Advertisement

Functions and Modulation of Neuronal SK Channels

  • E. S. Louise FaberEmail author
Review Article

Abstract

Small conductance (SK) channels are calcium-activated potassium channels that, when cloned in 1996, were thought solely to contribute to the afterhyperpolarisation that follows action potentials, and to control repetitive firing patterns of neurons. However, discoveries over the past few years have identified novel roles for SK channels in controlling dendritic excitability, synaptic transmission and synaptic plasticity. More recently, modulation of SK channel calcium sensitivity by casein kinase 2, and of SK channel trafficking by protein kinase A, have been demonstrated. This article will discuss recent findings regarding the function and modulation of SK channels in central neurons.

Keywords

Calcium-activated potassium channels Synaptic transmission Synaptic plasticity Afterhyperpolarisation Dendritic integration Learning and memory Hippocampus Amygdala Midbrain dopaminergic neurons 

References

  1. 1.
    Kohler, M., Hirschberg, B., Bond, C. T., et al. (1996). Small-conductance, calcium-activated potassium channels from mammalian brain. Science, 273, 1709–1714.PubMedCrossRefGoogle Scholar
  2. 2.
    Blatz, A. L., & Magleby, K. L. (1986). Single apamin-blocked Ca2+-activated K+ channels of small conductance in cultured rat skeletal muscle. Nature, 323, 718–720.PubMedCrossRefGoogle Scholar
  3. 3.
    Park, Y.-B. (1994). Ion selectivity and gating of small conductance Ca2+-activated K+ channels in cultured rat adrenal chromaffin cells. Journal of Physiology, 481, 555–570.PubMedGoogle Scholar
  4. 4.
    Hirschberg, B., Maylie, J., Adelman, J. P., & Marrion, N. V. (1998). Gating of recombinant small-conductance Ca2+-activated K+ channels by calcium. Journal of General Physiology, 111, 565–581.PubMedCrossRefGoogle Scholar
  5. 5.
    Xia, X.-M., Falker, B., Rivard, A., et al. (1998). Mechanism of calcium gating in small-conductance calcium-activated potassium channels. Nature, 395, 503–507.PubMedCrossRefGoogle Scholar
  6. 6.
    Schumacher, M. A., Rivard, A. F., Bachinger, H. P., & Adelman, J. P. (2001). Structure of the gating domain of a Ca2+-activated K+ channel complexed with Ca2+/calmodulin. Nature, 410, 1120–1124.PubMedCrossRefGoogle Scholar
  7. 7.
    Keen, J. E., Khawaled, R., Farrens, D. L., et al. (1999). Domains responsible for constitutive and Ca2+-dependent interactions between calmodulin and small conductance Ca2+-activated potassium channels. Journal of Neuroscience, 19, 8830–8838.PubMedGoogle Scholar
  8. 8.
    Soh, H., & Park, C. S. (2001). Inwardly rectifying current-voltage relationship of small-conductance Ca2+-activated K+ channels rendered by intracellular divalent cation blockade. Biophysical Journal, 80, 2207–2215.PubMedCrossRefGoogle Scholar
  9. 9.
    Soh, H., & Park, C. S. (2002). Localization of divalent cation-binding site in the pore of a small conductance Ca2+-activated K+ channel and its role in determining current-voltage relationship. Biophysical Journal, 83, 2528–2538.PubMedCrossRefGoogle Scholar
  10. 10.
    Shmukler, B. E., Bond, C. T., Wilhelm, S., et al. (2001). Structure and complex transcription pattern of the mouse SK1 KCa channel gene, KCNN1. Biochimica et Biophysica Acta, 1518, 36–46.PubMedGoogle Scholar
  11. 11.
    Strassmaier, T., Bond, C. T., Sailer, C. A., Knaus, H. G., Maylie, J., & Adelman, J. P. (2005). A novel isoform of SK2 assembles with other SK subunits in mouse brain. Journal of Biological Chemistry, 280, 21231–21236.PubMedCrossRefGoogle Scholar
  12. 12.
    Murthy, S. R., Teodorescu, G., Nijholt, I. M., et al. (2008). Identification and characterization of a novel, shorter isoform of the small conductance Ca2+-activated K+ channel SK2. Journal of Neurochemistry, 106, 2312–2321.PubMedCrossRefGoogle Scholar
  13. 13.
    Tomita, H., Shakkottai, V. G., Gutman, G. A., et al. (2003). Novel truncated isoform of SK3 potassium channel is a potent dominant-negative regulator of SK currents: implications in schizophrenia. Molecular Psychiatry, 8, 524–535, 460.Google Scholar
  14. 14.
    Wittekindt, O. H., Visan, V., Tomita, H., et al. (2004). An apamin- and scyllatoxin-insensitive isoform of the human SK3 channel. Molecular Pharmacology, 65, 788–801.PubMedCrossRefGoogle Scholar
  15. 15.
    Wittekindt, O. H., Dreker, T., Morris-Rosendahl, D. J., Lehmann-Horn, F., & Grissmer, S. (2004). A novel non-neuronal hSK3 isoform with a dominant-negative effect on hSK3 currents. Cellular Physiology and Biochemistry, 14, 23–30.PubMedCrossRefGoogle Scholar
  16. 16.
    Kolski-Andreaco, A., Tomita, H., Shakkottai, V. G., et al. (2004). SK3-1C, a dominant-negative suppressor of SKCa and IKCa channels. Journal of Biological Chemistry, 279, 6893–6904.PubMedCrossRefGoogle Scholar
  17. 17.
    Benton, D. C., Monaghan, A. S., Hosseini, R., Bahia, P. K., Haylett, D. G., & Moss, G. W. (2003). Small conductance Ca2+-activated K+ channels formed by the expression of rat SK1 and SK2 genes in HEK 293 cells. Journal of Physiology, 553, 13–19.PubMedCrossRefGoogle Scholar
  18. 18.
    D’Hoedt, D., Hirzel, K., Pedarzani, P., & Stocker, M. (2004). Domain analysis of the calcium-activated potassium channel SK1 from rat brain. Functional expression and toxin sensitivity. Journal of Biological Chemistry, 279, 12088–12092.PubMedCrossRefGoogle Scholar
  19. 19.
    Monaghan, A. S., Benton, D. C., Bahia, P. K., et al. (2004). The SK3 subunit of small conductance Ca2+-activated K+ channels interacts with both SK1 and SK2 subunits in a heterologous expression system. Journal of Biological Chemistry, 279, 1003–1009.PubMedCrossRefGoogle Scholar
  20. 20.
