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Activity-dependent changes in voltage-dependent calcium currents and transmitter release

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Abstract

Voltage-dependent Ca2+ channels are important in the regulation of neuronal structure and function, and as a result, they have received considerable attention. Recent studies have begun to characterize the diversity of their properties and the relationship of this diversity to their various cellular functions. In particular, Ca2+ channels play a prominent role in depolarization-secretion coupling, where the release of neurotransmitter is very sensitive to changes in voltage-dependent Ca2+ currents. An important feature of Ca2+ channels is their regulation by electrical activity. Depolarization can selectively modulate the properties of Ca2+ channel types, thus shaping the response of the neuron to future electrical activity. In this article, we examine the diversity of Ca2+ channels found in vertebrate and invertebrate neurons, and their short- and long-term regulation by membrane potential and Ca2+ influx. Additionally, we consider the extent to which this activity-dependent regulation of Ca2+ currents contributes to the development and plasticity of transmitter releasing properties. In the studies of long-term regulation, we focus on crustacean motoneurons where activity levels, Ca2+ channel properties, and transmitter releasing properties can be followed in identified neurons.

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References

  • Akaike N., Kostyuk P. G., and Osipchuk Y. V. (1989) dihydropyridine-sensitive low-threshold calcium channels is isolated rat hypothalamic neurones.J. Physiol. (Lond.) 412, 181–195.

    CAS  Google Scholar 

  • Anglister L., Farber I. C., Shahar A., and Grinvald A. (1982) Localization of voltage-sensitive calcium channels along developing neurites: their possible role in regulating neurite elongation.Dev. Biol. 94, 351–365.

    PubMed  CAS  Google Scholar 

  • Angstadt J. D. and Calabrese R. L. (1991) Calcium currents and graded synaptic transmission between heart interneurons of the leech.J. Neurosci. 11(3), 746–759.

    PubMed  CAS  Google Scholar 

  • Araque A., Clarac F., and Buño W. (1994) P-type Ca2+ channels mediate excitatory and inhibitory synaptic transmitter release in crayfish muscle.Proc. Natl. Acad. Sci. USA 91, 4224–4228.

    PubMed  CAS  Google Scholar 

  • Arcaro K. and Lnenicka G. A. (1997) Differential effects of depolarization on the growth of crayfish tonic and phasic motor axons in culture.J. Neurobiol., in press

  • Artalejo C. R., Dahmer M. K., Perlman R. L., and Fox A. P. (1991) Two types of Ca2+ currents are found in bovine chromaffin cells: facilitation is due to the recruitment of one type.J. Physiol. (Lond.) 432, 681–707.

    CAS  Google Scholar 

  • Artalejo C. R., Rossie S., Perlman R., and Fox A. P. (1992) Voltage-dependent phosphorylation may recruit Ca2+ current facilitation in chromaffin cells.Nature 358, 63–66.

    PubMed  CAS  Google Scholar 

  • Artalejo C. R., Adams M. E., and Fox A. P. (1994) Three types of Ca2+ channels trigger secretion with different efficacies in chromaffin cells.Nature 367, 72–76.

    PubMed  CAS  Google Scholar 

  • Artola A. and Singer W. (1993) Long-term depression of excitatory synaptic transmission and its relationship to long-term potentiation.Trends Neurosci. 16(11), 480–487.

    PubMed  CAS  Google Scholar 

  • Artola A., Brocher S., and Singer W. (1990) Different voltage-dependent thresholds for inducing long-term depression and long-term potentiation in slices of rat visual cortex.Nature 347, 69–72.

    PubMed  CAS  Google Scholar 

  • Atwood H. L. and Johnston H. S. (1968) Neuromuscular synapses of a crab motor axon.J. Exp. Zool. 167, 457–470.

    Google Scholar 

  • Atwood H. L. and Wojtowicz J. M. (1986) Short-term and long-term plasticity and physiological differentiation of crustacean motor synapses.Int. Rev. Neurobiol. 28, 275–362.

    PubMed  CAS  Google Scholar 

  • Augustine G. J. and Eckert R. (1984) Calcium-dependent inactivation of presynaptic calcium channels.Soc. Neurosci. Abstract 10, 194.

    Google Scholar 

  • Augustine G. J., Charlton M. P., and Smith S. J. (1987) Calcium action in synaptic transmitter release.Annu Rev. Neurosci. 10, 633–693.

    PubMed  CAS  Google Scholar 

  • Bailey C. H. and Chen M. (1988a) Morphological basis of short-term habituation inAplysia.J. Neurosci. 8(7), 2452–2459.

    PubMed  CAS  Google Scholar 

  • Bailey C. H. and Chen M. (1988b) Long-term memory inAplysia modulates the total number of varicosities of single identified sensory neurons.Proc. Natl. Acad. Sci. USA 85, 2373–2377.

    PubMed  CAS  Google Scholar 

  • Baimbridge K. G., Mody I., and Miller J. J. (1985) Reduction of rat hippocampal calcium-binding protein following commissural, amygdala, septal, perforant path and olfactory bulb kindling.Epilepsia 26, 460–465.

    PubMed  CAS  Google Scholar 

  • Bargas J., Howe A., Eberwine J., Cao Y., and Surmeier D. J. (1994) Cellular and molecular characterization of Ca2+ currents in acutely isolated, adult rat neostriatal neurons.J. Neurosci. 14, 6667–6686.

    PubMed  CAS  Google Scholar 

  • Bar-Sagi D. and Prives J. (1985) Negative modulation of sodium channels in cultured chick muscle cells by the channel activator batrachotoxin.J. Biol. Chem. 260(8), 4740–4744.

    PubMed  CAS  Google Scholar 

  • Belles B., Hescheler J., Blomgren W., and Karlsson J. O. (1988) A possible physiological role of Ca2+-dependent protease calpain and its inhibitor calpastatin on the Ca2+ current in guinea pig myocytes.Pflügers Arch. 412, 554–556.

    PubMed  CAS  Google Scholar 

  • Bennett M. K., Calakos N., and Scheller R. H. (1992) Syntaxin: a synaptic protein implicated in docking of synaptic vesicles at presynaptic active zones.Science 257, 255–259.

    PubMed  CAS  Google Scholar 

  • Berdan R. C., Easaw J. C., and Wang R. (1993b) Alterations in membrane potential after axotomy at different distances from the soma of an identified neuron and the effect of depolarization on neurite outgrowth and calcium channel expression.J. Neurophysiol. 69(1), 151–164.

    PubMed  CAS  Google Scholar 

  • Blatz A. L. and Magleby K. L. (1987) Calcium-activated potassium channels.Trends Neurosci. 10, 463–467.

    CAS  Google Scholar 

  • Blundon J. A., Wright S. N., Brodwick M. S., and Bittner G. D. (1995) Presynaptic calcium-activated potassium channels and calcium channels at a crayfish neuromuscular junction.J. Neurophysiol. 73, 178–189.

    PubMed  CAS  Google Scholar 

  • Bolshakov V. Y. and Siegelbaum S. A. (1994) Postsynaptic induction and presynaptic expression of hippocampal long-term depression.Science 264, 1148–1152.

    PubMed  CAS  Google Scholar 

  • Bookman R. J. and Liu Y. (1990) Analysis of calcium channel properties in cultured leech Retzius cells by internal perfusion, voltage-clamp and single-channel recording.J. Exp. Biol. 149, 223–237.

    PubMed  CAS  Google Scholar 

  • Bossu J.-L. and Feltz A. (1986) Inactivation of the low-threshold transient calcium current in rat sensory neurones: evidence for a dual process.J. Physiol. (Lond.) 376, 341–357.

