Skip to main content
Log in

Roles of somatic A-type K+ channels in the synaptic plasticity of hippocampal neurons

  • Review
  • Published:
Neuroscience Bulletin Aims and scope Submit manuscript

Abstract

In the mammalian brain, information encoding and storage have been explained by revealing the cellular and molecular mechanisms of synaptic plasticity at various levels in the central nervous system, including the hippocampus and the cerebral cortices. The modulatory mechanisms of synaptic excitability that are correlated with neuronal tasks are fundamental factors for synaptic plasticity, and they are dependent on intracellular Ca2+-mediated signaling. In the present review, the A-type K+ (I A) channel, one of the voltage-dependent cation channels, is considered as a key player in the modulation of Ca2+ influx through synaptic NMDA receptors and their correlated signaling pathways. The cellular functions of I A channels indicate that they possibly play as integral parts of synaptic and somatic complexes, completing the initiation and stabilization of memory.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Aizenman CD, Linden DJ. Rapid, synaptically driven increases in the intrinsic excitability of cerebellar deep nuclear neurons. Nat Neurosci 2000, 3: 109–111.

    Article  CAS  PubMed  Google Scholar 

  2. Jung SC, Hoffman DA. Biphasic somatic A-type K+ channel downregulation mediates intrinsic plasticity in hippocampal CA1 pyramidal neurons. PLoS One 2009, 4: e6549.

    Article  PubMed Central  PubMed  Google Scholar 

  3. Kim SJ, Linden DJ. Ubiquitous plasticity and memory storage. Neuron 2007, 56: 582–592.

    Article  CAS  PubMed  Google Scholar 

  4. Xu J, Kang N, Jiang L, Nedergaard M, Kang J. Activity-dependent long-term potentiation of intrinsic excitability in hippocampal CA1 pyramidal neurons. J Neurosci 2005, 25: 1750–1760.

    Article  CAS  PubMed  Google Scholar 

  5. Zhang W, Linden DJ. The other side of the engram: experience-driven changes in neuronal intrinsic excitability. Nat Rev Neurosci 2003, 4: 885–900.

    Article  CAS  PubMed  Google Scholar 

  6. Franks KM, Isaacson JS. Synapse-specific downregulation of NMDA receptors by early experience: a critical period for plasticity of sensory input to olfactory cortex. Neuron 2005, 47: 101–114.

    Article  CAS  PubMed  Google Scholar 

  7. Lapointe V, Morin F, Ratte S, Croce A, Conquet F, Lacaille JC. Synapse-specific mGluR1-dependent long-term potentiation in interneurones regulates mouse hippocampal inhibition. J Physiol 2004, 555: 125–135.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  8. Singla S, Kreitzer AC, Malenka RC. Mechanisms for synapse specificity during striatal long-term depression. J Neurosci 2007, 27: 5260–5264.

    Article  CAS  PubMed  Google Scholar 

  9. Bliss TV, Lomo T. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol 1973, 232: 331–356.

    CAS  PubMed Central  PubMed  Google Scholar 

  10. Campanac E, Debanne D. Spike timing-dependent plasticity: a learning rule for dendritic integration in rat CA1 pyramidal neurons. J Physiol 2008, 586: 779–793.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  11. Bergquist S, Dickman DK, Davis GW. A hierarchy of cell intrinsic and target-derived homeostatic signaling. Neuron 2010, 66: 220–234.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  12. Tsunoda S, Salkoff L. Genetic analysis of Drosophila neurons: Shal, Shaw, and Shab encode most embryonic potassium currents. J Neurosci 1995, 15: 1741–1754.

    CAS  PubMed  Google Scholar 

  13. Solc CK, Zagotta WN, Aldrich RW. Single-channel and genetic analyses reveal two distinct A-type potassium channels in Drosophila. Science 1987, 236: 1094–1098.

    Article  CAS  PubMed  Google Scholar 

  14. Cash S, Yuste R. Input summation by cultured pyramidal neurons is linear and position-independent. J Neurosci 1998, 18: 10–15.

