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The Journal of Neuroscience, December 15, 2001, 21(24):9585-9597

Presynaptic Ca²⁺-Activated K⁺ Channels in Glutamatergic Hippocampal Terminals and Their Role in Spike Repolarization and Regulation of Transmitter Release

Hua Hu¹, Li-Rong Shao¹, Sorush Chavoshy², Ning Gu¹, Maria Trieb⁴, Ralf Behrens⁵, Petter Laake³, Olaf Pongs⁵, Hans Günther Knaus⁴, Ole Petter Ottersen², and Johan F. Storm¹

Institutes of ¹ Physiology, ² Anatomy and ³ Medical Statistics, University of Oslo, Blindern, N-0317 Oslo, Norway, ⁴ Institute of Biochemical Pharmacology, A-6020 Innsbruck, Austria, and ⁵ Institut für Neurale Signalverarbeitung, Zentrum für Moleculare Neurobiologie, Universität Hamburg, D-20246 Hamburg, Germany

Large-conductance Ca²⁺-activated K⁺ channels (BK, also called Maxi-K or Slo channels) are widespread in the vertebrate nervous system, but their functional roles in synaptic transmission in the mammalian brain are largely unknown. By combining electrophysiology and immunogold cytochemistry, we demonstrate the existence of functional BK channels in presynaptic terminals in the hippocampus and compare their functional roles in somata and terminals of CA3 pyramidal cells. Double-labeling immunogold analysis with BK channel and glutamate receptor antibodies indicated that BK channels are targeted to the presynaptic membrane facing the synaptic cleft in terminals of Schaffer collaterals in stratum radiatum. Whole-cell, intracellular, and field-potential recordings from CA1 pyramidal cells showed that the presynaptic BK channels are activated by calcium influx and can contribute to repolarization of the presynaptic action potential (AP) and negative feedback control of Ca²⁺ influx and transmitter release. This was observed in the presence of 4-aminopyridine (4-AP, 40-100 µM), which broadened the presynaptic compound action potential. In contrast, the presynaptic BK channels did not contribute significantly to regulation of action potentials or transmitter release under basal experimental conditions, i.e., without 4-AP, even at high stimulation frequencies. This is unlike the situation in the parent cell bodies (CA3 pyramidal cells), where BK channels contribute strongly to action potential repolarization. These results indicate that the functional role of BK channels depends on their subcellular localization.

Key words: calcium-activated potassium channels; BK channels; Slo; Maxi-K; presynaptic mechanisms; hippocampus; CA1; CA3; action potential repolarization; glutamatergic synapses; immunogold cytochemistry; BK-4; KCNMB4

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Copyright © 2001 Society for Neuroscience  0270-6474/01/21249585-13$05.00/0

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