    CAS  Google Scholar 

  • Bourinet E., Charnet P., Tomlinson W. J., Stea A., Snutch T. P., and Nargeot J. (1994) Voltage-dependent facilitation of a neuronal α1C L-type calcium channel.EMBO J. 13(21), 5032–5039.

    PubMed  CAS  Google Scholar 

  • Bradacs H., Mercier A. J., and Atwood H. L. (1990) Long-term adaptation in lobster motor neurons and compensation of transmitter release by synergistic inputs.Neurosci. Lett. 108, 110–115.

    PubMed  CAS  Google Scholar 

  • Brehm P. and Eckert R. (1978) Calcium entry leads to inactivation of calcium channel inParamecium.Science 202, 1203–1206.

    PubMed  CAS  Google Scholar 

  • Brown A. M., Morimoto K., Tsuda Y., and Wilson D. L. (1981) Calcium current-dependent and voltage-dependent inactivation of calcium channels inHelix aspersa.J. Physiol. (Lond.) 320, 193–218.

    CAS  Google Scholar 

  • Bruner J. and Kennedy D. (1970) Habituation: occurrence at a neuromuscular junction.Science 169, 92–94.

    PubMed  CAS  Google Scholar 

  • Byrne J. H. (1982) Analysis of synaptic depression contributing to habituation of gill-withdrawal reflex inAplysia californica.J. Neurophysiol. 48(2), 431–438.

    PubMed  CAS  Google Scholar 

  • Byerly L. and Hagiwara S. (1988) Calcium channel diversity, inCalcium and Ion Channel Modulation (Grinnell A. D., Armstrong D., and Jackson M. B., eds.), Plenum, New York, pp. 3–18.

    Google Scholar 

  • Carbone E. and Lux H. D. (1984) A low voltage-activated, fully inactivating Ca2+ channel in vertebrate sensory neurones.Nature 310, 501,502.

    PubMed  CAS  Google Scholar 

  • Carbone E. and Lux H. D. (1987) Kinetics and selectivity of a low-voltage-activated calcium current in chick and rat sensory neurons.J. Physiol. (Lond.) 386, 547–570.

    CAS  Google Scholar 

  • Case C. and Lnenicka G. A. (1992) Mitochondrial content and transport in phasic and tonic motor axons of the crayfish.Soc. Neurosci. Abstract 18, 1413.

    Google Scholar 

  • Castellucci V. F. and Kandel E. R. (1974) A quantal analysis of the synaptic depression underlying habituation of the gill-withdrawal reflex inAplysia.Proc. Natl. Acad. Sci. USA 71(12), 5004–5008.

    PubMed  CAS  Google Scholar 

  • Castellucci V., Pinsker H., Kupfermann I., and Kandel E. R. (1970) Neuronal mechanisms of habituation and dishabituation of the gill-with-drawal reflex inAplysia.Science 167, 1745–1748.

    PubMed  CAS  Google Scholar 

  • Castellucci V. F., Carew T. J., and Kandel E. R. (1978) Cellular analysis of long-term habituation of the gill-withdrawal reflex ofAplysia californica.Science 202(22), 1306–1308.

    PubMed  CAS  Google Scholar 

  • Castillo P. E., Weisskopf M. G., and Nicoll R. A. (1994) The role of Ca2+ channels in hippocampal mossy fiber synaptic transmission and long term potentiation.Neuron 12, 261–269.

    PubMed  CAS  Google Scholar 

  • Celio M. R. (1986) Parvalbumin in most gamma-aminobutyric acid-containing neurons of the rat cerebral cortex.Science 231, 995–997.

    PubMed  CAS  Google Scholar 

  • Chad J. E. and Eckert R.. (1984) Calcium domains associated with individual channels can account for anomalous voltage relations of Ca2+-dependent.Biophys. J. 45, 993–999.

    PubMed  CAS  Google Scholar 

  • Chad J. E. and Eckert R. (1986) An enzymatic mechanism for calcium current inactivation in dialysedHelix neurones.J. Physiol. (Lond.) 378, 31–51.

    CAS  Google Scholar 

  • Charlton M. P., Smith S. J., and Zucker R. S. (1982) Role of presynaptic calcium ions and channels in synaptic facilitation and depression at the squid giant synapse.J. Physiol. (Lond.) 323, (1 73–193.

    Google Scholar 

  • Choi D. W. (1988) Calcium-mediated neurotoxicity: relationship to specific channel types and role in ischemic damage.Trends Neurosci. 11, 465–469.

    PubMed  CAS  Google Scholar 

  • Chrachri A. (1995) Ionic currents in identified swimmeret motor neurones of the crayfishPacifastacus leniusculus.J. Exp. Biol. 198, 1483–1492.

    PubMed  Google Scholar 

  • Christie B. R. and Abraham W. C. (1992) Priming of associative long-term depression in the dentate gyrus by ϕ frequency synaptic activity.Neuron 9, 79–84.

    PubMed  CAS  Google Scholar 

  • Cohan C. S. (1990) Frequency-dependent and cell-specific effects of electrical activity on growth cone movements of cultured Helisoma neurons.J. Neurobiol. 21, 400–413.

    PubMed  CAS  Google Scholar 

  • Cox D. H. and Dunlap K. (1992) Pharmacological discrimination of N-type from L-type calcium current and its selective modulation by transmiters.J. Neurosci. 12, 906–914.

    PubMed  CAS  Google Scholar 

  • Cox D. H. and Dunlap K. (1994) Inactivation of N-type calcium current in chick sensory neurons: calcium and voltage dependence.J. Gen. Physiol. 104, 311–336.

    PubMed  CAS  Google Scholar 

  • Czternasty G., Kado R. T., and Bruner J. (1989) Analysis of mechanisms of spiking in normally “non-spiking” motoneurone somata in crayfish.J. Exp. Biol. 147, 91–110.

    Google Scholar 

  • Delaney K. R. and Tank D. W. (1994) A quantitative measurement of the dependence of short-term synaptic enhancement on presynaptic residual calcium.J. Neurosci. 14(10), 5885–5902.

    PubMed  CAS  Google Scholar 

  • Delaney K. R., Zucker R. S., and Tank D. W. (1989) Calcium in motor nerve terminals associated with posttetanic potentiation.J. Neurosci. 9(10), 3558–3567.

    PubMed  CAS  Google Scholar 

  • Del Castillo J. and Katz B. (1954) Statistical factors involved in neuromuscular facilitation and depression.J. Physiol. (Lond.) 124, 574–585.

    Google Scholar 

  • de Leon M., Wang Y., Jones L., Perez-Reyes E., Wei X., Soong T. W., Snutch T. P., and Yue D. T. (1995) Essential Ca2+-binding motif for Ca2+-sensitive inactivation of L-type Ca2+ channels.Science 270, 1502–1506.

    PubMed  Google Scholar 

  • DeLorme E. M. and McGee R. Jr. (1986) Regulation of voltage-dependent Ca2+ channels of neuronal cells by chronic changes in membrane potential.Brain Res. 397, 189–192.

    PubMed  CAS  Google Scholar 

  • DeLorme E. M., Rabe C. S., and McGee R. (1988) Regulation of the number of functional voltagesensitive calcium channels on PC12 cells by chronic changes in membrane potential.J. Pharmacol. Exp. Ther. 244(3), 838–843.

    PubMed  CAS  Google Scholar 

  • Dubel S. J., Starr T. V. B., Hell J., Ahlijanian M. K., Enyeart J. J., Catterall W. A., and Snutch T. P. (1992) Molecular cloning of the α1 subunit of an ω-conotoxin-sensitive calcium channel.Proc. Natl. Acad. Sci. USA 89, 5058–5062.

