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ISRN Neuroscience
Volume 2013 (2013), Article ID 354262, 14 pages
http://dx.doi.org/10.1155/2013/354262
Review Article

Slack, Slick, and Sodium-Activated Potassium Channels

Departments of Pharmacology and Cellular and Molecular Physiology, Yale University School of Medicine, 333 Cedar Street, New Haven, CT 06520-8066, USA

Received 24 February 2013; Accepted 18 April 2013

Academic Editors: Y. Bozzi, A. Kulik, and W. Van Drongelen

Copyright © 2013 Leonard K. Kaczmarek. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. B. Hille, Ionic Channels of Excitable Membranes, Sinauer Associates, Sunderland, Mass, USA, 3rd edition, 2001.
  2. G. Barcia, M. R. Fleming, A. Deligniere et al., “De novo gain-of-function KCNT1 channel mutations cause malignant migrating partial seizures of infancy,” Nature Genetics, vol. 44, pp. 1255–1259, 2012.
  3. S. E. Heron, K. R. Smith, M. Bahlo et al., “Missense mutations in the sodium-gated potassium channel gene KCNT1 cause severe autosomal dominant nocturnal frontal lobe epilepsy,” Nature Genetics, vol. 44, pp. 1188–1190, 2012.
  4. A. Bhattacharjee, W. J. Joiner, M. Wu, Y. Yang, F. J. Sigworth, and L. K. Kaczmarek, “Slick (Slo2. 1), a rapidly-gating sodium-activated potassium channel inhibited by ATP,” The Journal of Neuroscience, vol. 23, no. 37, pp. 11681–11691, 2003. View at Scopus
  5. T. J. Tamsett, K. E. Picchione, and A. Bhattacharjee, “NAD+ activates KNa channels in dorsal root ganglion neurons,” The Journal of Neuroscience, vol. 29, no. 16, pp. 5127–5134, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. M. R. Brown, J. Kronengold, V. R. Gazula et al., “Fragile X mental retardation protein controls gating of the sodium-activated potassium channel Slack,” Nature Neuroscience, vol. 13, no. 7, pp. 819–821, 2010. View at Publisher · View at Google Scholar · View at Scopus
  7. M. Kameyama, M. Kakei, and R. Sato, “Intracellular Na+ activates a K+ channel in mammalian cardiac cells,” Nature, vol. 309, no. 5966, pp. 354–356, 1984. View at Scopus
  8. C. R. Bader, L. Bernheim, and D. Bertrand, “Sodium-activated potassium current in cultured avian neurones,” Nature, vol. 317, no. 6037, pp. 540–542, 1985. View at Scopus
  9. K. Hartung, “Potentiation of a transient outward current by Na+ influx in crayfish neurones,” Pflugers Archiv, vol. 404, no. 1, pp. 41–44, 1985. View at Scopus
  10. S. E. Dryer, J. T. Fujii, and A. R. Martin, “A Na+-activated K+ current in cultured brain stem neurones from chicks,” The Journal of Physiology, vol. 410, pp. 283–296, 1989. View at Scopus
  11. P. C. Schwindt, W. J. Spain, and W. E. Crill, “Long-lasting reduction of excitability by a sodium-dependent potassium current in cat neocortical neurons,” Journal of Neurophysiology, vol. 61, no. 2, pp. 233–244, 1989. View at Scopus
  12. C. Haimann, L. Bernheim, D. Bertrand, and C. R. Bader, “Potassium current activated by intracellular sodium in quail trigeminal ganglion neurons,” Journal of General Physiology, vol. 95, no. 5, pp. 961–979, 1990. View at Publisher · View at Google Scholar · View at Scopus
  13. S. E. Dryer, “Na+-activated K+ channels and voltage-evoked ionic currents in brain stem and parasympathetic neurones of the chick,” The Journal of Physiology, vol. 435, pp. 513–532, 1991. View at Scopus
  14. M. Saito and C. F. Wu, “Expression of ion channels and mutational effects in giant Drosophila neurons differentiated from cell division-arrested embryonic neuroblasts,” The Journal of Neuroscience, vol. 11, no. 7, pp. 2135–2150, 1991. View at Scopus
  15. T. M. Egan, D. Dagan, J. Kupper, and I. B. Levitan, “Properties and rundown of sodium-activated potassium channels in rat olfactory bulb neurons,” The Journal of Neuroscience, vol. 12, no. 5, pp. 1964–1976, 1992. View at Scopus
  16. C. Haimann, J. Magistretti, and B. Pozzi, “Sodium-activated potassium current in sensory neurons: a comparison of cell-attached and cell-free single-channel activities,” Pflugers Archiv, vol. 422, no. 3, pp. 287–294, 1992. View at Publisher · View at Google Scholar · View at Scopus
