Response properties from turtle auditory hair cell afferent fibers suggest spike generation is driven by synchronized release both between and within synapses

Journal of Neurophysiology

Volumn 110, Issue 1, 2013, Pages 204-220

  Schnee, M E ^a   Castellano Munoz M ^a   Ricci, A J ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Auditory hair cell afferent fibers; Excitatory postsynaptic currents; Multivesicular release

Indexed keywords

AMPA RECEPTOR; CADMIUM; CALCIUM ION; POTASSIUM; STRONTIUM;

ANIMAL TISSUE; ARTICLE; CELL KINETICS; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; HAIR CELL; HISTOGRAM; NONHUMAN; PRIORITY JOURNAL; SPIKE; SYNAPSE; SYNAPSE VESICLE; TEMPORAL SUMMATION; TURTLE;

AUDITORY HAIR CELL AFFERENT FIBERS; EXCITATORY POSTSYNAPTIC CURRENTS; MULTIVESICULAR RELEASE;

ACTION POTENTIALS; ANIMALS; AUDITORY PATHWAYS; EXCITATORY POSTSYNAPTIC POTENTIALS; HAIR CELLS, AUDITORY; SYNAPSES; SYNAPTIC VESICLES; TURTLES;

EID: 84879634416     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00121.2013     Document Type: Article

References (44)