    PubMed  CAS  Google Scholar 

  • Dudek S. M. and Bear M. F. (1992) Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-d-aspartate receptor blockade.proc. Natl. Acad. Sci. USA 89, 4363–4367.

    PubMed  CAS  Google Scholar 

  • Dupont J.-L., Bossu J.-L., and Feltz A. (1986) Effect of internal calcium concentration on calcium currents in rat sensory neurones.Pflügers Arch. 406, 433–435.

    PubMed  CAS  Google Scholar 

  • Eckert R. and Ewald D. (1981) Inactivation of Ca2+ conductance characterized by tail current measurements in neurones ofAplysia californica.J. Physiol. (Lond.) 314, 265–280.

    CAS  Google Scholar 

  • Eckert R. and Tillotson D. L. (1981) Calcium-mediated inactivation of the calcium conductance in caesium-loaded giant neurones ofAplysia californica.J. Physiol. (Lond.) 314, 265–280.

    CAS  Google Scholar 

  • Edmonds B., Klein M., Dale N., and Kandel E. R. (1990) Contributions of two types of calcium channels to synaptic transmission and plasticity.Science 250, 1142–1147.

    PubMed  CAS  Google Scholar 

  • Eliot L. S., Kandel E. R., and Hawkins R. D. (1994) Modulation of spontaneous transmitter release during depression and posttetanic potentiation ofAplysia sensory-motor neuron synapses isolated in culture.J. Neurosci. 14(5), 3280–3292.

    PubMed  CAS  Google Scholar 

  • Ellinor P. T., Zhang J.-F., Randall A. D., Zhou M., Schwarz T. L., Tsien R. W., and Horne W. A. (1993) Functional expression of a rapidly inactivating neuronal calcium channel.Nature 363, 455–458.

    PubMed  CAS  Google Scholar 

  • Farinas I., Egea G., Blasi J., Cases C., and Marsal J. (1993) Calcium channel antagonist omegacontoxin binds to intramembrane particles of isolated nerve terminals.Neuroscience 54(3), 745–752.

    PubMed  CAS  Google Scholar 

  • Fenwick E. M., Marty A., and Neher E. (1982) Sodium and calcium channels in bovine chromaffin cells.J. Physiol. (Lond.) 331, 599–635.

    CAS  Google Scholar 

  • Feron O. and Godfraind T. (1995) Regulation of the L-type calcium channel α1 subunit by chronic depolarization in the neuron-like PC12 and aortic smooth muscle A7r5 cell lines.Eur. J. Physiol. (Lond.) 430, 323–332.

    CAS  Google Scholar 

  • Ferrante J., Triggle D. J., and Rutleedge A. (1991) The effects of chronic depolarization of L-type 1,4-dihydropyridine-sensitive, voltage-dependent Ca2+ channels in chick neural retina and rat cardiac cells.Can. J. Physiol. Pharmacol. 69, 914–920.

    PubMed  CAS  Google Scholar 

  • Fields R. D., Neale E. A., and Nelson P. G. (1990) Effects of patterned electrical activity on neurite outgrowth from mouse sensory neurons.J. Neurosci. 10, 2950–2964.

    PubMed  CAS  Google Scholar 

  • Fields R. D., Guthrie P. B., Russell J. T., Kater S. B., Malhotra B. S., and Nelson P. G. (1993) Accommodation of mouse DRG growth cones to electrically induced collapse: kinetic analysis of calcium transients and set-point theory.J. Neurobiol. 24(8), 1080–1098.

    PubMed  CAS  Google Scholar 

  • Fogelson A. L. and Zucker R. S. (1985) Presynaptic calcium diffusion from various arrays of single channels.Biophys. J. 48, 1003–1017.

    PubMed  CAS  Google Scholar 

  • Fossier P., Baux G., and Tauc L. (1994) N- and P-type Ca2+ channels are involved in acetylcholine release at a neuroneuronal synapse: Only the N-type channel is the target of neuromodulators.Proc. Natl. Acad. Sci. USA 91, 4771–4775.

    PubMed  CAS  Google Scholar 

  • Fox A. P., Nowycky M. C., and Tsien R. W. (1987a) Kinetic and pharmacological properties distinguishing three types of calcium channels in chick sensory neurones.J. Physiol. (Lond.) 394, 149–172.

    CAS  Google Scholar 

  • Fox A. P., Nowycky M. C., and Tsien R. W. (1987b) Single-channel recordings of three types of calcium channels in chick sensory neurones.J. Physiol. (Lond.) 394, 173–200.

    CAS  Google Scholar 

  • Franklin J. L., Fickbohm D. J., and Willard A. L. (1992) Long-term regulation of neuronal calcium currents by prolonged changes of membrane potential.J. Neurosci. 12(5), 1726–1735.

    PubMed  CAS  Google Scholar 

  • Fryer M. W. and Zucker R. S. (1993) Ca2+-dependent inactivation of Ca2+ current inAplysia neurons: kinetic studies using photolabile Ca2+ chelators.J. Physiol. (Lond.) 464, 501–528.

    CAS  Google Scholar 

  • Fujita Y., Mynlieff M., Dirksen R. T., Kim M. S., Nidome T., Nakai J., Fredruck T., Iwabe N., Miyata T., and Furuichi T. (1993) Primary structure and functional expression of the ω-conotoxin-sensitive N-type calcium channel from rabbit brain.Neuron 10, 585–598.

    PubMed  CAS  Google Scholar 

  • Gallego R. and Geijo E. (1987) Chronic block of the cervical trunk increases synaptic efficacy in the superior and stellate ganglia of the guinea-pig.J. Physiol. (Lond.) 382, 449–462.

    CAS  Google Scholar 

  • Gallego R., Kuno M., Nunez R., and Snider W. D. (1979) Disuse enhances synaptic efficacy in spinal motoneurones.J. Physiol. (Lond.) 291, 191–205.

    CAS  Google Scholar 

  • Gingrich K. J. and Byrne J. H. (1985) Simulation of synaptic depression, posttetanic potentiation, and presynaptic facilitation of synaptic potentials from sensory neurons mediating gill-withdrawal reflex inAplysia.J. Neurophysiol. 53(3), 652–669.

    PubMed  CAS  Google Scholar 

  • Gottmann K. and Lux H. D. (1990) Low- and high-voltage-activated Ca2+ conductance in n electrically excitable growth cones of chick dorsal root ganglion neurons.Neurosci. Lett. 110, 34–39.

    PubMed  CAS  Google Scholar 

  • Grabner M., Bachmann A., Rosenthal F., Striessnig J., Schulz C., Tautz D., and Glossmann H. (1994) Molecular cloning of an α1-subunit from housefly (Musca Domestica) muscle.FEBS Lett. 339, 189–194.

    PubMed  CAS  Google Scholar 

  • Grassi F. and Lux H. D. (1989) Voltage-dependent GABA-induced modulation of calcium currents in chick sensory neurons.Neurosci. Lett. 105, 113–119.

    PubMed  CAS  Google Scholar 

  • Gutnick M. J., Lux H. D., Swandulla D., and Zucker H. (1989) Voltage-dependent and calcium-dependent inactivation of calcium channel current in identified snail neurones.J. Physiol. (Lond.) 412, 197–220.

    CAS  Google Scholar 

  • Hadley R. W. and Lederer W. J. (1991) Ca2+ and voltage inactivate Ca2+ channels in guinea-pig ventricular myocytes through independent mechanisms.J. Physiol. (Lond.) 444, 257–268.

