Voltage-dependent currents in neurones of the nuclei of the solitary tract of rat brainstem slices

  • J. Champagnat
  • T. Jacquin
  • D. W. Richter
Excitable Tissues and Central Nervous Physiology


Neurones within the ventral and ventrolateral nuclei of the solitary tract were analyzed under single-electrode current- and voltage-clamp conditions in rat brainstem slices. We present direct and indirect evidence for the existence of five different sorts of membrane currents:
  1. 1.

    a tetrodotoxin-sensitive sodium current,

  2. 2.

    a tetrodotoxin-resistant calcium current,

  3. 3.

    a calcium-dependent potassium current,

  4. 4.

    a non-inactivating potassium current which is inhibited by muscarine,

  5. 5.

    an inactivating potassium current, which is inhibited by 4-aminopyridine.


These membrane properties do not produce spontaneous bursting in these neurones. Assuming that neurones with such properties belong to the respiratory network, we discuss how conductances of this type may be involved in mechanisms regulating central respiratory activity.

Key words

Brainstem slices Nuclei of the solitary tract Respiratory control Single-electrode voltage-clamp Calcium current Potassium currents 


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  1. Acker H, Richter D (1985) Changes in potassium activity, calcium activity, and oxygen tension in the extracellular space of inspiratory neurones within the NTS of cats. In: Bianchi AL, Denavit-Saubié M (eds) Neurogenesis of central respiratory rhythm. MTP Press, Lancester, pp 183–185Google Scholar
  2. Adams PR (1982) Voltage-dependent conductances of vertebrate neurones. TINS 5:1–4Google Scholar
  3. Adams PR, Brown DA, Constanti A (1982) M-currents and other potassium currents in bullfrog sympathetic neurones. J Physiol (Lond) 330:537–572Google Scholar
  4. Akaike N, Lee KS, Brown AM (1978) The calcium current of Helix neurons. J Gen Physiol 71:509–531PubMedCrossRefGoogle Scholar
  5. Amoroso EC, Bainbridge JG, Bell FR, Lawn AM, Rosenberg H (1951) Central respiratory spike potentials. Nature 169:603–604CrossRefGoogle Scholar
  6. Ballantyne D, Richter DW (1984) Post-synaptic inhibition of bulbar inspiratory neurones in the cat. J Physiol (Lond) 348:67–87Google Scholar
  7. Ballantyne B, Richter DW (1985) The non-uniform character of expiratory synaptic activity in expiratory bulbospinal neurones of the cat. J Physiol (Lond) (in press)Google Scholar
  8. Barrett EF, Barrett JN, Crill WE (1980) Voltage-sensitive outward currents in cat motoneurones. J Physiol (Lond) 304:251–276Google Scholar
  9. Berger AJ, Averill DB, Cameron WE (1984) Morphology of inspiratory neurons located in the ventrolateral nucleus of the tractus solitarius of the cat. J Comp Neurol 224:60–70PubMedCrossRefGoogle Scholar
  10. Brennecke R, Lindemann B (1971) A chopped-current clamp for current injection and recording of membrane polarization with single electrodes of changing resistance. TITJ Life Sci 1:53–58Google Scholar
  11. Brennecke R, Lindemann B (1974) Theory of a membrane-voltageclamp with discontinuous feedback through a pulsed current clamp. Rev Sci Instr 45:184–188CrossRefGoogle Scholar
  12. Brown DA (1983) Slow cholinergic excitation—a mechanism for increasing neuronal excitability. TINS 6:302–307Google Scholar
  13. Carbone E, Lux HD (1984) A low voltage-activated, fully inactivated Ca channel in vertebrate sensory neurones. Nature 310:501–503PubMedCrossRefGoogle Scholar
  14. Champagnat J, Denavit-Saubié M, Velluti JC (1980) Excitability of bullar respiratory neurones: a study using microiontophoretic applications of depolarizing agents. Brain Res 191:359–377PubMedCrossRefGoogle Scholar
  15. Champagnat J, Denavit-Saubié M, Moyanova S, Rondouin G (1982) Involvement of amino acids in periodic inhibitions of bulbar respiratory neurones. Brain Res 237:351–365PubMedCrossRefGoogle Scholar
  16. Champagnat J, Denavit-Saubié M, Siggins GR (1983) Rhythmic neuronal activities in the nucleus of the tractus solitarius isolated in vitro. Brain Res 280:155–159PubMedCrossRefGoogle Scholar
