Mechanism of spontaneous activity in afferent neurons of the zebrafish lateral-line organ

Journal of Neuroscience

Volumn 31, Issue 5, 2011, Pages 1614-1623

  Trapani, Josef G ^a   Nicolson, Teresa ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL; NEUROTRANSMITTER; VESICULAR GLUTAMATE TRANSPORTER 3;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DEPOLARIZATION; ELECTRIC CURRENT; HAIR CELL; HYPERPOLARIZATION; LARVA; LATERAL LINE SYSTEM; MECHANOTRANSDUCTION; MEMBRANE STEADY POTENTIAL; MUTANT; NERVE CONDUCTION; NERVE POTENTIAL; NERVE STIMULATION; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; SENSORY NERVE; ZEBRA FISH;

ACTION POTENTIALS; ANIMALS; BENZAZEPINES; CALCIUM CHANNELS, L-TYPE; CYCLIC NUCLEOTIDE-GATED CATION CHANNELS; ELECTRIC STIMULATION; ELECTROPHYSIOLOGY; HAIR CELLS, AUDITORY; LATERAL LINE SYSTEM; MECHANOTRANSDUCTION, CELLULAR; MEMBRANE POTENTIALS; NEURONS, AFFERENT; PHYSICAL STIMULATION; POTASSIUM CHANNELS; PYRIMIDINES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; VESICULAR GLUTAMATE TRANSPORT PROTEINS; ZEBRAFISH;

EID: 79551522275     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3369-10.2011     Document Type: Article

References (74)