    Pedarzani, P., Kulik, A., Muller, M., Ballanyi, K., & Stocker, M. (2000). Molecular determinants of Ca2+-dependent K+ channel function in rat dorsal vagal neurones. Journal of Physiology, 27(Pt 2), 283–290.CrossRefGoogle Scholar
  21. 21.
    Stocker, M., & Pedarzani, P. (2000). Differential distribution of three Ca2+-activated K+ channel subunits, SK1, SK2, and SK3, in the adult rat central nervous system. Molecular and Cellular Neurosciences, 15, 476–493.PubMedCrossRefGoogle Scholar
  22. 22.
    Wolfart, J., Neuhoff, H., & Franz, O. J. R. (2001). Differential expression of the small-conductance, calcium-activated potassium channel SK3 is critical for pacemaker control in dopaminergic midbrain neurons. The Journal of Neuroscience, 21, 3443–3456.Google Scholar
  23. 23.
    Sailer, C. A., Hu, H., Kaufmann, W. A., et al. (2002). Regional differences in distribution and functional expression of small-conductance Ca2+-activated K+ channels in rat brain. Journal of Neuroscience, 22, 9698–9707.PubMedGoogle Scholar
  24. 24.
    Sailer, C. A., Kaufmann, W. A., Marksteiner, J., & Knaus, H. G. (2004). Comparative immunohistochemical distribution of three small-conductance Ca2+-activated potassium channel subunits, SK1, SK2, and SK3 in mouse brain. Molecular and Cellular Neurosciences, 26, 458–469.PubMedCrossRefGoogle Scholar
  25. 25.
    Burgess, G. M., Claret, M., & Jenkinson, D. H. (1981). Effects of quinine and apamin on the calcium-dependent potassium permeability of mammalian hepatocytes and red cells. Journal of Physiology, 317, 67–90.PubMedGoogle Scholar
  26. 26.
    Romey, G., Hugues, M., Schmid-Antomarchi, H., & Lazdunski, M. (1984). Apamin: a specific toxin to study a class of Ca2+-dependent K+ channels. Journal of Physiology, 79, 259–264.Google Scholar
  27. 27.
    Johnson, S. W., & Seutin, V. (1997). Bicuculline methiodide potentiates NMDA-dependent burst firing in rat dopamine neurons by blocking apamin-sensitive Ca2+-activated K+ currents. Neuroscience Letters, 231, 13–16.PubMedCrossRefGoogle Scholar
  28. 28.
    Seutin, V., & Johnson, S. W. (1999). Recent advances in the pharmacology of quaternary salts of bicuculline. TIPS, 20, 268–270.PubMedGoogle Scholar
  29. 29.
    Castle, N. A., & Strong, P. N. (1986). Identification of two toxins from scorpion (Leiurus quinquestriatus) venom which block distinct classes of calcium-activated potassium channel. FEBS Letters, 209, 117–121.PubMedCrossRefGoogle Scholar
  30. 30.
    Chicchi, G. G., Gimenez-Gallego, G., Ber, E., Garcia, M. L., Winquist, R., & Cascieri, M. A. (1988). Purification and characterization of a unique, potent inhibitor of apamin binding from Leiurus quinquestriatus hebraeus venom. Journal of Biological Chemistry, 263, 10192–10197.PubMedGoogle Scholar
  31. 31.
    Auguste, P., Hugues, M., Grave, B., et al. (1990). Leiurotoxin I (scyllatoxin), a peptide ligand for Ca2+-activated K+ channels. Chemical synthesis, radiolabeling, and receptor characterization. Journal of Biological Chemistry, 265, 4753–4759.PubMedGoogle Scholar
  32. 32.
    Strobaek, D., Hougaard, C., Johansen, T. H., et al. (2006). Inhibitory gating modulation of small conductance Ca2+-activated K+ channels by the synthetic compound (R)-N-(benzimidazol-2-yl)-1, 2, 3, 4-tetrahydro-1-naphtylamine (NS8593) reduces afterhyperpolarizing current in hippocampal CA1 neurons. Molecular Pharmacology, 70, 1771–1782.PubMedCrossRefGoogle Scholar
  33. 33.
    Dunn, P. M. (1994). Dequalinium, a selective blocker of the slow afterhyperpolarization in rat sympathetic neurones in culture. European Journal of Pharmacology, 252, 189–194.PubMedCrossRefGoogle Scholar
  34. 34.
    Campos Rosa, J., Galanakis, D., Piergentili, A., et al. (2000). Synthesis, molecular modeling, and pharmacological testing of bis-quinolinium cyclophanes: potent, non-peptidic blockers of the apamin-sensitive Ca2+-activated K+ channel. Journal of Medicinal Chemistry, 43, 420–431.PubMedCrossRefGoogle Scholar
  35. 35.
    Chen, J.-Q., Galanakis, D., Ganellin, C. R., Dunn, P. M., & Jenkinson, D. H. (2000). bis-quinolinium cyclophanes: 8, 14-diaza-1, 7(1, 4)-diquinolinacyclotetradecaphane (UCL 1848), a highly potent and selective, nonpeptidic blocker of the apamin-sensitive Ca2+-activated K+ channel. Journal of Medicinal Chemistry, 43, 3478–3481.PubMedCrossRefGoogle Scholar
  36. 36.
    Liégeois, J. F., Mercier, F., Graulich, A., Graulich-Lorge, F., Scuvée-Moreau, J., & Seutin, V. (2003). Modulation of small conductance calcium-activated potassium (SK) channels: a new challenge in medicinal chemistry. Current Medicinal Chemistry, 10, 625–647.PubMedCrossRefGoogle Scholar
  37. 37.
    Wulff, H., Kolski-Andreaco, A., Sankaranarayanan, A., Sabatier, J. M., & Shakkottai, V. (2007). Modulators of small- and intermediate-conductance calcium-activated potassium channels and their therapeutic indications. Current Medicinal Chemistry, 14, 1437–1457.PubMedCrossRefGoogle Scholar
  38. 38.
    Faber, E. S. L., & Sah, P. (2007). Functions of SK channels in central neurons. CEPP, 34, 1077–1083.PubMedGoogle Scholar
  39. 39.
