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Cited by 743Ion channel regulation and functionNeuroscience and Neuropharmacology ResearchCardiac electrophysiology and arrhythmias

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Chapter 12 Potassium currents in hippocampal pyramidal cells

Storm, Johan F.·1990·Progress in Brain Research
DOI 10.1016/s0079-6123(08)61248-0
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Abstract

The hippocampal pyramidal cells provide an example of how multiple potassium (K) currents co-exist and function in central mammalian neurones. The data come from CA1 and CA3 neurones in hippocampal slices, cell cultures and acutely dissociated cells from rats and guinea-pigs. Six voltage- or calcium(Ca)-dependent K currents have so far been described in CA1 pyramidal cells in slices. Four of them (IA, ID, IK, IM) are activated by depolarization alone; the two others (IC, IAHP) are activated by voltage-dependent influx of Ca ions (IC may be both Ca- and voltage-gated). In addition, a transient Ca-dependent K current (ICT) has been described in certain preparations, but it is not yet clear whether it is distinct from IC and IA. (1) IA activates fast (within 10 ms) and inactivates rapidly (time constant typically 15-50 ms) at potentials positive to -60 mV; it probably contributes to early spike-repolarization, it can delay the first spike for about 0.1 s, and may regulate repetitive firing. (2) ID activates within about 20 ms but inactivates slowly (seconds) below the spike threshold (-90 to -60 mV), causing a long delay (0.5-5 s) in the onset of firing. Due to its slow recovery from inactivation (seconds), separate depolarizing inputs can be "integrated". ID probably also participates in spike repolarization. (3) IK activates slowly (time constant, tau, 20-60 ms) in response to depolarizations positive to -40 mV and inactivates (tau about 5s) at -80 to -40 mV; it probably participates in spike repolarization. (4) IM activates slowly (tau about 50 ms) positive to -60 mV and does not inactivate; it tends to attenuate excitatory inputs, it reduces the firing rate during maintained depolarization (adaptation) and contributes to the medium after-hyperpolarization (mAHP); IM is suppressed by acetylcholine (via muscarinic receptors), but may be enhanced by somatostatin. (5) IC is activated by influx of Ca ions during the action potential and is thought to cause the final spike repolarization and the fast AHP (although ICT may be involved). Like IM, it also contributes to the medium AHP and early adaptation. It differs from IAHP by being sensitive to tetraethylammonium (TEA, 1 mM), but insensitive to noradrenaline and muscarine. Large-conductance (BK; about 200 pS) Ca-activated K channels, which may mediate IC, have been recorded. (6) IAHP is slowly activated by Ca-influx during action potentials, causing spike-frequency adaptation and the slow AHP. Thus, IAHP exerts a strong negative feedback control of discharge activity.(ABSTRACT TRUNCATED AT 400 WORDS)

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Citations

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Research works printed but not linked: 33

