Abstract
During high-frequency network activities, fast-spiking, parvalbumin-expressing basket cells (PV+-BCs) generate barrages of fast synaptic inhibition to control the probability and precise timing of action potential (AP) initiation in principal neurons. Here we describe a subcellular specialization that contributes to the high speed of synaptic inhibition mediated by PV+-BCs. Mapping of hyperpolarization-activated cyclic nucleotide-gated (HCN) channel distribution in rat hippocampal PV+-BCs with subcellular patch-clamp methods revealed that functional HCN channels are exclusively expressed in axons and completely absent from somata and dendrites. HCN channels not only enhance AP initiation during sustained high-frequency firing but also speed up the propagation of AP trains in PV+-BC axons by dynamically opposing the hyperpolarization produced by Na+-K+ ATPases. Since axonal AP signaling determines the timing of synaptic communication, the axon-specific expression of HCN channels represents a specialization for PV+-BCs to operate at high speed.
Highlights
During high-frequency network activities, fast-spiking, parvalbumin-expressing basket cells (PV+-BCs) generate barrages of fast synaptic inhibition to control the probability and precise timing of action potential (AP) initiation in principal neurons
PV+-BCs can be functionally identified by the fast-spiking phenotype, in which the interneuron maintains the discharge of brief action potentials (APs) at tens to hundreds of hertz with little spike frequency adaptation[3,4,5]
The current was resistant to barium[27] but sensitive to cesium
Summary
During high-frequency network activities, fast-spiking, parvalbumin-expressing basket cells (PV+-BCs) generate barrages of fast synaptic inhibition to control the probability and precise timing of action potential (AP) initiation in principal neurons. Based on the stoichiometry of the Na+ pump[14], the combination of the fast-spiking phenotype and the dense expression of Na+-K+ ATPases is expected to generate a strong Na+ pump-mediated hyperpolarization that can potentially slow down the generation and propagation of APs in PV+-BC axons in an activity-dependent manner[15] In contrast to this prediction, PV+-BCs display little spike frequency adaptation even during sustained high-frequency firing[3]. Subcellular patchclamp recordings have revealed that the speed and reliability of AP propagation in PV+-BC axons are maintained during a long train of high-frequency APs7
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