    Pedarzani, P., & Stocker, M. (2008). Molecular and cellular basis of small- and intermediate-conductance, calcium-activated potassium channel function in the brain. Cellular and Molecular Life Sciences, 65, 3196–3217.PubMedCrossRefGoogle Scholar
  40. 40.
    Scuvée-Moreau, J., Boland, A., Graulich, A., et al. (2004). Electrophysiological characterization of the SK channel blockers methyl-laudanosine and methyl-noscapine in cell lines and rat brain slices. British Journal of Clinical Pharmacology, 143, 753–764.Google Scholar
  41. 41.
    Graulich, A., Mercier, F., Scuvée-Moreau, J., Seutin, V., & Liégeois, J. F. (2005). Synthesis and biological evaluation of N-methyl-laudanosine iodide analogues as potential SK channel blockers. Bioorganic & Medicinal Chemistry, 13, 1201–1209.CrossRefGoogle Scholar
  42. 42.
    Graulich, A., Dilly, S., Farce, A., et al. (2007). Synthesis and radioligand binding studies of bis-isoquinolinium derivatives as small conductance Ca2+-activated K+ channel blockers. Journal of Medicinal Chemistry, 50, 5070–5075.PubMedCrossRefGoogle Scholar
  43. 43.
    Graulich, A., Lamy, C., Alleva, L., et al. (2008). Bis-tetrahydroisoquinoline derivatives: AG525E1, a new step in the search for non-quaternary non-peptidic small conductance Ca2+-activated K+ channel blockers. Bioorganic & Medicinal Chemistry Letters, 18, 3440–3445.CrossRefGoogle Scholar
  44. 44.
    Pedarzani, P., D’Hoedt, D., Doorty, K. B., et al. (2002). Tamapin, a venom peptide from the Indian red scorpion (Mesobuthus tamulus) that targets small conductance Ca2+-activated K+ channels and afterhyperpolarization currents in central neurons. Journal of Biological Chemistry, 277, 46101–46109.PubMedCrossRefGoogle Scholar
  45. 45.
    Shakkottai, V. G., Regaya, I., Wulff, H., et al. (2001). Design and characterization of a highly selective peptide inhibitor of the small conductance calcium-activated K+ channel, SKCa2. Journal of Biological Chemistry, 276, 43145–43151.PubMedCrossRefGoogle Scholar
  46. 46.
    Olesen, S. P., Munch, E., Moldt, P., & Drejer, J. (1994). Selective activation of Ca2+-dependent K+ channels by novel benzimidazolone. European Journal of Pharmacology, 251, 53–59.PubMedCrossRefGoogle Scholar
  47. 47.
    Pedarzani, P., Mosbacher, J., Rivard, A., et al. (2001). Control of electrical activity in central neurons by modulating the gating of small conductance Ca2+-activated K+ channels. Journal of Biological Chemistry, 276, 9762–9769.PubMedCrossRefGoogle Scholar
  48. 48.
    Pedarzani, P., McCutcheon, J. E., Rogge, G., et al. (2005). Specific enhancement of SK channel activity selectively potentiates the afterhyperpolarizing current IAHP and modulates the firing properties of hippocampal pyramidal neurons. Journal of Biological Chemistry, 280, 41404–41411.PubMedCrossRefGoogle Scholar
  49. 49.
    Schwartzkroin, P. A., & Stafstrom, C. E. (1980). Effects of EGTA on the calcium-activated afterhyperpolarization in hippocampal CA3 pyramidal cells. Science, 210, 1125–1126.PubMedCrossRefGoogle Scholar
  50. 50.
    Sah, P. (1996). Ca2+-activated K+ currents in neurones: types, physiological roles and modulation. TINS, 19, 150–154.PubMedGoogle Scholar
  51. 51.
    Ishii, T. M., Maylie, J., & Adelman, J. P. (1997). Determinants of apamin and d-tubocurarine block in SK potassium channels. Journal of Biological Chemistry, 272, 23195–23200.PubMedCrossRefGoogle Scholar
  52. 52.
    Shah, M., & Haylett, D. G. (2000). The pharmacology of hSK1 Ca2+-activated K+ channels expressed in mammalian cell lines. British Journal of Pharmacology, 129, 627–630.PubMedCrossRefGoogle Scholar
  53. 53.
    Strobaek, D., Jorgensen, T. D., Christophersen, P., Ahring, P. K., & Olesen, O. (2000). Pharmacological characterization of small-conductance Ca2+-activated K+ channels stably expressed in HEK 293 cells. British Journal of Pharmacology, 129, 991–999.Google Scholar
  54. 54.
    Nolting, A., Ferraro, T., D’Hoedt, D., & Stocker, M. (2007). An amino acid outside the pore region influences apamin sensitivity in small conductance Ca2+-activated K+ channels. Journal of Biological Chemistry, 282, 3478–3486.PubMedCrossRefGoogle Scholar
  55. 55.
    Sah, P., & Faber, E. S. L. (2002). Channels underlying neuronal calcium-activated potassium currents. Progress in Neurobiology, 66, 345–353.PubMedCrossRefGoogle Scholar
  56. 56.
    Faber, E. S. L., & Sah, P. (2003). Calcium-activated potassium channels: multiple contributions to neuronal function. Neuroscientist, 9, 181–194.PubMedCrossRefGoogle Scholar
  57. 57.
    Lancaster, B., & Adams, P. R. (1986). Calcium-dependent current generating the afterhyperpolarization of hippocampal neurons. Journal of Neurophysiology, 55, 1268–1282.PubMedGoogle Scholar
  58. 58.
    Storm, J. F. (1987). Action potential repolarization and a fast after-hyperpolarization in rat hippocampal pyramidal cells. Journal of Physiology, 385, 733–759.PubMedGoogle Scholar
  59. 59.
    Adams, P. R., Constanti, A., Brown, D. A., & Clark, R. B. (1982). Intracellular Ca2+ activates a fast voltage-sensitive K+ current in vertebtrate sensory neurones. Nature, 296, 746–749.PubMedCrossRefGoogle Scholar
  60. 60.
    Lancaster, B., & Nicoll, R. A. (1987). Properties of two calcium-activated hyperpolarizations in rat hippocampal neurones. Journal of Physiology, 389, 187–204.PubMedGoogle Scholar
  61. 61.
    Sah, P. (1992). The role of calcium influx and calcium buffering in the kinetics of a Ca2+ activated K+ current in rat vagal motoneurons. Journal of Neurophysiology, 68, 2237–2248.PubMedGoogle Scholar
  62. 62.