  1. Alger, 1988, Whole-cell voltage-clamp study of two distinct components of “A current” in hippocampal neurons., Soc. Neurosci. Abstr., 14, 947
  2. Barrett, 1972, Voltage clamp analysis of conductances underlying cat motoneuron action potentials., Fed. Proc., 31, 305A
  3. Brett, 1985, Activation of potassium channels by rapid application of calcium to inside-out patches of cultured hippocampal neurons., Soc. Neurosci. Abstr., 11, 954
  4. Brown, 1988, M-currents., Vol. 1, 55
  5. Brown, 1982, Calcium-dependence of a component of transient outward current in bullfrog ganglion cells., Soc. Neurosci. Abstr., 8, 252
  6. Brown, 1988, Acetylcholine modulates resting K-current through a pertussis-toxin-resistant G-protein in hippocampal neurons., Soc. Neurosci. Abstr., 14, 1328
  7. Docherty, 1983, Excitatory effects of dendrotoxin on the hippocampus in vitro., J. Physiol. (Lond.), 336, 58P
  8. Dryer, 1988, A sodium-activated potassium current in cultured brain stem neurones., J. Physiol. (Lond.), 398, 12P
  9. Dryer, 1988, A sodium-activated potassium current in brain stem neurons., Biophys. J., 53, 552a
  10. Dubois, 1986, Toxin I from the snake Dendroaspis polylepis polylepis: a highly specific blocker of one type of potassum channel in myelinated nerve fiber., Brain Res., 377, 374, 10.1016/0006-8993(86)90884-X · DOI
  11. Edwards, 1988, The patch clamp technique applied to synaptically connected cells in mammalian brain slices. GABA receptor mediated synaptic and single channel currents measured in rat hippocampal granule cells., Eur. J. Neurosci., 342
  12. ffrench-Mullen, 1988, Phencyclidine: blockade of K+ channels and NMDA receptor-coupled cation channels occurs at distinct sites in hippocampal neurons., Biophys. J., 53, 544a
  13. Gruner, 1989, Three kinetic components to M-currents in bullfrog sympathetic neurons., Soc. Neurosci. Abstr., 15, 990
  14. Jones, 1987, GTP-y-S inhibitis the M-current of dissociated bullfrog sympathetic neurons., Soc. Neurosci. Abstr., 13, 532
  15. Krnjević, 1988, Are there hippocampal ATP-sensitive K channels that are activated by anoxia?, Pflüg. Arch., 211, R145
  16. Lancaster, 1986, Charybdotoxin selectively blocks a fast, Ca-dependent afterhyperpolarization (AHP) in hippocampal pyramidal cells., Soc. Neurosci. Abstr., 12, 560
  17. Lancaster, 1987, Small conductance Ca2+-activated K+ channels in hippocampal neurons., Soc. Neurosci. Abstr., 13, 176
  18. Lopez, 1987, Possible involvement of GTP-binding proteins in coupling of muscarinic receptors to M-current in bullfrog ganglion cells., Soc. Neurosci. Abstr., 13, 533
  19. Masukawa, 1987, Regional distribution of voltage-dependent single channel conductances in cultured hippocampal neurons from the rat., Soc. Neurosci. Abstr., 13, 1442
  20. Owen, 1987, Three types of inward rectifier currents in cultured hippocampal neurones., Neurosci. Lett., 518
  21. Owen, 1988, Three types of chloride channels in cultured rat hippocampal neurones., Soc. Neurosci. Abstr., 14, 1203
  22. Pennefather, 1986, The rate of activation of M current at positive potentials in bullfrog sympathetic ganglion cells., Biophys. J., 49, 166a
  23. Pfaffinger, 1988, M-current suppression by agonists: the role of the phospholipase C pathway., Biophys. J., 53, 637a
  24. Spain, 1988, Repetitive firing patterns in cat neocortical neurons depend on preceding subthreshold membrane potential., Soc. Neurosci. Abstr., 14, 298
  25. Storm, 1984, Two components of slow prepotentials in CA1 hippocampal pyramidal cells., Acta Physiol. Scand., 120, 15A
  26. Storm, 1985, Calcium-dependent spike repolarization, and three kinds of afterhyperpolarization (AHP) in hippocampal pyramidal cells., Soc. Neurosci. Abstr., 11, 1183
  27. Storm, 1986, A-current and Ca-dependent transient outward current control the intial repetitive firing in hippocampal neurons., Biophys. J., 49, 369a
  28. Storm, 1987, Potassium currents underlying afterhyperpolarizations (AHPs) and spike repolarization in rat hippocampal pyramidal cells (CA1)., Neurosci. Abstr., 13, 176
  29. Storm, 1988, Four voltage-dependent potassium currents in adult hippocampal pyramidal cells., Biophys. J., 53, 148a
  30. Storm, 1988, Evidence that two 4-aminopyridine (4-AP)-sensitive potassium currents, IA and ID, contribute to spike repolarization in rat hippocampal pyramidal cells., Eur. J. Neurosci., 42
  31. Storm, 1987, A passive component of the afterdepolarization (ADP) in rat hippocampal pyramidal cells., Biophys. J., 51, 65a
  32. Storm, 1989, Evidence that a barium-sensitive potassium current contributes to the resting potential and spike repolarization in rat hippocampal neurons., Soc. Neurosci. Abstr., 15, 77
  33. Williamson, 1987, A transient Ca-dependent K potential follows a brief spike train in hippocampus., Soc. Neurosci. Abstr., 13, 156

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Metadata

Authors
Storm, J. F.
Corresponding author
Storm, Johan F.
ORCID
Storm, Johan F.
Venue
Progress in Brain Research
Publisher
Elsevier
Published
1990
Volume
83
Pages
161-187
ISSN
0079-6123 (ISSN-L)
DOI
10.1016/s0079-6123(08)61248-0
OpenAlex
W1570612396
Cited by
743
References
202
Citations by year
2026: 6 · 2025: 5 · 2024: 16 · 2023: 7 · 2022: 10 · 2021: 11 · 2020: 12 · 2019: 16 · 2018: 14 · 2017: 6 · 2016: 13 · 2015: 11 · 2014: 23 · 2013: 24 · 2012: 14
FWCI
12.29
Type
book chapter
Language
en
Open access
closed
Locations
  • Progress in brain research (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • Norges Forskningsråd
  • Medical Research Council
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac electrophysiology and arrhythmias
Keywords
potassium currents, hippocampal pyramidal neurons, CA1, CA3, transient outward potassium current, calcium-activated potassium current, afterhyperpolarization, neural adaptation, acetylcholine, muscarinic receptors, somatostatin, repetitive firing, neural integration
MeSH terms
Animals, Guinea Pigs, Hippocampus, Membrane Potentials, Potassium, Rats, In Vitro Techniques

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