Abstract
Type I and Type II hair cells, and Type II hair cells located in different zones of the semicircular canal crista, express different patterns of voltage-dependent K channels, each one specifically shaping the hair cell receptor potential. We report here that, close to hatching, chicken embryo semicircular canal Type I and Type II hair cells express a similar voltage-dependent L-type calcium current (ICa), whose main features are: activation above −60 mV, fast activation kinetics, and scarce inactivation. ICa should be already active at rest in Zone 1 Type II hair cells, whose resting membrane potential was on average slightly less negative than −60 mV. Conversely, ICa would not be active at rest in Type II hair cells from Zone 2 and 3, nor in Type I hair cells, since their resting membrane potential was significantly more negative than −60 mV. However, even small depolarising currents would activate ICa steadily in Zone 2 and 3 Type II hair cells, but not in Type I hair cells because of the robust repolarising action of their specific array of K+ currents. The implications of the present findings in the afferent discharge are discussed.
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References
Allen TJ (1996) Temperature dependence of macroscopic L-type calcium channel currents in single guinea pig ventricular myocytes. J Cardiovasc Electrophysiol 7(4):307–321
Almanza A, Vega R, Soto E (2003) Calcium current in Type I hair cells isolated from the semicircular canal crista ampullaris of the rat. Brain Res 994(2):175–180
Assad JA, Hacohen N, Corey DP (1989) Voltage dependence of adaptation and active bundle movement in bullfrog saccular hair cells. Proc Natl Acad Sci USA 86(8):2918–2922
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(1):155–164
Behrend O, Schwark C, Kunihiro T, Strupp M. (1997) Cyclic GMP inhibits and shifts the activation curve of the delayed-rectifier (I[K1]) of Type I mammalian vestibular hair cells. Neuroreport 8(12):2687–2690
Beutner D, Moser T (2001) The presynaptic function of mouse cochlear inner hair cells during development of hearing. J Neurosci 21(13):4593–4599
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(6):3259–3278
Carbone E, Swandulla D (1989) Neuronal calcium channels: kinetics, blockade and modulation. Prog Biophys Mol Biol 54(1):31–58
Chabbert C, Mechaly I, Sieso V, Giraud P, Brugeaud A, Lehouelleur J, Couraud F, Valmier J, Sans A (2003) Voltage-gated Na+ channel activation induces both action potentials in utricular hair cells and brain-derived neurotrophic factor release in the rat utricle during a restricted period of development. J Physiol 553(Pt 1):113–123
Chen JW, Eatock RA (2000) Major potassium conductance in Type I hair cells from rat semicircular canals: characterization and modulation by nitric oxide. J Neurophysiol 84(1):139–151
Correia MJ, Ricci AJ, Rennie KJ (1996) Filtering properties of vestibular hair cells: an update. Ann N Y Acad Sci 781:138–149
Dickman JD, Correia MJ (1989) Responses of pigeon horizontal semicircular canal afferent fibers. II. High-frequency mechanical stimulation. J Neurophysiol 62(5):1102–1112
Dou H, Vazquez AE, Namkung Y, Chu H, Cardell EL, Nie L, Parson S, Shin HS, Yamoah EN (2004) Null mutation of alpha1D Ca2+ channel gene results in deafness but no vestibular defect in mice. J Assoc Res Otolaryngol 5(2):215–226
Elmslie KS, Kammermeier PJ, Jones SW (1994) Reevaluation of Ca2+ channel types and their modulation in bullfrog sympathetic neurons. Neuron 13(1):217–228
Fettiplace R, Crawford AC, Evans MG (1992) The hair cell’s mechanoelectrical transducer channel. Ann N Y Acad Sci 656:1–11
Geleoc GS, Risner JR, Holt JR. (2004) Developmental acquisition of voltage-dependent conductances and sensory signaling in hair cells of the embryonic mouse inner ear. J Neurosci 24(49):11148–11159
Goldberg JM (1996) Theoretical analysis of intercellular communication between the vestibular Type I hair cell and its calyx ending. J Neurophysiol 76(3):1942–1957
Goldberg JM (2000) Afferent diversity and the organization of central vestibular pathways. Exp Brain Res 130(3):277–297
Goldberg JM, Brichta AM (2002) Functional analysis of whole cell currents from hair cells of the turtle posterior crista. J Neurophysiol 88(6):3279–3292