  17. Champagnat J, Grant K, Shen KF, Denavit-Saubié M (1985a) Neuronal morphology and synaptic transmission in the solitary complex in vitro. In: Bianchi AL, Denavit-Saubié M (eds) Neurogenesis of central respiratory rhythm. MTP Press, Lancester, pp 157–164Google Scholar
  18. Champagnat J, Shen KF, Siggins GR, Koda L, Denavit-Saubié M (1985b) Effects of neurotransmitters and synaptic processing of neurovegetative afferents in the brainstem of the rat. J Auton Nerv Syst (in press)Google Scholar
  19. Champagnat J, Siggins GR, Koda L, Denavit-Saubié M (1985c) Synaptic responses of neurones of the nucleus tractus solitarius in vitro. Brain Res 325:49–56PubMedCrossRefGoogle Scholar
  20. Chesnoy-Marchais D (1983) Characterization of a chloride conductance activated by hyperpolarization in Aplysia neurones. J Physiol (Lond) 342:277–308Google Scholar
  21. Cohen MI (1979) Neurogenesis of the respiratory rhythm in the mammal. Physiol Rev 59:1105–1173PubMedGoogle Scholar
  22. Connor JA, Stevens CF (1971a) Voltage-clamp studies of a transient outward membrane current in gastropod neural somata. J Physiol (Lond) 213:21–30Google Scholar
  23. Connor JA, Stevens CF (1971b) Prediction of repetitive firing behaviour from voltage-clamp data on an isolated neurone soma. J Physiol (Lond) 213:31–53Google Scholar
  24. Dekin MS, Getting PA (1984) Firing pattern of neurons in the nucleus tractus solitarius: modulation by membrane hyperpolarization. Brain Res 324:180–184PubMedCrossRefGoogle Scholar
  25. Eckert R, Lux HD (1975) A non-inactivating inward current recorded during small depolarizing voltage steps in snail pacemaker neurons. Brain Res 83:486–489PubMedCrossRefGoogle Scholar
  26. Eckert R, Lux HD (1976) A voltage-sensitive persistent calcium conductance in neuronal somata of Helix. J Physiol (Lond) 254:129–151Google Scholar
  27. Eckert R, Tillotson DL, Brehm P (1981) Calcium-mediated control of Ca and K currents. Fed Proc 40:2226–2232PubMedGoogle Scholar
  28. Finkel AS, Redman SJ (1984) Theory and operation of a single microelectrode voltage-clamp. J Neurosci Methods 11:101–127PubMedCrossRefGoogle Scholar
  29. Gustafsson B, Wigström H (1981) Evidence for two types of after hyperpolarization in CA1 pyramidal cells in the hippocampus. Brain Res 206:462–468PubMedCrossRefGoogle Scholar
  30. Hagiwara S (1981) Calcium channel. Annu Rev Neurosci 4:69–125PubMedCrossRefGoogle Scholar
  31. Hagiwara S, Byerly L (1983) The calcium channel. TINS 6:189–193Google Scholar
  32. Halliwell JV, Adams PR (1982) Voltage-clamp analysis of muscarinic excitation in hippocampal neurons. Brain Res 250:71–92PubMedCrossRefGoogle Scholar
  33. Hermann A, Hartung K (1983) Ca2+ activated K+ conductance in molluscan neurones. Cell Calcium 4:387–405PubMedCrossRefGoogle Scholar
  34. Heyer CB, Lux HD (1976) Properties of a facilitating calcium current in pace-maker neurones of the snailHelix pomatia. J Physiol (Lond) 262:319–348Google Scholar
  35. Hodgkin AL, Huxley AF (1952) Currents carried by sodium and potassium ions through the membrane of the giant axon ofLoligo. J Physiol (Lond) 116:449–472Google Scholar
  36. Hodgkin AL, Keynes RD (1957) Movements of labelled calcium in squid giant axons. J Physiol (Lond) 138:253–281Google Scholar
  37. Howard BR, Tabatabai M (1975) Localization of the medullary respiratory neurons in rats by microelectrode recording. J Appl Physiol 39:812–817PubMedGoogle Scholar
  38. Johnston D, Brown TH (1983) Interpretation of voltage-clamp measurements in hippocampal neurons. J Neurophysiol 50:464–496PubMedGoogle Scholar
  39. Kalia M, Sullivan JM (1982) Brainstem projections of sensory and motor components of the vagus nerve in the rat. J Comp Neurol 211:248–264PubMedCrossRefGoogle Scholar
  40. Kessler JP, Jean A (1984) Identification of the medullary swallowing regions in the rat. Exp Brain Res 57:148–155Google Scholar