    Faber, E. S. L., & Sah, P. (2002). Physiological role of calcium-activated potassium currents in the rat lateral amygdala. Journal of Neuroscience, 22, 1618–1628.PubMedGoogle Scholar
  63. 63.
    Schwindt, P. C., Spain, W. J., Foehring, R. C., Stafstrom, C. E., Chubb, M. C., & Crill, W. E. (1988). Multiple potassium conductances and their functions in neurons from cat sensorimotor cortex in vitro. Journal of Neurophysiology, 59, 424–449.PubMedGoogle Scholar
  64. 64.
    Sah, P., & McLachlan, E. M. (1991). Ca2+ activated K+ currents underlying the afterhyperpolarization in guinea pig vagal neurons: a role for Ca2+ activated Ca2+ release. Neuron, 7, 257–264.PubMedCrossRefGoogle Scholar
  65. 65.
    Sah, P., & McLachlan, E. M. (1992). Potassium currents contributing to action potential repolarization and the afterhyperpolarization in rat vagal motoneurons. Journal of Neurophysiology, 68, 1834–1841.PubMedGoogle Scholar
  66. 66.
    Pennefather, P., Lancaster, B., Adams, P. R., & Nicoll, R. A. (1985). Two distinct Ca-dependent K currents in bullfrog sympathetic ganglionic cells. PNAS USA, 82, 3040–3044.PubMedCrossRefGoogle Scholar
  67. 67.
    Power, J. M., & Sah, P. (2008). Competition between calcium-activated K+ channels determines cholinergic action on firing properties of basolateral amygdala projection neurons. Journal of Neuroscience, 28, 3209–3220.PubMedCrossRefGoogle Scholar
  68. 68.
    Hallworth, N. E., Wilson, C. J., & Bevan, M. D. (2003). Apamin-sensitive small conductance calcium-activated potassium channels, through their selective coupling to voltage-gated calcium channels, are critical determinants of the precision, pace, and pattern of action potential generation in rat subthalamic nucleus neurons in vitro. Journal of Neuroscience, 23, 7525–7542.PubMedGoogle Scholar
  69. 69.
    Cingolani, L. A., Gymnopoulos, M., Boccaccio, A., Stocker, M., & Pedarzani, P. (2002). Developmental regulation of small-conductance Ca2+-activated K+ channel expression and function in rat Purkinje neurons. Journal of Neuroscience, 22, 4456–4467.PubMedGoogle Scholar
  70. 70.
    Womack, M. D., & Khodakhah, K. (2003). Somatic and dendritic small-conductance calcium-activated potassium channels regulate the output of cerebellar purkinje neurons. Journal of Neuroscience, 23, 2600–2607.PubMedGoogle Scholar
  71. 71.
    Shakkottai, V. G., Chou, C. H., Oddo, S., et al. (2004). Enhanced neuronal excitability in the absence of neurodegeneration induces cerebellar ataxia. Journal of Clinical Investigation, 113, 582–590.PubMedGoogle Scholar
  72. 72.
    Maher, B. J., & Westbrook, G. L. (2005). SK channel regulation of dendritic excitability and dendrodendritic inhibition in the olfactory bulb. Journal of Neurophysiology, 94, 3743–3750.PubMedCrossRefGoogle Scholar
  73. 73.
    Kasten, M. R., Rudy, B., & Anderson, M. P. (2007). Differential regulation of action potential firing in adult murine thalamocortical neurons by Kv3.2, Kv1, and SK potassium and N-type calcium channels. Journal of Physiology, 584, 565–582.PubMedCrossRefGoogle Scholar
  74. 74.
    Zavala-Tecuapetla, C., Aguileta, M. A., Lopez-Guerrero, J. J., Gonzalez-Marin, M. C., & Pena, F. (2008). Calcium-activated potassium currents differentially modulate respiratory rhythm generation. European Journal of Neuroscience, 27, 2871–2884.PubMedCrossRefGoogle Scholar
  75. 75.
    Deister, C. A., Chan, C. S., Surmeier, D. J., & Wilson, C. J. (2009). Calcium-activated SK channels influence voltage-gated ion channels to determine the precision of firing in globus pallidus neurons. Journal of Neuroscience, 29, 8452–8461.PubMedCrossRefGoogle Scholar
  76. 76.
    Storm, J. F. (1989). An after-hyperpolarization of medium duration in rat hippocampal pyramidal cells. Journal of Physiology, 409, 171–190.PubMedGoogle Scholar
  77. 77.
    Williamson, A., & Alger, B. E. (1990). Characterization of an early afterhyperpolarization after a brief train of action potentials in rat hippocampal neurons in vitro. Journal of Neurophysiology, 63, 72–81.PubMedGoogle Scholar
  78. 78.
    Stocker, M., Krause, M., & Pedarzani, P. (1999). An apamin-sensitive Ca2+-activated K+ current in hippocampal pyramidal neurons. PNAS, USA, 96, 4662–4667.CrossRefGoogle Scholar
  79. 79.
    Stackman, R. W., Hammond, R. S., Linardatos, E., et al. (2002). Small conductance Ca2+-activated K+ channels modulate synaptic plasticity and memory encoding. Journal of Neuroscience, 22, 10163–10171.PubMedGoogle Scholar
  80. 80.
    Bond, C. T., Herson, P. S., Strassmaier, T., et al. (2004). Small conductance Ca2+-activated K+ channel knock-out mice reveal the identity of calcium-dependent afterhyperpolarization currents. Journal of Neuroscience, 24, 5301–5306.PubMedCrossRefGoogle Scholar
  81. 81.
    Gu, N., Vervaeke, K., Hu, H., & Storm, J. F. (2005). Kv7/KCNQ/M and HCN/h, but not KCa2/SK channels, contribute to the somatic medium after-hyperpolarization and excitability control in CA1 hippocampal pyramidal cells. Journal of Physiology, 566, 689–715.PubMedCrossRefGoogle Scholar
  82. 82.
    Lin, M. T., Lujan, R., Watanabe, M., Adelman, J. P., & Maylie, J. (2008). SK2 channel plasticity contributes to LTP at Schaffer collateral-CA1 synapses. Nature Neuroscience, 11, 170–177.PubMedCrossRefGoogle Scholar
  83. 83.
    Faber, E. S. L., Delaney, A. J., Power, J. M., Sedlak, P. L., Crane, J. W., & Sah, P. (2008). Modulation of SK channel trafficking by beta adrenoceptors enhances excitatory synaptic transmission and plasticity in the amygdala. Journal of Neuroscience, 28, 10803–10813.PubMedCrossRefGoogle Scholar
  84. 84.
