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Depolarization elicits two distinct calcium currents in vertebrate sensory neurones

  • Excitable Tissues and Central Nervous Physiology
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Abstract

The calcium currents of rat sensory neurones (of the IX and X cranial nerves) grown in culture were studied using whole cell recordings. In cells loaded with CsCl, and bathed in a solution where Na was replaced by choline or Tris, a step depolarization from −80 mV to 0 mV elicited the well-documented sustained Ca current (i Ca,s). In contrast, depolarization from −80 mV to −60 mV and up to −20 mV evoked a distinct transient inward current (i Ca,t) which could be isolated by imposing an internal pCa 7. It relaxed in about 100 ms and could possibly occur independently of the former current. The transient current was only affected by manipulation of the Ca concentration in the external medium and therefore was considered to be also a transfer of Ca. Ba was shown to act as a substitute with a lower affinity than Ca. The maximal amplitude of this current was in the order of a few hundred pA in Ca 5 mM and Mg 2 mM. Both activation and inactivation occurred in the same voltage span. The underlying event was studied using noise analysis and compared to the Ca transfer occurring during the sustained current as measured in chromaffin cells by Fenwick et al. (1982). We found them to be of similar amplitude.

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References

  • Anglister L, Farber IC, Shahar A, Grinwald A (1982) Localisation of voltage sensitive Ca2+ channels along developing neurites: their possible role in regulating neurite elongation. Dev Biol 94:351–365

    Google Scholar 

  • Baccaglini PI, Cooper E (1982) Electrophysiological studies of newborn rat nodose neurones in cell culture. J Physiol (Lond) 324:429–439

    Google Scholar 

  • Baccaglini PI, Hogan PG (1983) Some rat sensory neurons in culture express characteristics of differentiated pain sensory cells. Proc Natl Acad Sci (USA) 80:594–598

    Google Scholar 

  • Belmonte C, Gallego R (1983) Membrane properties of cat sensory neurones with chemoreceptor and baroreceptor endings. J Physiol (Lond) 342:603–614

    Google Scholar 

  • Bossu JL, Feltz A (1982) Intracellular recordings of dopamine sensitive sinus nerve afferents. Neurosci Lett 37:S364

    Google Scholar 

  • Bossu JL, Feltz A (1984) Patch-clamp study of the tetrodotoxineresistant sodium current in group C sensory neurones. Neurosci Letters 51:241–246

    Google Scholar 

  • Bossu JL, Feltz A, Thomann JM (1984) Depolarization elicits two distinct calcium currents in vertebrate sensory neurones. Neurosci Letters 18:S153

    Google Scholar 

  • Brown AM, Morimoto K, Tsuda Y, Wilson D (1981) Calcium current-dependent and voltage-dependent inactivation of calcium channels in Helix aspersa. J Physiol (Lond) 320:193–218

    Google Scholar 

  • Brown DA, Adams PR (1980) Muscarinic suppression of a novel voltage-sensitive K+ current in a vertebrate neurone. Nature 283:673–676

    Google Scholar 

  • Caldwell PC (1970) Calcium chelation and buffers. In: Cuthbert AW (ed) Calcium and cellular function. MacMillan, London, pp 10–16

    Google Scholar 

  • Carbone E, Lux HD (1984a) A low voltage-activated calcium conductance in embryonic chick sensory neurons. Biophys J 46:413–418

    Google Scholar 

  • Carbone E, Lux HD (1984b) A low voltage-activated, fully inactivating Ca channel in vertebrate sensory neurones. Nature 310:501–502

    Google Scholar 

  • Cuello AC, Del Fiacco M, Paxinos G (1978) The central and peripheral ends of the substance P-containing sensory neurones in the rat trigeminal system. Brain Res 152:499–509

    Google Scholar 

  • Deitmer JW (1984) Evidence for two voltage-dependent calcium currents in the membrane of the ciliate Stylonychia. J Physiol (Lond) 355:137–160

