Skip to main content
Top
Published in: Journal of the Association for Research in Otolaryngology 1/2012

01-02-2012

Exocytosis in the Frog Amphibian Papilla

Authors: Patricia M. Quiñones, Cindy Luu, Felix E. Schweizer, Peter M. Narins

Published in: Journal of the Association for Research in Otolaryngology | Issue 1/2012

Login to get access

Abstract

Using whole-cell patch-clamp recordings, we measured changes in membrane capacitance (ΔC m) in two subsets of hair cells from the leopard frog amphibian papilla (AP): the low-frequency (100–500 Hz), rostral hair cells and the high-frequency (500–1200 Hz), caudal hair cells, in order to investigate tonotopic differences in exocytosis. Depolarizations of both rostral and caudal hair cells evoked robust ΔC m responses of similar amplitude. However, the calcium dependence of release, i.e., the relationship between ΔC m relative to the amount of calcium influx (Q Ca 2+ ), was found to be linear in rostral hair cells but supra-linear in caudal hair cells. In addition, the higher numbers of vesicles released at caudal hair cell active zones suggests increased temporal precision of caudal hair cell exocytosis. ΔC m responses were also obtained in response to sinusoidal stimuli of varying frequency, but neither rostral nor caudal hair cell ΔC m revealed any frequency selectivity. While all AP hair cells express both otoferlin and synaptotagmin IV (SytIV), we obtained evidence of a tonotopic distribution of the calcium buffer calretinin which may further increase temporal resolution at the level of the hair cell synapse. Our findings suggest that the low (rostral) and high (caudal) frequency hair cells apply different mechanisms for fine-tuning exocytosis.
Literature
go back to reference Augustine GJ, Santamaria F, Tanaka K (2003) Local calcium signaling in neurons. Neuron 40:331–346PubMedCrossRef Augustine GJ, Santamaria F, Tanaka K (2003) Local calcium signaling in neurons. Neuron 40:331–346PubMedCrossRef
go back to reference Bernard C, Ferrary E, Sterkers O (1986) Production of endolymph in the semicircular canal of the frog Rana esculenta. J Physiol 371:17–28PubMed Bernard C, Ferrary E, Sterkers O (1986) Production of endolymph in the semicircular canal of the frog Rana esculenta. J Physiol 371:17–28PubMed
go back to reference Beurg M, Michalski N, Safieddine S, Bouleau Y, Schneggenburger R, Chapman ER, Petit C, Dulon D (2010) Control of exocytosis by synaptotagmins and otoferlin in auditory hair cells. J Neurosci 30:13281–13290PubMedCrossRef Beurg M, Michalski N, Safieddine S, Bouleau Y, Schneggenburger R, Chapman ER, Petit C, Dulon D (2010) Control of exocytosis by synaptotagmins and otoferlin in auditory hair cells. J Neurosci 30:13281–13290PubMedCrossRef
go back to reference 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 25:11577–11585PubMedCrossRef 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 25:11577–11585PubMedCrossRef
go back to reference Buran BN, Strenzke N, Neef A, Gundelfinger ED, Moser T, Liberman MC (2010) Onset coding is degraded in auditory nerve fibers from mutant mice lacking synaptic ribbons. J Neurosci 30:7587–7597PubMedCrossRef Buran BN, Strenzke N, Neef A, Gundelfinger ED, Moser T, Liberman MC (2010) Onset coding is degraded in auditory nerve fibers from mutant mice lacking synaptic ribbons. J Neurosci 30:7587–7597PubMedCrossRef
