Skip to main content
PMC home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1984 Nov;356:315–333. doi: 10.1113/jphysiol.1984.sp015467

Multiple actions of a molluscan cardioexcitatory neuropeptide and related peptides on identified Helix neurones.

G A Cottrell, N W Davies, K A Green
PMCID: PMC1193166  PMID: 6097674

Abstract

The effects of the molluscan neuropeptide Phe-Met-Arg-Phe-NH2 (FMRF amide) and related peptides (Price & Greenberg, 1977) were tested on Helix aspersa neurones. Ionophoretic application of FMRFamide depolarized and excited some neurones, but hyperpolarized and inhibited others. In some neurones the sign of the response was dependent on the membrane potential. Two responses resulted from an increase in membrane conductance, a depolarizing response mediated mainly by an increase in Na+ ion permeability, and a hyperpolarizing response mediated by an increase in K+ ion permeability. In the C1 neurone a voltage-dependent response was observed, which only occurred when the neurone was depolarized from its resting level. This response was recorded as an inward current during voltage clamp and resulted from a decrease in K current(s), possibly Ca-activated K current. More than one response may occur in a single neurone. In the C1 neurone, the K-mediated hyperpolarization occurred as well as the voltage-dependent response, while the depolarization seen in the F2 neurone was a combination of an increase in Na conductance and an increase in K conductance.