1. Assad JA, Shepherd GM, Corey DP (1991) Tip-link integrity and mechanical transduction in vertebrate hair cells. Neuron 7:985-994.
2. Bailey GP, Sewell WF (2000) Contribution of glutamate receptors to spontaneous and stimulus-evoked discharge in afferent fibers innervating hair cells of the Xenopus lateral line organ. Hear Res 144:8-20.
3. Beurg M, Fettiplace R, Nam JH, Ricci AJ (2009) Localization of inner hair cell mechanotransducer channels using high-speed calcium imaging. Nat Neurosci 12:553-558.
4. Biel M, Wahl-Schott C, Michalakis S, Zong X (2009) Hyperpolarization- activated cation channels: from genes to function. Physiol Rev 89:847-885.
5. Brandt A, Striessnig J, Moser T (2003) CaV1.3 channels are essential for development and presynaptic activity of cochlear inner hair cells. J Neurosci 23:10832-10840. (Pubitemid 37499690)
6. Brandt A, Khimich D, Moser T (2005) Few CaV1.3 channels regulate the exocytosis of a synaptic vesicle at the hair cell ribbon synapse. J Neurosci 25:11577-11585. (Pubitemid 43098450)
7. 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.
8. Chevaleyre V, Castillo PE (2002) Assessing the role of Ih channels in synaptic transmission and mossy fiber LTP. Proc Natl Acad Sci U S A 99:9538-9543.
9. Corey DP, Hudspeth AJ (1983) Analysis of the microphonic potential of the bullfrog's sacculus. J Neurosci 3:942-961.
10. Dawkins R, Sewell WF (2004) Afferent synaptic transmission in a hair cell organ: pharmacological and physiological analysis of the role of the extended refractory period. J Neurophysiol 92:1105-1115.
11. Del Castillo J, Katz B (1954) Quantal components of the end-plate potential. J Physiol 124:560-573.
12. Douglass JK, Wilkens L, Pantazelou E, Moss F (1993) Noise enhancement of information transfer in crayfish mechanoreceptors by stochastic resonance. Nature 365:337-340.
13. Farris HE, LeBlanc CL, Goswami J, Ricci AJ (2004) Probing the pore of the auditory hair cell mechanotransducer channel in turtle. J Physiol 558:769-792.
14. 2+]. J Neurosci 26:12526-12536.
15. Faucherre A, Pujol-Martí J, Kawakami K, Ló pez-Schier H (2009) Afferent neurons of the zebrafish lateral line are strict selectors of hair-cell orientation. PLoS One 4:e4477.
16. Flock A, Wersall J (1962) A study of the orientation of the sensory hairs of the receptor cells in the lateral line organ of fish, with special reference to the function of the receptors. J Cell Biol 15:19-27.
17. Garcia ML, King VF, Shevell JL, Slaughter RS, Suarez-Kurtz G, Winquist RJ, Kaczorowski GJ (1990) Amiloride analogs inhibit L-type calcium channels and display calcium entry blocker activity. J Biol Chem 265:3763-3771. (Pubitemid 20096005)
18. Goldberg JM, Brown PB (1969) Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: some physiological mechanisms of sound localization. J Neurophysiol 32:613-636.
19. Goodman MB, Art JJ (1996) Positive feedback by a potassium-selective inward rectifier enhances tuning in vertebrate hair cells. Biophys J 71:430-442.
20. Grant L, Fuchs P (2008) Calcium-and calmodulin-dependent inactivation of calcium channels in inner hair cells of the rat cochlea. J Neurophysiol 99:2183-2193.
21. Heil P, Neubauer H, Irvine DRF, Brown M (2007) Spontaneous activity of auditory-nerve fibers: insights into stochastic processes at ribbon synapses. J Neurosci 27:8457-8474.
22. Hoagland H (1933) Electrical responses from the lateral-line nerves of catfish. I. J Gen Physiol 16:695-714.
23. Holt JR, Eatock RA (1995) Inwardly rectifying currents of saccular hair cells from the leopard frog. J Neurophysiol 73:1484-1502.
24. Horwitz GC, Lelli A, Géléoc GSG, Holt JR (2010) HCN channels are not required for mechanotransduction in sensory hair cells of the mouse inner ear. PLoS One 5:e8627.
25. Hudspeth AJ, Lewis RS (1988) A model for electrical resonance and frequency tuning in saccular hair cells of the bull-frog, Rana catesbeiana. J Physiol 400:275-297.
26. Johnson SL, Marcotti W (2008) Biophysical properties of CaV1.3 calcium channels in gerbil inner hair cells. J Physiol 586:1029-1042.
