Skip to main content
PMC home page
Biophysical Journal logoLink to Biophysical Journal
. 1994 Mar;66(3 Pt 1):710–718. doi: 10.1016/s0006-3495(94)80845-8

Analysis of the modulation by serotonin of a voltage-dependent potassium current in sensory neurons of Aplysia.

J A White 1, D A Baxter 1, J H Byrne 1
PMCID: PMC1275768  PMID: 8011902

Abstract

Potassium currents in pleural sensory neurons of Aplysia were studied under control conditions and in the presence of serotonin (5-HT). Using pharmacological techniques we isolated a current that we refer to as IK,V. Although it is not known whether IK,V represents a distinct type of membrane channel, we described its properties using a Hodgkin-Huxley type model. The effects of 5-HT on IK,V were complex. 5-HT decreased by 50% the steady-state magnitude (Iss) of IK,V in response to a voltage-clamp pulse from -50 mV to +20 mV. In addition, 5-HT significantly slowed both activation kinetics (the time constant of activation was increased by 29% at +20 mV) and inactivation kinetics (the time constant of inactivation was increased by 518% at +20 mV). Mathematical descriptions of IK,V in control conditions and in the presence of 5-HT were used to estimate the relative contribution of serotonergic modulation of IK,V to the total 5-HT-induced modulation of membrane currents. Effects of 5-HT on IK,V account for more than 87% of the 5-HT-induced reduction in outward current during the first 20 ms of a voltage-clamp pulse to +20 mV. This result implies that 5-HT exerts many of its effects on spike width in sensory neurons via modulation of IK,V. Effects of 5-HT on IK,V are consistent with a model in which the maximal conductance underlying the current is decreased by 50%, and the rate constants between open and closed states of both the activation and inactivation processes are diminished in magnitude across all membrane potentials.