    Gu, N., Hu, H., Vervaeke, K., & Storm, J. F. (2008). SK (KCa2) channels do not control somatic excitability in CA1 pyramidal neurons but can be activated by dendritic excitatory synapses and regulate their impact. Journal of Neurophysiology, 100, 2589–2604.PubMedCrossRefGoogle Scholar
  85. 85.
    Peters, H. C., Hu, H., Pongs, O., Storm, J. F., & Isbrandt, D. (2005). Conditional transgenic suppression of M channels in mouse brain reveals functions in neuronal excitability, resonance and behavior. Nature Neuroscience, 8, 51–60.PubMedCrossRefGoogle Scholar
  86. 86.
    Tzingounis, A. V., & Nicoll, R. A. (2008). Contribution of KCNQ2 and KCNQ3 to the medium and slow afterhyperpolarization currents. PNAS USA, 105, 19974–19979.PubMedCrossRefGoogle Scholar
  87. 87.
    Villalobos, C., Shakkottai, V. G., Chandy, K. G., Michelhaugh, S. K., & Andrade, R. (2004). SKCa channels mediate the medium but not the slow calcium-activated afterhyperpolarization in cortical neurons. Journal of Neuroscience, 24, 3537–3542.PubMedCrossRefGoogle Scholar
  88. 88.
    Kato, M., Tanaka, N., Usui, S., & Sakuma, Y. (2006). The SK channel blocker apamin inhibits slow afterhyperpolarization currents in rat gonadotropin-releasing hormone neurones. Journal of Physiology, 574, 431–442.PubMedCrossRefGoogle Scholar
  89. 89.
    Paterlini, M., Revilla, V., Grant, A. L., & Wisden, W. (2000). Expression of the neuronal calcium sensor protein family in the rat brain. Neuroscience, 99, 205–216.PubMedCrossRefGoogle Scholar
  90. 90.
    Tzingounis, A. V., Kobayashi, M., Takamatsu, K., & Nicoll, R. A. (2007). Hippocalcin gates the calcium activation of the slow afterhyperpolarization in hippocampal pyramidal cells. Neuron, 53, 487–493.PubMedCrossRefGoogle Scholar
  91. 91.
    Lang, E. J., Sugihara, I., & Llinas, R. (1997). Differential roles of apamin- and charybdotoxin-sensitive K+ conductances in the generation of inferior olive rhythmicity in vivo. Journal of Neuroscience, 17, 2825–2838.PubMedGoogle Scholar
  92. 92.
    Bal, T., & McCormick, D. A. (1997). Synchronized oscillations in the inferior olive are controlled by the hyperpolarization-activated cation current Ih. Journal of Neurophysiology, 77, 3145–3156.PubMedGoogle Scholar
  93. 93.
    de Waele, C., Serafin, M., Khateb, A., Yabe, T., Vidal, P. P., & Muhlethaler, M. (1993). Medial vestibular nucleus in the guinea-pig: apamin-induced rhythmic burst firing - an in vitro and in vivo study. Experimental Brain Research, 95, 213–222.CrossRefGoogle Scholar
  94. 94.
    Zhang, L., & Krnjevic, K. (1987). Apamin depresses selectively the after-hyperpolarization of cat spinal motoneurons. Neuroscience Letters, 74, 58–62.PubMedCrossRefGoogle Scholar
  95. 95.
    Viana, F., Bayliss, D. A., & Berger, A. J. (1993). Multiple potassium conductances and their role in action potential repolarization and repetitive firing behavior of neonatal rat hypoglossal motoneurons. Journal of Neurophysiology, 69, 2150–2163.PubMedGoogle Scholar
  96. 96.
    Tacconi, S., Carletti, R., Bunnemann, B., Plumpton, C., Merlo Pich, E., & Terstappen, G. C. (2001). Distribution of the messenger RNA for the small conductance calcium- activated potassium channel SK3 in the adult rat brain and correlation with immunoreactivity. Neuroscience, 102, 209–215.PubMedCrossRefGoogle Scholar
  97. 97.
    Sarpal, D., Koenig, J. I., Adelman, J. P., Brady, D., Prendeville, L. C., & Shepard, P. D. (2004). Regional distribution of SK3 mRNA-containing neurons in the adult and adolescent rat ventral midbrain and their relationship to dopamine-containing cells. Synapse, 53, 104–113.PubMedCrossRefGoogle Scholar
  98. 98.
    Shepard, P. D., & Bunney, B. S. (1988). Effects of apamin on the discharge properties of putative dopamine-containing neurons in vitro. Brain Research, 463, 380–384.PubMedCrossRefGoogle Scholar
  99. 99.
    Shepard, P. D., & Bunney, B. S. (1991). Repetitive firing properites of putative dopamine-containing neurons in vitro: regulation by an apamin-sensitive Ca2+ -activated K+ conductance. Experimental Brain Research, 86, 141–150.CrossRefGoogle Scholar
  100. 100.
    Gu, X., Blatz, A. L., & German, D. C. (1992). Subtypes of substantia nigra dopaminergic neurons revealed by apamin: autoradiographic and electrophysiological studies. Brain Research Bulletin, 28, 435–440.PubMedCrossRefGoogle Scholar
  101. 101.
    Ping, H. X., & Shepard, P. D. (1996). Apamin-sensitive Ca2+-activated K+ channels regulate pacemaker activity in nigral dopamine neurons. NeuroReport, 7, 809–814.PubMedCrossRefGoogle Scholar
  102. 102.
    Seutin, V., Johnson, S. W., & North, R. A. (1993). Apamin increases NMDA-induced burst-firing of rat mesencephalic dopamine neurons. Brain Research, 630, 341–344.PubMedCrossRefGoogle Scholar
  103. 103.
    Waroux, O., Massotte, L., Alleva, L., et al. (2005). SK channels control the firing pattern of midbrain dopaminergic neurons in vivo. European Journal of Neuroscience, 22, 3111–3121.PubMedCrossRefGoogle Scholar
  104. 104.
    Ji, H., & Shepard, P. D. (2006). SK Ca2+-activated K+ channel ligands alter the firing pattern of dopamine-containing neurons in vivo. Neuroscience, 140, 623–633.PubMedCrossRefGoogle Scholar
  105. 105.