go back to reference Cho S, Li GL, von Gersdorff H (2011) Recovery from short-term depression and facilitation is ultrafast and Ca2+ dependent at auditory hair cell synapses. J Neurosci 31:5682–5692PubMedCrossRef Cho S, Li GL, von Gersdorff H (2011) Recovery from short-term depression and facilitation is ultrafast and Ca2+ dependent at auditory hair cell synapses. J Neurosci 31:5682–5692PubMedCrossRef
go back to reference Christensen-Dalsgaard J, Narins PM (1993) Sound and vibration sensitivity of VIIIth nerve fibers in the frogs Leptodactylus albilabris and Rana pipiens pipiens. J Comp Physiol A 172:653–662PubMedCrossRef Christensen-Dalsgaard J, Narins PM (1993) Sound and vibration sensitivity of VIIIth nerve fibers in the frogs Leptodactylus albilabris and Rana pipiens pipiens. J Comp Physiol A 172:653–662PubMedCrossRef
go back to reference Dodge FA Jr, Rahamimoff R (1967) Co-operative action a calcium ions in transmitter release at the neuromuscular junction. J Physiol 193:419–432PubMed Dodge FA Jr, Rahamimoff R (1967) Co-operative action a calcium ions in transmitter release at the neuromuscular junction. J Physiol 193:419–432PubMed
go back to reference Dulon D, Safieddine S, Jones SM, Petit C (2009) Otoferlin is critical for a highly sensitive and linear calcium-dependent exocytosis at vestibular hair cell ribbon synapses. J Neurosci 29:10474–10487PubMedCrossRef Dulon D, Safieddine S, Jones SM, Petit C (2009) Otoferlin is critical for a highly sensitive and linear calcium-dependent exocytosis at vestibular hair cell ribbon synapses. J Neurosci 29:10474–10487PubMedCrossRef
go back to reference Edmonds B, Reyes R, Schwaller B, Roberts WM (2000) Calretinin modifies presynaptic calcium signaling in frog saccular hair cells. Nat Neurosci 3:786–790PubMedCrossRef Edmonds B, Reyes R, Schwaller B, Roberts WM (2000) Calretinin modifies presynaptic calcium signaling in frog saccular hair cells. Nat Neurosci 3:786–790PubMedCrossRef
go back to reference Edmonds BW, Gregory FD, Schweizer FE (2004) Evidence that fast exocytosis can be predominantly mediated by vesicles not docked at active zones in frog saccular hair cells. J Physiol 560:439–450PubMedCrossRef Edmonds BW, Gregory FD, Schweizer FE (2004) Evidence that fast exocytosis can be predominantly mediated by vesicles not docked at active zones in frog saccular hair cells. J Physiol 560:439–450PubMedCrossRef
go back to reference el Barbary A (1991) Auditory nerve of the normal and jaundiced rat. I. Spontaneous discharge rate and cochlear nerve histology. Hear Res 54:75–90PubMedCrossRef el Barbary A (1991) Auditory nerve of the normal and jaundiced rat. I. Spontaneous discharge rate and cochlear nerve histology. Hear Res 54:75–90PubMedCrossRef
go back to reference Evans EF (1972) The frequency response and other properties of single fibres in the guinea-pig cochlear nerve. J Physiol 226:263–287PubMed Evans EF (1972) The frequency response and other properties of single fibres in the guinea-pig cochlear nerve. J Physiol 226:263–287PubMed
go back to reference Farahbakhsh NA, Narins PM (2006) Slow motility in hair cells of the frog amphibian papilla: Ca2+-dependent shape changes. Hear Res 212:140–159PubMedCrossRef Farahbakhsh NA, Narins PM (2006) Slow motility in hair cells of the frog amphibian papilla: Ca2+-dependent shape changes. Hear Res 212:140–159PubMedCrossRef
go back to reference Feng AS, Narins PM, Capranica RR (1975) Three populations of primary auditory fibers in bullfrog (Rana catesbeiana)—their peripheral origins and frequency sensitivities. J Comp Physiol 100:221–229CrossRef Feng AS, Narins PM, Capranica RR (1975) Three populations of primary auditory fibers in bullfrog (Rana catesbeiana)—their peripheral origins and frequency sensitivities. J Comp Physiol 100:221–229CrossRef