27. Jones TA, Jones SM (2000) Spontaneous activity in the statoacoustic ganglion of the chicken embryo. J Neurophysiol 83:1452-1468.
28. Jones TA, Jones SM, Paggett KC (2001) Primordial rhythmic bursting in embryonic cochlear ganglion cells. J Neurosci 21:8129-8135.
29. Jørgensen F, Kroese ABA (2005) Ion channel regulation of the dynamical instability of the resting membrane potential in saccular hair cells of the green frog (Rana esculenta). Acta Physiol Scand 185:271-290.
30. Jørgensen F, Ohmori H (1988) Amiloride blocks the mechano-electrical transduction channel of hair cells of the chick. J Physiol 403:577-588.
31. Keen EC, Hudspeth AJ (2006) Transfer characteristics of the hair cell's afferent synapse. Proc Natl Acad Sci U S A 103:5537-5542.
32. Kiang NYS, Watanabe T, Thomas E, Clark L (1965) Discharge patterns of single fibers in the cat's auditory nerve. Cambridge MA: MIT Press.
33. Kimmel CB, Patterson J, Kimmel RO (1974) The development and behavioral characteristics of the startle response in the zebra fish. Dev Psychobiol 7:47-60.
34. Köppl C (1997) Frequency tuning and spontaneous activity in the auditory nerve and cochlear nucleus magnocellularis of the barn owl Tyto alba. J Neurophysiol 77:364-377.
35. Kroese AB, Das A, Hudspeth AJ (1989) Blockage of the transduction channels of hair cells in the bullfrog's sacculus by aminoglycoside antibiotics. Hear Res 37:203-217.
36. Lestienne R (2001) Spike timing, synchronization and information processing on the sensory side of the central nervous system. Prog Neurobiol 65:545-591.
37. Li GL, Keen E, Andor-Ardó D, Hudspeth AJ, von Gersdorff H (2009) The unitary event underlying multiquantal EPSCs at a hair cell's ribbon synapse. J Neurosci 29:7558-7568.
38. Manley GA, Robertson D (1976) Analysis of spontaneous activity of auditory neurones in the spiral ganglion of the guinea-pig cochlea. J Physiol 258:323-336.
39. Marcotti W, Géléoc GS, Lennan GW, Kros CJ (1999) Transient expression of an inwardly rectifying potassium conductance in developing inner and outer hair cells along the mouse cochlea. Pflugers Arch 439:113-122.
40. Moser T, Beutner D (2000) Kinetics of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse of the mouse. Proc Natl Acad Sci U S A 97:883-888.
41. Nagiel A, Andor-Ardó D, Hudspeth AJ (2008) Specificity of afferent synapses onto plane-polarized hair cells in the posterior lateral line of the zebrafish. J Neurosci 28:8442-8453.
42. Nemzou N RM, Bulankina AV, Khimich D, Giese A, 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.
43. Neubauer H, Köppl C, Heil P (2009) Spontaneous activity of auditory nerve fibers in the barn owl (Tyto alba): analyses of interspike interval distributions. J Neurophysiol 101:3169-3191.
44. Nicolson T (2005) The genetics of hearing and balance in zebrafish. Annu Rev Genet 39:9-22.
45. Nicolson T, Rüsch A, Friedrich RW, Granato M, Ruppersberg JP, Nüsslein-Volhard C (1998) Genetic analysis of vertebrate sensory hair cell mechanosensation: the zebrafish circler mutants. Neuron 20:271-283. (Pubitemid 28125071)
46. Obholzer N, Wolfson S, Trapani JG, Mo W, Nechiporuk A, Busch-Nentwich E, Seiler C, Sidi S, Söllner C, Duncan RN, Boehland A, Nicolson T (2008) Vesicular glutamate transporter 3 is required for synaptic transmission in zebrafish hair cells. J Neurosci 28:2110-2118.
47. Ohmori H (1987) Gating properties of the mechano-electrical transducer channel in the dissociated vestibular hair cell of the chick. J Physiol 387:589-609.
48. Ricci A (2002) Differences in mechano-transducer channel kinetics underlie tonotopic distribution of fast adaptation in auditory hair cells. J Neurophysiol 87:1738-1748.
49. Roberts WM, Howard J, Hudspeth AJ (1988) Hair cells: transduction, tuning, and transmission in the inner ear. Annu Rev Cell Biol 4:63-92.
50. Robertson D, Paki B (2002) Role of L-type Ca2+ channels in transmitter release from mammalian inner hair cells. II. Single-neuron activity. J Neurophysiol 87:2734-2740.
51. Rutherford MA, Roberts WM (2009) Spikes and membrane potential oscillations in hair cells generate periodic afferent activity in the frog sacculus. J Neurosci 29:10025-10037.
