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Small-Conductance Ca²⁺-Dependent K⁺ Channels Are the Target of Spike-Induced Ca²⁺ Release in a Feedback Regulation of Pyramidal Cell Excitability

Departments of ¹Geriatric Medicine, ²Cardiovascular Medicine, and ³Integrative Brain Science, Kyoto University Graduate School of Medicine, Kyoto 606-8501, Japan

Submitted 30 October 2003; accepted in final form 17 December 2003

Cooperative regulation of inosiol-1,4,5-trisphosphate receptors (IP₃Rs) by Ca²⁺ and IP₃ has been increasingly recognized, although its functional significance is not clear. The present experiments first confirmed that depolarization-induced Ca²⁺ influx triggers an outward current in visual cortex pyramidal cells in normal medium, which was mediated by apamin-sensitive, small-conductance Ca²⁺-dependent K⁺ channels (SK channels). With IP₃-mobilizing neurotransmitters bath-applied, a delayed outward current was evoked in addition to the initial outward current and was mediated again by SK channels. Calcium turnover underlying this biphasic SK channel activation was investigated. By voltage-clamp recording, Ca²⁺ influx through voltage-dependent Ca²⁺ channels (VDCCs) was shown to be responsible for activating the initial SK current, whereas the IP₃R blocker heparin abolished the delayed component. High-speed Ca²⁺ imaging revealed that a biphasic Ca²⁺ elevation indeed underlays this dual activation of SK channels. The first Ca²⁺ elevation originated from VDCCs, whereas the delayed phase was attributed to calcium release from IP₃Rs. Such enhanced SK currents, activated dually by incoming and released calcium, were shown to intensify spike-frequency adaptation. We propose that spike-induced calcium release from IP₃Rs leads to SK channel activation, thereby fine tuning membrane excitability in central neurons.

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