Fast-spiking parvalbumin-expressing basket cells (BCs) mediate fast feedforward and feedback inhibition in cortical neuronal networks. How excitatory synaptic events from different sources are converted into action potential (AP) output in these neurons has remained unknown. Furthermore, the site of AP initiation and the rules of AP backpropagation, a key factor for the induction of synaptic plasticity, have not been determined.

To address these questions, we made patch-clamp recordings from the dendrites of BCs at a distance of up to 300 mm from the soma in slices from 17- to 22-day-old rats at 22–25°C. Simultaneous recording from the soma and dendrites of BCs revealed that in 20 out of 22 recordings from the apical dendrite and 10 out of 12 recordings from the basal dendrite somatic APs preceded dendritic APs, independently of the site of current injection. Morphological analysis in the remaining recordings revealed that the reason for the "soma first" behaviour was dendritic origin of the axon rather than dendritic AP initiation. Both depolarization of distal dendrites by brief current pulses and activation of perforant path synapses consistently failed to initiate dendritic spikes. Thus, APs are invariably initiated in the BC axon. The amplitude of dendritic APs decreased as a function of distance from the soma (length constant 106 mm for the apical dendrite), suggesting that backpropagation is largely passive. To examine the distance dependence of active conductances, outside-out patches were excised from the soma, apical dendrites, and basal dendrites of BCs. Whereas the density of voltage-gated Na⁺ channels decreased sharply with distance from the soma (length constant 126 mm for the apical dendrite), the density of voltage-gated K⁺ channels was relatively constant. The outward current in dendritic outside-out patches showed fast activation, high activation threshold (~-40 mV), minimal inactivation, and high sensitivity to 1 mM external tetraethylammonium⁺, consistent with the properties of Kv3-type delayed rectifier K⁺ channels. Thus, BC dendrites show a low Na⁺ channel density, but a high density of Kv3-type K⁺ channels. To determine the functional significance of these dendritic properties for excitatory postsynaptic potential (EPSP)-AP coupling, a detailed passive cable model of a BC was endowed with different densities of Na⁺ and K⁺ conductances. With K⁺ channel-dominated dendrites, distributed excitatory synaptic input evoked single APs with high temporal precision. In contrast with both Na⁺ channel-dominated and passive dendrites, synaptic activation evoked bursts of APs with greatly reduced temporal precision.

In conclusion, APs in BCs are invariably initiated in the axon, and spread nearly passively into the dendrites of BCs. These dendritic properties maximize the reliability and temporal precision of coupling between excitatory synaptic input and AP output.