go back to reference Gale JE, Meyers JR, Corwin JT (2000) Solitary hair cells are distributed throughout the extramacular epithelium in the bullfrog’s saccule. J Assoc Res Otolaryngol 1:172–182PubMedCrossRef Gale JE, Meyers JR, Corwin JT (2000) Solitary hair cells are distributed throughout the extramacular epithelium in the bullfrog’s saccule. J Assoc Res Otolaryngol 1:172–182PubMedCrossRef
go back to reference Geisler CD, Vanbergeijk WA, Frishkopf LS (1964) The inner ear of the bullfrog. J Morphol 114:43–57PubMedCrossRef Geisler CD, Vanbergeijk WA, Frishkopf LS (1964) The inner ear of the bullfrog. J Morphol 114:43–57PubMedCrossRef
go back to reference Gentet LJ, Stuart GJ, Clements JD (2000) Direct measurement of specific membrane capacitance in neurons. Biophys J 79:314–320PubMedCrossRef Gentet LJ, Stuart GJ, Clements JD (2000) Direct measurement of specific membrane capacitance in neurons. Biophys J 79:314–320PubMedCrossRef
go back to reference Goodyear RJ, Legan PK, Christiansen JR, Xia B, Korchagina J, Gale JE, Warchol ME, Corwin JT, Richardson GP (2010) Identification of the hair cell soma-1 antigen, HCS-1, as otoferlin. J Assoc Res Otolaryngol 11:573–586PubMedCrossRef Goodyear RJ, Legan PK, Christiansen JR, Xia B, Korchagina J, Gale JE, Warchol ME, Corwin JT, Richardson GP (2010) Identification of the hair cell soma-1 antigen, HCS-1, as otoferlin. J Assoc Res Otolaryngol 11:573–586PubMedCrossRef
go back to reference Goutman JD, Glowatzki E (2007) Time course and calcium dependence of transmitter release at a single ribbon synapse. Proc Natl Acad Sci USA 104:16341–16346PubMedCrossRef Goutman JD, Glowatzki E (2007) Time course and calcium dependence of transmitter release at a single ribbon synapse. Proc Natl Acad Sci USA 104:16341–16346PubMedCrossRef
go back to reference Gregory FD, Quiñones PM (2011) Deciphering the roles of C2-domain-containing proteins (synaptotagmins and otoferlin) in the inner ear. J Neurosci 31:4765–4767PubMedCrossRef Gregory FD, Quiñones PM (2011) Deciphering the roles of C2-domain-containing proteins (synaptotagmins and otoferlin) in the inner ear. J Neurosci 31:4765–4767PubMedCrossRef
go back to reference Hau LW, Simmons DD, Narins PM (2004) Frequency-dependence of auditory-nerve latency in the northern leopard frog, Rana pipiens pipiens. In: Abstr. 27th ARO Res. Mtg. 336 Hau LW, Simmons DD, Narins PM (2004) Frequency-dependence of auditory-nerve latency in the northern leopard frog, Rana pipiens pipiens. In: Abstr. 27th ARO Res. Mtg. 336
go back to reference Heil P, Neubauer H (2010) Summing across different active zones can explain the quasi-linear Ca2+-dependencies of exocytosis by receptor cells. Front Synaptic Neurosci 2:1–15 Heil P, Neubauer H (2010) Summing across different active zones can explain the quasi-linear Ca2+-dependencies of exocytosis by receptor cells. Front Synaptic Neurosci 2:1–15
go back to reference Hillery CM, Narins PM (1987) Frequency and time domain comparison of low-frequency auditory fiber responses in two anuran amphibians. Hear Res 25:233–248PubMedCrossRef Hillery CM, Narins PM (1987) Frequency and time domain comparison of low-frequency auditory fiber responses in two anuran amphibians. Hear Res 25:233–248PubMedCrossRef