  17. N. Dale, “A large, sustained Na+- and voltage-dependent K+ current in spinal neurons of the frog embryo,” The Journal of Physiology, vol. 462, pp. 349–372, 1993. View at Scopus
  18. B. V. Safronov and W. Vogel, “Properties and functions of Na+-activated K+ channels in the soma of rat motoneurones,” The Journal of Physiology, vol. 497, no. 3, pp. 727–734, 1996. View at Scopus
  19. U. Bischoff, W. Vogel, and B. V. Safronov, “Na+-activated K+ channels in small dorsal root ganglion neurones of rat,” The Journal of Physiology, vol. 510, part 3, pp. 743–754, 1998. View at Scopus
  20. S. E. Dryer, “Na+-activated K+ channels: a new family of large-conductance ion channels,” Trends in Neurosciences, vol. 17, no. 4, pp. 155–160, 1994. View at Publisher · View at Google Scholar · View at Scopus
  21. A. Bhattacharjee and L. K. Kaczmarek, “For K+ channels, Na+ is the new Ca2+,” Trends in Neurosciences, vol. 28, no. 8, pp. 422–428, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. S. B. Gao, Y. Wu, C. X. Lü, Z. H. Guo, C. H. Li, and J. P. Ding, “Slack and Slick KNa channels are required for the depolarizing afterpotential of acutely isolated, medium diameter rat dorsal root ganglion neurons,” Acta Pharmacologica Sinica, vol. 29, no. 8, pp. 899–905, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. M. O. Nuwer, K. E. Picchione, and A. Bhattacharjee, “PKA-induced internalization of Slack KNa channels produces dorsal root ganglion neuron hyperexcitability,” The Journal of Neuroscience, vol. 30, no. 42, pp. 14165–14172, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. D. Hess, E. Nanou, and A. El Manira, “Characterization of Na+-activated K+ currents in larval lamprey spinal cord neurons,” Journal of Neurophysiology, vol. 97, no. 5, pp. 3484–3493, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. E. Nanou and A. El Manira, “A postsynaptic negative feedback mediated by coupling between AMPA receptors and Na+-activated K+ channels in spinal cord neurones,” European Journal of Neuroscience, vol. 25, no. 2, pp. 445–450, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. P. Wallén, B. Robertson, L. Cangiano et al., “Sodium-dependent potassium channels of a Slack-like subtype contribute to the slow afterhyperpolarization in lamprey spinal neurons,” The Journal of Physiology, vol. 585, no. 1, pp. 75–90, 2007. View at Publisher · View at Google Scholar · View at Scopus
  27. E. Nanou, A. Kyriakatos, A. Bhattacharjee, L. K. Kaczmarek, G. Paratcha, and A. El Manira, “Na+-mediated coupling between AMPA receptors and KNa channels shapes synaptic transmission,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 52, pp. 20941–20946, 2008. View at Publisher · View at Google Scholar · View at Scopus
  28. E. Nanou and A. El Manira, “Mechanisms of modulation of AMPA-induced Na+-activated K+ current by mGluR1,” Journal of Neurophysiology, vol. 103, no. 1, pp. 441–445, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. A. R. Mercer and J. G. Hildebrand, “Developmental changes in the density of ionic currents in antennal-lobe neurons of the sphinx moth, Manduca sexta,” Journal of Neurophysiology, vol. 87, no. 6, pp. 2664–2675, 2002. View at Scopus
  30. K. Aoki, K. Kosakai, and M. Yoshino, “Monoaminergic modulation of the Na+-activated K+ channel in kenyon cells isolated from the mushroom body of the cricket (Gryllus bimaculatus) brain,” Journal of Neurophysiology, vol. 100, no. 3, pp. 1211–1222, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. G. Klees, P. Hochstrate, and P. W. Dierkes, “Sodium-dependent potassium channels in leech P neurons,” Journal of Membrane Biology, vol. 208, no. 1, pp. 27–38, 2005. View at Publisher · View at Google Scholar · View at Scopus
  32. Y. Zhang, M. R. Brown, C. Hyland et al., “Regulation of neuronal excitability by interaction of fragile X mental retardation protein with Slack potassium channels,” The Journal of Neuroscience, vol. 32, pp. 15318–15327, 2012.