Griguer C, Sans A, Lehouelleur J (1993) Non-typical K(+)-current in cesium-loaded guinea pig Type I vestibular hair cell. Pfluegers Arch 422(4):407–409
Herve JC, Yamaoka K, Twist VW, Powell T, Ellory JC, Wang LC (1992) Temperature dependence of electrophysiological properties of guinea pig and ground squirrel myocytes. Am J Physiol 263(1 Pt 2):R177–R184
Hille B (2001) Ion channels of excitable membrane, 3rd edn. Sinauer Associates Inc., Sunderland
Holt JR, Corey DP, Eatock RA (1997) Mechanoelectrical transduction and adaptation in hair cells of the mouse utricle, a low-frequency vestibular organ. J Neurosci 17(22):8739–8748
Horn R, Marty A (1988) Muscarinic activation of ionic currents measured by a new whole-cell recording method. J Gen Physiol 92:145–159
Huguenard JR, Prince DA (1992) A novel T-type current underlies prolonged Ca(2+)-dependent burst firing in GABAergic neurons of rat thalamic reticular nucleus. J Neurosci 12(10):3804–3817
Hurley KM, Eatock RA (1999) Characterization and modulation of a delayed rectifier in vestibular Type I hair cells. ARO Annu Meet Assoc Res Otolaryngol Abstr N. 764
Jones SW (1998) Overview of voltage-dependent Ca channels. J Bioenerg Biomembr 30(4):299–312
Kenyon JL, Goff HR (1998) Temperature dependencies of Ca2+ current, Ca(2+) -activated Cl− current and Ca2+ transients in sensory neurones. Cell Calcium 24(1):35–48
Kollmar R, Montgomery LG, Fak J, Henry LJ, Hudspeth AJ (1997) 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(26):14883–14888
Kros CJ, Ruppersberg JP, Rusch A (1998) Expression of a potassium current in inner hair cells during development of hearing in mice. Nature 394(6690):281–284
Lang DG, Correia MJ (1989) Studies of solitary semicircular canal hair cells in the adult pigeon. II. Voltage-dependent ionic conductances. J Neurophysiol 62(4):935–945
Lennan GW, Steinacker A, Lehouelleur J, Sans A (1999) Ionic currents and current-clamp depolarisations of Type I and Type II hair cells from the developing rat utricle. Pfluegers Arch 438(1):40–46
Lorenzon NM, Foehring RC (1995) Characterization of pharmacologically identified voltage-gated calcium channel currents in acutely isolated rat neocortical neurons. I. Adult neurons. J Neurophysiol 73(4):1430–1442
Manley GA, Kaiser A, Brix J, Gleich O (1991) Activity patterns of primary auditory-nerve fibres in chickens: development of fundamental properties. Hear Res 57(1):1–15
Marcotti W, Russo G, Prigioni I (1999) Position-dependent expression of inwardly rectifying K+ currents by hair cells of frog semicircular canals. Neuroreport 10(3):601–606
Masetto S, Russo G, Prigioni I (1994) Differential expression of potassium currents by hair cells in thin slices of frog crista ampullaris. J Neurophysiol 72:443–455
Masetto S, Correia MJ (1997) Electrophysiological properties of vestibular sensory and supporting cells in the labyrinth slice before and during regeneration. J Neurophysiol 78(4):1913–1927
Masetto S, Weng T, Valli P, Correia MJ (1999) Artifactual voltage response recorded from hair cells with patch-clamp amplifiers. Neuroreport 10(9):1837–1841
Masetto S, Perin P, Malusa A, Zucca G, Valli P (2000) Membrane properties of chick semicircular canal hair cells in situ during embryonic development. J Neurophysiol 83(5):2740–2756
Masetto S, Bosica M, Correia MJ, Ottersen OP, Zucca G, Perin P, Valli P (2003) Na+ currents in vestibular Type I and Type II hair cells of the embryo and adult chicken. J Neurophysiol 90(2):1266–1278
Meza G, Hinojosa R (1987) Ontogenetic approach to cellular localization of neurotransmitters in the chick vestibule. Hear Res 28(1):73–85
Narahashi T, Tsunoo A, Yoshii M (1987) Characterization of two types of calcium channels in mouse neuroblastoma cells. J Physiol 383:231–249
Nobile M, Carbone E, Lux HD, Zucker H (1990) Temperature sensitivity of Ca currents in chick sensory neurones. Pflugers Arch 415(6):658–663
Perin P, Masetto S, Martini M, Rossi ML, Rubbini G, Rispoli G, Guth P, Zucca G, Valli P (2001) Regional distribution of calcium currents in frog semicircular canal hair cells. Hear Res 152(1–2):67–76
Platzer J, Engel J, Schrott-Fischer A, Stephan K, Bova S, Chen H, Zheng H, Striessnig J (2000) Congenital deafness and sinoatrial node dysfunction in mice lacking class D L-type Ca2+ channels. Cell 102(1):89–97
