expression of nicotinic acetylcholine receptor mRNA in the adult rat peripheral vestibular system. Brain Res 738:347-352.
28. Holladay MW, Dart MJ, Lynch JK (1997) Neuronal nicotinic acetylcholine receptors as targets for drug discovery. J Med Chem 40:4169-4194.
29. Holt JC, Lioudyno M, Athas G, Garcia MM, Perin P, Guth PS (2001) The effect of proteolytic enzymes on the α9-nicotinic receptor-mediated response in isolated frog vestibular hair cells. Hear Res 152:25-42.
30. Holt JC, Lioudyno M, Guth PS (2003) A pharmacologically distinct nicotinic ACh receptor is found in a subset of frog semicircular canal hair cells. J Neurophysiol 90:525-536.
31. Holt JC, Xue JT, Brichta AM, Goldberg JM (2006) Transmission between type II hair cells and bouton afferents in the turtle posterior crista. J Neurophysiol 95:428-452.
32. Holt JR, Eatock RA (1995) Inwardly rectifying currents of saccular hair cells from the leopard frog. J Neurophysiol 73:1484-1502.
33. Ishiyama A, Lopez I, Wackym PA (1995) Distribution of efferent cholinergic terminals and alpha-bungarotoxin binding to putative nicotinic acetylcholine receptors in the human vestibular end-organs. Laryngoscope 105:1167-1172.
34. Karadsheh MS, Shah MS, Tang X, Macdonald RL, Stitzel JA (2004) Functional characterization of mouse α4β2 nicotinic acetylcholine receptors stably expressed in HEK293T cells. J Neurochem 91:1138-1150.
35. Lioudyno M, Hiel H, Kong JH, Katz E, Waldman E, Parameshwaran-Iyer S, Glowatzki E, Fuchs PA (2004) A "synaptoplasmic cistern" mediates rapid inhibition of cochlear hair cells. J Neurosci 24:1160-1164.
36. Locke R, Vautrin J, Highstein SM (1999) Miniature EPSPs and sensory encoding in the primary afferents of the vestibular lagena of the toadfish, Opsanus tau. Ann NY Acad Sci 871:135-150.
37. López I, Ishiyama G, Ishiyama A, Jen JC, Liu F, Baloh RW (1999) Differential subcellular immunolocalization of voltage-gated calcium channel α1 subunits in the chinchilla cristae ampullaris. Neuroscience 92:773-782.
38. Luebke AE, Maroni PD, Guth SM, Lysakowski A (2005) Alpha-9 nicotinic acetylcholine receptor subunit immunoreactivity in the rodent vestibular labyrinth. J Comp Neurol 492:323-333.
39. Lysakowski A (1996) Synaptic organization of the crista ampullaris in vertebrates. Ann NY Acad Sci 781:164-182.
40. Lysakowski A, Goldberg JM (1997) A regional ultrastructural analysis of the cellular and synaptic architecture in the chinchilla cristae ampullares. J Comp Neurol 389:419-443.
41. Lysakowski A, Goldberg JM (2004) Morphophysiology of the vestibular periphery. In: The vestibular system (Highstein SM, Popper A, Fay RR, eds), pp 57-152, New York: Springer.
42. + currents by hair cells of frog semicircular canals. NeuroReport 10:601-606.
43. Marlinski V, Plotnik M, Goldberg JM (2004) Efferent actions in the chinchilla vestibular labyrinth. J Assoc Res Otolaryngol 5:126-143.
44. Martini M, Rossi ML, Rubbini G, Rispoli G (2000) Calcium currents in hair cells isolated from semicircular canals of the frog. Biophys J 78:1240-1254.
45. Meredith GE (1988) Comparative view of the central organization of afferent and efferent circuitry for the inner ear. Acta Biol Hung 39:229-249.
46. Neher E, Sakaba T (2003) Combining deconvolution and fluctuation analysis to determine quantal parameters and release rates. J Neurosci Methods 130:143-157.
47. + channel. Hear Res 101:149-172.