go back to reference Johnson SL, Thomas MV, Kros CJ (2002) Membrane capacitance measurement using patch clamp with integrated self-balancing lock-in amplifier. Pflugers Arch 443:653–663PubMedCrossRef Johnson SL, Thomas MV, Kros CJ (2002) Membrane capacitance measurement using patch clamp with integrated self-balancing lock-in amplifier. Pflugers Arch 443:653–663PubMedCrossRef
go back to reference Johnson SL, Forge A, Knipper M, Munkner S, Marcotti W (2008) Tonotopic variation in the calcium dependence of neurotransmitter release and vesicle pool replenishment at mammalian auditory ribbon synapses. J Neurosci 28:7670–7678PubMedCrossRef Johnson SL, Forge A, Knipper M, Munkner S, Marcotti W (2008) Tonotopic variation in the calcium dependence of neurotransmitter release and vesicle pool replenishment at mammalian auditory ribbon synapses. J Neurosci 28:7670–7678PubMedCrossRef
go back to reference Johnson SL, Franz C, Knipper M, Marcotti W (2009) Functional maturation of the exocytotic machinery at gerbil hair cell ribbon synapses. J Physiol 587:1715–1726PubMedCrossRef Johnson SL, Franz C, Knipper M, Marcotti W (2009) Functional maturation of the exocytotic machinery at gerbil hair cell ribbon synapses. J Physiol 587:1715–1726PubMedCrossRef
go back to reference Johnson SL, Franz C, Kuhn S, Furness DN, Ruttiger L, Munkner S, Rivolta MN, Seward EP, Herschman HR, Engel J, Knipper M, Marcotti W (2010) Synaptotagmin IV determines the linear Ca2+ dependence of vesicle fusion at auditory ribbon synapses. Nat Neurosci 13:45–52PubMedCrossRef Johnson SL, Franz C, Kuhn S, Furness DN, Ruttiger L, Munkner S, Rivolta MN, Seward EP, Herschman HR, Engel J, Knipper M, Marcotti W (2010) Synaptotagmin IV determines the linear Ca2+ dependence of vesicle fusion at auditory ribbon synapses. Nat Neurosci 13:45–52PubMedCrossRef
go back to reference Keen EC, Hudspeth AJ (2006) Transfer characteristics of the hair cell’s afferent synapse. Proc Natl Acad Sci USA 103:5537–5542PubMedCrossRef Keen EC, Hudspeth AJ (2006) Transfer characteristics of the hair cell’s afferent synapse. Proc Natl Acad Sci USA 103:5537–5542PubMedCrossRef
go back to reference Koyama H, Lewis ER, Leverenz EL, Baird RA (1982) Acute seismic sensitivity in the bullfrog ear. Brain Res 250:168–172PubMedCrossRef Koyama H, Lewis ER, Leverenz EL, Baird RA (1982) Acute seismic sensitivity in the bullfrog ear. Brain Res 250:168–172PubMedCrossRef
go back to reference Lenzi D, Runyeon JW, Crum J, Ellisman MH, Roberts WM (1999) Synaptic vesicle populations in saccular hair cells reconstructed by electron tomography. J Neurosci 19:119–132PubMed Lenzi D, Runyeon JW, Crum J, Ellisman MH, Roberts WM (1999) Synaptic vesicle populations in saccular hair cells reconstructed by electron tomography. J Neurosci 19:119–132PubMed
go back to reference Lewis ER (1976) Surface morphology of the bullfrog amphibian papilla. Brain Behav Evol 13:196–215PubMedCrossRef Lewis ER (1976) Surface morphology of the bullfrog amphibian papilla. Brain Behav Evol 13:196–215PubMedCrossRef
go back to reference Lewis ER, Narins PM (1999) The acoustic periphery of amphibians: anatomy and physiology. In: Comparative hearing: fish and amphibians. Springer, New York, pp 101–154CrossRef Lewis ER, Narins PM (1999) The acoustic periphery of amphibians: anatomy and physiology. In: Comparative hearing: fish and amphibians. Springer, New York, pp 101–154CrossRef
go back to reference Lewis ER, Baird RA, Leverenz EL, Koyama H (1982) Inner ear: dye injection reveals peripheral origins of specific sensitivities. Science 215:1641–1643PubMedCrossRef Lewis ER, Baird RA, Leverenz EL, Koyama H (1982) Inner ear: dye injection reveals peripheral origins of specific sensitivities. Science 215:1641–1643PubMedCrossRef