    Goldman-Rakic, P. S. (1999). The physiological approach: functional architecture of working memory and disordered cognition in schizophrenia. Biological Psychiatry, 46, 650–661.PubMedCrossRefGoogle Scholar
  106. 106.
    Kitai, S. T., Shepard, P. D., Callaway, J. C., & Scroggs, R. (1999). Afferent modulation of dopamine neuron firing patterns. Current Opinion in Neurobiology, 9, 690–697.PubMedCrossRefGoogle Scholar
  107. 107.
    Schultz, W. (2000). Multiple reward signals in the brain. Nature Reviews. Neuroscience, 1, 199–207.PubMedCrossRefGoogle Scholar
  108. 108.
    Rouchet, N., Waroux, O., Lamy, C., et al. (2008). SK channel blockade promotes burst firing in dorsal raphe serotonergic neurons. European Journal of Neuroscience, 28, 1108–1115.PubMedCrossRefGoogle Scholar
  109. 109.
    Hornung, J. P. (2003). The human raphe nuclei and the serotonergic system. Journal of Chemical Neuroanatomy, 26, 331–343.PubMedCrossRefGoogle Scholar
  110. 110.
    Bal, T., & McCormick, D. A. (1993). Mechanisms of oscillatory activity in guinea-pig nucleus reticularis thalami in vitro: a mammalian pacemaker. Journal of Physiology, 468, 669–691.PubMedGoogle Scholar
  111. 111.
    Cueni, L., Canepari, M., Lujan, R., et al. (2008). T-type Ca2+ channels, SK2 channels and SERCAs gate sleep-related oscillations in thalamic dendrites. Nature Neuroscience, 11, 683–692.PubMedCrossRefGoogle Scholar
  112. 112.
    Lorenzon, N. M., & Foehring, R. C. (1992). Relationship between repetitive firing and afterhyperpolarizations in human neocortical neurons. Journal of Neurophysiology, 67, 350–363.PubMedGoogle Scholar
  113. 113.
    Hagenston, A. M., Fitzpatrick, J. S., & Yeckel, M. F. (2008). MGluR-mediated calcium waves that invade the soma regulate firing in layer V medial prefrontal cortical pyramidal neurons. Cerebral Cortex, 18, 407–423.PubMedCrossRefGoogle Scholar
  114. 114.
    Netzeband, J. G., & Gruol, D. L. (2008). mGluR1 agonists elicit a Ca2+ signal and membrane hyperpolarization mediated by apamin-sensitive potassium channels in immature rat purkinje neurons. Journal of Neuroscience Research, 86, 293–305.PubMedCrossRefGoogle Scholar
  115. 115.
    Yamada, S., Takechi, H., Kanchiku, I., Kita, T., & Kato, N. (2004). Small-conductance Ca2+-dependent K+ channels are the target of spike-induced Ca2+ release in a feedback regulation of pyramidal cell excitability. Journal of Neurophysiology, 91, 2322–2329.PubMedCrossRefGoogle Scholar
  116. 116.
    Gulledge, A. T., Park, S. B., Kawaguchi, Y., & Stuart, G. J. (2007). Heterogeneity of phasic cholinergic signaling in neocortical neurons. Journal of Neurophysiology, 97, 2215–2229.PubMedCrossRefGoogle Scholar
  117. 117.
    Gulledge, A. T., & Stuart, G. J. (2005). Cholinergic inhibition of neocortical pyramidal neurons. Journal of Neuroscience, 25, 10308–10320.PubMedCrossRefGoogle Scholar
  118. 118.
    Cai, X., Liang, C. W., Muralidharan, S., Kao, J. P., Tang, C. M., & Thompson, S. M. (2004). Unique roles of SK and Kv4.2 potassium channels in dendritic integration. Neuron, 44, 351–364.PubMedCrossRefGoogle Scholar
  119. 119.
    Isaacson, J. S., & Strowbridge, B. W. (1998). Olfactory reciprocal synapses: dendritic signaling in the CNS. Neuron, 20, 749–761.PubMedCrossRefGoogle Scholar
  120. 120.
    Fiorillo, C. D., & Williams, J. T. (1998). Glutamate mediates an inhibitory postsynaptic potential in dopamine neurons. Nature, 394, 78–82.PubMedCrossRefGoogle Scholar
  121. 121.
    Morikawa, H., Khodakhah, K., & Williams, J. T. (2003). Two intracellular pathways mediate metabotropic glutamate receptor-induced Ca2+ mobilization in dopamine neurons. Journal of Neuroscience, 23, 149–157.PubMedGoogle Scholar
  122. 122.
    Fiorillo, C. D., & Williams, J. T. (2000). Cholinergic inhibition of ventral midbrain dopamine neurons. Journal of Neuroscience, 20, 7855–7860.PubMedGoogle Scholar
  123. 123.
    Paladini, C. A., & Williams, J. T. (2004). Noradrenergic inhibition of midbrain dopamine neurons. Journal of Neuroscience, 24, 4568–4575.PubMedCrossRefGoogle Scholar
  124. 124.
    Riegel, A. C., & Williams, J. T. (2008). CRF facilitates calcium release from intracellular stores in midbrain dopamine neurons. Neuron, 57, 559–570.PubMedCrossRefGoogle Scholar
  125. 125.
    Riegel, A. C., & Lupica, C. R. (2004). Independent presynaptic and postsynaptic mechanisms regulate endocannabinoid signaling at multiple synapses in the ventral tegmental area. Journal of Neuroscience, 24, 11070–11078.PubMedCrossRefGoogle Scholar
  126. 126.
    Faber, E. S. L., Delaney, A. J., & Sah, P. (2005). SK channels regulate excitatory synaptic transmission and plasticity in the lateral amygdala. Nature Neuroscience, 8, 635–641.PubMedCrossRefGoogle Scholar
  127. 127.
    Ngo-Anh, T. J., Bloodgood, B. L., Lin, M., Sabatini, B. L., Maylie, J., & Adelman, J. P. (2005). SK channels and NMDA receptors form a Ca2+-mediated feedback loop in dendritic spines. Nature Neuroscience, 8, 642–649.PubMedCrossRefGoogle Scholar
  128. 128.
    Bloodgood, B. L., & Sabatini, B. L. (2007). Nonlinear regulation of unitary synaptic signals by CaV2.3 voltage-sensitive calcium channels located in dendritic spines. Neuron, 53, 249–260.PubMedCrossRefGoogle Scholar
  129. 129.
