Molecular and cellular basis of small- and intermediate-conductance, calcium-activated potassium channel function in the brain

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Abstract.

Small conductance calcium-activated potassium (SK or K _Ca2) channels link intracellular calcium transients to membrane potential changes. SK channel subtypes present different pharmacology and distribution in the nervous system. The selective blocker apamin, SK enhancers and mice lacking specific SK channel subunits have revealed multifaceted functions of these channels in neurons, glia and cerebral blood vessels. SK channels regulate neuronal firing by contributing to the afterhyperpolarization following action potentials and mediating I _AHP, and partake in a calcium-mediated feedback loop with NMDA receptors, controlling the threshold for induction of hippocampal long-term potentiation. The function of distinct SK channel subtypes in different neurons often results from their specific coupling to different calcium sources. The prominent role of SK channels in the modulation of excitability and synaptic function of limbic, dopaminergic and cerebellar neurons hints at their possible involvement in neuronal dysfunction, either as part of the causal mechanism or as potential therapeutic targets.

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Most cited references 252

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Long-term potentiation and memory.

M A Lynch (2004)

One of the most significant challenges in neuroscience is to identify the cellular and molecular processes that underlie learning and memory formation. The past decade has seen remarkable progress in understanding changes that accompany certain forms of acquisition and recall, particularly those forms which require activation of afferent pathways in the hippocampus. This progress can be attributed to a number of factors including well-characterized animal models, well-defined probes for analysis of cell signaling events and changes in gene transcription, and technology which has allowed gene knockout and overexpression in cells and animals. Of the several animal models used in identifying the changes which accompany plasticity in synaptic connections, long-term potentiation (LTP) has received most attention, and although it is not yet clear whether the changes that underlie maintenance of LTP also underlie memory consolidation, significant advances have been made in understanding cell signaling events that contribute to this form of synaptic plasticity. In this review, emphasis is focused on analysis of changes that occur after learning, especially spatial learning, and LTP and the value of assessing these changes in parallel is discussed. The effect of different stressors on spatial learning/memory and LTP is emphasized, and the review concludes with a brief analysis of the contribution of studies, in which transgenic animals were used, to the literature on memory/learning and LTP.

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The control of firing pattern in nigral dopamine neurons: burst firing.

AA Grace, BS Bunney (1984)

In addition to firing in a single spiking mode, dopamine (DA) cells have been observed to fire in a bursting pattern with consecutive spikes in a burst displaying progressively decreasing amplitude and increasing duration. In vivo intracellular recording demonstrated the bursts to typically ride on a depolarizing wave (5 to 15 mV amplitude). Although the burst-firing frequency of DA cells showed little correlation with the base line firing rate, increases in firing rate were usually associated with an increase in burst firing. Increases in burst firing could also be elicited by intracellular calcium injection and could be prevented by intracellular injection of EGTA, suggesting a calcium involvement in bursting. Blockade of potassium conductances with extracellular iontophoresis of barium or intracellular injection of tetraethylammonium bromide could also trigger an increased degree of burst firing in DA cells. These data suggest that the increased calcium influx accompanying an increased firing rate triggers burst firing, possibly by inactivating a potassium conductance. A switch from a single spiking mode to a burst-firing mode may be important in modulating striatal DA release, as shown for burst firing in other preparations.

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SK channels and NMDA receptors form a Ca2+-mediated feedback loop in dendritic spines.

Thu Ngo-Anh, Brenda L. Bloodgood, Michael Lin … (2005)

Small-conductance Ca(2+)-activated K(+) channels (SK channels) influence the induction of synaptic plasticity at hippocampal CA3-CA1 synapses. We find that in mice, SK channels are localized to dendritic spines, and their activity reduces the amplitude of evoked synaptic potentials in an NMDA receptor (NMDAR)-dependent manner. Using combined two-photon laser scanning microscopy and two-photon laser uncaging of glutamate, we show that SK channels regulate NMDAR-dependent Ca(2+) influx within individual spines. SK channels are tightly coupled to synaptically activated Ca(2+) sources, and their activity reduces the amplitude of NMDAR-dependent Ca(2+) transients. These effects are mediated by a feedback loop within the spine head; during an excitatory postsynaptic potential (EPSP), Ca(2+) influx opens SK channels that provide a local shunting current to reduce the EPSP and promote rapid Mg(2+) block of the NMDAR. Thus, blocking SK channels facilitates the induction of long-term potentiation by enhancing NMDAR-dependent Ca(2+) signals within dendritic spines.

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Author and article information

Contributors

: p.pedarzani@ucl.ac.uk

Journal

Journal ID (nlm-ta): Cell Mol Life Sci

Title: Cellular and Molecular Life Sciences

Publisher: Birkhäuser-Verlag (Basel )

ISSN (Print): 1420-682X

ISSN (Electronic): 1420-9071

Publication date (Electronic): 4 July 2008

Publication date (Print): October 2008

Volume: 65

Issue: 20

Pages: 3196-3217

Affiliations

Research Department of Neuroscience, Physiology and Pharmacology, University College London, Gower Street, London, WC1E 6BT UK

Article

Publisher ID: 8216

DOI: 10.1007/s00018-008-8216-x

PMC ID: 2798969

PubMed ID: 18597044

SO-VID: c693ea63-a192-42e4-a52c-6d9aa458b1e1

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ScienceOpen disciplines: Molecular biology

Keywords: iahp,pacemaking neuron,afterhyperpolarization,calcium-activated potassium channel,glial cell,cerebral blood vessel endothelium,long-term potentiation,apamin

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ScienceOpen disciplines: Molecular biology

Keywords: iahp, pacemaking neuron, afterhyperpolarization, calcium-activated potassium channel, glial cell, cerebral blood vessel endothelium, long-term potentiation, apamin

Molecular and cellular basis of small- and intermediate-conductance, calcium-activated potassium channel function in the brain

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Higher order chromatin architecture

Most cited references 252

Long-term potentiation and memory.

The control of firing pattern in nigral dopamine neurons: burst firing.

SK channels and NMDA receptors form a Ca2+-mediated feedback loop in dendritic spines.

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