    CAS  Google Scholar 

  • Hagiwara S. and Byerly L. (1981) Calcium channel.Ann. Rev. Neurosci. 4, 69–125.

    PubMed  CAS  Google Scholar 

  • Hagiwara S. and Nakajima S. (1966) Effects of the intracellular Ca2+ ion concentration upon the excitability of the muscle fiber membrane of a barnacle.J. Gen. Physiol. 49, 807–818.

    PubMed  CAS  Google Scholar 

  • Hagiwara S., Ozawa S., and Sand O. (1975) Voltageclamp analysis of two inward current mechanisms in the egg cell membrane of a starfish.J. Gen. Physiol. 65, 617–644.

    PubMed  CAS  Google Scholar 

  • Hay M., Hasser E. M., and Lindsley K. A. (1996) Area postrema voltage-activated calcium currents.J. Neurophysiol. 75, 133–141.

    PubMed  CAS  Google Scholar 

  • Hayashi J. H. and Levine R. B. (1992) Calcium and potassium currents in leg motoneurons during postembryonic development in the hawkmothManduca sexta.J. Exp. Biol. 171, 15–42.

    PubMed  CAS  Google Scholar 

  • Haydon P. G. and Man-Son-Hing H. (1988) Low-and high-voltage-activated calcium currents: Their relationship to the site of neurotransmitter release in an identified neuron ofHelisoma.Neuron 1, 919–927.

    PubMed  CAS  Google Scholar 

  • Hernández-Cruz A. and Pape H.-C. (1989) Identification of two calcium currents in acutely dissociated neurons from the rat lateral geniculate nucleus.J. Neurophysiol. 61, 1270–1283.

    PubMed  Google Scholar 

  • Hill R. J. and Govind C. K. (1981) Comparison of fast and slow synaptic terminals in lobster.Cell Tissue Res. 221, 303–310.

    PubMed  CAS  Google Scholar 

  • Hinz I. and Wernig A. (1988) Prolonged nerve stimulation causes changes in transmitter release at the frog neuromuscular junction.J. Physiol. (Lond.) 401, 557–565.

    CAS  Google Scholar 

  • Hirning L. D., Fox A. P., McCleskey E. W., Olivera B. M., Thayer S. A., Miller R. J., and Tsien R. W. (1988) Dominant role of N-type Ca2+ channels in evoked release of norepinephrine from sympathetic neurons.Science 239, 57–61.

    PubMed  CAS  Google Scholar 

  • Hong S. J. and Lnenicka G. A. (1993) Long-term changes in the neuromuscular synapses of a crayfish motoneuron produced by calcium influx.Brain Res. 605, 121–127.

    PubMed  CAS  Google Scholar 

  • Hong S. J. and Lnenicka G. A. (1995) Activity-dependent reduction in voltage-dependent calcium current in a crayfish motoneuron.J. Neurosci. 15, 3539–3547.

    PubMed  CAS  Google Scholar 

  • Hong S. J. and Lnenicka G. A. (1997) Characterization of a P-type calcium current in a cray-fish motoneuron and its selective modulation by impulse activity.J. Neurophysiol.,77, 76–85.

    PubMed  CAS  Google Scholar 

  • Hoshi T. and Smith S. J. (1987) Large depolarization induces long openings of voltage-dependent calcium channels in adrenal chromaffin cells.J. Neurosci. 7(2), 571–580.

    PubMed  CAS  Google Scholar 

  • Hoshi T., Rothlein J., and Smith S. J. (1984) Facilitation of Ca2+-channel currents in bovine adrenal chromaffin cells.Proc. Natl. Acad. Sci. USA 81, 5871–5875.

    PubMed  CAS  Google Scholar 

  • Ikeda S. R. (1991) Double-pulse calcium channel current facilitation in a dult rat sympathetic neurones.J. Physiol. (Lond.) 439, 181–214.

    CAS  Google Scholar 

  • Imredy J. P. and Yue D. T. (1992) Submicroscopic Ca2+ diffusion mediates inhibitory coupling between individual Ca2+ channels.Neuron 9, 197–207.

    PubMed  CAS  Google Scholar 

  • Imredy J. P. and Yue D. T. (1994) Mechanism of Ca2+-sensitive inactivation of L-type Ca2+ channels.Neuron 12, 1301–1318.

    PubMed  CAS  Google Scholar 

  • Ito M., Sakurai M., and Tongroach P. (1982) Climbing fibre induced depression of both mossy fibre responsiveness and glutamate sensitivity of cerebellar purkinje cells.J. Physiol. (Lond.) 324, 113–134.

    CAS  Google Scholar 

  • Jia M. and Nelson P. G. (1986) Calcium currents and transmitter output in cultured spinal cord and dorsal root ganglion neurons.J. Neurophysiol. 56, 1257–1267.

    PubMed  CAS  Google Scholar 

  • Johansen J., Yang J., and Kleinhaus A. L. (1987) Voltage-clamp analysis of the ionic conductances in a leech neuron with a purely calcium-dependent action potential.J. Neurophysiol. 58, 1468–1484.

    PubMed  CAS  Google Scholar 

  • Johnson B. D. and Byerly L. (1993a) Photo-released intracellular Ca2+ rapidly blocks Ba2+ current inLymnaea neurons.J. Physiol. (Lond.) 462, 321–347.

    CAS  Google Scholar 

  • Johnson B. D. and Byerly L. (1993b) A cytoskeletal mechanism for Ca2+ channel metabolic dependence and inactivation by intracellular Ca2+.Neuron 10, 797–804.

    PubMed  CAS  Google Scholar 

  • Jones S. W. and Marks T. N. (1989) Calcium currents in bullfrog sympathetic neurons.J. Gen. Physiol. 94, 151–167.

    PubMed  CAS  Google Scholar 

  • Kamiya H., Sawada S., and Yamamoto C. (1988) Synthetic ω-conotoxin blocks synaptic transmission in the hippocampus in vitro.Neurosci. Lett. 91, 84–88.

    PubMed  CAS  Google Scholar 

  • Kamphuis W., Huisman E., Wadman W. J., Heizmann C. W., and Lopes da Silva F. H. (1989) Kindling induced changes in parvalbumin immunoreactivity in rat hippocampus and its relation to long-term decrease in GABA-immunoreactivity.Brain Res. 479, 23–34.

    PubMed  CAS  Google Scholar 

  • Kasai H. and Aosaki T. (1988) Divalent cation dependent inactivation of the high-voltage-activated Ca2+-channel current in chick sensory neurons.Pflügers Arch. 411, 695–697.

    PubMed  CAS  Google Scholar 

  • Kasai H. and Neher E. (1992) Dihydropyridine-sensitive and ω-conotoxin-sensitive calcium channels in a mammalian neuroblastoma-glioma cell line.J. Physiol. (Lond.) 448, 161–188.

    CAS  Google Scholar 

  • Kater S. B., and Mills L. R. (1991) Regulation of growth cone behavior by calcium.J. Neurosci. 11, 891–899.

    PubMed  CAS  Google Scholar 

  • Kater S. B., Mattson M. P., Cohan C., and Connor J. (1988) Calcium regulation of the neuronal growth cone.Trends Neurosci. 11(7), 315–321.

    PubMed  CAS  Google Scholar 

  • Kavalali E. T. and Plummer M. R. (1996) Multiple voltage-dependent mechanisms potentiate calcium channel activity in hippocampal neurons.J. Neurosci. 16(3), 1072–1082.