    Brosh, I., Rosenblum, K., & Barkai, E. (2007). Learning-induced modulation of SK channels-mediated effect on synaptic transmission. European Journal of Neuroscience, 26, 3253–3260.PubMedCrossRefGoogle Scholar
  130. 130.
    Oliver, D., Klocker, N., Schuck, J., Baukrowitz, T., Ruppersberg, J. P., & Fakler, B. (2000). Gating of Ca2+-activated K+ channels controls fast inhibitory synaptic transmission at auditory outer hair cells. Neuron, 26, 595–601.PubMedCrossRefGoogle Scholar
  131. 131.
    Obermair, G. J., Kaufmann, W. A., Knaus, H. G., & Flucher, B. E. (2003). The small conductance Ca2+-activated K+ channel SK3 is localized in nerve terminals of excitatory synapses of cultured mouse hippocampal neurons. European Journal of Neuroscience, 17, 721–731.PubMedCrossRefGoogle Scholar
  132. 132.
    Faber, E. S. L. (2008). SK channels regulate excitatory synaptic transmission in the rat medial prefrontal cortex. Abstracts–Society for Neuroscience, 36, 13.Google Scholar
  133. 133.
    Kramar, E. A., Lin, B., Lin, C. Y., Arai, A. C., Gall, C. M., & Lynch, G. (2004). A novel mechanism for the facilitation of theta-induced long-term potentiation by brain-derived neurotrophic factor. Journal of Neuroscience, 24, 5151–5161.PubMedCrossRefGoogle Scholar
  134. 134.
    Behnisch, T., & Reymann, K. G. (1998). Inhibition of apamin-sensitive calcium dependent potassium channels facilitate the induction of long-term potentiation in the CA1 region of rat hippocampus in vitro. Neuroscience Letters, 253, 91–94.PubMedCrossRefGoogle Scholar
  135. 135.
    Norris, C. M., halpain, S., & Foster, T. C. (1998). Reversal of age-related alterations in synaptic plasticity by blockade of L-type Ca2+ channels. Journal of Neuroscience, 18, 3171–3179.PubMedGoogle Scholar
  136. 136.
    Hammond, R. S., Bond, C. T., Strassmaier, T., et al. (2006). Small-conductance Ca2+-activated K+ channel type 2 (SK2) modulates hippocampal learning, memory, and synaptic plasticity. Journal of Neuroscience, 26, 1844–1853.PubMedCrossRefGoogle Scholar
  137. 137.
    Ris, L., Capron, B., Sclavons, C., Liégeois, J. F., Seutin, V., & Godaux, E. (2007). Metaplastic effect of apamin on LTP and paired-pulse facilitation. Learning and Memory, 14, 390–399.PubMedCrossRefGoogle Scholar
  138. 138.
    van der Staay, F. J., Fanelli, R. J., Blokland, A., & Schmidt, B. H. (1999). Behavioral effects of apamin, a selective inhibitor of the SKCa-channel, in mice and rats. Neuroscience and Biobehavioral Reviews, 23, 1087–1110.PubMedCrossRefGoogle Scholar
  139. 139.
    Deschaux, O., Bizot, J. C., & Goyffon, M. (1997). Apamin improves learning in an object recognition task in rats. Neuroscience Letters, 222, 159–162.PubMedCrossRefGoogle Scholar
  140. 140.
    Belcadi-Abbassi, W., & Destrade, C. (1995). Post-test apamin injection suppresses a Kamin-like effect following a learning session in mice. Neuroreport, 6, 1293–1296.PubMedCrossRefGoogle Scholar
  141. 141.
    Messier, C., Mourre, C., Bontempi, B., Sif, J., Lazdunski, M., & Destrade, C. (1991). Effect of apamin, a toxin that inhibits Ca2+-dependent K+ channels, on learning and memory processes. Brain Research, 551, 322–326.PubMedCrossRefGoogle Scholar
  142. 142.
    Fournier, C., Kourrich, S., Soumireu-Mourat, B., & Mourre, C. (2001). Apamin improves reference memory but not procedural memory in rats by blocking small conductance Ca2+-activated K+ channels in an olfactory discrimination task. Behavioural Brain Research, 121, 81–93.PubMedCrossRefGoogle Scholar
  143. 143.
    Ikonen, S., & Riekkinen, P., Jr. (1999). Effects of apamin on memory processing of hippocampal-lesioned mice. European Journal of Pharmacology, 382, 151–156.PubMedCrossRefGoogle Scholar
  144. 144.
    Ikonen, S., Schmidt, B., & Riekkinen, P., Jr. (1998). Apamin improves spatial navigation in medial septal-lesioned mice. European Journal of Pharmacology, 347, 13–21.PubMedCrossRefGoogle Scholar
  145. 145.
    Brennan, A. R., Dolinsky, B., Vu, M. A., Stanley, M., Yeckel, M. F., & Arnsten, A. F. (2008). Blockade of IP3-mediated SK channel signaling in the rat medial prefrontal cortex improves spatial working memory. Learning and Memory, 15, 93–96.PubMedCrossRefGoogle Scholar
  146. 146.
    Blank, T., Nijholt, I., Kye, M. J., Radulovic, J., & Spiess, J. (2003). Small-conductance, Ca2+-activated K+ channel SK3 generates age-related memory and LTP deficits. Nature Neuroscience, 6, 911–912.PubMedCrossRefGoogle Scholar
  147. 147.
    Stackman, R. W., Jr., Bond, C. T., & Adelman, J. P. (2008). Contextual memory deficits observed in mice overexpressing small conductance Ca2+-activated K+ type 2 (KCa2.2, SK2) channels are caused by an encoding deficit. Learning and Memory, 15, 208–213.PubMedCrossRefGoogle Scholar
  148. 148.
    Ren, Y., Barnwell, L. F., Alexander, J. C., et al. (2006). Regulation of surface localization of the small conductance Ca2+-activated potassium channel, SK2, through direct phosphorylation by cAMP-dependent protein kinase. Journal of Biological Chemistry, 281, 11769–11779.PubMedCrossRefGoogle Scholar
  149. 149.
    McGaugh, J. L. (2004). The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annual Review of Neuroscience, 27, 1–28.PubMedCrossRefGoogle Scholar
  150. 150.
    Martina, M., Turcotte, M. E., Halman, S., & Bergeron, R. (2007). The sigma-1 receptor modulates NMDA receptor synaptic transmission and plasticity via SK channels in rat hippocampus. Journal of Physiology, 578, 143–157.PubMedCrossRefGoogle Scholar
  151. 151.
