Calcium-activated potassium (K+) channels are distributed throughout the central nervous system as well as many other peripheral tissues and comprise three distinct classes of K+ channels: small conductance (SK), intermediate conductance, and large conductance. This update focuses on SK channels. Increases in cytosolic calcium in response to depolarization activate SK channels. Activation of these channels decreases neuronal excitability. In this review, the authors discuss the role of SK channels in the induction of synaptic plasticity and their influence on learning and memory. A testable model that synthesizes the current literature is offered, suggesting that SK channels represent an important regulator of synaptic plasticity and memory.
Get full access to this article
View all access options for this article.
References
1.
Artola A, Singer W. 1993. Long-term depression of excitatory synaptic transmission and its relationship to long-term potentiation. Trends Neurosci16:480–487.
2.
Behnisch T, Reymann KG. 1998. Inhibition of apamin-sensitive calcium dependent potassium channels facilitate the induction of longterm potentiation in the CA1 region of rat hippocampus in vitro. Neurosci Lett253:91–94.
3.
Bond CT, Sprengel R, Bissonnette JM, Kaufmann WA, Pribnow D, Neelands T, and others. 2000. Respiration and parturition affected by conditional overexpression of the Ca2+-activated K+ channel subunit, SK3. Science289:1942–1946.
4.
Cangiano L, Wallen P, Grillner S. 2002. Role of apamin-sensitive K+(ca) channels for reticulospinal synaptic transmission to motoneuron and for the afterhyperpolarization. J Neurophysiol88:289–299.
5.
Clark RE, Zola SM, Squire LR. 2000. Impaired recognition memory in rats after damage to the hippocampus. J Neurosci20:8853–8860.
6.
Deschaux O, Bizot JC. 1997. Effect of apamin, a selective blocker of Ca2+-activated K+-channel, on habituation and passive avoidance responses in rats. Neurosci Lett227:57–60.
7.
Deschaux O, Bizot JC, Goyffon M. 1997. Apamin improves learning in an object recognition task in rats. Neurosci Lett222:159–162.
8.
Foster TC. 1999. Involvement of hippocampal synaptic plasticity in age-related memory decline. Brain Res Rev30:236–249.
9.
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. Behav Brain Res121:81–93.
10.
Ghelardini C, Galeotti N, Bartolini A. 1998. Influence of potassium channel modulators on cognitive processes in mice. Br J Pharmacol123:1079–1084.
11.
Grunnet M, Jensen BS, Olesen SP, Klaerke DA. 2001. Apamin interacts with all subtypes of cloned small-conductance Ca2+-activated K+ channels. Pflugers Arch441:544–550.
12.
Ikonen S, Riekkinen P, Jr. 1999. Effects of apamin on memory processing of hippocampal-lesioned mice. Eur J Pharmacol382: 151–156.
13.
Ikonen S, Schmidt B, Riekkinen P, Jr. 1998.Apamin improves spatial navigation in medial septal-lesioned mice. Eur J Pharmacol347:13–21.
14.
Inan SY, Aksu F, Baysal F. 2000. The effects of some K(+) channel blockers on scopolamine- or electroconvulsive shock–induced amnesia in mice. Eur J Pharmacol407:159–164.
15.
Kohler M, Hirschberg B, Bond CT, Kinzie JM, Marrion NV, Maylie J, and others. 1996. Small-conductance, calcium-activated potassium channels from mammalian brain. Science273:1709–1714.
16.
Malenka RC, Lancaster B, Zucker RS. 1992. Temporal limits on the rise in postsynaptic calcium required for the induction of long-term potentiation. Neuron9:121–128.
17.
Malenka RC, Nicoll RA. 1993. NMDA-receptor-dependent synaptic plasticity: multiple forms and mechanisms. Trends Neurosci16: 521–527.
18.
Mayer ML, Westbrook GL, Vyklicky L, Jr. 1988. Sites of antagonist action on N-methyl-D-aspartic acid receptors studied using fluctuation analysis and a rapid perfusion technique. J Neurophysiol60:645–663.
19.
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 Res551: 322–326.
20.
Morris RGM, Garrud P, Rawlins JNP, O’Keefe J. 1982. Place navigation impaired in rats with hippocampal lesions. Nature297:681–683.
21.
Mulkey RM, Malenka RC. 1992. Mechanisms underlying induction of homosynaptic long-term depression in area CA1 of the hippocampus. Neuron9:967–975.
22.
Norris CM, Halpain S, Foster TC. 1998. Reversal of age-related alterations in synaptic plasticity by blockade of L-type Ca2+ channels. J Neurosci18:3171–3179.
23.
Sailer CA, Hu H, Kaufmann WA, Trieb M, Schwarzer C, Storm JF, and others. 2002. Regional differences in distribution and functional expression of small-conductance Ca2+-activated K+ channels in rat brain. J Neurosci22:9698–9707.
24.
Stackman RW, Hammond RS, Linardatos E, Gerlach A, Maylie J,Adelman JP, and others. 2002. Small conductance Ca2+-activated K+ channels modulate synaptic plasticity and memory encoding. J Neurosci22:10163–71.
25.
Stocker M, Krause M, Pedarzani P. 1999. An apamin-sensitive Ca2+activated K+ current in hippocampal pyramidal neurons. Proc Natl Acad Sci USA96:4662–4667.
26.
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. Mol Cell Neurosci15:476–493.
Tacconi S, Carletti R, Bunnemann B, Plumpton C, Merlo Pich E, Terstappen GC. 2001. Distribution of the messenger RNA for the small conductance calcium-activated potassium channel SK3 in the adult rat brain and correlation with immunoreactivity. Neuroscience102:209–215.
29.
van der Staay FJ, Fanelli RJ, Blokland A, Schmidt BH. 1999. Behavioral effects of apamin, a selective inhibitor of the SK(Ca)-channel, in mice and rats. Neurosci Biobehav Rev23:1087–1110.
30.
Womack MD, Khodakhah K. 2003. Somatic and dendritic small-conductance calcium-activated potassium channels regulate the output of cerebellar Purkinje neurons. J Neurosci23:2600–2607.