Full text

PDF
317

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adams P. R., Brown D. A. Luteinizing hormone-releasing factor and muscarinic agonists act on the same voltage-sensitive K+-current in bullfrog sympathetic neurones. Br J Pharmacol. 1980 Mar;68(3):353–355. doi: 10.1111/j.1476-5381.1980.tb14547.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Akaike N., Lee K. S., Brown A. M. The calcium current of Helix neuron. J Gen Physiol. 1978 May;71(5):509–531. doi: 10.1085/jgp.71.5.509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Ascher P. Inhibitory and excitatory effects of dopamine on Aplysia neurones. J Physiol. 1972 Aug;225(1):173–209. doi: 10.1113/jphysiol.1972.sp009933. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Barish M. E., Thompson S. H. Calcium buffering and slow recovery kinetics of calcium-dependent outward current in molluscan neurones. J Physiol. 1983 Apr;337:201–219. doi: 10.1113/jphysiol.1983.sp014620. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Berry M. S., Cottrell G. A. Excitatory, inhibitory and biphasic synaptic potentials mediated by an identified dopamine-containing neurone. J Physiol. 1975 Jan;244(3):589–612. doi: 10.1113/jphysiol.1975.sp010814. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brown D. A., Adams P. R. Muscarinic suppression of a novel voltage-sensitive K+ current in a vertebrate neurone. Nature. 1980 Feb 14;283(5748):673–676. doi: 10.1038/283673a0. [DOI] [PubMed] [Google Scholar]
  7. Cottrell G. A. An unusual synaptic response mediated by a serotonin neurone. Q J Exp Physiol. 1981 Oct;66(4):475–485. doi: 10.1113/expphysiol.1981.sp002589. [DOI] [PubMed] [Google Scholar]
  8. Cottrell G. A. FMRFamide neuropeptides simultaneously increase and decrease K+ current in an identified neurone. Nature. 1982 Mar 4;296(5852):87–89. doi: 10.1038/296087a0. [DOI] [PubMed] [Google Scholar]
  9. Cottrell G. A. Physiological role of a slow, voltage-sensitive, synaptic response mediated by an identified serotonin-containing neurone. Q J Exp Physiol. 1982 Jan;67(1):179–183. doi: 10.1113/expphysiol.1982.sp002612. [DOI] [PubMed] [Google Scholar]
  10. Cottrell G. A., Schot L. P., Dockray G. J. Identification and probable role of a single neurone containing the neuropeptide Helix FMRFamide. Nature. 1983 Aug 18;304(5927):638–640. doi: 10.1038/304638a0. [DOI] [PubMed] [Google Scholar]
  11. Dingledine R. N-methyl aspartate activates voltage-dependent calcium conductance in rat hippocampal pyramidal cells. J Physiol. 1983 Oct;343:385–405. doi: 10.1113/jphysiol.1983.sp014899. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Dodd J., Kelly S. Is somatostatin an excitatory transmitter in the hippocampus? Nature. 1978 Jun 22;273(5664):674–675. doi: 10.1038/273674a0. [DOI] [PubMed] [Google Scholar]
  13. Gerschenfeld H. M. Chemical transmission in invertebrate central nervous systems and neuromuscular junctions. Physiol Rev. 1973 Jan;53(1):1–119. doi: 10.1152/physrev.1973.53.1.1. [DOI] [PubMed] [Google Scholar]
  14. Gerschenfeld H. M., Paupardin-Tritsch D. Ionic mechanisms and receptor properties underlying the responses of molluscan neurones to 5-hydroxytryptamine. J Physiol. 1974 Dec;243(2):427–456. doi: 10.1113/jphysiol.1974.sp010761. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Ginsborg B. L., Kado R. T. Voltage-current relationship of a carbachol-induced potassium-ion pathway in Aplysia neurones. J Physiol. 1975 Mar;245(3):713–725. doi: 10.1113/jphysiol.1975.sp010870. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Grafe P., Mayer C. J., Wood J. D. Synaptic modulation of calcium-dependent potassium conductance in myenteric neurones in the guinea-pig. J Physiol. 1980 Aug;305:235–248. doi: 10.1113/jphysiol.1980.sp013360. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. HODGKIN A. L., KATZ B. The effect of sodium ions on the electrical activity of giant axon of the squid. J Physiol. 1949 Mar 1;108(1):37–77. doi: 10.1113/jphysiol.1949.sp004310. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Haas H. L., Konnerth A. Histamine and noradrenaline decrease calcium-activated potassium conductance in hippocampal pyramidal cells. 1983 Mar 31-Apr 6Nature. 302(5907):432–434. doi: 10.1038/302432a0. [DOI] [PubMed] [Google Scholar]
  19. Hamill O. P., Marty A., Neher E., Sakmann B., Sigworth F. J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981 Aug;391(2):85–100. doi: 10.1007/BF00656997. [DOI] [PubMed] [Google Scholar]
  20. Hermann A., Gorman A. L. Effects of tetraethylammonium on potassium currents in a molluscan neurons. J Gen Physiol. 1981 Jul;78(1):87–110. doi: 10.1085/jgp.78.1.87. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Hille B. Ionic channels in nerve membranes. Prog Biophys Mol Biol. 1970;21:1–32. doi: 10.1016/0079-6107(70)90022-2. [DOI] [PubMed] [Google Scholar]
  22. Hökfelt T., Johansson O., Ljungdahl A., Lundberg J. M., Schultzberg M. Peptidergic neurones. Nature. 1980 Apr 10;284(5756):515–521. doi: 10.1038/284515a0. [DOI] [PubMed] [Google Scholar]