Prigioni I, Masetto S, Russo G, Taglietti V (1992) Calcium currents in solitary hair cells isolated from frog crista ampullaris. J Vestib Res 2(1):31–39
Prigioni I, Russo G, Marcotti W (1996) Potassium currents of pear-shaped hair cells in relation to their location in frog crista ampullaris. Neuroreport 7(11):1841–1845
Rennie KJ, Correia MJ (1994) Potassium currents in mammalian and avian isolated Type I semicircular canal hair cells. J Neurophysiol 71:317–329
Rennie KJ, Ricci AJ, Correia MJ (1996) Electrical filtering in gerbil isolated Type I semicircular canal hair cells. J Neurophysiol 75(5):2117–2123
Rennie KJ, Correia MJ (2000) Effects of cationic substitutions on delayed rectifier current in Type I vestibular hair cells. J Membr Biol 173(2):139–148
Ricci AJ, Fettiplace R (1998) Calcium permeation of the turtle hair cell mechanotransducer channel and its relation to the composition of endolymph. J Physiol 506(1):159–173
Ricci AJ, Crawford AC, Fettiplace R (2003) Tonotopic variation in the conductance of the hair cell mechanotransducer channel. Neuron 40(5):983–990
Roberts WM, Jacobs RA, Hudspeth AJ (1991) The hair cell as a presynaptic terminal. Ann N Y Acad Sci 635:221–233
Rodriguez-Contreras A, Yamoah EN (2001) Direct measurement of single-channel Ca(2+) currents in bullfrog hair cells reveals two distinct channel subtypes. J Physiol 534(Pt 3):669–689
Rüsch A, Eatock RA (1996) A delayed rectifier conductance in Type I hair cells of the mouse utricle. J Neurophysiol 76:994–1004
Rüsch A, Eatock RA (1996) Voltage responses of mouse utricular hair cells to injected currents. Ann N Y Acad Sci 781:71–84
Russo G, Lelli A, Marcotti W, Prigioni I (2001) Gradients of expression of calcium and potassium currents in frog crista ampullaris. Pfluegers Arch 442(6):814–820
Russo G, Lelli A, Gioglio L, Prigioni I (2003) Nature and expression of dihydropyridine-sensitive and -insensitive calcium currents in hair cells of frog semicircular canals. Pfluegers Arch 446(2):189–197
Soto E, Vega R, Budelli R (2002) The receptor potential in Type I and Type II vestibular system hair cells: a model analysis. Hear Res 165:35–47
Spassova M, Eisen MD, Saunders JC, Parsons TD (2001) Chick cochlear hair cell exocytosis mediated by dihydropyridine-sensitive calcium channels. J Physiol 535(3):689–696
Sugihara I, Furukawa T (1989) Morphological and functional aspects of two different types of hair cells in the goldfish sacculus. J Neurophysiol 62(6):1330–1343
Todorovic SM, Lingle CJ (1998) Pharmacological properties of T-type Ca2+ current in adult rat sensory neurons: effects of anticonvulsant and anesthetic agents. J Neurophysiol 79(1):240–252
Weng TX, Correia MJ (1999) Regional distribution of ionic currents and membrane voltage responses of Type II hair cells in the vestibular neuroepithelium. J Neurophysiol 82(5):2451–2461
Wong WH, Hurley KM, Eatock RA (2004) Differences between the negatively activating potassium conductances of Mammalian cochlear and vestibular hair cells. J Assoc Res Otolaryngol 5(3):270–284
Xu W, Lipscombe D (2001) Neuronal Ca(V)1.3alpha(1) L-type channels activate at relatively hyperpolarized membrane potentials and are incompletely inhibited by dihydropyridines. J Neurosci 21(16):5944–5951
Zhang JF, Randall AD, Ellinor PT, Horne WA, Sather WA, Tanabe T, Schwarz TL, Tsien RW (1993) Distinctive pharmacology and kinetics of cloned neuronal Ca2+ channels and their possible counterparts in mammalian CNS neurons. Neuropharmacology 32(11):1075–1088
Zidanic M, Fuchs PA (1995) Kinetic analysis of barium currents in chick cochlear hair cells. Biophys J 68(4):1323–1336
Acknowledgments
We thank Dr. M. J. Correia and Dr. P. S. Guth, for valuable comments on the manuscript. This work was supported by the Ministero della Ricerca Scientifica e Tecnologica (MURST), Rome, Italy.
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Masetto, S., Zampini, V., Zucca, G. et al. Ca2+ currents and voltage responses in Type I and Type II hair cells of the chick embryo semicircular canal. Pflugers Arch - Eur J Physiol 451, 395–408 (2005). https://doi.org/10.1007/s00424-005-1466-7
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DOI: https://doi.org/10.1007/s00424-005-1466-7