    Google Scholar 

  • Deschênes M, Roy JP, Stériade M (1982) Thalamic bursting mechanism: An inward slow current revealed by membrane hyperpolarisation. Brain Res 239:289–293

    Google Scholar 

  • Fenwick EM, Marty A, Neher E (1982) Sodium and calcium channels in bovine chromaffin cells. J Physiol (Lond) 331:599–636

    Google Scholar 

  • Fox AP (1981) Voltage-dependent inactivation of a calcium channel. Proc Natl Acad Sci (USA) 78:953–956

    Google Scholar 

  • Gallego R (1983) The ionic basis of action potentials in petrosal ganglion cells of the cat. J Physiol (Lond) 342:591–602

    Google Scholar 

  • Gallego R, Eyzaguirre C (1978) Membrane and action potentials characteristics of A and C nodose ganglion cells studied in whole ganglia and in tissue slices. J Neurophysiol 41:1217–1232

    Google Scholar 

  • Galvan M, Adams PR (1982) Control of calcium current in rat sympathetic neurons by norepinephrine. Brain Res 244: 135–144

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Halliwell JV (1983) Caesium loading reveals two distinct Cacurrents in voltage clamped guinea pig hippocampal neurones in vitro. J Physiol (Lond) 341:10P

  • Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ (1981) Improved patch clamp techniques for high resolution current recording from cells and cell-free patches. Pflügers Arch 391:85–100

    Google Scholar 

  • Hawrot E, Patterson PH (1979) Long term culture of dissociated sympathetic neurons. Meth Enzym 58:574–584

    Google Scholar 

  • Higashi H, Nishi S (1982) 5-Hydroxytryptamine receptors of visceral primary afferent neurones on rabbit nodose ganglia. J Physiol (Lond) 323:543–567

    Google Scholar 

  • Hökfelt T, Kellerth JO, Nilsson G, Pernow B (1975) Substance P: Localization in the central nervous system and in some primary sensory neurons. Science 190:889–890

    Google Scholar 

  • Kostyuk PG (1984) Intracellular perfusion of nerve cells and its effects in membrane currents. Physiol Rev 64:435–454

    Google Scholar 

  • Kostyuk PG, Krishtal OA (1977) Separation of sodium and calcium currents in the somatic membrane of mollusc neurones. J Physiol (Lond) 270:545–568

    Google Scholar 

  • Kostyuk PG, Veselovsky NS, Tsyndrenko AY (1981) Ionic currents in the somatic membrane of rat dorsal root ganglion neurons. I. Sodium currents. Neuroscience 6:2423–2430

    Google Scholar 

  • Llinas R, Sugimori M (1980) Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices. J Physiol (Lond) 305:197–213

    Google Scholar 

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

    Google Scholar 

  • Moolenaar WH, Spector I (1979) The calcium current and the activation of a slow potassium conductance in voltage-clamped mouse neuroblastoma cells. J Physiol (Lond) 292:307–323

    Google Scholar 

  • Nowycky MC, Fox AP, Tsien RW (1984) Propertics of two types of calcium channel and their regulation in cultured DRG cells. IUPHAR satellite meeting at St Andrews, July 1984

  • Schlichter R, Bossu JL, Feltz A, Désarmenien M, Feltz P (1984) Characterization of the multiple currents underlying spike activity in sensory neurones: an attempt to determine the physiological role of GABA-B receptor activation on slow conducting primary afferents. Neuropharmacology 23:869–872

    Google Scholar 

  • Tsien RW (1983) Calcium channels in excitable cell membranes. Ann Rev Physiol 45:341–358

    Google Scholar 

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Bossu, J.L., Feltz, A. & Thomann, J.M. Depolarization elicits two distinct calcium currents in vertebrate sensory neurones. Pflugers Arch. 403, 360–368 (1985). https://doi.org/10.1007/BF00589247

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  • DOI: https://doi.org/10.1007/BF00589247

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