go back to reference Li CW, Lewis ER (1974) Morphogenesis of auditory receptor epithelia in the bullfrog. Scan Electron Microsc 1974:791–798 Li CW, Lewis ER (1974) Morphogenesis of auditory receptor epithelia in the bullfrog. Scan Electron Microsc 1974:791–798
go back to reference Li GL, Keen E, Andor-Ardo D, Hudspeth AJ, von Gersdorff H (2009) The unitary event underlying multiquantal EPSCs at a hair cell’s ribbon synapse. J Neurosci 29:7558–7568PubMedCrossRef Li GL, Keen E, Andor-Ardo D, Hudspeth AJ, von Gersdorff H (2009) The unitary event underlying multiquantal EPSCs at a hair cell’s ribbon synapse. J Neurosci 29:7558–7568PubMedCrossRef
go back to reference Martinez-Dunst C, Michaels RL, Fuchs PA (1997) Release sites and calcium channels in hair cells of the chick’s cochlea. J Neurosci 17:9133–9144PubMed Martinez-Dunst C, Michaels RL, Fuchs PA (1997) Release sites and calcium channels in hair cells of the chick’s cochlea. J Neurosci 17:9133–9144PubMed
go back to reference Meyer AC, Frank T, Khimich D, Hoch G, Riedel D, Chapochnikov NM, Yarin YM, Harke B, Hell SW, Egner A, Moser T (2009) Tuning of synapse number, structure and function in the cochlea. Nat Neurosci 12:444–453PubMedCrossRef Meyer AC, Frank T, Khimich D, Hoch G, Riedel D, Chapochnikov NM, Yarin YM, Harke B, Hell SW, Egner A, Moser T (2009) Tuning of synapse number, structure and function in the cochlea. Nat Neurosci 12:444–453PubMedCrossRef
go back to reference 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 USA 97:883–888PubMedCrossRef 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 USA 97:883–888PubMedCrossRef
go back to reference Narins PM (1987) Coding of signals in noise by amphibian auditory nerve fibers. Hear Res 26:145–154PubMedCrossRef Narins PM (1987) Coding of signals in noise by amphibian auditory nerve fibers. Hear Res 26:145–154PubMedCrossRef
go back to reference Nouvian R, Beutner D, Parsons TD, Moser T (2006) Structure and function of the hair cell ribbon synapse. J Membr Biol 209:153–165PubMedCrossRef Nouvian R, Beutner D, Parsons TD, Moser T (2006) Structure and function of the hair cell ribbon synapse. J Membr Biol 209:153–165PubMedCrossRef
go back to reference Ospeck M, Eguiluz VM, Magnasco MO (2001) Evidence of a Hopf bifurcation in frog hair cells. Biophys J 80:2597–2607PubMedCrossRef Ospeck M, Eguiluz VM, Magnasco MO (2001) Evidence of a Hopf bifurcation in frog hair cells. Biophys J 80:2597–2607PubMedCrossRef
go back to reference Parsons TD, Lenzi D, Almers W, Roberts WM (1994) Calcium-triggered exocytosis and endocytosis in an isolated presynaptic cell: capacitance measurements in saccular hair cells. Neuron 13:875–883PubMedCrossRef Parsons TD, Lenzi D, Almers W, Roberts WM (1994) Calcium-triggered exocytosis and endocytosis in an isolated presynaptic cell: capacitance measurements in saccular hair cells. Neuron 13:875–883PubMedCrossRef
go back to reference Pitchford S, Ashmore JF (1987) An electrical resonance in hair cells of the amphibian papilla of the frog Rana temporaria. Hear Res 27:75–83PubMedCrossRef Pitchford S, Ashmore JF (1987) An electrical resonance in hair cells of the amphibian papilla of the frog Rana temporaria. Hear Res 27:75–83PubMedCrossRef
go back to reference Roberts WM (1994) Localization of calcium signals by a mobile calcium buffer in frog saccular hair cells. J Neurosci 14:3246–3262PubMed Roberts WM (1994) Localization of calcium signals by a mobile calcium buffer in frog saccular hair cells. J Neurosci 14:3246–3262PubMed
