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The Journal of Neuroscience, November 2, 2005, 25(44):10230-10238; doi:10.1523/JNEUROSCI.2734-05.2005

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Behavioral/Systems/Cognitive
Control of Spontaneous Firing Patterns by the Selective Coupling of Calcium Currents to Calcium-Activated Potassium Currents in Striatal Cholinergic Interneurons

Joshua A. Goldberg and Charles J. Wilson

Department of Biology, University of Texas at San Antonio, San Antonio, Texas 78249

The spontaneous firing patterns of striatal cholinergic interneurons are sculpted by potassium currents that give rise to prominent afterhyperpolarizations (AHPs). Large-conductance calcium-activated potassium (BK) channel currents contribute to action potential (AP) repolarization; small-conductance calcium-activated potassium channel currents generate an apamin-sensitive medium AHP (mAHP) after each AP; and bursts of APs generate long-lasting slow AHPs (sAHPs) attributable to apamin-insensitive currents. Because all these currents are calcium dependent, we conducted voltage- and current-clamp whole-cell recordings while pharmacologically manipulating calcium channels of the plasma membrane and intracellular stores to determine what sources of calcium activate the currents underlying AP repolarization and the AHPs. The Ca_v2.2 (N-type) blocker -conotoxin GVIA (1 µM) was the only blocker that significantly reduced the mAHP, and it induced a transition to rhythmic bursting in one-third of the cells tested. Ca_v1 (L-type) blockers (10 µM dihydropyridines) were the only ones that significantly reduced the sAHP. When applied to cells induced to burst with apamin, dihydropyridines reduced the sAHPs and abolished bursting. Depletion of intracellular stores with 10 mM caffeine also significantly reduced the sAHP current and reversibly regularized firing. Application of 1 µM -conotoxin MVIIC (a Ca_v2.1/2.2 blocker) broadened APs but had a negligible effect on APs in cells in which BK channels were already blocked by submillimolar tetraethylammonium chloride, indicating that Ca_v2.1 (Q-type) channels provide the calcium to activate BK channels that repolarize the AP. Thus, calcium currents are selectively coupled to the calcium-dependent potassium currents underlying the AHPs, thereby creating mechanisms for control of the spontaneous firing patterns of these neurons.

Key words: tonically active neurons; high-voltage-activated calcium currents; basal ganglia; ongoing activity; potassium currents; afterhyperpolarization; calcium-induced calcium release; intracellular stores; ryanodine; xestospongin C

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Received July 1, 2005; revised September 12, 2005; accepted September 30, 2005.

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