    CAS  PubMed  Google Scholar 

  15. Goldberg JH, Tamas G, Yuste R. Ca2+ imaging of mouse neocortical interneurone dendrites: Ia-type K+ channels control action potential backpropagation. J Physiol 2003, 551: 49–65.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  16. Hoffman DA, Magee JC, Colbert CM, Johnston D. K+ channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons. Nature 1997, 387: 869–875.

    Article  CAS  PubMed  Google Scholar 

  17. Kim J, Wei DS, Hoffman DA. Kv4 potassium channel subunits control action potential repolarization and frequency-dependent broadening in rat hippocampal CA1 pyramidal neurones. J Physiol 2005, 569: 41–57.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  18. Ramakers GM, Storm JF. A postsynaptic transient K(+) current modulated by arachidonic acid regulates synaptic integration and threshold for LTP induction in hippocampal pyramidal cells. Proc Natl Acad Sci U S A 2002, 99: 10144–10149.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  19. Schoppa NE, Westbrook GL. Regulation of synaptic timing in the olfactory bulb by an A-type potassium current. Nat Neurosci 1999, 2: 1106–1113.

    Article  CAS  PubMed  Google Scholar 

  20. Chen X, Yuan LL, Zhao C, Birnbaum SG, Frick A, Jung WE, et al. Deletion of Kv4.2 gene eliminates dendritic A-type K+ current and enhances induction of long-term potentiation in hippocampal CA1 pyramidal neurons. J Neurosci 2006, 26: 12143–12151.

    Article  CAS  PubMed  Google Scholar 

  21. Frick A, Magee J, Johnston D. LTP is accompanied by an enhanced local excitability of pyramidal neuron dendrites. Nat Neurosci 2004, 7: 126–135.

    Article  CAS  PubMed  Google Scholar 

  22. Jung SC, Kim J, Hoffman DA. Rapid, bidirectional remodeling of synaptic NMDA receptor subunit composition by A-type K+ channel activity in hippocampal CA1 pyramidal neurons. Neuron 2008, 60: 657–671.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  23. Kim J, Jung SC, Clemens AM, Petralia RS, Hoffman DA. Regulation of dendritic excitability by activity-dependent trafficking of the A-type K+ channel subunit Kv4.2 in hippocampal neurons. Neuron 2007, 54: 933–947.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  24. Watanabe S, Hoffman DA, Migliore M, Johnston D. Dendritic K+ channels contribute to spike-timing dependent long-term potentiation in hippocampal pyramidal neurons. Proc Natl Acad Sci U S A 2002, 99: 8366–8371.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  25. Cooper EC, Milroy A, Jan YN, Jan LY, Lowenstein DH. Presynaptic localization of Kv1.4-containing A-type potassium channels near excitatory synapses in the hippocampus. J Neurosci 1998, 18: 965–974.

    CAS  PubMed  Google Scholar 

  26. Kampa BM, Stuart GJ. Calcium spikes in basal dendrites of layer 5 pyramidal neurons during action potential bursts. J Neurosci 2006, 26: 7424–7432.

    Article  CAS  PubMed  Google Scholar 

  27. Losonczy A, Makara JK, Magee JC. Compartmentalized dendritic plasticity and input feature storage in neurons. Nature 2008, 452: 436–441.

    Article  CAS  PubMed  Google Scholar 

  28. Sheng M, Tsaur ML, Jan YN, Jan LY. Subcellular segregation of two A-type K+ channel proteins in rat central neurons. Neuron 1992, 9: 271–284.

    Article  CAS  PubMed  Google Scholar 

  29. Hagiwara S. Nervous activities of the heart in Crustacea. Ergeb Biol 1961, 24: 287–311.

    CAS  PubMed  Google Scholar 

  30. Johnston D, Narayanan R. Active dendrites: colorful wings of the mysterious butterflies. Trends Neurosci 2008, 31: 309–316.

    Article  CAS  PubMed  Google Scholar 

  31. Marsh SJ, Brown DA. Potassium currents contributing to action potential repolarization in dissociated cultured rat superior cervical sympathetic neurones. Neurosci Lett 1991, 133: 298–302.