    PubMed  CAS  Google Scholar 

  • Kay A. R. (1991) Inactivation kinetics of calcium current of acutely dissociated CA1 pyramidal cells of the mature guinea-pig hippocampus.J. Physiol. (Lond.) 437, 27–48.

    CAS  Google Scholar 

  • Kerr L. M. and Yoshikami D. (1984) A venom peptide with a novel presynaptic blocking action.Nature 308, 282–284.

    PubMed  CAS  Google Scholar 

  • King H. L., Atwood H. L., and Govind C. K. (1996) Structural features of crayfish phasic and tonic neuromuscular terminals.J. Comp. Neurol.,372, 618–626.

    PubMed  CAS  Google Scholar 

  • Klein M., Shapiro E., and Kandel E. R. (1980) Synaptic plasticity and the modulation of the Ca2+ current.J. Exp. Biol. 89, 117–157.

    PubMed  CAS  Google Scholar 

  • Kostyuk P. G. and Krishtal O. A. (1977) Effects of calcium and calcium-chelating agents on the inward and outward current in the membrane of mollusc neurones.J. Physiol. (Lond.) 270, 569–580.

    CAS  Google Scholar 

  • Liley A. W. and North K. A. K. (1953) An electrical investigation of effects of repetitive stimulation on mammalian neuromuscular junction.J. Neurophysiol. 16, 509–527.

    PubMed  CAS  Google Scholar 

  • Linden D. J. and Connor J. A. (1995) Long-term synaptic depression.Ann. Rev. Neurosci. 18, 319–357.

    PubMed  CAS  Google Scholar 

  • Linsdell P. and Moody W. J. (1995) Electrical activity and calcium influx regulate ion channel development in embryonic Xenopus skeletal muscle.J. Neurosci. 15(6), 4507–4514.

    PubMed  CAS  Google Scholar 

  • Lipscombe D., Madison D. V., Poenie M., Reuter H., Tsien R. Y., and Tsien R. W. (1988) Spatial distribution of calcium channels and cytosolic calcium transients in growth cones and cell bodies of sympathetic neurons.Proc. Natl. Acad. Sci. USA 85, 2398–2402.

    PubMed  CAS  Google Scholar 

  • Liu J., Bangalore R., Rutledge A., and Triggle D. J. (1994) Modulation of L-type Ca2+ channels in clonal rat pituitary cells by membrane depolarization.Mol. Pharmacol. 45, 1198–1206.

    PubMed  CAS  Google Scholar 

  • Llinás R. and Yarom Y. (1981) Electrophysiology of mammalian inferior olivary neuronesin vitro. Different types of voltage-dependent ionic conductances.J. Physiol. (Lond.) 315, 549–567.

    Google Scholar 

  • Llinás R., Steinberg I. Z., and Walton K. (1981) Relationship between presynaptic calcium current and postsynaptic potential in squid giant synapse.Biochem. J. 33, 323–352.

    Google Scholar 

  • Llinás R., Sugimori M., Lin J. W., and Cherksey B. (1989) Blocking and isolation of a calcium channel from neurons in mammals and cephalopods utilizing a toxin fraction (FTX) from funnel-web spider poison.Proc. Natl. Acad. Sci. USA 86, 1689–1693.

    PubMed  Google Scholar 

  • Llinás R., Sugimori M., and Silver R. B. (1992) Microdomains of high calcium concentration in a presynaptic terminal.Science 256, 677–679.

    PubMed  Google Scholar 

  • Lloyd D. P. C. (1949) Post-tetanic potentiation of response in the monosynaptic reflex pathway of the spinal cord.J. Gen. Physiol. 33, 147–170.

    PubMed  CAS  Google Scholar 

  • Lnenicka G. A. (1991) The role of activity in the development of phasic and tonic synaptic terminals.Ann. NY Acad. Sci. 627, 197–211.

    PubMed  CAS  Google Scholar 

  • Lnenicka G. A. (1993) Seasonal differences in motor terminals.Comp. Biochem. Physiol. 104A, 423–429.

    Google Scholar 

  • Lnenicka G. A. and Atwood H. L. (1985) Age-dependent long-term adaptation of crayfish phasic motor axon synapses to altered activity.J. Neurosci. 5, 459–467.

    PubMed  CAS  Google Scholar 

  • Lnenicka G. A. and Atwood H. L. (1989) Impulse activity of a crayfish motoneuron regulates its neuromuscular synaptic properties.J. Neurophysiol. 61, 91–96.

    PubMed  CAS  Google Scholar 

  • Lnenicka G. A. and Zhao Y. (1991) Seasonal differences in the physiology and morphology of crayfish motor terminals.J. Neurobiol. 22, 561–569.

    PubMed  CAS  Google Scholar 

  • Lnenicka G. A., Atwood H. L., and Marin L. (1986) Morphological transformation of synaptic terminals of a phasic motoneuron by long-term tonic stimulation.J. Neurosci. 6(8), 2252–2258.

    PubMed  CAS  Google Scholar 

  • Luebke J. I., Dunlap K., and Turner T. J. (1993) Multiple calcium channel types control glutamatergic synaptic transmission in the hippocampus.Neuron 11, 895–902.

    PubMed  CAS  Google Scholar 

  • Lux H. D. and Brown A. M. (1984) Single channel studies on inactivation of calcium currents.Science 225, 432–434.

    PubMed  CAS  Google Scholar 

  • Lynch G. S., Dunwiddie T., and Gribkoff V. (1977) Heterosynaptic depression: a postsynaptic correlate of long-term potentiation.Nature 266, 737–739.

    PubMed  CAS  Google Scholar 

  • Manabe T., Kaneko C. R. S., and Kuno M. (1990) Disuse-induced enhancement of Ia synaptic transmission in spinal motoneurons of the rat.J. Neurosci. 9(7), 2455–2461.

    Google Scholar 

  • Manalan A. S. and Klee C. B. (1983) Activation of calcineurin by limited proteolysis.Proc. Natl. Acad. Sci. USA 80, 4291–4295.

    PubMed  CAS  Google Scholar 

  • Mattson M. P., Taylor-Hunter A., and Kater S. B. (1988) Neurite outgrowth in individual neurons of a neuronal population is differentially regulated by cyclic AMP and calcium.J. Neurosci. 8, 1704–1711.

    PubMed  CAS  Google Scholar 

  • Mazzanti M., DeFelice L. J., and Liu Y. (1991) Gating of L-type Ca2+ channels in embryonic chick ventricle cells: dependence on voltage, current and channel density.J. Physiol. (Lond.) 443, 307–334.

    CAS  Google Scholar 

  • McCarthy R. T. and TanPiengco P. E. (1992) Multiple types of high-threshold calcium channels in rabbit sensory neurons: high-affinity block of neuronal L-type by nimodipine.J. Neurosci. 12, 2225–2234.

    PubMed  CAS  Google Scholar 

  • McCobb D. P., Haydon P. G., and Kater S. B. (1988) Dopamine and serotonin inhibition of neurite elongation of different identified neurons.J. Neurosci. Res. 19, 19–26.

    PubMed  CAS  Google Scholar 

  • Mendelowitz D. and Kunze D. L. (1992) Characterization of calcium currents in aortic baroreceptor neurons.J. Neurosci. 68(2), 509–517.

    CAS  Google Scholar 

  • Mercier A. J. and Atwood H. L. (1990) Long-term adaptation of a phasic extensor motoneurone in crayfish.J. Exp. Biol. 145, 9–22.

    Google Scholar 

  • Meyers D. E. R., Graf R. A., and Cooke I. M. (1992) Ionic currents of morphologically distinct peptidergic neurons in defined culture.J. Neurophysiol. 67, 1301–1315.