1. Andor-Ardo D, Hudspeth AJ, Magnasco MO, Piro O. Modeling the resonant release of synaptic transmitter by hair cells as an example of biological oscillators with cooperative steps. Proc Natl Acad Sci USA 107: 2019-2024, 2010.
2. Andor-Ardo D, Keen EC, Hudspeth AJ, Magnasco MO. Fast, automated implementation of temporally precise blind deconvolution of multiphasic excitatory postsynaptic currents. PLoS One 7: e38198, 2012.
3. Bender KJ, Allen CB, Bender VA, Feldman DE. Synaptic basis for whisker deprivation-induced synaptic depression in rat somatosensory cortex. J Neurosci 26: 4155-4165, 2006.
4. Beurg M, Michalski N, Safieddine S, Bouleau Y, Schneggenburger R, Chapman ER, Petit C, Dulon D. Control of exocytosis by synaptotagmins and otoferlin in auditory hair cells. J Neurosci 30: 13281-13290, 2010.
5. Clements JD, Silver RA. Unveiling synaptic plasticity: a new graphical and analytical approach. Trends Neurosci 23: 105-113, 2000.
6. Crawford AC, Fettiplace R. An electrical tuning mechanism in turtle cochlear hair cells. J Physiol 312: 377-412, 1981.
7. Crawford AC, Fettiplace R. The frequency selectivity of auditory nerve fibres and hair cells in the cochlea of the turtle. J Physiol 306: 79-125, 1980.
8. Dulon D, Safieddine S, Jones SM, Petit C. Otoferlin is critical for a highly sensitive and linear calcium-dependent exocytosis at vestibular hair cell ribbon synapses. J Neurosci 29: 10474-10487, 2009.
9. Dzubay JA, Jahr CE. The concentration of synaptically released glutamate outside of the climbing fiber-Purkinje cell synaptic cleft. J Neurosci 19: 5265-5274, 1999.
10. 2+]. J Neurosci 26: 12526-12536, 2006.
11. 2+ signals and their heterogeneity in hair cells. Proc Natl Acad Sci USA 106: 4483-4488, 2009.
12. Fuchs PA, Glowatzki E, Moser T. The afferent synapse of cochlear hair cells. Curr Opin Neurobiol 13: 452-458, 2003.
13. Glowatzki E, Fuchs PA. Transmitter release at the hair cell ribbon synapse. Nat Neurosci 5: 147-154, 2002.
14. Grant L, Yi E, Glowatzki E. Two modes of release shape the postsynaptic response at the inner hair cell ribbon synapse. J Neurosci 30: 4210-4220, 2010.
15. Grant L, Yi E, Goutman JD, Glowatzki E. Postsynaptic recordings at afferent dendrites contacting cochlear inner hair cells: monitoring multivesicular release at a ribbon synapse. J Vis Exp 2011: 2442, 2011.
16. 2+ nanodomains beneath the ribbon promote highly synchronous multivesicular release at hair cell synapses. J Neurosci 31: 16637-16650, 2011.
17. Hu Y, Qu L, Schikorski T. Mean synaptic vesicle size varies among individual excitatory hippocampal synapses. Synapse 62: 953-957, 2008.
18. Keen EC, Hudspeth AJ. Transfer characteristics of the hair cell's afferent synapse. Proc Natl Acad Sci USA 103: 5537-5542, 2006.
19. Li GL, Keen E, Andor-Ardo D, Hudspeth AJ, von Gersdorff H. The unitary event underlying multiquantal EPSCs at a hair cell's ribbon synapse. J Neurosci 29: 7558-7568, 2009.
20. Liberman LD, Wang H, Liberman MC. Opposing gradients of ribbon size and AMPA receptor expression underlie sensitivity differences among cochlear-nerve/hair-cell synapses. J Neurosci 31: 801-808, 2011.
21. Martinez-Dunst C, Michaels RL, Fuchs PA. Release sites and calcium channels in hair cells of the chick's cochlea. J Neurosci 17: 9133-9144, 1997.
22. Matthews G, Fuchs P. The diverse roles of ribbon synapses in sensory neurotransmission. Nat Rev Neurosci 11: 812-822, 2010.
23. Matthews G, Sterling P. Evidence that vesicles undergo compound fusion on the synaptic ribbon. J Neurosci 28: 5403-5411, 2008.
24. Mehta B, Snellman J, Chen S, Li W, Zenisek D. Synaptic ribbons influence the size and frequency of miniature-like evoked postsynaptic currents. Neuron 77: 516-527, 2013.
25. Meyer AC, Frank T, Khimich D, Hoch G, Riedel D, Chapochnikov NM, Yarin YM, Harke B, Hell SW, Egner A, Moser T. Tuning of synapse number, structure and function in the cochlea. Nat Neurosci 12: 444-453, 2009.
26. Partin KM, Fleck MW, Mayer ML. AMPA receptor flip/flop mutants affecting deactivation, desensitization, and modulation by cyclothiazide, aniracetam, and thiocyanate. J Neurosci 16: 6634-6647, 1996.
27. Partin KM, Patneau DK, Mayer ML. Cyclothiazide differentially modulates desensitization of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor splice variants. Mol Pharmacol 46: 129-138, 1994.
28. Partin KM, Patneau DK, Winters CA, Mayer ML, Buonanno A. Selective modulation of desensitization at AMPA versus kainate receptors by cyclothiazide and concanavalin A. Neuron 11: 1069-1082, 1993.
29. Qu L, Akbergenova Y, Hu Y, Schikorski T. Synapse-to-synapse variation in mean synaptic vesicle size and its relationship with synaptic morphology and function. J Comp Neurol 514: 343-352, 2009.
30. Reisinger E, Bresee C, Neef J, Nair R, Reuter K, Bulankina A, Nouvian R, Koch M, Buckers J, Kastrup L, Roux I, Petit C, Hell SW, Brose N, Rhee JS, Kugler S, Brigande JV, Moser T. Probing the functional equivalence of otoferlin and synaptotagmin 1 in exocytosis. J Neurosci 31: 4886-4895, 2011.
31. Ricci AJ, Gray-Keller M, Fettiplace R. Tonotopic variations of calcium signalling in turtle auditory hair cells. J Physiol 524: 423-436, 2000.
32. 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. Otoferlin, defective in a human deafness form, is essential for exocytosis at the auditory ribbon synapse. Cell 127: 277-289, 2006.
33. Rutherford MA, Chapochnikov NM, Moser T. Spike encoding of neurotransmitter release timing by spiral ganglion neurons of the cochlea. J Neurosci 32: 4773-4789, 2012.
34. Safieddine S, Wenthold RJ. SNARE complex at the ribbon synapses of cochlear hair cells: analysis of synaptic vesicle-and synaptic membraneassociated proteins. Eur J Neurosci 11: 803-812, 1999.
35. Schnee ME, Lawton DM, Furness DN, Benke TA, Ricci AJ. Auditory hair cell-afferent fiber synapses are specialized to operate at their best frequencies. Neuron 47: 243-254, 2005.
36. Schnee ME, Ricci AJ. Biophysical and pharmacological characterization of voltage-gated calcium currents in turtle auditory hair cells. J Physiol 549: 697-717, 2003.
37. Schnee ME, Santos-Sacchi J, Castellano-Munoz M, Kong JH, Ricci AJ. Calcium-dependent synaptic vesicle trafficking underlies indefatigable release at the hair cell afferent fiber synapse. Neuron 70: 326-338, 2011.
38. Sneary MG. Auditory receptor of the red-eared turtle. II. Afferent and efferent synapses and innervation patterns. J Comp Neurol 276: 588-606, 1988.
39. Tucker T, Fettiplace R. Confocal imaging of calcium microdomains and calcium extrusion in turtle hair cells. Neuron 15: 1323-1335, 1995.
40. Tucker TR, Fettiplace R. Monitoring calcium in turtle hair cells with a calcium-activated potassium channel. J Physiol 494: 613-626, 1996.
41. Wu XS, Xue L, Mohan R, Paradiso K, Gillis KD, Wu LG. The origin of quantal size variation: vesicular glutamate concentration plays a significant role. J Neurosci 27: 3046-3056, 2007.
42. Xu-Friedman MA, Regehr WG. Presynaptic strontium dynamics and synaptic transmission. Biophys J 76: 2029-2042, 1999.
43. Xu-Friedman MA, Regehr WG. Probing fundamental aspects of synaptic transmission with strontium. J Neurosci 20: 4414-4422, 2000.
44. Yi E, Roux I, Glowatzki E. Dendritic HCN channels shape excitatory postsynaptic potentials at the inner hair cell afferent synapse in the mammalian cochlea. J Neurophysiol 103: 2532-2543, 2010.