    Article  CAS  PubMed  Google Scholar 

  32. Sah P, McLachlan EM. Potassium currents contributing to action potential repolarization and the afterhyperpolarization in rat vagal motoneurons. J Neurophysiol 1992, 68: 1834–1841.

    CAS  PubMed  Google Scholar 

  33. Lorincz A, Notomi T, Tamas G, Shigemoto R, Nusser Z. Polarized and compartment-dependent distribution of HCN1 in pyramidal cell dendrites. Nat Neurosci 2002, 5: 1185–1193.

    Article  PubMed  Google Scholar 

  34. Notomi T, Shigemoto R. Immunohistochemical localization of Ih channel subunits, HCN1–4, in the rat brain. J Comp Neurol 2004, 471: 241–276.

    Article  CAS  PubMed  Google Scholar 

  35. Sanguinetti MC, Jurkiewicz NK. Role of external Ca2+ and K+ in gating of cardiac delayed rectifier K+ currents. Pflugers Arch 1992, 420: 180–186.

    Article  CAS  PubMed  Google Scholar 

  36. Snyders DJ. Structure and function of cardiac potassium channels. Cardiovasc Res 1999, 42: 377–390.

    Article  CAS  PubMed  Google Scholar 

  37. Varro A, Papp JG. The impact of single cell voltage clamp on the understanding of the cardiac ventricular action potential. Cardioscience 1992, 3: 131–144.

    CAS  PubMed  Google Scholar 

  38. Lei M, Honjo H, Kodama I, Boyett MR. Characterisation of the transient outward K+ current in rabbit sinoatrial node cells. Cardiovasc Res 2000, 46: 433–441.

    Article  CAS  PubMed  Google Scholar 

  39. Shibasaki T. Conductance and kinetics of delayed rectifier potassium channels in nodal cells of the rabbit heart. J Physiol 1987, 387: 227–250.

    CAS  PubMed Central  PubMed  Google Scholar 

  40. Carrasquillo Y, Burkhalter A, Nerbonne JM. A-type K+ channels encoded by Kv4.2, Kv4.3 and Kv1.4 differentially regulate intrinsic excitability of cortical pyramidal neurons. J Physiol 2012, 590: 3877–3890.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  41. Coetzee WA, Amarillo Y, Chiu J, Chow A, Lau D, McCormack T, et al. Molecular diversity of K+ channels. Ann N Y Acad Sci 1999, 868: 233–285.

    Article  CAS  PubMed  Google Scholar 

  42. Song WJ. Genes responsible for native depolarization-activated K+ currents in neurons. Neurosci Res 2002, 42: 7–14.

    Article  CAS  PubMed  Google Scholar 

  43. Lauver A, Yuan LL, Jeromin A, Nadin BM, Rodriguez JJ, Davies HA, et al. Manipulating Kv4.2 identifies a specific component of hippocampal pyramidal neuron A-current that depends upon Kv4.2 expression. J Neurochem 2006, 99: 1207–1223.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  44. Malinow R, Malenka RC. AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 2002, 25: 103–126.

    Article  CAS  PubMed  Google Scholar 

  45. Nicoll RA, Malenka RC. Expression mechanisms underlying NMDA receptor-dependent long-term potentiation. Ann N Y Acad Sci 1999, 868: 515–525.

    Article  CAS  PubMed  Google Scholar 

  46. Stuart G, Spruston N, Sakmann B, Hausser M. Action potential initiation and backpropagation in neurons of the mammalian CNS. Trends Neurosci 1997, 20: 125–131.

    Article  CAS  PubMed  Google Scholar 

  47. Lisman J, Spruston N. Postsynaptic depolarization requirements for LTP and LTD: a critique of spike timing-dependent plasticity. Nat Neurosci 2005, 8: 839–841.

    Article  CAS  PubMed  Google Scholar 

  48. Magee JC, Johnston D. A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science 1997, 275: 209–213.

    Article  CAS  PubMed  Google Scholar 

  49. Stuart GJ, Sakmann B. Active propagation of somatic action potentials into neocortical pyramidal cell dendrites. Nature 1994, 367: 69–72.