go back to reference Roberts WM, Jacobs RA, Hudspeth AJ (1990) Colocalization of ion channels involved in frequency selectivity and synaptic transmission at presynaptic active zones of hair cells. J Neurosci 10:3664–3684PubMed Roberts WM, Jacobs RA, Hudspeth AJ (1990) Colocalization of ion channels involved in frequency selectivity and synaptic transmission at presynaptic active zones of hair cells. J Neurosci 10:3664–3684PubMed
go back to reference Robles L, Ruggero MA (2001) Mechanics of the mammalian cochlea. Physiol Rev 81:1305–1352PubMed Robles L, Ruggero MA (2001) Mechanics of the mammalian cochlea. Physiol Rev 81:1305–1352PubMed
go back to reference 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 127:277–289PubMedCrossRef 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 127:277–289PubMedCrossRef
go back to reference Rutherford MA, Roberts WM (2006) Frequency selectivity of synaptic exocytosis in frog saccular hair cells. Proc Natl Acad Sci USA 103:2898–2903PubMedCrossRef Rutherford MA, Roberts WM (2006) Frequency selectivity of synaptic exocytosis in frog saccular hair cells. Proc Natl Acad Sci USA 103:2898–2903PubMedCrossRef
go back to reference Rutherford MA, Roberts WM (2009) Spikes and membrane potential oscillations in hair cells generate periodic afferent activity in the frog sacculus. J Neurosci 29:10025–10037PubMedCrossRef Rutherford MA, Roberts WM (2009) Spikes and membrane potential oscillations in hair cells generate periodic afferent activity in the frog sacculus. J Neurosci 29:10025–10037PubMedCrossRef
go back to reference Schmiedt RA (1989) Spontaneous rates, thresholds and tuning of auditory-nerve fibers in the gerbil: comparisons to cat data. Hear Res 42:23–35PubMedCrossRef Schmiedt RA (1989) Spontaneous rates, thresholds and tuning of auditory-nerve fibers in the gerbil: comparisons to cat data. Hear Res 42:23–35PubMedCrossRef
go back to reference Schnee ME, Lawton DM, Furness DN, Benke TA, Ricci AJ (2005) Auditory hair cell-afferent fiber synapses are specialized to operate at their best frequencies. Neuron 47:243–254PubMedCrossRef Schnee ME, Lawton DM, Furness DN, Benke TA, Ricci AJ (2005) Auditory hair cell-afferent fiber synapses are specialized to operate at their best frequencies. Neuron 47:243–254PubMedCrossRef
go back to reference Schwaller B (2009) The continuing disappearance of “pure” Ca2+ buffers. Cell Mol Life Sci 66:275–300PubMedCrossRef Schwaller B (2009) The continuing disappearance of “pure” Ca2+ buffers. Cell Mol Life Sci 66:275–300PubMedCrossRef
go back to reference Simmons DD, Bertolotto C, Narins PM (1992) Innervation of the amphibian and basilar papillae in the leopard frog: reconstructions of single labeled fibers. J Comp Neurol 322:191–200PubMedCrossRef Simmons DD, Bertolotto C, Narins PM (1992) Innervation of the amphibian and basilar papillae in the leopard frog: reconstructions of single labeled fibers. J Comp Neurol 322:191–200PubMedCrossRef
go back to reference Simmons DD, Bertolotto C, Narins PM (1994) Morphological gradients in sensory hair cells of the amphibian papilla of the frog, Rana pipiens pipiens. Hear Res 80:71–78PubMedCrossRef Simmons DD, Bertolotto C, Narins PM (1994) Morphological gradients in sensory hair cells of the amphibian papilla of the frog, Rana pipiens pipiens. Hear Res 80:71–78PubMedCrossRef