Full text

PDF
716

Images in this article

714FIGURE 5
on p.714

Selected References

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

  1. Baxter D. A., Byrne J. H. Differential effects of cAMP and serotonin on membrane current, action-potential duration, and excitability in somata of pleural sensory neurons of Aplysia. J Neurophysiol. 1990 Sep;64(3):978–990. doi: 10.1152/jn.1990.64.3.978. [DOI] [PubMed] [Google Scholar]
  2. Baxter D. A., Byrne J. H. Serotonergic modulation of two potassium currents in the pleural sensory neurons of Aplysia. J Neurophysiol. 1989 Sep;62(3):665–679. doi: 10.1152/jn.1989.62.3.665. [DOI] [PubMed] [Google Scholar]
  3. Bean B. P., Nowycky M. C., Tsien R. W. Beta-adrenergic modulation of calcium channels in frog ventricular heart cells. 1984 Jan 26-Feb 1Nature. 307(5949):371–375. doi: 10.1038/307371a0. [DOI] [PubMed] [Google Scholar]
  4. Belardetti F., Kandel E. R., Siegelbaum S. A. Neuronal inhibition by the peptide FMRFamide involves opening of S K+ channels. Nature. 1987 Jan 8;325(7000):153–156. doi: 10.1038/325153a0. [DOI] [PubMed] [Google Scholar]
  5. Braha O., Edmonds B., Sacktor T., Kandel E. R., Klein M. The contributions of protein kinase A and protein kinase C to the actions of 5-HT on the L-type Ca2+ current of the sensory neurons in Aplysia. J Neurosci. 1993 May;13(5):1839–1851. doi: 10.1523/JNEUROSCI.13-05-01839.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Byrne J. H. Cellular analysis of associative learning. Physiol Rev. 1987 Apr;67(2):329–439. doi: 10.1152/physrev.1987.67.2.329. [DOI] [PubMed] [Google Scholar]
  7. Byrne J. H., Zwartjes R., Homayouni R., Critz S. D., Eskin A. Roles of second messenger pathways in neuronal plasticity and in learning and memory. Insights gained from Aplysia. Adv Second Messenger Phosphoprotein Res. 1993;27:47–108. [PubMed] [Google Scholar]
  8. Camardo J. S., Shuster M. J., Siegelbaum S. A., Kandel E. R. Modulation of a specific potassium channel in sensory neurons of Aplysia by serotonin and cAMP-dependent protein phosphorylation. Cold Spring Harb Symp Quant Biol. 1983;48(Pt 1):213–220. doi: 10.1101/sqb.1983.048.01.024. [DOI] [PubMed] [Google Scholar]
  9. Critz S. D., Baxter D. A., Byrne J. H. Modulatory effects of serotonin, FMRFamide, and myomodulin on the duration of action potentials, excitability, and membrane currents in tail sensory neurons of Aplysia. J Neurophysiol. 1991 Dec;66(6):1912–1926. doi: 10.1152/jn.1991.66.6.1912. [DOI] [PubMed] [Google Scholar]
  10. Ewald D. A., Williams A., Levitan I. B. Modulation of single Ca2+-dependent K+-channel activity by protein phosphorylation. Nature. 1985 Jun 6;315(6019):503–506. doi: 10.1038/315503a0. [DOI] [PubMed] [Google Scholar]
  11. FRANKENHAEUSER B., HODGKIN A. L. The action of calcium on the electrical properties of squid axons. J Physiol. 1957 Jul 11;137(2):218–244. doi: 10.1113/jphysiol.1957.sp005808. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Giles W., Nakajima T., Ono K., Shibata E. F. Modulation of the delayed rectifier K+ current by isoprenaline in bull-frog atrial myocytes. J Physiol. 1989 Aug;415:233–249. doi: 10.1113/jphysiol.1989.sp017720. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Goldsmith B. A., Abrams T. W. cAMP modulates multiple K+ currents, increasing spike duration and excitability in Aplysia sensory neurons. Proc Natl Acad Sci U S A. 1992 Dec 1;89(23):11481–11485. doi: 10.1073/pnas.89.23.11481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gunning R. Increased numbers of ion channels promoted by an intracellular second messenger. Science. 1987 Jan 2;235(4784):80–82. doi: 10.1126/science.2432659. [DOI] [PubMed] [Google Scholar]
  15. HODGKIN A. L., HUXLEY A. F. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol. 1952 Aug;117(4):500–544. doi: 10.1113/jphysiol.1952.sp004764. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hochner B., Kandel E. R. Modulation of a transient K+ current in the pleural sensory neurons of Aplysia by serotonin and cAMP: implications for spike broadening. Proc Natl Acad Sci U S A. 1992 Dec 1;89(23):11476–11480. doi: 10.1073/pnas.89.23.11476. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hurst A. M., Hunter M. Acute changes in channel density of amphibian diluting segment. Am J Physiol. 1990 Dec;259(6 Pt 1):C1005–C1009. doi: 10.1152/ajpcell.1990.259.6.C1005. [DOI] [PubMed] [Google Scholar]
  18. Kaczmarek L. K., Strumwasser F. A voltage-clamp analysis of currents underlying cyclic AMP-induced membrane modulation in isolated peptidergic neurons of Aplysia. J Neurophysiol. 1984 Aug;52(2):340–349. doi: 10.1152/jn.1984.52.2.340. [DOI] [PubMed] [Google Scholar]
  19. Kandel E. R., Schwartz J. H. Molecular biology of learning: modulation of transmitter release. Science. 1982 Oct 29;218(4571):433–443. doi: 10.1126/science.6289442. [DOI] [PubMed] [Google Scholar]