    Sourdet, V., Russier, M., Daoudal, G., Ankri, N., & Debanne, D. (2003). Long-term enhancement of neuronal excitability and temporal fidelity mediated by metabotropic glutamate receptor subtype 5. Journal of Neuroscience, 23, 10238–10248.PubMedGoogle Scholar
  152. 152.
    Han, P., Nakanishi, S. T., Tran, M. A., & Whelan, P. J. (2007). Dopaminergic modulation of spinal neuronal excitability. Journal of Neuroscience, 27, 13192–13204.PubMedCrossRefGoogle Scholar
  153. 153.
    Ruan, M., & Brown, C. H. (2009). Feedback inhibition of action potential discharge by endogenous adenosine enhancement of the medium afterhyperpolarization. Journal of Physiology, 587, 1043–1056.PubMedCrossRefGoogle Scholar
  154. 154.
    Bosch, M. A., Kelly, M. J., & Ronnekleiv, O. K. (2002). Distribution, neuronal colocalization, and 17beta-E2 modulation of small conductance calcium-activated K+ channel (SK3) mRNA in the guinea pig brain. Endocrinology, 143, 1097–1107.PubMedCrossRefGoogle Scholar
  155. 155.
    Bildl, W., Strassmaier, T., Thurm, H., et al. (2004). Protein kinase CK2 is coassembled with small conductance Ca2+-activated K+ channels and regulates channel gating. Neuron, 43, 847–858.PubMedCrossRefGoogle Scholar
  156. 156.
    Allen, D., Fakler, B., Maylie, J., & Adelman, J. P. (2007). Organization and regulation of small conductance Ca2+-activated K+ channel multiprotein complexes. Journal of Neuroscience, 27, 2369–2376.PubMedCrossRefGoogle Scholar
  157. 157.
    Maingret, F., Coste, B., Hao, J., et al. (2008). Neurotransmitter modulation of small-conductance Ca2+-activated K+ channels by regulation of Ca2+ gating. Neuron, 59, 439–449.PubMedCrossRefGoogle Scholar
  158. 158.
    Terstappen, G. C., Pula, G., Carignani, C., Chen, M. X., & Roncarati, R. (2001). Pharmacological characterisation of the human small conductance calcium-activated potassium channel hSK3 reveals sensitivity to tricyclic antidepressants and antipsychotic phenothiazines. Neuropharmacology, 40, 772–783.PubMedCrossRefGoogle Scholar
  159. 159.
    Stocker, M., Hirzel, K., D’Hoedt, D., & Pedarzani, P. (2004). Matching molecules to function: neuronal Ca2+-activated K+ channels and afterhyperpolarizations. Toxicon, 43, 933–949.PubMedCrossRefGoogle Scholar
  160. 160.
    Gargus, J. J., Fantino, E., & Gutman, G. A. (1998). A piece in the puzzle: an ion channel candidate gene for schizophrenia. Molecular Medicine Today, 4, 518–524.PubMedCrossRefGoogle Scholar
  161. 161.
    Chandy, K. G., Fantino, E., Wittekindt, O., et al. (1998). Isolation of a novel potassium channel gene hSKCa3 containing a polymorphic CAG repeat: a candidate for schizophrenia and bipolar disorder? Molecular Psychiatry, 3, 32–37.PubMedCrossRefGoogle Scholar
  162. 162.
    Dror, V., Shamir, E., Ghanshani, S., et al. (1999). hKCa3/KCNN3 potassium channel gene: association of longer CAG repeats with schizophrenia in Israeli Ashkenazi Jews, expression in human tissues and localization to chromosome 1q21. Molecular Psychiatry, 4, 254–260.PubMedCrossRefGoogle Scholar
  163. 163.
    Ritsner, M., Modai, I., Ziv, H., et al. (2002). An association of CAG repeats at the KCNN3 locus with symptom dimensions of schizophrenia. Biological Psychiatry, 51, 788–794.PubMedCrossRefGoogle Scholar
  164. 164.
    Miller, M. J., Rauer, H., Tomita, H., et al. (2001). Nuclear localization and dominant-negative suppression by a mutant SKCa3 N-terminal channel fragment identified in a patient with schizophrenia. Journal of Biological Chemistry, 276, 27753–27756.PubMedCrossRefGoogle Scholar
  165. 165.
    Aumann, T. D., Gantois, I., Egan, K., et al. (2008). SK channel function regulates the dopamine phenotype of neurons in the substantia nigra pars compacta. Experimental Neurology, 213, 419–430.PubMedCrossRefGoogle Scholar
  166. 166.
    Wightman, R. M., & Zimmerman, J. B. (1990). Control of dopamine extracellular concentration in rat striatum by impulse flow and uptake. Brain Research. Brain Research Reviews, 15, 135–144.PubMedCrossRefGoogle Scholar
  167. 167.
    Keefe, K. A., Sved, A. F., Zigmond, M. J., & Abercrombie, E. D. (1993). Stress-induced dopamine release in the neostriatum: evaluation of the role of action potentials in nigrostriatal dopamine neurons or local initiation by endogenous excitatory amino acids. Journal of Neurochemistry, 61, 1943–1952.PubMedCrossRefGoogle Scholar
  168. 168.
    Stokes, A. H., Hastings, T. G., & Vrana, K. E. (1999). Cytotoxic and genotoxic potential of dopamine. Journal of Neuroscience Research, 55, 659–665.PubMedCrossRefGoogle Scholar
  169. 169.
    Anderson, N. J., Slough, S., & Watson, W. P. (2006). In vivo characterisation of the small-conductance KCa (SK) channel activator 1-ethyl-2-benzimidazolinone (1-EBIO) as a potential anticonvulsant. European Journal of Pharmacology, 546, 48–53.PubMedCrossRefGoogle Scholar
  170. 170.
    Kim, J., Jung, S. C., Clemens, A. M., Petralia, R. S., & Hoffman, D. A. (2007). Regulation of dendritic excitability by activity-dependent trafficking of the A-type K+ channel subunit Kv4.2 in hippocampal neurons. Neuron, 54, 933–947.PubMedCrossRefGoogle Scholar

Copyright information

© Humana Press Inc. 2009

Authors and Affiliations

  1. 1.The University of QueenslandQueensland Brain InstituteBrisbaneAustralia

Personalised recommendations