  41. Kostyuk PG, Krishtal OA (1977) Effects of calcium and calciumchelating agents on the inward and outward current in the membrane of mollusc neurones. J Physiol (Lond) 315:569–584Google Scholar
  42. Long SE, Duffin J (1984) The medullary respiratory neurons: a review. Can J Physiol Pharmacol 62:161–182PubMedCrossRefGoogle Scholar
  43. Lux HD, Hofmeier G (1982) Properties of a calcium- and voltage-activated potassium current inHelix pomatia neurons. Pflügers Arch 394:61–69PubMedCrossRefGoogle Scholar
  44. Lux HD, Neher E, Marty A (1981) Single channel activity associated with the calcium dependent outward current inHelix pomatia. Pflügers Arch 389:293–295PubMedCrossRefGoogle Scholar
  45. Madison DV, Nicoll RA (1984) Control of the repetitive discharge of rat CA1 pyramidal neurones in vitro. J Physiol (Lond) 354:319–331Google Scholar
  46. Marty A (1983) Ca2+-dependent K+ channels with large unitary conductance. TINS 6:262–265Google Scholar
  47. Meech RW (1978) Calcium-dependent potassium activation in nervous tissues. Annu Rev Biophys Bioeng 7:1–18PubMedCrossRefGoogle Scholar
  48. Merill EG (1974) Finding a respiratory function for the medullary respiratory neurons. In: Bellairs R, Gray EG (eds) Essays on the nervous system. Clarendon Press, Oxford, pp 451–486Google Scholar
  49. Mifflin SW, Ballantyne D, Backman SB, Richter DW (1984) Effects of EGTA injection into medullary respiratory neurones. Pflügers Arch 400:R48Google Scholar
  50. Mifflin S, Ballantyne D, Backman SB, Richter DW (1985) Evidence for a calcium activated potassium conductance in medullary respiratory neurones. In: Bianchi AL, Denavit-Saubié (eds) Neurogenesis of central respiratory rhythm. MTP Press, Lancester, pp 179–181Google Scholar
  51. Miles R (1985) Synaptic integration in the nucleus of the solitary tract studied in vitro. In: Bianchi AL, Denavit-Saubié M (eds) Neurogenesis of central respiratory rhythm. MTP Press, Lancester, pp 165–168Google Scholar
  52. Miller AJ (1982) Deglutition. Physiol Rev 62:129–186PubMedGoogle Scholar
  53. Morin-Surun MP, Champagnat J, Denavit-Saubié M, Moyanova S (1984) The effects of acetylcholine on bulbar respiratory related neurones. Naunyn-Schmiedeberg's Arch Pharmacol 325:205–208CrossRefGoogle Scholar
  54. Neher E (1971) Two fast transient current components during voltage clamp on snail neurons. J Gen Physiol 58:36–53PubMedCrossRefGoogle Scholar
  55. Richter DW (1982) Generation and maintenance of the respiratory rhythm. J Exp Biol 100:93–107PubMedGoogle Scholar
  56. Richter DW, Camerer H, Meesmann M, Röhrig N (1979) Studies on the synaptic interaction between bulbar respiratory neurones of cats. Pflügers Arch 380:245–257PubMedCrossRefGoogle Scholar
  57. Richter DW, Ballantyne D, Mifflin S (1985) Interaction between postsynaptic activities and membrane properties in medullary respiratory neurones. In: Bianchi AL, Denavit-Saubié M (eds) Neurogenesis of central respiratory rhythm. MTP Press, Lancester, pp 172–178Google Scholar
  58. Spyer KM (1984) Central control of the cardiovascular system. In: Baker PF (ed) Recent advances in physiology. Churchill Livingston, London, pp 163–200Google Scholar
  59. Stinnakre J (1981) Detection and measurement of intracellular calcium. TINS 4:46–50Google Scholar
  60. Wilson W, Goldner MA (1975) Voltage-clamping with single microelectrode. J Neurobiol 4:411–422CrossRefGoogle Scholar
  61. Yarom Y, Llinas R (1979) Electrophysiological properties of mammalian olive neuron in in vitro brain stem slice and in vitro whole brain stem. Soc Neurosci Abstr 5:109Google Scholar
  62. Yarom Y, Sugimori M, Llinas R (1980) Inactivating fast potassium conductance in vagal motoneurons in guinea pigs: an in vitro study. Soc Neurosci Abstr 6:198Google Scholar

Copyright information

© Springer-Verlag 1986

Authors and Affiliations

  • J. Champagnat
    • 1
  • T. Jacquin
    • 1
  • D. W. Richter
    • 2
  1. 1.Labotaroire de Physiologie NerveuseCNRSGif-sur-YvetteFrance
  2. 2.I. Physiologisches Institut des Universität HeidelbergHeidelbergFederal Republic of Germany

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