  33. C. Lawrence and G. C. Rodrigo, “A Na+-activated K+ current (IK,Na) is present in guinea-pig but not rat ventricular myocytes,” Pflugers Archiv, vol. 437, no. 6, pp. 831–838, 1999. View at Publisher · View at Google Scholar · View at Scopus
  34. M. Zhou, Z. Liu, C. Hu, Z. Zhang, and Y. Mei, “Developmental regulation of a Na+-activated fast outward K+ current in rat myoblasts,” Cellular Physiology and Biochemistry, vol. 14, no. 4–6, pp. 225–230, 2004. View at Publisher · View at Google Scholar · View at Scopus
  35. C. K. Young, H. S. Jae, M. K. Tong et al., “Sodium-activated potassium current in guinea pig gastric myocytes,” Journal of Korean Medical Science, vol. 22, no. 1, pp. 57–62, 2007. View at Scopus
  36. L. Re, V. Moretti, L. Rossini, and P. Giusti, “Sodium-activated potassium current in mouse diaphragm,” FEBS Letters, vol. 270, no. 1-2, pp. 195–197, 1990. View at Publisher · View at Google Scholar · View at Scopus
  37. Y. Zhang and W. G. Paterson, “Functional evidence for Na+-activated K+ channels in circular smooth muscle of the opossum lower esophageal sphincter,” American The Journal of Physiology, vol. 292, no. 6, pp. G1600–G1606, 2007. View at Publisher · View at Google Scholar · View at Scopus
  38. M. Paulais, S. Lachheb, and J. Teulon, “A Na+- and Cl-activated K+ channel in the thick ascending limb of mouse kidney,” Journal of General Physiology, vol. 127, no. 2, pp. 205–215, 2006. View at Publisher · View at Google Scholar · View at Scopus
  39. T. M. Egan, D. Dagan, J. Kupper, and I. B. Levitan, “Na+-activated K+ channels are widely distributed in rat CNS and in Xenopus oocytes,” Brain Research, vol. 584, no. 1-2, pp. 319–321, 1992. View at Publisher · View at Google Scholar · View at Scopus
  40. W. J. Joiner, M. D. Tang, L. Y. Wang et al., “Formation of intermediate-conductance calcium-activated potassium channels by interaction of Slack and Slo subunits,” Nature Neuroscience, vol. 1, no. 6, pp. 462–469, 1998. View at Scopus
  41. A. Yuan, C. M. Santi, A. Wei et al., “The sodium-activated potassium channel is encoded by a member of the Slo gene family,” Neuron, vol. 37, no. 5, pp. 765–773, 2003. View at Publisher · View at Google Scholar · View at Scopus
  42. Y. Jiang, A. Pico, M. Cadene, B. T. Chait, and R. MacKinnon, “Structure of the RCK domain from the E. coli K+ channel and demonstration of its presence in the human BK channel,” Neuron, vol. 29, no. 3, pp. 593–601, 2001. View at Publisher · View at Google Scholar · View at Scopus
  43. P. Yuan, M. D. Leonetti, A. R. Pico, Y. Hsiung, and R. MacKinnon, “Structure of the human BK channel Ca2+-activation apparatus at 3.0 Å resolution,” Science, vol. 329, no. 5988, pp. 182–186, 2010. View at Publisher · View at Google Scholar · View at Scopus
  44. Z. Zhang, A. Rosenhouse-Dantsker, Q. Y. Tang, S. Noskov, and D. E. Logothetis, “The RCK2 domain uses a coordination site present in Kir channels to confer sodium sensitivity to Slo2.2 channels,” The Journal of Neuroscience, vol. 30, no. 22, pp. 7554–7562, 2010. View at Publisher · View at Google Scholar · View at Scopus
  45. J. L. Sui, K. W. Chan, and D. E. Logothetis, “Na+ activation of the muscarinic K+ channel by a G-protein-independent mechanism,” Journal of General Physiology, vol. 108, no. 5, pp. 381–391, 1996. View at Publisher · View at Google Scholar · View at Scopus