    PubMed  CAS  Google Scholar 

  • Mikami A. K., Imoto K., Tanabe T., Niidome T., Mori Y., Takeshima H., Narumiya S., and Numa S. (1989) Primary structure and functional expression of the cardiac dihydropyridine-sensitive calcium channel.Nature 340, 230–233.

    PubMed  CAS  Google Scholar 

  • Miller R. J. (1991) The control of neuronal calcium homeostasis.Prog. Neurobiol. 37, 255–285.

    PubMed  CAS  Google Scholar 

  • Miller J. J. and Baimbridge K. G. (1983) Biochemical and immunohistochemical correlates of kindling-induced epilepsy: role of calcium binding protein.Brain Res. 278, 322–326.

    PubMed  CAS  Google Scholar 

  • Mintz I. M., Venema V. J., Swiderek K. M., Lee T. D., Bean B. P., and Adams M. E. (1992) P-type calcium channels blocked by the spider toxin ω-Aga-IVA.Nature 355, 827–829.

    PubMed  CAS  Google Scholar 

  • Morgan J. I. and Curran T. (1991) Stimulus-transcription coupling in the nervous system: involvement of the inducible proto-oncogenesfos andjun.Annu. Rev. Neurosci. 14, 421–452.

    PubMed  CAS  Google Scholar 

  • Mori Y., Friedrich T., Kim M.-S., Mikami A., Nakai J., Ruth P., Bosse E., Hofmann F., Flockerzi V., Furuichi T., Mikoshiba K., Imoto K., Tanabe T., and Numa S. (1991) Primary structure and functional expression from complementary DNA of a brain calcium channel.Nature 350, 398–402.

    PubMed  CAS  Google Scholar 

  • Mynlieff M. and Beam K. G. (1992) Characterization of voltage-dependent calcium currents in mouse motoneurons.J. Neurophysiol. 68, 85–92.

    PubMed  CAS  Google Scholar 

  • Neely D. M. (1993) Role of substrate and calcium in neurite retraction of leech neurons following depolarization.J. Neurosci. 13(3), 1292–1301.

    PubMed  CAS  Google Scholar 

  • Nerbonne J. M. and Gurney A. M. (1987) Blockade of Ca2+ and K+ currents in bag cell neurons ofAplysia californica by dihydropyridine Ca2+ antagonists.J. Neurosci. 7, 882–893.

    PubMed  CAS  Google Scholar 

  • Nguyen P. V. and Atwood H. L. (1990) Expression of long-term adaptation of synaptic transmission requires a critical period of protein synthesis.J. Neurosci. 10(4), 1099–1109.

    PubMed  CAS  Google Scholar 

  • Nguyen P. V. and Atwood H. L. (1994) Altered impulse activity modifies synaptic physiology and mitochondria in crayfish phasic motor neurons.J. Neurophysiol. 72(6), 2944–2955.

    PubMed  CAS  Google Scholar 

  • Nowycky M. C., Fox A. P., and Tsien R. W. (1985) Three types of neuronal calcium currents with different calcium agonist sensitivity.Nature 316, 440–443.

    PubMed  CAS  Google Scholar 

  • Offord J. and Catterall W. A. (1989) Electrical activity, cAMP, and cytosolic calcium regulate mRNA encoding sodium channel α subunits in rat muscle cells.Neuron 2, 1447–1452.

    PubMed  CAS  Google Scholar 

  • Ohya Y., Kitamura K., and Kuriyama H. (1988) Regulation of calcium current by intracellular calcium in smooth muscle cells of rabbit portal vein.Circ. Res. 62, 375–383.

    PubMed  CAS  Google Scholar 

  • Pahapill P. A., Lnenicka G. A., and Atwood H. L. (1985) Asymmetry of motor impulses and neuromuscular synapses produced in crayfish claws by unilateral immobilization.J. Comp. Physiol. 157, 461–467.

    Google Scholar 

  • Partridge L. D. and Swandulla D. (1988) Calcium-activated non-specific cation channels.Trends Neurosci. 11, 698–72.

    Google Scholar 

  • Passafaro M., Clementi F., Pollo A., Carbone E., and Sher E. (1994) ω-conotoxin and Cd2+ stimulate the recruitment to the plasmamembrane of an intracellular pool of voltage-operated Ca2+ channels.Neuron 12, 317–326.

    PubMed  CAS  Google Scholar 

  • Penington N. J. and Fox A. P. (1995) Toxin-insensitive Ca2+ current in dorsal raphe neurons.J. Neurosci. 15, 5719–5726.

    PubMed  CAS  Google Scholar 

  • Perez-Reyes E., Kim H. S., Lacerda A. E., Horne W., Wei X. Y., Rampe D., and Campbell K. P. (1989) Induction of calcium currents by the expression of the alpha 1-subunit of thedihydropyridine receptor from skeletal muscle.Nature 340, 233–236.

    PubMed  CAS  Google Scholar 

  • Plant T. D. and Standen N. B. (1981) Calcium current inactivation in identified neurones ofHelix aspersa.J. Physiol. (Lond.) 321, 273–285.

    CAS  Google Scholar 

  • Plant T. D., Standen N. B., and Ward T. A. (1983) The effects of injection of calcium ions and calcium chelators on calcium channel inactivation inHelix neurones.J. Physiol. (Lond.) 334, 189–212.

    CAS  Google Scholar 

  • Plummer M. R., Logothetis D. E., and Hess P. (1989) Elementary properties and pharmacological sensitivities of calcium channels in mammalian peripheral neurons.Neuron 2, 1453–1463.

    PubMed  CAS  Google Scholar 

  • Pockett S., Brookes N. H., and Bindman L. J. (1990) Long-term depression at synapses in slices of rat hippocampus can be induced by bursts of postsynaptic activity.Exp. Brain Res. 80, 196–200.

    PubMed  CAS  Google Scholar 

  • Przysiezniak J. and Spencer A. N. (1992) Voltage-activated calcium currents in identified neurons from a hydrozoan jellyfish,Polyorchis penicillatus.J. Neurosci. 12, 2065–2078.

    PubMed  CAS  Google Scholar 

  • Pumplin D. W., Reese T. S., and Llinás R. (1981) Are the presynaptic membrane particles the calcium channels?Proc. Natl. Acad. Sci. USA 78, 7210–7213.

    PubMed  CAS  Google Scholar 

  • Randall A. and Tsien R. W. (1995) Pharmacological dissection of multiple types of Ca2+ channel currents in rat cerebellar granule neurons.J. Neurosci. 15, 2995–3012.

    PubMed  CAS  Google Scholar 

  • Regan L. J., Sah D. W. Y., and Bean B. P. (1991) Ca2+ channels in rat central and peripheral neurons: high-threshold current resistant to dihydropyridine blockers and ω-conotoxin.Neuron 6, 269–280.

    PubMed  CAS  Google Scholar 

  • Regehr W. G. and Mintz I. M. (1994) Participation of multiple calcium channel types in transmission at single climbing fiber to Purkinje cell synapses.Neuron 12, 605–613.

    PubMed  CAS  Google Scholar 

  • Reynolds I. J., Wagner J. A., Snyder S. H., Thayer S. A., Olivera B. M., and Miller R. J. (1986) Brain voltage-sensitive calcium channel subtypes differentiated by ω-conotoxin fraction GVIA.Proc. Natl. Acad. Sci. USA 83, 8804–8807.

    PubMed  CAS  Google Scholar 

  • Rheuben M. B. (1985) Quantitative comparison of the structural features of slow and fast junctions inManduca.J. Neurosci. 5(7), 1704–1716.