    Article  CAS  PubMed  Google Scholar 

  50. Bellone C, Nicoll RA. Rapid bidirectional switching of synaptic NMDA receptors. Neuron 2007, 55: 779–785.

    Article  CAS  PubMed  Google Scholar 

  51. Kerchner GA, Nicoll RA. Silent synapses and the emergence of a postsynaptic mechanism for LTP. Nat Rev Neurosci 2008, 9: 813–825.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  52. Kim E, Hoffman DA. Dynamic regulation of synaptic maturation state by voltage-gated A-type K+ channels in CA1 hippocampal pyramidal neurons. J Neurosci 2012, 32: 14427–14432.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  53. Campanac E, Daoudal G, Ankri N, Debanne D. Downregulation of dendritic I(h) in CA1 pyramidal neurons after LTP. J Neurosci 2008, 28: 8635–8643.

    Article  CAS  PubMed  Google Scholar 

  54. Daoudal G, Debanne D. Long-term plasticity of intrinsic excitability: learning rules and mechanisms. Learn Mem 2003, 10: 456–465.

    Article  PubMed  Google Scholar 

  55. Disterhoft JF, Oh MM. Learning, aging and intrinsic neuronal plasticity. Trends Neurosci 2006, 29: 587–599.

    Article  CAS  PubMed  Google Scholar 

  56. Storm JF. Potassium currents in hippocampal pyramidal cells. Prog Brain Res 1990, 83: 161–187.

    Article  CAS  PubMed  Google Scholar 

  57. Alkon DL, Sakakibara M, Forman R, Harrigan J, Lederhendler I, Farley J. Reduction of two voltage-dependent K+ currents mediates retention of a learned association. Behav Neural Biol 1985, 44: 278–300.

    Article  CAS  PubMed  Google Scholar 

  58. Fan Y, Fricker D, Brager DH, Chen X, Lu HC, Chitwood RA, et al. Activity-dependent decrease of excitability in rat hippocampal neurons through increases in I(h). Nat Neurosci 2005, 8: 1542–1551.

    Article  CAS  PubMed  Google Scholar 

  59. Hess G, Gustafsson B. Changes in field excitatory postsynaptic potential shape induced by tetanization in the CA1 region of the guinea-pig hippocampal slice. Neuroscience 1990, 37: 61–69.

    Article  CAS  PubMed  Google Scholar 

  60. Jester JM, Campbell LW, Sejnowski TJ. Associative EPSP-spike potentiation induced by pairing orthodromic and antidromic stimulation in rat hippocampal slices. J Physiol 1995, 484(Pt 3): 689–705.

    CAS  PubMed Central  PubMed  Google Scholar 

  61. Reyes A. Influence of dendritic conductances on the input-output properties of neurons. Annu Rev Neurosci 2001, 24: 653–675.

    Article  CAS  PubMed  Google Scholar 

  62. Bayliss DA, Viana F, Bellingham MC, Berger AJ. Characteristics and postnatal development of a hyperpolarization-activated inward current in rat hypoglossal motoneurons in vitro. J Neurophysiol 1994, 71: 119–128.

    CAS  PubMed  Google Scholar 

  63. Chetkovich DM, Gray R, Johnston D, Sweatt JD. N-methyl-D-aspartate receptor activation increases cAMP levels and voltage-gated Ca2+ channel activity in area CA1 of hippocampus. Proc Natl Acad Sci U S A 1991, 88: 6467–6471.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  64. Havik B, Rokke H, Bardsen K, Davanger S, Bramham CR. Bursts of high-frequency stimulation trigger rapid delivery of pre-existing alpha-CaMKII mRNA to synapses: a mechanism in dendritic protein synthesis during long-term potentiation in adult awake rats. Eur J Neurosci 2003, 17: 2679–2689.

    Article  PubMed  Google Scholar 

  65. Huang YY, Kandel ER. Postsynaptic induction and PKA-dependent expression of LTP in the lateral amygdala. Neuron 1998, 21: 169–178.