  46. M. R. Brown, J. Kronengold, V. R. Gazula et al., “Amino-termini isoforms of the Slack K+ channel, regulated by alternative promoters, differentially modulate rhythmic firing and adaptation,” The Journal of Physiology, vol. 586, no. 21, pp. 5161–5179, 2008. View at Publisher · View at Google Scholar · View at Scopus
  47. A. Yuan, M. Dourado, A. Butler, N. Walton, A. Wei, and L. Salkoff, “SLO-2, a K+ channel with an unusual Cl dependence,” Nature Neuroscience, vol. 3, no. 8, pp. 771–779, 2000. View at Publisher · View at Google Scholar · View at Scopus
  48. M. Schreiber and L. Salkoff, “A novel calcium-sensing domain in the BK channel,” Biophysical Journal, vol. 73, no. 3, pp. 1355–1363, 1997. View at Scopus
  49. H. Chen, J. Kronengold, Y. Yan et al., “The N-terminal domain of slack determines the formation and trafficking of slick/slack heteromeric sodium-activated potassium channels,” The Journal of Neuroscience, vol. 29, no. 17, pp. 5654–5665, 2009. View at Publisher · View at Google Scholar · View at Scopus
  50. A. Bhattacharjee, L. Gan, and L. K. Kaczmarek, “Localization of the Slack potassium channel in the rat central nervous system,” Journal of Comparative Neurology, vol. 454, no. 3, pp. 241–254, 2002. View at Publisher · View at Google Scholar · View at Scopus
  51. A. Bhattacharjee, C. A. A. von Hehn, X. Mei, and L. K. Kaczmarek, “Localization of the Na+-activated K+ channel slick in the rat central nervous system,” Journal of Comparative Neurology, vol. 484, no. 1, pp. 80–92, 2005. View at Publisher · View at Google Scholar · View at Scopus
  52. D. S. Koh, P. Jonas, and W. Vogel, “Na+-activated K+ channels localized in the nodal region of myelinated axons of Xenopus,” The Journal of Physiology, vol. 479, no. 2, pp. 183–197, 1994. View at Scopus
  53. K. Mori, T. Saito, Y. Masuda, and H. Nakaya, “Effects of class III antiarrhythmic drugs on the Na+-activated K+ channels in guinea-pig ventricular cells,” British Journal of Pharmacology, vol. 119, no. 1, pp. 133–141, 1996. View at Scopus
  54. K. Mori, S. Kobayashi, T. Saito, Y. Masuda, and H. Nakaya, “Inhibitory effects of class I and IV antiarrhythmic drugs on the Na+- activated K+ channel current in guinea pig ventricular cells,” Naunyn-Schmiedeberg's Archives of Pharmacology, vol. 358, no. 6, pp. 641–648, 1998. View at Scopus
  55. Y. Li, T. Sato, and M. Arita, “Bepridil blunts the shortening of action potential duration caused by metabolic inhibition via blockade of ATP-sensitive K+ channels and Na+- activated K+ channels,” Journal of Pharmacology and Experimental Therapeutics, vol. 291, no. 2, pp. 562–568, 1999. View at Scopus
  56. B. Yang, V. K. Gribkoff, J. Pan et al., “Pharmacological activation and inhibition of Slack (Slo2. 2) channels,” Neuropharmacology, vol. 51, no. 4, pp. 896–906, 2006. View at Publisher · View at Google Scholar · View at Scopus
  57. M. D. Tejada, K. Stolpe, A. K. Meinild, and D. A. Klaerke, “Clofilium inhibits Slick and Slack potassium channels,” Biologics, vol. 6, pp. 465–470, 2012.
  58. B. Yang, R. Desai, and L. K. Kaczmarek, “Slack and slick KNa channels regulate the accuracy of timing of auditory neurons,” The Journal of Neuroscience, vol. 27, no. 10, pp. 2617–2627, 2007. View at Publisher · View at Google Scholar · View at Scopus
  59. B. Biton, S. Sethuramanujam, K. E. Picchione et al., “The antipsychotic drug loxapine is an opener of the sodium-activated potassium channel slack (Slo2. 2),” The Journal of Pharmacology and Experimental Therapeutics, vol. 340, pp. 706–715, 2012.
  60. C. M. Santi, G. Ferreira, B. Yang et al., “Opposite regulation of Slick and Slack K+ channels by neuromodulators,” The Journal of Neuroscience, vol. 26, no. 19, pp. 5059–5068, 2006. View at Publisher · View at Google Scholar · View at Scopus
  61. M. R. Fleming and L. K. Kaczmarek, “Use of optical biosensors to detect modulation of Slack potassium channels by G protein-coupled receptors,” Journal of Receptors and Signal Transduction, vol. 29, no. 3-4, pp. 173–181, 2009. View at Publisher · View at Google Scholar · View at Scopus
  62. M. D. Tejada, L. J. Jensen, and D. A. Klaerke, “PIP(2) modulation of Slick and Slack K(+) channels,” Biochemical and Biophysical Research Communications, vol. 424, pp. 208–213, 2012.
  63. L. Zhang, M. Sukhareva, J. L. Barker et al., “Direct binding of estradiol enhances Slack (sequence like a calcium-activated potassium channel) channels' activity,” Neuroscience, vol. 131, no. 2, pp. 275–282, 2005. View at Publisher · View at Google Scholar · View at Scopus
  64. V. A. Ruffin, X. Q. Gu, D. Zhou et al., “The sodium-activated potassium channel Slack is modulated by hypercapnia and acidosis,” Neuroscience, vol. 151, no. 2, pp. 410–418, 2008. View at Publisher · View at Google Scholar · View at Scopus
  65. M. O. Nuwer, K. E. Picchione, and A. Bhattacharjee, “cAMP-dependent kinase does not modulate the Slack sodium-activated potassium channel,” Neuropharmacology, vol. 57, no. 3, pp. 219–226, 2009. View at Publisher · View at Google Scholar · View at Scopus
  66. B. C. Suh and B. Hille, “Regulation of ion channels by phosphatidylinositol 4,5-bisphosphate,” Current Opinion in Neurobiology, vol. 15, no. 3, pp. 370–378, 2005. View at Publisher · View at Google Scholar · View at Scopus
  67. L. K. Kaczmarek, “Non-conducting functions of voltage-gated ion channels,” Nature Reviews Neuroscience, vol. 7, no. 10, pp. 761–771, 2006. View at Publisher · View at Google Scholar · View at Scopus
  68. C. R. Rose, “Na+ signals at central synapses,” Neuroscientist, vol. 8, no. 6, pp. 532–539, 2002. View at Publisher · View at Google Scholar · View at Scopus
  69. C. R. Rose and B. R. Ransom, “Regulation of intracellular sodium in cultured rat hippocampal neurones,” The Journal of Physiology, vol. 499, part 3, pp. 573–587, 1997. View at Scopus
  70. C. R. Rose and A. Konnerth, “Nmda receptor-mediated Na+ signals in spines and dendrites,” The Journal of Neuroscience, vol. 21, no. 12, pp. 4207–4214, 2001. View at Scopus
  71. N. Zhong, V. Beaumont, and R. S. Zucker, “Roles for mitochondrial and reverse mode Na+/Ca2+ exchange and the plasmalemma Ca2+ ATPase in post-tetanic potentiation at crayfish neuromuscular junctions,” The Journal of Neuroscience, vol. 21, no. 24, pp. 9598–9607, 2001. View at Scopus
  72. G. Budelli, T. A. Hage, A. Wei et al., “Na+-activated K+ channels express a large delayed outward current in neurons during normal physiology,” Nature Neuroscience, vol. 12, no. 6, pp. 745–750, 2009. View at Publisher · View at Google Scholar · View at Scopus
  73. T. A. Hage and L. Salkoff, “Sodium-activated potassium channels are functionally coupled to persistent sodium currents,” The Journal of Neuroscience, vol. 32, pp. 2714–2721, 2012.
  74. M. R. Markham, L. K. Kaczmarek, and H. H. Zakon, “A sodium-activated potassium channe supports high frequency firing and reduces energetic costs during rapid modulations of action potential amplitude,” Journal of Neurophysiology, vol. 109, no. 7, pp. 1713–1723, 2013.