  20. Klein M., Camardo J., Kandel E. R. Serotonin modulates a specific potassium current in the sensory neurons that show presynaptic facilitation in Aplysia. Proc Natl Acad Sci U S A. 1982 Sep;79(18):5713–5717. doi: 10.1073/pnas.79.18.5713. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Klein M., Kandel E. R. Mechanism of calcium current modulation underlying presynaptic facilitation and behavioral sensitization in Aplysia. Proc Natl Acad Sci U S A. 1980 Nov;77(11):6912–6916. doi: 10.1073/pnas.77.11.6912. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Levitan I. B. Modulation of ion channels in neurons and other cells. Annu Rev Neurosci. 1988;11:119–136. doi: 10.1146/annurev.ne.11.030188.001003. [DOI] [PubMed] [Google Scholar]
  23. Numann R., Catterall W. A., Scheuer T. Functional modulation of brain sodium channels by protein kinase C phosphorylation. Science. 1991 Oct 4;254(5028):115–118. doi: 10.1126/science.1656525. [DOI] [PubMed] [Google Scholar]
  24. Ocorr K. A., Byrne J. H. Membrane responses and changes in cAMP levels in Aplysia sensory neurons produced by serotonin, tryptamine, FMRFamide and small cardioactive peptideB (SCPB). Neurosci Lett. 1985 Apr 9;55(2):113–118. doi: 10.1016/0304-3940(85)90004-7. [DOI] [PubMed] [Google Scholar]
  25. Perozo E., Bezanilla F., Dipolo R. Modulation of K channels in dialyzed squid axons. ATP-mediated phosphorylation. J Gen Physiol. 1989 Jun;93(6):1195–1218. doi: 10.1085/jgp.93.6.1195. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Perozo E., Bezanilla F. Phosphorylation affects voltage gating of the delayed rectifier K+ channel by electrostatic interactions. Neuron. 1990 Nov;5(5):685–690. doi: 10.1016/0896-6273(90)90222-2. [DOI] [PubMed] [Google Scholar]
  27. Pollock J. D., Bernier L., Camardo J. S. Serotonin and cyclic adenosine 3':5'-monophosphate modulate the potassium current in tail sensory neurons in the pleural ganglion of Aplysia. J Neurosci. 1985 Jul;5(7):1862–1871. doi: 10.1523/JNEUROSCI.05-07-01862.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Pollock J. D., Camardo J. S. Regulation of single potassium channels by serotonin in the cell bodies of the tail mechanosensory neurons of Aplysia californica. Brain Res. 1987 May 5;410(2):367–370. doi: 10.1016/0006-8993(87)90340-4. [DOI] [PubMed] [Google Scholar]
  29. Rudy B. Diversity and ubiquity of K channels. Neuroscience. 1988 Jun;25(3):729–749. doi: 10.1016/0306-4522(88)90033-4. [DOI] [PubMed] [Google Scholar]
  30. Scholz K. P., Byrne J. H. Intracellular injection of cAMP induces a long-term reduction of neuronal K+ currents. Science. 1988 Jun 17;240(4859):1664–1666. doi: 10.1126/science.2837826. [DOI] [PubMed] [Google Scholar]
  31. Scholz K. P., Byrne J. H. Long-term sensitization in Aplysia: biophysical correlates in tail sensory neurons. Science. 1987 Feb 6;235(4789):685–687. doi: 10.1126/science.2433766. [DOI] [PubMed] [Google Scholar]
  32. Shuster M. J., Camardo J. S., Siegelbaum S. A. Comparison of the serotonin-sensitive and Ca(2+)-activated K+ channels in Aplysia sensory neurons. J Physiol. 1991;440:601–621. doi: 10.1113/jphysiol.1991.sp018727. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Shuster M. J., Camardo J. S., Siegelbaum S. A., Kandel E. R. Cyclic AMP-dependent protein kinase closes the serotonin-sensitive K+ channels of Aplysia sensory neurones in cell-free membrane patches. 1985 Jan 31-Feb 6Nature. 313(6001):392–395. doi: 10.1038/313392a0. [DOI] [PubMed] [Google Scholar]
  34. Shuster M. J., Siegelbaum S. A. Pharmacological characterization of the serotonin-sensitive potassium channel of Aplysia sensory neurons. J Gen Physiol. 1987 Oct;90(4):587–608. doi: 10.1085/jgp.90.4.587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. 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]
  36. Soliven B., Nelson D. J. Beta-adrenergic modulation of K+ current in human T lymphocytes. J Membr Biol. 1990 Sep;117(3):263–274. doi: 10.1007/BF01868456. [DOI] [PubMed] [Google Scholar]
  37. Strong J. A., Kaczmarek L. K. Multiple components of delayed potassium current in peptidergic neurons of Aplysia: modulation by an activator of adenylate cyclase. J Neurosci. 1986 Mar;6(3):814–822. doi: 10.1523/JNEUROSCI.06-03-00814.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Strong J. A. Modulation of potassium current kinetics in bag cell neurons of Aplysia by an activator of adenylate cyclase. J Neurosci. 1984 Nov;4(11):2772–2783. doi: 10.1523/JNEUROSCI.04-11-02772.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Sugita S., Goldsmith J. R., Baxter D. A., Byrne J. H. Involvement of protein kinase C in serotonin-induced spike broadening and synaptic facilitation in sensorimotor connections of Aplysia. J Neurophysiol. 1992 Aug;68(2):643–651. doi: 10.1152/jn.1992.68.2.643. [DOI] [PubMed] [Google Scholar]
  40. Walsh J. P., Byrne J. H. Modulation of a steady-state Ca2+-activated, K+ current in tail sensory neurons of Aplysia: role of serotonin and cAMP. J Neurophysiol. 1989 Jan;61(1):32–44. doi: 10.1152/jn.1989.61.1.32. [DOI] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES