A-Current Diversity: Differences in Channel Hardware or Second Messengers?

  • Deborah J. Baro
Conference paper


The pyloric network generates a rhythmic motor behavior that is continuously adaptive (Harris-Warrick et al. 1992). This patterned activity is based not only on synaptic connectivity, but also on the unique firing properties of the component neurons. There are many molecular devices that could establish different firing properties between neurons, ranging from relatively static mechanisms like differential gene expression, to more dynamic methods such as changes in ion channel phosphorylation states. The strategies involved most likely reflect elementary principles of the system. Defining these strategies for the pyloric network could provide insights into its dynamic nature.


Voltage Dependence Somatodendritic Compartment Shaker Channel Pyloric Network Transient Potassium Current 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. An W, Bowlby M, Betty M, Cao J, Ling H-P, Mendoza G, Hinson J, Mattson K, Strassle B, Trimmer J, Rhodes K (2000) Modulation of A-type potassium channels by a family of calcium sensors. Nature 403: 553–556PubMedCrossRefGoogle Scholar
  2. Baro DJ, Coniglio LM, Cole CL, Rodriguez HE, Lubell JK, Kim MT, Harris-Warrick RM (1996a) Lobster shal: comparison with Drosophila shal and native potassium currents in identified neurons. J Neurosci 16: 1689–1701PubMedGoogle Scholar
  3. Baro DJ, Cole CL, Harris-Warrick RM (1996b) RT-PCR analysis of shaker, shab, shaw, and shal gene expression in single neurons and glial cells. Receptors Channels 4: 149–159PubMedGoogle Scholar
  4. Baro DJ, Levini RM, Kim MT, Willms AR, Lanning CC, Rodriguez HE, Harris-Warrick RM (1997) Quantitative single-cell-reverse transcription-PCR demonstrates that A-current magnitude varies as a linear function of shal gene expression in identified stomatogastric neurons. J Neurosci 17: 6597–6610PubMedGoogle Scholar
  5. Baro DJ, Ayali A, French L, Scholz NL, Labenia J, Lanning CC, Graubard K, Harris-Warrick RM (2000a) Molecular underpinnings of motor pattern generation: differential targeting of shal and shaker in the pyloric motor system. J Neurosci 20: 6619–6630PubMedGoogle Scholar
  6. Baro, D.J., Quinones, L., Lanning, CC, Harris-Warrick, R.M., and Ruiz, M. (2001) Stable differences in α-subunit gene expression cannot account for IA diversity in the components of a dynamic motor network, in pressGoogle Scholar
  7. Bowlby MR, Mendoza G, Hinson J, An WF, Cao J, Wardwell-Swanson J, Mattson KI, Rhodes KJ (1999) Modulation of Kv4-family K+ channels by a novel family of neuronal calcium sensor homologs. Soc Neurosci Abstr 25: 982Google Scholar
  8. Chandy CK GG (1995) Voltage-gated potassium channel genes. In: North RA (ed) Handbook of receptors and channels: ligand- and voltage-gated ion channels. CRC, Boca Raton, pp 1–71Google Scholar
  9. Chen M-L, Hoshi T, Wu C-F (1996) Heteromultimeric interactions among K+ channel subunits from Shaker and eag families in Xenopus oocytes. Neuron 17: 535–542PubMedCrossRefGoogle Scholar
  10. Connor JA (1975) Neural repetitive firing: a comparitve study of membrane properties of crustacean walking leg axons. J Neurophysiol 351: 922–932Google Scholar
  11. Covarrubias M, Wei A, Salkoff L, Vyas TB (1994) Elimination of rapid potassium channel inactivation by phosphorylation of the inactivation gate. Neuron 13: 1403–1412PubMedCrossRefGoogle Scholar
  12. Debanne D, Guerineau NC, Gahwiler BH, Thompson SM (1997) Action-potential propagation gated by an axonal I(A)-like K+ conductance in hippocampus [published erratum appears in Nature 1997 Dec 4;390(6659): 536]. Nature 389: 286–289PubMedCrossRefGoogle Scholar
  13. Derst C, Karschin A (1998) Review: evolutionary link between prokaryotic and eukaryotic K+ channels. J Exp Biol 201: 2791–2799Google Scholar
  14. Doliveira LC, Nawoschik SP, An WF, Bowlby MR, Trimmer JS, Rhodes KJ (1999) Effects of two novel neuronal calcium sensor homologs on surface expression of Kv4 a-subunits in COSI cells. Soc Neurosci Abstr 25: 982Google Scholar
  15. Drain P, Dubin AE, Aldrich RW (1994) Regulation of Shaker K+ channel inactivation gating by the cAMP-dependent protein kinase. Neuron 12: 1097–1109PubMedCrossRefGoogle Scholar
  16. Fink M, Lesage F, Duprat F, Heurteaux C, Reyes R, Fosset M, Lazdunski M (1998) A neuronal two P domain K+ channel stimulated by arachidonic acid and polyunsaturated fatty acids. Embo J 17: 3297–3308PubMedCrossRefGoogle Scholar
  17. Graubard K, Hartline DK (1991) Voltage clamp analysis of intact stomatogastric neurons. Brain Res 557: 241–254PubMedCrossRefGoogle Scholar
  18. Harris-Warrick R, Marder E, Selverston A, Moulins M (eds) (1992) Cellular and synaptic properties in the crustacean stomatogastric nervous system. In: Dynamic biological networks. MIT Press, CambridgeGoogle Scholar
  19. Harris-Warrick RM, Coniglio LM, Barazangi N, Guckenheimer J, Gueron S (1995a) Dopamine modulation of transient potassium current evokes phase shifts in a central pattern generator network. J Neurosci 15: 342–358PubMedGoogle Scholar
  20. Harris-Warrick RM, Coniglio LM, Levini RM, Gueron S, Guckenheimer J (1995b) Dopamine modulation of two subthreshold currents produces phase shifts in activity of an identified motoneuron. J Neurophysiol 74: 1404–1420PubMedGoogle Scholar
  21. Hartline D, Graubard K (1992) Cellular and synaptic properties in the crustacean stomatogastric nervous system. In: Harris-Warrick R, Marder E, Selverston A, Moulins M (eds) Dynamic biological networks. MIT Press, Cambridge, pp 31–85Google Scholar
  22. Hartline DK (1979) Pattern generation in the lobster (Panulirus) stomatogastric ganglion. II Pyloric network simulation. Biol Cybern 33: 223–236PubMedCrossRefGoogle Scholar
  23. Hartline DK, Gassie DV, Jones BR (1993) Effects of soma isolation on outward currents measured under voltage clamp in spiny lobster stomatogastric motor neurons. J Neurophysiol 69: 2056–2071PubMedGoogle Scholar
  24. Hoger JH, Walter AE, Vance D, Yu L, Lester HA, Davidson N (1991) Modulation of a cloned mouse brain potassium channel. Neuron 6: 227–236PubMedCrossRefGoogle Scholar
  25. Holmes TC, Fadool DA, Levitan IB (1996) Tyrosine phosphorylation of the Kvl.3 potassium channel. J Neurosci 16: 1581–1590PubMedGoogle Scholar
  26. Huang X-Y, Morelli AD, Peralta EG (1993) Tyrosine kinase dependent supression of a potassium channel by the G protein-coupled ml muscarinic receptor. Cell 75: 1145–1156PubMedCrossRefGoogle Scholar
  27. Huang X-Y, Morelli AD, Peralta EG (1994) Molecular basis of cardiac potassium channel stimulation by protein kinase A. PNAS 94: 624–628CrossRefGoogle Scholar
  28. Hugnot JP, Salinas M, Lesage F, Guillemare E, de Weille J, Heurteaux C, Mattei MG, Lazdunski M (1996) Kv8.1, a new neuronal potassium channel subunit with specific inhibitory properties towards Shab and Shaw channels. Embo J 15: 3322–3331PubMedGoogle Scholar
  29. Jan LY, Jan NY (1997) Cloned potassium channels from eukaryotes and prokaryotes. Annu Rev Neurosci 20: 91–124PubMedCrossRefGoogle Scholar
  30. Jegla T, Salkoff L (1997) A novel subunit for shal K+ channels radically alters activation and inactivation. J Neurosci 17: 32–44PubMedGoogle Scholar
  31. Jonas EA, Kaczmarek LK (1996) Regulation of potassium channels by protein kinases. Curr Opin Neurobiol 6: 318–323PubMedCrossRefGoogle Scholar
  32. Ketchum KA, Joiner WJ, Sellers AJ, Kaczmarek LK, Goldstein SA (1995) A new family of outwardly rectifying potassium channel proteins with two pore domains in tandem. Nature 376: 690–695PubMedCrossRefGoogle Scholar
  33. Kim M, Baro DJ, Lanning CC, Doshi M, Farnham J, Moskowitz HS, Peck JH, Olivera BM, Harris-Warrick RM (1997) Alternative splicing in the pore-forming region of shaker potassium channels. J Neurosci 17: 8213–8224PubMedGoogle Scholar
  34. Kim M, Baro DJ, Lanning CC, Doshi M, Moskowitz HS, Farnham J, Harris-Warrick RM (1998) Expression of Panulirus shaker potassium channel splice variants. Receptors Channels 5: 291–304PubMedGoogle Scholar
  35. Kindler CH, Yost CS, Gray AT (1999) Local anesthetic inhibition of baseline potassium channels with two pore domains in tandem. Anesthesiology 90: 1092–1102PubMedCrossRefGoogle Scholar
  36. Kloppenburg P, Levini RM, Harris-Warrick RM (1999) Dopamine modulates two potassium currents and inhibits the intrinsic firing properties of an identified motor neuron in a central pattern generator network. J Neurophysiol 81: 29–38PubMedGoogle Scholar
  37. Levitan IB (1994) Modulation of ion channels by protein phosphorylation and dephosphorylation. Annu Rev Physiol 56: 193–212PubMedCrossRefGoogle Scholar
  38. Meyrand P, Weimann JM, Marder E (1992) Multiple axonal spike initiation zones in a motor neuron: serotonin activation. J Neurosci 12:2803–2812.PubMedGoogle Scholar
  39. Miller JP (1980) Mechanisms underlying pattern generation in the lobster stomatogastric ganglion. University of California, San DiegoGoogle Scholar
  40. Moran O, Dascal N, Lotan I (1991) Modulation of a Shaker potassium A-channel by protein kinase C activation. FEBS Lett 279: 256–260PubMedCrossRefGoogle Scholar
  41. Patel AJ, Honore E, Maingret F, Lesage F, Fink M, Duprat F, Lazdunski M (1998) A mammalian two pore domain mechano-gated S-like K+ channel. Embo J 17: 4283–4290PubMedCrossRefGoogle Scholar
  42. Patel AJ, Honore E, Lesage F, Fink M, Romey G, Lazdunski M (1999) Inhalational anesthetics activate two-pore-domain background K+ channels. Nat Neurosci 2: 422–426PubMedCrossRefGoogle Scholar
  43. Pongs O (1999) Voltage-gated potassium channels: from hyperexcitability to excitement. FEBS Lett 452: 31–35PubMedCrossRefGoogle Scholar
  44. Qian Y, DeRubies D, Pfaffiinger PJ (1999) The N-terminal and C-terminal domain of voltage-dependent potassium channels are processed and may act as signaling molecules. Soc Neurosc Abstr 25: 531Google Scholar
  45. Raper JA (1979) Nonimpulse-mediated synaptic transmission during the generation of a cyclic motor program. Science 205: 304–306PubMedCrossRefGoogle Scholar
  46. Reimann F, Ashcroft FM (1999) Inwardly rectifying potassium channels. Curr Opin Cell Biol 11:503–508PubMedCrossRefGoogle Scholar
  47. Roeper J, Lorra C, Pongs O (1997) Frequency-dependent inactivation of mammalian A-type K+ channel KV1.4 regulated by Ca2+/calmodulin-dependent protein kinase. J Neurosci 17: 3379–3391PubMedGoogle Scholar
  48. Rogero O, Hammerle B, Tejedor FJ (1997) Diverse expression and distribution of Shaker potassium channels during the development of the Drosophila nervous system. J Neurosci 17: 5108–5118PubMedGoogle Scholar
  49. Rosenthal JJ, Vickery RG, Gilly WF (1996) Molecular identification of SqKvlA. A candidate for the delayed rectifier K channel in squid giant axon. J Gen Physiol 108: 207–219PubMedCrossRefGoogle Scholar
  50. Rosenthal JJ, Liu TI, Gilly WF (1997) A family of delayed rectifier Kvl cDNAs showing cell type-specific expression in the squid stellate ganglion/giant fiber lobe complex. J Neurosci 17: 5070–5079PubMedGoogle Scholar
  51. Salkoff L, Jegla T (1995) Surfing the DNA databases for K+ channels nets yet more diversity. Neuron 15: 489–492PubMedCrossRefGoogle Scholar
  52. Salkoff L, Baker K, Butler A, Covarrubias M, Pak MD, Wei A (1992) An essential ‘set’ of K+ channels conserved in flies, mice and humans. Trends Neurosci 15: 161–166PubMedCrossRefGoogle Scholar
  53. Schulman H (1995) Protein phosphorylation in neuronal plasticity and gene expression. Curr Opin Neurobiol 5: 375–381PubMedCrossRefGoogle Scholar
  54. Shi G, Nakahira K, Hammond S, Rhodes KJ, Schechter LE, Trimmer JS (1996) β-subunits promote K channel surface expression through effects early in biosynthesis. Neuron 16: 843–852Google Scholar
  55. Snyders DJ (1999) Structure and function of cardiac potassium channels. Cardiovasc Res 42: 377–390PubMedCrossRefGoogle Scholar
  56. Stowell JN, Craig AM (1999) Axon/dendrite targeting of metabotropic glutamate receptors by their cytoplasmic carboxy-terminal domains. Neuron 22: 525–536PubMedCrossRefGoogle Scholar
  57. Tang CY, Schulteis CT, Jimenez RM, Papazian DM (1998) Shaker and ether-a-go-go K+ channel subunits fail to coassemble in Xenopus oocytes. Biophys J 75: 1263–1270PubMedCrossRefGoogle Scholar
  58. Tierney AJ, Harris-Warrick RM (1992) Physiological role of the transient potassium current in the pyloric circuit of the lobster stomatogastric ganglion. J Neurophysiol 67: 599–609PubMedGoogle Scholar
  59. Trimmer JS (1999) Sorting out receptor trafficking. Neuron 22: 411–412PubMedCrossRefGoogle Scholar
  60. Villarroel A, Schwarz TL (1996) Inhibition of the Kv4 (Shal) family of transient K+ currents by arachidonic acid. J Neurosci 16: 1016–1025PubMedGoogle Scholar
  61. Wang H, Kunkel DD, Martin TM, Schwartzkroin PA, Tempel BL (1993) Heteromultimeric K+ channels in terminal and juxtaparanodal regions of neurons. Nature 365: 75–79PubMedCrossRefGoogle Scholar
  62. Wang ZW, Kunkel MT, Wei A, Butler A, Salkoff L (1999) Genomic organization of nematode 4TM K+ channels. Ann N Y Acad Sci 868: 286–303PubMedCrossRefGoogle Scholar
  63. Wei A, Jegla T, Salkoff L (1996) Eight potassium channel families revealed by the C. elegans genome project. Neuropharmacology 35: 805–829PubMedCrossRefGoogle Scholar
  64. Willms AR, Baro DJ, Harris-Warrick RM, Guckenheimer J (1999) An improved parameter estimation method for Hodgkin-Huxley models. J Computational Neuroscience 6: 145–168CrossRefGoogle Scholar
  65. Wilson GG, O’Neill CA, Sivaprasadarao A, Findlay JBC, Wray D (1994) Modulation by protein kinase A of a cloned rat brain potassium channel expressed in Xenopus oocytes. Pfluegers Arch 428: 186–193CrossRefGoogle Scholar
  66. Yang EK, Alvira M, Levitan ES, Takimoto K (1999) Association of Kv4 family channels with β subunits. Soc Neurosci Abstr 25: 983Google Scholar
  67. Yu W, Jia X, Li M (1996) NAB domain is essential for the subunit assembly of both α-α and α-β complexes of shaker-like potassium channels. Neuron 16: 441–453PubMedCrossRefGoogle Scholar
  68. Zhong Y, Wu CF (1991) Alteration of four identified K+ currents in Drosophila muscle by mutations in eag. Science 252: 1562–1564PubMedCrossRefGoogle Scholar
  69. Zhong Y, Wu CF (1993) Modulation of different K+ currents in Drosophila: a hypothetical role for the Eag subunit in multimeric K+ channels. J Neurosci 13: 4669–4679PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2002

Authors and Affiliations

  • Deborah J. Baro
    • 1
  1. 1.Institute of Neurobiology and Department of BiochemistryUniversity of Puerto Rico- Medical Sciences CampusSan JuanPuerto Rico

Personalised recommendations