go back to reference Simmons DD, Bertolotto C, Leong M (1995) Synaptic ultrastructure within the amphibian papilla Rana pipiens pipiens: rostrocaudal differences. Audit Neurosci 1:183–193 Simmons DD, Bertolotto C, Leong M (1995) Synaptic ultrastructure within the amphibian papilla Rana pipiens pipiens: rostrocaudal differences. Audit Neurosci 1:183–193
go back to reference Smotherman MS, Narins PM (1999) The electrical properties of auditory hair cells in the frog amphibian papilla. J Neurosci 19:5275–5292PubMed Smotherman MS, Narins PM (1999) The electrical properties of auditory hair cells in the frog amphibian papilla. J Neurosci 19:5275–5292PubMed
go back to reference Solsona C, Innocenti B, Fernandez JM (1998) Regulation of exocytotic fusion by cell inflation. Biophys J 74:1061–1073PubMedCrossRef Solsona C, Innocenti B, Fernandez JM (1998) Regulation of exocytotic fusion by cell inflation. Biophys J 74:1061–1073PubMedCrossRef
go back to reference Spassova M, Eisen MD, Saunders JC, Parsons TD (2001) Chick cochlear hair cell exocytosis mediated by dihydropyridine-sensitive calcium channels. J Physiol 535:689–696PubMedCrossRef Spassova M, Eisen MD, Saunders JC, Parsons TD (2001) Chick cochlear hair cell exocytosis mediated by dihydropyridine-sensitive calcium channels. J Physiol 535:689–696PubMedCrossRef
go back to reference Stiebler IB, Narins PM (1990) Temperature-dependence of auditory nerve response properties in the frog. Hear Res 46:63–81PubMedCrossRef Stiebler IB, Narins PM (1990) Temperature-dependence of auditory nerve response properties in the frog. Hear Res 46:63–81PubMedCrossRef
go back to reference Van Dijk P, Mason MJ, Schoffelen RL, Narins PM, Meenderink SWF (2011) Mechanics of the frog ear. Hear Res 273:46–58PubMedCrossRef Van Dijk P, Mason MJ, Schoffelen RL, Narins PM, Meenderink SWF (2011) Mechanics of the frog ear. Hear Res 273:46–58PubMedCrossRef
go back to reference Wittig JH Jr, Parsons TD (2008) Synaptic ribbon enables temporal precision of hair cell afferent synapse by increasing the number of readily releasable vesicles: a modeling study. J Neurophysiol 100:1724–1739PubMedCrossRef Wittig JH Jr, Parsons TD (2008) Synaptic ribbon enables temporal precision of hair cell afferent synapse by increasing the number of readily releasable vesicles: a modeling study. J Neurophysiol 100:1724–1739PubMedCrossRef
go back to reference Zakon HH, Wilczynski W (1988) The physiology of the anuran VIIIth nerve. In: Fritzsch B, Wolkowiak W, Ryan MJ, Wilczynski W, Hetherington T (eds) The evolution of the amphibian auditory system. Wiley, New York, pp 125–155 Zakon HH, Wilczynski W (1988) The physiology of the anuran VIIIth nerve. In: Fritzsch B, Wolkowiak W, Ryan MJ, Wilczynski W, Hetherington T (eds) The evolution of the amphibian auditory system. Wiley, New York, pp 125–155
go back to reference Zelick R, Narins PM (1985) Temporary threshold shift, adaptation, and recovery characteristics of frog auditory nerve fibers. Hear Res 17:161–176PubMedCrossRef Zelick R, Narins PM (1985) Temporary threshold shift, adaptation, and recovery characteristics of frog auditory nerve fibers. Hear Res 17:161–176PubMedCrossRef
Metadata
Title
Exocytosis in the Frog Amphibian Papilla
Authors
Patricia M. Quiñones
Cindy Luu
Felix E. Schweizer
Peter M. Narins
Publication date
01-02-2012
Publisher
Springer-Verlag
Published in
Journal of the Association for Research in Otolaryngology / Issue 1/2012
Print ISSN: 1525-3961
Electronic ISSN: 1438-7573
DOI
https://doi.org/10.1007/s10162-011-0304-1

Other articles of this Issue 1/2012

Journal of the Association for Research in Otolaryngology 1/2012 Go to the issue