48. 2+ channels in the mouse. 29th Midwinter Meeting for The Association for Research in Otolaryngology Abstract 748. Retrieved December 13, 2006 from http://www.aro.org/archives/2005/2005_748.html.
49. + channels controls fast inhibitory synaptic transmission at auditory outer hair cells. Neuron 26:595-601.
50. Rice SO (1944) Mathematical analysis of random noise. Bell Sys Tech J 23:282-332.
51. Robinson RB, Siegelbaum SA (2003) Hyperpolarization-activated cation currents: from molecules to physiological function. Annu Rev Physiol 65:453-480.
52. Rossi ML, Martini M (1991) Efferent control of posterior canal afferent receptor discharge in the frog labyrinth. Brain Res 555:123-134.
53. Rossi ML, Prigioni I, Valli P, Casella C (1980) Activation of the efferent system in the isolated frog labyrinth: effects on the afferent EPSPs and spike discharge recorded from single fibres of the posterior nerve. Brain Res 185:125-137.
54. Rothlin CV, Lioudyno MI, Silbering AF, Plazas PV, Casati ME, Katz E, Guth PS, Elgoyhen AB (2003) Direct interaction of serotonin type 3 receptor ligands with recombinant and native α9β10-containing nicotinic cholinergic receptors. Mol Pharmacol 63:1067-1074.
55. Russell IJ (1968) Influence of efferent fibres on a receptor. Nature 219:177-178.
56. + channels and afterhyperpolarizations. Toxicon 43:933-949.
57. Sugai T, Sugitani M, Ooyama H (1991) Effects of activation of the divergent efferent fibers on the spontaneous activity of vestibular afferent fibers in the toad. Jpn J Physiol 41:217-232.
58. Sugai T, Yano J, Sugitani M, Ooyama H (1992) Actions of cholinergic agonists and antagonists on the efferent synapse in the frog sacculus. Hear Res 61:56-64.
59. Tucker T, Art JJ, Fettiplace R (1996) Routes of calcium entry and extrusion in turtle hair cells. Ann NY Acad Sci 781:123-137.
60. Verbitsky M, Rothlin CV, Katz E, Elgoyhen AB (2000) Mixed nicotinic-muscarinic properties of the α9 nicotinic cholinergic receptor. Neuropharmacology 39:2515-2524.
61. Wackym PA, Popper P, Lopez I, Ishiyama A, Micevych PE (1995) Expression of α4 and β2 nicotinic acetylcholine receptor subunit mRNA and localization of alpha-bungarotoxin binding proteins in the rat vestibular periphery. Cell Biol Int 19:291-300.
62. Warr WB, Guinan JJ (1979) Efferent innervation in the organ or Corti: two separate systems. Brain Res 173:660-686.
63. Weisstaub N, Vetter DE, Elgoyhen AB, Katz E (2002) The α9α10 nicotinic acetylcholine receptor is permeable to and is modulated by divalent cations. Hear Res 167:122-135.
64. Wu YC, Tucker T, Fettiplace R (1996) A theoretical study of calcium microdomains in turtle hair cells. Biophys J 71:2256-2275.
65. Xia XM, Fakler B, Rivard A, Wayman G, Johnson-Pais T, Keen JE, Ishii T, Hirschberg B, Bond CT, Lutsenko S, Maylie J, Adelman JP (1998) Mechanism of calcium gating in small-conductance calcium-activated potassium channels. Nature 395:503-507.
66. Yamashita M (1986) Monosynaptic connexions of low threshold muscle afferents with hindlimb motoneurones in the turtle spinal cord. Exp Brain Res 63:519-529.
67. Yuhas WA, Fuchs PA (1999) Apamin-sensitive, small-conductance, calcium-activated potassium channels mediate cholinergic inhibition of chick auditory hair cells. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 185:455-462.
68. Zoli M, Le Novere N, Hill JA, Changeux JP (1995) Developmental regulation of nicotinic ACh receptor subunit mRNAs in the rat central and peripheral nervous systems. J Neurosci 15:1912-1939.