    PubMed  CAS  Google Scholar 

  • Robbins N. and Fischbach G. D. (1971) Effect of chronic disuse of rat soleus neuromuscular junctions on postsynaptic membrane.J. Neurophysiol. 34, 562–569.

    PubMed  Google Scholar 

  • Roberts W. M. (1994) Localization of calcium signals by a mobile calcium buffer in frog saccular hair cells.J. Neurosci. 14(5), 3246–3262.

    PubMed  CAS  Google Scholar 

  • Robitaille R., Adler E. M., and Charlton M. P. (1990) Strategic location of calcium channels at transmitter release sites of frog neuromuscular synapses.Neuron 5, 773–779.

    PubMed  CAS  Google Scholar 

  • Sather W. A., Tanabe T., Zhang J.-F., Mori Y., Adams M. E., and Tsien R. W. (1993) Distinctive biophysical and pharmacological properties of class A (BI) calcium channel al subunits.Neuron 11, 291–303.

    PubMed  CAS  Google Scholar 

  • Scott R. H. and Dolphin A. C. (1990) Voltage-dependent modulation of rat sensory neurone calcium channel currents by G protein activation: effect of a dihydropyridine antagonist.Br. J. Pharmacol. 99, 629–630.

    PubMed  CAS  Google Scholar 

  • Scott R. H., Pearson H. A., and Dolphin A. C. (1991) Aspects of vertebrate neuronal voltage-activated calcium currents and their regulation.Prog. Neurobiol. 36, 485–520.

    PubMed  CAS  Google Scholar 

  • Sherman S. J. and Catterall W. A. (1984) Electrical activity and cytosolic calcium regulate levels of tetrodotoxin-sensitive sodium channels in cultured rat muscle cells.Proc. Natl. Acad. Sci. USA 81, 262–266.

    PubMed  CAS  Google Scholar 

  • Sherman S. J., Lawrence D. J., Messner D. J., Jacoby K., and Catterall W. A. (1983) Tetrodotoxin sensitive sodium channels in rat muscle cells developing in vitro.J. Biol. Chem. 258, 2488–2495.

    PubMed  CAS  Google Scholar 

  • Silver R. A., Lamb A. G., and Bolsover S. R. (1990) Calcium hotspots caused by L-channel clustering promote morphological changes in neuronal growth cones.Nature 343, 751–754.

    PubMed  CAS  Google Scholar 

  • Simon S. M. and Llinás R. R. (1985) Compartmentalization of the submembrane calcium activity during calcium influx and its significance in transmitter release.Biophys. J. 48, 485–498.

    PubMed  CAS  Google Scholar 

  • Singer D., Biel M., Lotan I., Flockerzi V., Hofmann F., and Dascal N. (1991) The roles of the subunits in the function of the calcium channel.Science 253, 1553–1557.

    PubMed  CAS  Google Scholar 

  • Skattebol A., Brown A. M., and Triggle D. J. (1989) Homologous regulation of voltage-dependent calcium channels by 1,4-dihydropyridines.Biochem. Biophys. Res. Commun. 160, 929–936.

    PubMed  CAS  Google Scholar 

  • Skeer J. M., Norman R. I., and Sattelle D. B. (1996) Invertebrate voltage-dependent calcium channel subtypes.Biol. Rev. 71, 137–154.

    Google Scholar 

  • Snider W. D. and Harris G. L. (1979) A physiological correlate of disuse-induced sprouting at the neuromuscular junction.Nature 281, 69–71.

    PubMed  CAS  Google Scholar 

  • Snutch T. P. and Reiner P. B. (1992) Ca2+ channels: diversity of form and function.Curr. Opinion Neurobiol. 2, 247–253.

    CAS  Google Scholar 

  • Snutch T. P., Leonard J. P., Gilbert M. M., Lester H. A., and Davidson N. (1990) Rat brain expresses a heterogenous family of calcium channels.Proc. Natl. Acad. Sci. USA 87, 3391–3395.

    PubMed  CAS  Google Scholar 

  • Stanley E. F. (1993) Single calcium channels and acetylcholine release at a presynaptic nerve terminal.Neuron 11, 1007–1011.

    PubMed  CAS  Google Scholar 

  • Stanley E. F. and Goping G. (1991) Characterization of a calcium current in a vertebrate cholinergic presynaptic nerve terminal.J. Neurosci. 11, 985–993.

    PubMed  CAS  Google Scholar 

  • Stanton P. and Sejnowski T. (1989) Associative longterm depression in the hippocampus induced by hebbian covariance.Nature 339, 215–218.

    PubMed  CAS  Google Scholar 

  • Stea A., Tomlinson W. J., Soong T. W., Bourinet E., Dubel S. J., Vincent S. R., and Snutch T. P. (1994) Localization and functional properties of a rat brain a1A calcium channel reflect similarities to neuronal Q- and P-type channels.Proc. Natl. Acad. Sci. USA 91, 10,576–10,580.

    CAS  Google Scholar 

  • Stea A., Soong T. W., and Snutch T. P. (1995) Voltage-gated calcium channels, inHandbook of Receptors and Channels: Ligand- and Voltage-Gated Ion Channels (North R. A., ed.), Boca Raton, FL, CRC, pp. 113–152.

    Google Scholar 

  • Streit J. and Lux H. D. (1987) Voltage dependent calcium currents in PC12 growth cones and cells during NGF-induced cell growth.Pflügers Arch.408, 634–641.

    PubMed  CAS  Google Scholar 

  • Streit J. and Lux H. D. (1989) Distribution of calcium currents in sprouting PC12 cells.J. Neurosci. 9(12), 4190–4199.

    PubMed  CAS  Google Scholar 

  • Sugimori M., Lang E. J., Silver R. B., and Llinás R. (1994) High-resolution measurement of the time course of calcium-concentration microdomains at squid presynaptic terminals.Biol. Bull. 187, 300–303.

    PubMed  CAS  Google Scholar 

  • Sun Y. A. and Poo M. A. (1987) Evoked release of acetylcholine from the growing embryonic neuron.Proc. Natl. Acad. Sci. USA 84, 2540–2544.

    PubMed  CAS  Google Scholar 

  • Swandulla D., Carbone E., and Lux H. D. (1991) Do calcium channel classifications account for neuronal calcium channel diversity.Trends Neurosci. 14, 46–51.

    PubMed  CAS  Google Scholar 

  • Takahashi T., and Momiyama A. (1993) Different types of calcium channels mediate central synaptic transmission.Nature 366, 156–158.

    PubMed  CAS  Google Scholar 

  • Tallant E. A., Brumley L. M., and Wallace R. W. (1988) Activation of a calmodulin-dependent phosphatase by a Ca2+-dependent protease.Biochemistry 27, 2205–2211.

    PubMed  CAS  Google Scholar 

  • Tanabe T., Takeshima H., Mikami A., Flockerzi V., Takahashi H., Kangawa K., Kojimi M., Matsuo H., Hirose T., and Numa S. (1987) Primary structure of the receptor for calcium channel blockers from skeletal muscle.Nature 328, 313–318.

    PubMed  CAS  Google Scholar 

  • Tareilus E., Schoch J., Adams M., and Breer H. (1993) Analysis of rapid calcium signals in synaptosomes.Neurochem. Int. 23(4), 331–341.

    PubMed  CAS  Google Scholar 

  • Tareilus E., Schoch J., and Breer H. (1994) Ca2+-dependent inactivation of P-type calcium channels in nerve terminals.J. Neurochem. 62, 2283–2291.

