Auditory hair cell-afferent fiber synapses are specialized to operate at their best frequencies

Neuron

Volumn 47, Issue 2, 2005, Pages 243-254

  Schnee, M E ^a   Lawton, D M ^b   Furness, D N ^b   Benke, T A ^c   Ricci, A J ^a  

^a LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b KEELE UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUDITORY STIMULATION; CALCIUM TRANSPORT; CELL FUNCTION; DENSE BODY; ELECTRIC CAPACITANCE; EVOKED AUDITORY RESPONSE; FREQUENCY ANALYSIS; HAIR CELL; MORPHOLOGICAL TRAIT; NONHUMAN; PRIORITY JOURNAL; SENSORY NERVE; SIGNAL TRANSDUCTION; SYNAPSE; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION;

ANIMALS; AUDITORY PATHWAYS; CADMIUM; CALCIUM; DIAGNOSTIC IMAGING; DOSE-RESPONSE RELATIONSHIP, RADIATION; ELECTRIC CAPACITANCE; ELECTRIC STIMULATION; HAIR CELLS; MEMBRANE POTENTIALS; MICROSCOPY, ELECTRON, TRANSMISSION; MODELS, NEUROLOGICAL; ORGAN OF CORTI; PATCH-CLAMP TECHNIQUES; PRESYNAPTIC TERMINALS; SYNAPSES; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES; TIME FACTORS; TURTLES;

EID: 22544477826     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2005.06.004     Document Type: Article

References (52)