  75. S. Uchino, H. Wada, S. Honda et al., “Slo2 sodium-activated K+ channels bind to the PDZ domain of PSD-95,” Biochemical and Biophysical Research Communications, vol. 310, no. 4, pp. 1140–1147, 2003. View at Publisher · View at Google Scholar · View at Scopus
  76. T. Zamalloa, C. P. Bailey, and J. Pineda, “Glutamate-induced post-activation inhibition of locus coeruleus neurons is mediated by AMPA/kainate receptors and sodium-dependent potassium currents,” British Journal of Pharmacology, vol. 156, no. 4, pp. 649–661, 2009. View at Publisher · View at Google Scholar · View at Scopus
  77. S. Lu, P. Das, D. A. Fadool, and L. K. Kaczmarek, “The slack sodium-activated potassium channel provides a major outward current in olfactory neurons of Kv1.3-/- super-smeller mice,” Journal of Neurophysiology, vol. 103, no. 6, pp. 3311–3319, 2010. View at Publisher · View at Google Scholar · View at Scopus
  78. R. C. Foehring, P. C. Schwindt, and W. E. Crill, “Norepinephrine selectively reduces slow Ca2+- and Na+-mediated K+ currents in cat neocortical neurons,” Journal of Neurophysiology, vol. 61, no. 2, pp. 245–256, 1989. View at Scopus
  79. M. Kubota and N. Saito, “Sodium- and calcium-dependent conductances of neurones in the zebra finch hyperstriatum ventrale pars caudale in vitro,” The Journal of Physiology, vol. 440, pp. 131–142, 1991. View at Scopus
  80. U. Kim and D. A. Mccormick, “Functional and ionic properties of a slow afterhyperpolarization in ferret perigeniculate neurons in vitro,” Journal of Neurophysiology, vol. 80, no. 3, pp. 1222–1235, 1998. View at Scopus
  81. V. M. Sandler, E. Puil, and D. W. F. Schwarz, “Intrinsic response properties of bursting neurons in the nucleus principalis trigemini of the gerbil,” Neuroscience, vol. 83, no. 3, pp. 891–904, 1998. View at Publisher · View at Google Scholar · View at Scopus
  82. M. V. Sanchez-Vives, L. G. Nowak, and D. A. McCormick, “Cellular mechanisms of long-lasting adaptation in visual cortical neurons in vitro,” The Journal of Neuroscience, vol. 20, no. 11, pp. 4286–4299, 2000. View at Scopus
  83. S. Franceschetti, T. Lavazza, G. Curia et al., “Na+-activated K+ current contributes to postexcitatory hyperpolarization in neocortical intrinsically bursting neurons,” Journal of Neurophysiology, vol. 89, no. 4, pp. 2101–2111, 2003. View at Publisher · View at Google Scholar · View at Scopus
  84. V. F. Descalzo, L. G. Nowak, J. C. Brumberg, D. A. McCormick, and M. V. Sanchez-Vives, “Slow adaptation in fast-spiking neurons of visual cortex,” Journal of Neurophysiology, vol. 93, no. 2, pp. 1111–1118, 2005. View at Publisher · View at Google Scholar · View at Scopus
  85. J. Benda, L. Maler, and A. Longtin, “Linear versus nonlinear signal transmission in neuron models with adaptation currents or dynamic thresholds,” Journal of Neurophysiology, vol. 104, no. 5, pp. 2806–2820, 2010. View at Publisher · View at Google Scholar · View at Scopus
  86. X. Liu and L. S. Leung, “Sodium-activated potassium conductance participates in the depolarizing afterpotential following a single action potential in rat hippocampal CA1 pyramidal cells,” Brain Research, vol. 1023, no. 2, pp. 185–192, 2004. View at Publisher · View at Google Scholar · View at Scopus
  87. L. Cangiano, P. Wallén, and S. Grillner, “Role of apamin-sensitive KCa channels for reticulospinal synaptic transmission to motoneuron and for the afterhyperpolarization,” Journal of Neurophysiology, vol. 88, no. 1, pp. 289–299, 2002. View at Scopus
  88. Q. Y. Liu, A. E. Schaffner, and J. L. Barker, “Kainate induces an intracellular Na+-activated K+ current in cultured embryonic rat hippocampal neurones,” The Journal of Physiology, vol. 510, part 3, pp. 721–734, 1998. View at Scopus
  89. I. Rishal, T. Keren-Raifman, D. Yakubovich et al., “Na+ promotes the dissociation between GαGDP and Gβγ, activating G protein-gated K+ channels,” The Journal of Biological Chemistry, vol. 278, no. 6, pp. 3840–3845, 2003. View at Publisher · View at Google Scholar · View at Scopus