    PubMed  CAS  Google Scholar 

  • Tazaki K. and Cooke I. M. (1986) Currents under voltage clamp of burst-forming neurons of the cardiac ganglion of the lobster (Homarus americanus).J. Neurophysiol. 56(6), 1739–1762.

    PubMed  CAS  Google Scholar 

  • Tazaki K. and Cooke I. M. (1990) Characterization of Ca2+ current underlying burst formation in lobster cardiac ganglion motoneurons.J. Physiol. (Lond.) 63, 370–384.

    CAS  Google Scholar 

  • Thayer S. A. and Miller R. J. (1990) Regulation of the intracellular free calcium concentration in single rat dorsal root ganglion neurones in vitro.J. Physiol. (Lond.) 425, 85–115.

    CAS  Google Scholar 

  • Tillotson D. (1979) Inactivation of Ca2+ conductance dependent on entry of Ca2+ ions in molluscan neurons.Proc. Natl. Acad. Sci. USA 76, 1497–1500.

    PubMed  CAS  Google Scholar 

  • Trautwein W. and Hescheler J. (1990) Regulation of cardiac calcium current by phosphorylation and G proteins.Annu. Rev. Physiol. 52, 527–574.

    Google Scholar 

  • Triggle D. J., Hawthorn M., Gopalakrishinan M., Minarini A., Avery S., Rutledge A., Bangalore R., and Zheng W. (1991) Synthetic organic ligands active at voltage-gated calcium channels.Ann. NY Acad. Sci. 635, 123–138.

    PubMed  CAS  Google Scholar 

  • Trudeau L.-E., Baux G., Fossier P., and Tauc L. (1993) Transmitter release and calcium currents at anAplysia buccal ganglion synapse-I. Characterization.Neuroscience 53, 571–580.

    PubMed  CAS  Google Scholar 

  • Tsujimoto T. and Kuno M. (1988) Calcitonin generelated peptide prevents disuse-induced sprouting of rat motor nerve terminals.J. Neurosci. 8(10, 3951–3957.

    PubMed  CAS  Google Scholar 

  • Turner T. J., Adams M. E., and Dunlap K. (1992) Calcium channels coupled to glutamate release identified by ω-Aga-IVA.Science 258, 310–313.

    PubMed  CAS  Google Scholar 

  • Uchitel O. D., Protti D. A., Sanchez V., Cherksey B. D., Sugimori M., and Llinás R. (1992) P-type voltage-dependent calcium channel mediates presynaptic calcium influx and transmitter release in mammalian synapses.Proc. Natl. Acad. Sci. USA 89, 3330–3333.

    PubMed  CAS  Google Scholar 

  • Von Gersdorff H. and Matthews G. (1996) Calciumdependent inactivation of calcium current in synaptic terminals of retinal bipolar neurons.J. Neurosci. 16(1), 115–122.

    Google Scholar 

  • Walrond J. P. and Reese T. S. (1985) Structure of axon terminals and active zones at synapses on lizard twitch and tonic muscle fibers.J. Neurosci. 5, 662–672.

    Google Scholar 

  • Walrond J. P., Govind C. K., and Huestis S. E. (1993) Two structural adaptations for regulating transmitter release at lobster neuromuscular synapses.J. Neurosci. 13(11), 4831–4845.

    PubMed  CAS  Google Scholar 

  • Webb C. B., and Cope T. C. (1992) Modulation of Ia EPSP amplitude: the effects of chronic synaptic inactivity.J. Neurosci. 12, 338–344.

    PubMed  CAS  Google Scholar 

  • Werth J. L. and Thayer S. A. (1994) Mitochondria buffer physiological calcium loads in cultured rat dorsal root ganglion neurons.J. Neurosci. 14, 348–356.

    PubMed  CAS  Google Scholar 

  • Williams M. E., Feldman D. H., McCue A. F., Brenner R., Velicelebi G., Ellis S. B., and Harpold M. M. (1992a) Structure and functional expression of α1, α2, and β-subunits of a novel human neuronal calcium channel subtype.Neuron 8, 71–84.

    PubMed  CAS  Google Scholar 

  • Williams M. E., Brust P. F., Feldman D. H., Patthi S., Simerson S., Maroufi A., McCue A. F., Velicelebi G., Ellis S. B., and Harpold M. M. (1992b) Structure and functional expression of an ω-conotoxin-sensitive human N-type calcium channel.Science 257, 389–395.

    PubMed  CAS  Google Scholar 

  • Wojtowicz J. M. and Atwood H. L. (1988) Presynaptic long-term facilitation at the crayfish neuromuscular junction: voltage-dependent and ion-dependent phases.J. Neurosci. 8 4667–4674.

    PubMed  CAS  Google Scholar 

  • Wojtowicz J. M., Marin L., and Atwood H. L. (1994) Activity-induced changes in synaptic release sites at the crayfish neuromuscular junction.J. Neurosci. 14, 3688–3703.

    PubMed  CAS  Google Scholar 

  • Xie Z.-P. and Poo M.-M. (1986) Initial events in the formation of neuromuscular synapses: rapid induction of acetylcholine release from embryonic neuron.Proc. Natl. Acad. Sci. USA 83, 7069–7073.

    PubMed  CAS  Google Scholar 

  • Yawo H. and Momiyama A. (1993) Re-evaluation of calcium currents in pre-and postsynaptic neurones of the chick ciliary ganglion.J. Physiol. (Lond.) 460, 153–172.

    CAS  Google Scholar 

  • Yue D. T., Backx P. H., and Imredy J. P. (1990) Calcium-sensitive inactivation in the gating of single calcium channels.Science 250 1735–1738.

    PubMed  CAS  Google Scholar 

  • Zhang J.-F., Randall A. D., Ellinor P. T., Horne W. A., Sather W. A., Tanabe T., Schwarz T. L., and Tsien R. W. (1993) Distinctive pharmacology and kinetics of cloned neuronal Ca2+ channels and their possible counterparts in mammalian CNS neurons.Neuropharmacology 32, 1075–1088.

    PubMed  CAS  Google Scholar 

  • Zhang J.-F., Ellinor P. T., Aldrich R. W., and Tsien R. W. (1994) Molecular determinants of voltagedependent inactivation in calcium channels.Nature 372, 97–100.

    PubMed  CAS  Google Scholar 

  • Zheng W., Feng G., Ren D., Eberl D. F., Hannan F., Dubald M., and Hall L. M. (1995) Cloning and characterization of a calcium channel α1 subunit fromDrosophila melanogaster with similarity to the rat brain type D isoform.J. Neurosci. 15, 1132–1143.

    PubMed  CAS  Google Scholar 

  • Zucker, R. S. (1972) Crayfish escape behavior and central synapses. II. Physiological mechanisms underlying behavioral habituation.J. Neurophysiol. 35, 621–637.

    PubMed  CAS  Google Scholar 

  • Zucker R.. (1989) Schort-term synaptic plasticity.Annu. Rev. Neurosci. 12, 13–31.

    PubMed  CAS  Google Scholar 

  • Zucker R. S. and Bruner J. (1977) Long-lasting depression and the depletion hypothesis at crayfish neuromuscular junctions.J. Comp. Physiol. 121, 223–240.

    Google Scholar 

  • Zucker R. S. and Fogelson A. L. (1986) Relationship between transmitter release and presynaptic calcium influx when calcium enters through discrete channels.Proc. Natl. Acad. Sci. USA 83, 3032–3036.

    PubMed  CAS  Google Scholar 

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Lnenicka, G.A., Hong, S.J. Activity-dependent changes in voltage-dependent calcium currents and transmitter release. Mol Neurobiol 14, 37–66 (1997). https://doi.org/10.1007/BF02740620

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