1. M.A. Adly, I. Spiwoks-Becker, and L. Vollrath Ultrastructural changes of photoreceptor synaptic ribbons in relation to time of day and illumination Invest. Ophthalmol. Vis. Sci. 40 1999 2165 2172
2. G.W. Balkema, K. Cusick, and T.H. Nguyen Diurnal variation in synaptic ribbon length and visual threshold Vis. Neurosci. 18 2001 789 797
3. A.C. Crawford, and R. Fettiplace The frequency selectivity of auditory nerve fibres and hair cells in the cochlea of the turtle J. Physiol. 306 1980 79 125
4. A.C. Crawford, and R. Fettiplace The mechanical properties of ciliary bundles of turtle cochlear hair cells J. Physiol. 364 1985 359 379
5. M.D. Eisen, M. Spassova, and T.D. Parsons Large releasable pool of synaptic vesicles in chick cochlear hair cells J. Neurophysiol. 91 2004 2422 2428
6. R. Fettiplace, and P.A. Fuchs Mechanisms of hair cell tuning Annu. Rev. Physiol. 61 1999 809 834
7. T. Furukawa, and S. Matsuura Adaptive rundown of excitatory post-synaptic potentials at synapses between hair cells and eight nerve fibres in the goldfish J. Physiol. 276 1978 193 209
8. T. Furukawa, Y. Hayashida, and S. Matsuura Quantal analysis of the size of excitatory post-synaptic potentials at synapses between hair cells and afferent nerve fibres in goldfish J. Physiol. 276 1978 211 226
9. L. Gleisner, A. Flock, and J. Wersall The ultrastructure of the afferent synapse on hair cells in the frog labyrinth Acta Otolaryngol. 76 1973 199 207
10. A. Gomis, J. Burrone, and L. Lagnado Two actions of calcium regulate the supply of releasable vesicles at the ribbon synapse of retinal bipolar cells J. Neurosci. 19 1999 6309 6317
11. E.G. Gray, and H.L. Pease On understanding the organisation of the retinal receptor synapses Brain Res. 35 1971 1 15
12. C.M. Hackney, R. Fettiplace, and D.N. Furness The functional morphology of stereociliary bundles on turtle cochlear hair cells Hear. Res. 69 1993 163 175
13. K. Hama, and K. Saito Fine structure of the afferent synapse of the hair cells in the saccular macula of the goldfish, with special reference to the anastomosing tubules J. Neurocytol. 6 1977 361 373
14. M. Holt, A. Cooke, A. Neef, and L. Lagnado High mobility of vesicles supports continuous exocytosis at a ribbon synapse Curr. Biol. 14 2004 173 183
15. N.P. Issa, and A.J. Hudspeth Clustering of Ca2+ channels and Ca(2+)-activated K+ channels at fluorescently labeled presynaptic active zones of hair cells Proc. Natl. Acad. Sci. USA 91 1994 7578 7582
16. R.A. Jacobs, and A.J. Hudspeth Ultrastructural correlates of mechanoelectrical transduction in hair cells of the bullfrog's internal ear Cold Spring Harb. Symp. Quant. Biol. 55 1990 547 561
17. S.L. Johnson, M.V. Thomas, and C.J. Kros Membrane capacitance measurement using patch clamp with integrated self-balancing lock-in amplifier Pflugers Arch. 443 2002 653 663
18. S.L. Johnson, W. Marcotti, and C.J. Kros Increase in efficiency and reduction in Ca2+ dependence of exocytosis during development of mouse inner hair cells J. Physiol. 563 2005 177 191
19. R. Kollmar, L.G. Montgomery, J. Fak, L.J. Henry, and A.J. Hudspeth Predominance of the alpha1D subunit in L-type voltage-gated Ca2+ channels of hair cells in the chicken's cochlea Proc. Natl. Acad. Sci. USA 94 1997 14883 14888
20. L. Lagnado Ribbon synapses Curr. Biol. 13 2003 R631
21. L. Lagnado, A. Gomis, and C. Job Continuous vesicle cycling in the synaptic terminal of retinal bipolar cells Neuron 17 1996 957 967
22. D. Lenzi, J.W. Runyeon, J. Crum, M.H. Ellisman, and W.M. Roberts Synaptic vesicle populations in saccular hair cells reconstructed by electron tomography J. Neurosci. 19 1999 119 132
23. D. Lenzi, J. Crum, M.H. Ellisman, and W.M. Roberts Depolarization redistributes synaptic membrane and creates a gradient of vesicles on the synaptic body at a ribbon synapse Neuron 36 2002 649 659
24. M.C. Liberman, L.W. Dodds, and S. Pierce Afferent and efferent innervation of the cat cochlea: quantitative analysis with light and electron microscopy J. Comp. Neurol. 301 1990 443 460
25. A. Majewska, G. Yiu, and R. Yuste A custom-made two-photon microscope and deconvolution system Pflugers Arch. 441 2000 398 408
26. C. Martinez-Dunst, R.L. Michaels, and P.A. Fuchs Release sites and calcium channels in hair cells of the chick's cochlea J. Neurosci. 17 1997 9133 9144
27. S. Mennerick, and G. Matthews Ultrafast exocytosis elicited by calcium current in synaptic terminals of retinal bipolar neurons Neuron 17 1996 1241 1249
28. T. Moser, and D. Beutner Kinetics of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse of the mouse Proc. Natl. Acad. Sci. USA 97 2000 883 888
29. E. Neher, and A. Marty Discrete changes of cell membrane capacitance observed under conditions of enhanced secretion in bovine adrenal chromaffin cells Proc. Natl. Acad. Sci. USA 79 1982 6712 6716
30. G. Neves, and L. Lagnado The kinetics of exocytosis and endocytosis in the synaptic terminal of goldfish retinal bipolar cells J. Physiol. 515 1999 181 202
31. V. Nikolenko, B. Nemet, and R. Yuste A two-photon and second-harmonic microscope Methods 30 2003 3 15
32. T.D. Parsons, and P. Sterling Synaptic ribbon. Conveyor belt or safety belt? Neuron 37 2003 379 382
33. T.D. Parsons, D. Lenzi, W. Almers, and W.M. Roberts Calcium-triggered exocytosis and endocytosis in an isolated presynaptic cell: capacitance measurements in saccular hair cells Neuron 13 1994 875 883
34. A.J. Ricci, and R. Fettiplace The effects of calcium buffering and cyclic AMP on mechano-electrical transduction in turtle auditory hair cells J. Physiol. 501 1997 111 124
35. A.J. Ricci, M. Gray-Keller, and R. Fettiplace Tonotopic variations of calcium signaling in turtle auditory hair cells J. Physiol. 524 2000 423 436
36. A.J. Ricci, A.C. Crawford, and R. Fettiplace Tonotopic variation in the conductance of the hair cell mechanotransducer channel Neuron 40 2003 983 990
37. W.M. Roberts, R.A. Jacobs, and A.J. Hudspeth Colocalization of ion channels involved in frequency selectivity and synaptic transmission at presynaptic active zones of hair cells J. Neurosci. 10 1990 3664 3684
38. N.C. Rouze, and E.A. Schwartz Continuous and transient vesicle cycling at a ribbon synapse J. Neurosci. 18 1998 8614 8624
39. M.E. Schnee, and A.J. Ricci Biophysical and pharmacological characterization of voltage-gated calcium currents in turtle auditory hair cells J. Physiol. 549 2003 697 717
40. M.G. Sneary Auditory receptor of the red-eared turtle: II. Afferent and efferent synapses and innervation patterns J. Comp. Neurol. 276 1988 588 606
41. H. Taschenberger, R.M. Leao, K.C. Rowland, G.A. Spirou, and H. von Gersdorff Optimizing synaptic architecture and efficiency for high-frequency transmission Neuron 36 2002 1127 1143
42. A.M. Taylor, and R.M. Enoka Optimization of input patterns and neuronal properties to evoke motor neuron synchronization J. Comput. Neurosci. 16 2004 139 157
43. W.B. Thoreson, K. Rabl, E. Townes-Anderson, and R. Heidelberger A highly Ca2+-sensitive pool of vesicles contributes to linearity at the rod photoreceptor ribbon synapse Neuron 42 2004 595 605
44. T. Tucker, and R. Fettiplace Confocal imaging of calcium microdomains and calcium extrusion in turtle hair cells Neuron 15 1995 1323 1335
45. T.R. Tucker, and R. Fettiplace Monitoring calcium in turtle hair cells with a calcium-activated potassium channel J. Physiol. 494 1996 613 626
46. J. Usukura, and E. Yamada Ultrastructure of the synaptic ribbons in photoreceptor cells of Rana catesbeiana revealed by freeze-etching and freeze-substitution Cell Tissue Res. 247 1987 483 488
47. H. von Gersdorff, and G. Matthews Dynamics of synaptic vesicle fusion and membrane retrieval in synaptic terminals Nature 367 1994 735 739
48. H. von Gersdorff, and G. Matthews Depletion and replenishment of vesicle pools at a ribbon-type synaptic terminal J. Neurosci. 17 1997 1919 1927
49. H. von Gersdorff, and G. Matthews Electrophysiology of synaptic vesicle cycling Annu. Rev. Physiol. 61 1999 725 752
50. H. von Gersdorff, E. Vardi, G. Matthews, and P. Sterling Evidence that vesicles on the synaptic ribbon of retinal bipolar neurons can be rapidly released Neuron 16 1996 1221 1227
51. I.J. Youngs Exploring the universal nature of electrical percolation exponents by genetic algorithm fitting with general effective medium theory J. Phys. D Appl. Phys. 35 2002 3127 3137
52. D. Zenisek, V. Davila, L. Wan, and W. Almers Imaging calcium entry sites and ribbon structures in two presynaptic cells J. Neurosci. 23 2003 2538 2548