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The Journal of Neuroscience, May 1, 2003, 23(9):3639

Calcium Influx via L- and N-Type Calcium Channels Activates a Transient Large-Conductance Ca²⁺-Activated K⁺ Current in Mouse Neocortical Pyramidal Neurons

Xiaolu Sun^{1, 3}, Xiang Q. Gu^{1, 3}, and Gabriel G. Haddad^{1, 2, 3, 4}

Departments of ¹ Pediatrics (Section of Respiratory Medicine) and ² Cellular and Molecular Physiology, Yale University School of Medicine, New Haven, Connecticut 06520, and Departments of ³ Pediatrics (Section of Respiratory Medicine) and ⁴ Neuroscience, Albert Einstein College of Medicine, Bronx, New York 10461

Ca²⁺-activated K⁺ currents and their Ca²⁺ sources through high-threshold voltage-activated Ca²⁺ channels were studied using whole-cell patch-clamp recordings from freshly dissociated mouse neocortical pyramidal neurons. In the presence of 4-aminopyridine, depolarizing pulses evoked transient outward currents and several components of sustained currents in a subgroup of cells. The fast transient current and a component of the sustained currents were Ca²⁺ dependent and sensitive to charybdotoxin and iberiotoxin but not to apamin, suggesting that they were mediated by large-conductance Ca²⁺-activated K⁺ (BK) channels. Thus, mouse neocortical neurons contain both inactivating and noninactivating populations of BK channels. Blockade of either L-type Ca²⁺ channels by nifedipine or N-type Ca²⁺ channels by -conotoxin GVIA reduced the fast transient BK current. These data suggest that the transient BK current is activated by Ca²⁺ entry through both N- and L-type Ca²⁺ channels. The physiological role of the fast transient BK current was also examined using current-clamp techniques. Iberiotoxin broadened action potentials (APs), indicating a role of BK current in AP repolarization. Similarly, both the extracellular Ca²⁺ channel blocker Cd²⁺ and the intracellular Ca²⁺ chelator BAPTA blocked the transient component of the outward current and broadened APs in a subgroup of cells. Our results indicate that the outward current in pyramidal mouse neurons is composed of multiple components. A fast transient BK current is activated by Ca²⁺ entry through high-threshold voltage-activated Ca²⁺ channels (L- and N-type), and together with other voltage-gated K⁺ currents, this transient BK current plays a role in AP repolarization.

Key words: Ca²⁺ channels; Ca²⁺-activated K⁺ channels; BK channels; neocortical pyramidal neurons; iberiotoxin; charybdotoxin; nifedipine; -conotoxin GVIA; BAPTA

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Copyright © 2003 Society for Neuroscience  0270-6474/03/2393639-10$05.00/0

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