    Article  CAS  PubMed  Google Scholar 

  66. Kirkwood A, Rioult MC, Bear MF. Experience-dependent modification of synaptic plasticity in visual cortex. Nature 1996, 381: 526–528.

    Article  CAS  PubMed  Google Scholar 

  67. Nishiyama M, Hong K, Mikoshiba K, Poo MM, Kato K. Calcium stores regulate the polarity and input specificity of synaptic modification. Nature 2000, 408: 584–588.

    Article  CAS  PubMed  Google Scholar 

  68. Perkel DJ, Petrozzino JJ, Nicoll RA, Connor JA. The role of Ca2+ entry via synaptically activated NMDA receptors in the induction of long-term potentiation. Neuron 1993, 11: 817–823.

    Article  CAS  PubMed  Google Scholar 

  69. Li XM, Gu Y, She JQ, Zhu DM, Niu ZD, Wang M, et al. Lead inhibited N-methyl-D-aspartate receptor-independent long-term potentiation involved ryanodine-sensitive calcium stores in rat hippocampal area CA1. Neuroscience 2006, 139: 463–473.

    Article  CAS  PubMed  Google Scholar 

  70. Mellentin C, Jahnsen H, Abraham WC. Priming of long-term potentiation mediated by ryanodine receptor activation in rat hippocampal slices. Neuropharmacology 2007, 52: 118–125.

    Article  CAS  PubMed  Google Scholar 

  71. Welsby P, Rowan M, Anwyl R. Nicotinic receptor-mediated enhancement of long-term potentiation involves activation of metabotropic glutamate receptors and ryanodine-sensitive calcium stores in the dentate gyrus. Eur J Neurosci 2006, 24: 3109–3118.

    Article  PubMed  Google Scholar 

  72. Xie CW. Calcium-regulated signaling pathways: role in amyloid beta-induced synaptic dysfunction. Neuromolecular Med 2004, 6: 53–64.

    Article  CAS  PubMed  Google Scholar 

  73. Chen J, Sroubek J, Krishnan Y, Li Y, Bian J, McDonald TV. PKA phosphorylation of HERG protein regulates the rate of channel synthesis. Am J Physiol Heart Circ Physiol 2009, 296: H1244–1254.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  74. Hammond RS, Lin L, Sidorov MS, Wikenheiser AM, Hoffman DA. Protein kinase a mediates activity-dependent Kv4.2 channel trafficking. J Neurosci 2008, 28: 7513–7519.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  75. Lin L, Sun W, Wikenheiser AM, Kung F, Hoffman DA. KChIP4a regulates Kv4.2 channel trafficking through PKA phosphorylation. Mol Cell Neurosci 2010, 43: 315–325.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  76. Nuwer MO, Picchione KE, Bhattacharjee A. PKA-induced internalization of slack KNa channels produces dorsal root ganglion neuron hyperexcitability. J Neurosci 2010, 30: 14165–14172.

    Article  CAS  PubMed  Google Scholar 

  77. Hoffman DA, Johnston D. Downregulation of transient K+ channels in dendrites of hippocampal CA1 pyramidal neurons by activation of PKA and PKC. J Neurosci 1998, 18: 3521–3528.

    CAS  PubMed  Google Scholar 

  78. Esteban JA, Shi SH, Wilson C, Nuriya M, Huganir RL, Malinow R. PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity. Nat Neurosci 2003, 6: 136–143.

    Article  CAS  PubMed  Google Scholar 

  79. Sokolova IV, Lester HA, Davidson N. Postsynaptic mechanisms are essential for forskolin-induced potentiation of synaptic transmission. J Neurophysiol 2006, 95: 2570–2579.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sung-Cherl Jung.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yang, YS., Kim, KD., Eun, SY. et al. Roles of somatic A-type K+ channels in the synaptic plasticity of hippocampal neurons. Neurosci. Bull. 30, 505–514 (2014). https://doi.org/10.1007/s12264-013-1399-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12264-013-1399-7

Keywords

Navigation