52. Santoro B, Tibbs GR (1999) The HCN gene family: molecular basis of the hyperpolarization-activated pacemaker channels. Ann N Y Acad Sci 868:741-764. (Pubitemid 29281192)
53. Schnee ME, Ricci AJ (2003) Biophysical and pharmacological characterization of voltage-gated calcium currents in turtle auditory hair cells. J Physiol 549:697-717.
54. Seiler C, Nicolson T (1999) Defective calmodulin-dependent rapid apical endocytosis in zebrafish sensory hair cell mutants. J Neurobiol 41:424-434.
55. Seiler C, Finger-Baier KC, Rinner O, Makhankov YV, Schwarz H, Neuhauss SCF, Nicolson T (2005) Duplicated genes with split functions: independent roles of protocadherin15 orthologues in zebrafish hearing and vision. Development 132:615-623.
56. Sewell WF (1990) Synaptic potentials in afferent fibers innervating hair cells of the lateral line organ in Xenopus laevis. Hear Res 44:71-81.
57. Sidi S, Friedrich RW, Nicolson T (2003) NompC TRP channel required for vertebrate sensory hair cell mechanotransduction. Science 301:96-99.
58. Sidi S, Busch-Nentwich E, Friedrich R, Schoenberger U, Nicolson T (2004) gemini encodes a zebrafish L-type calcium channel that localizes at sensory hair cell ribbon synapses. J Neurosci 24:4213-4223.
59. Söllner C, Rauch GJ, Siemens J, Geisler R, Schuster SC, Müller U, Nicolson T, Tübingen 2000 Screen Consortium (2004) Mutations in cadherin 23 affect tip links in zebrafish sensory hair cells. Nature 428:955-959.
60. Sonntag M, Englitz B, Kopp-Scheinpflug C, Rübsamen R (2009) Early post-natal development of spontaneous and acoustically evoked discharge activity of principal cells of the medial nucleus of the trapezoid body: an in vivo study in mice. J Neurosci 29:9510-9520.
61. Spassova M, Eisen MD, Saunders JC, Parsons TD (2001) Chick cochlear hair cell exocytosis mediated by dihydropyridine-sensitive calcium channels. J Physiol 535:689-696.
62. Sueta T, Zhang SY, Sellick PM, Patuzzi R, Robertson D (2004) Effects of a calcium channel blocker on spontaneous neural noise and gross action potential waveforms in the guinea pig cochlea. Hear Res 188:117-125.
63. Sugihara I, Furukawa T (1989) Morphological and functional aspects of two different types of hair cells in the goldfish sacculus. J Neurophysiol 62:1330-1343.
64. Sugihara I, Furukawa T (1996) Inwardly rectifying currents in hair cells and supporting cells in the goldfish sacculus. J Physiol 495:665-679.
65. Trapani JG, Nicolson T (2010) Physiological recordings from zebrafish lateral-line hair cells and afferent neurons. Methods Cell Biol 100:219-231.
66. Trapani JG, Obholzer N, Mo W, Brockerhoff SE, Nicolson T (2009) Synaptojanin1 is required for temporal fidelity of synaptic transmission in hair cells. PLoS Genet 5:e1000480.
67. Tritsch NX, Bergles DE (2010) Developmental regulation of spontaneous activity in the mammalian cochlea. J Neurosci 30:1539-1550.
68. Tritsch NX, Yi E, Gale JE, Glowatzki E, Bergles DE (2007) The origin of spontaneous activity in the developing auditory system. Nature 450:50-55. (Pubitemid 350070568)
69. Yi E, Roux I, Glowatzki E (2010) Dendritic HCN channels shape excitatory postsynaptic potentials at the inner hair cell afferent synapse in the mammalian cochlea. J Neurophysiol 103:2532-2543.
70. Yu CR, Power J, Barnea G, O'Donnell S, Brown HEV, Osborne J, Axel R, Gogos JA (2004) Spontaneous neural activity is required for the establishment and maintenance of the olfactory sensory map. Neuron 42:553-566.
71. Zampini V, Johnson SL, Franz C, Lawrence ND, Münkner S, Engel J, Knipper M, Magistretti J, Masetto S, Marcotti W (2010) Elementary properties of CaV1.3 Ca(2+) channels expressed in mouse cochlear inner hair cells. J Physiol 588:187-199.
72. Zeddies DG, Fay RR (2005) Development of the acoustically evoked behavioral response in zebrafish to pure tones. J Exp Biol 208:1363-1372.
73. Zhao Y, Yamoah EN, Gillespie PG (1996) Regeneration of broken tip links and restoration of mechanical transduction in hair cells. Proc Natl Acad Sci U S A 93:15469-15474.
74. Zimmerman DM (1979) Onset of neural function in the lateral line. Nature 282:82-84.