  23. Jan Y. N., Jan L. Y., Kuffler S. W. A peptide as a possible transmitter in sympathetic ganglia of the frog. Proc Natl Acad Sci U S A. 1979 Mar;76(3):1501–1505. doi: 10.1073/pnas.76.3.1501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Katz B., Miledi R. A study of synaptic transmission in the absence of nerve impulses. J Physiol. 1967 Sep;192(2):407–436. doi: 10.1113/jphysiol.1967.sp008307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kehoe J. Ionic mechanisms of a two-component cholinergic inhibition in Aplysia neurones. J Physiol. 1972 Aug;225(1):85–114. doi: 10.1113/jphysiol.1972.sp009930. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kerkut G. A., Lambert J. D., Gayton R. J., Loker J. E., Walker R. J. Mapping of nerve cells in the suboesophageal ganglia of Helix aspersa. Comp Biochem Physiol A Comp Physiol. 1975 Jan 1;50(1A):1–25. doi: 10.1016/s0010-406x(75)80194-0. [DOI] [PubMed] [Google Scholar]
  27. Klein M., Kandel E. R. Presynaptic modulation of voltage-dependent Ca2+ current: mechanism for behavioral sensitization in Aplysia californica. Proc Natl Acad Sci U S A. 1978 Jul;75(7):3512–3516. doi: 10.1073/pnas.75.7.3512. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Meech R. W., Standen N. B. Potassium activation in Helix aspersa neurones under voltage clamp: a component mediated by calcium influx. J Physiol. 1975 Jul;249(2):211–239. doi: 10.1113/jphysiol.1975.sp011012. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Meech R. W. The sensitivity of Helix aspersa neurones to injected calcium ions. J Physiol. 1974 Mar;237(2):259–277. doi: 10.1113/jphysiol.1974.sp010481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Morita K., North R. A., Tokimasa T. Muscarinic agonists inactivate potassium conductance of guinea-pig myenteric neurones. J Physiol. 1982 Dec;333:125–139. doi: 10.1113/jphysiol.1982.sp014443. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Mudge A. W., Leeman S. E., Fischbach G. D. Enkephalin inhibits release of substance P from sensory neurons in culture and decreases action potential duration. Proc Natl Acad Sci U S A. 1979 Jan;76(1):526–530. doi: 10.1073/pnas.76.1.526. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. North R. A., Tokimasa T. Depression of calcium-dependent potassium conductance of guinea-pig myenteric neurones by muscarinic agonists. J Physiol. 1983 Sep;342:253–266. doi: 10.1113/jphysiol.1983.sp014849. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Paupardin-Tritsch D., Deterre P., Gerschenfeld H. M. Relationship between two voltage-dependent serotonin responses of molluscan neurones. Brain Res. 1981 Jul 27;217(1):201–206. doi: 10.1016/0006-8993(81)90201-8. [DOI] [PubMed] [Google Scholar]
  34. Pellmar T. C., Carpenter D. O. Serotonin induces a voltage-sensitive calcium current in neurons of Aplysia californica. J Neurophysiol. 1980 Sep;44(3):423–439. doi: 10.1152/jn.1980.44.3.423. [DOI] [PubMed] [Google Scholar]
  35. Pellmar T. C., Wilson W. A. Unconventional serotonergic excitation in Aplysia. Nature. 1977 Sep 1;269(5623):76–78. doi: 10.1038/269076a0. [DOI] [PubMed] [Google Scholar]
  36. Price D. A., Greenberg M. J. Structure of a molluscan cardioexcitatory neuropeptide. Science. 1977 Aug 12;197(4304):670–671. doi: 10.1126/science.877582. [DOI] [PubMed] [Google Scholar]
  37. Siegelbaum S. A., Camardo J. S., Kandel E. R. Serotonin and cyclic AMP close single K+ channels in Aplysia sensory neurones. Nature. 1982 Sep 30;299(5882):413–417. doi: 10.1038/299413a0. [DOI] [PubMed] [Google Scholar]
  38. Swann J. W., Carpenter D. O. Organisation of receptors for neurotransmitters on Aplysia neurones. Nature. 1975 Dec 25;258(5537):751–754. doi: 10.1038/258751a0. [DOI] [PubMed] [Google Scholar]
  39. Thomas R. C. Intracellular sodium activity and the sodium pump in snail neurones. J Physiol. 1972 Jan;220(1):55–71. doi: 10.1113/jphysiol.1972.sp009694. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Thompson S. H. Three pharmacologically distinct potassium channels in molluscan neurones. J Physiol. 1977 Feb;265(2):465–488. doi: 10.1113/jphysiol.1977.sp011725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Tillotson D., Horn R. Inactivation without facilitation of calcium conductance in caesium-loaded neurones of Aplysia. Nature. 1978 May 25;273(5660):312–314. doi: 10.1038/273312a0. [DOI] [PubMed] [Google Scholar]
  42. WERMAN R., GRUNDFEST H. Graded and all-or-none electrogenesis in arthropod muscle. II. The effects of alkali-earth and onium ions on lobster muscle fibers. J Gen Physiol. 1961 May;44:997–1027. doi: 10.1085/jgp.44.5.997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Wilson W. A., Goldner M. M. Voltage clamping with a single microelectrode. J Neurobiol. 1975 Jul;6(4):411–422. doi: 10.1002/neu.480060406. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES