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Peptidergic Counter-Regulation of Ca²⁺- and Na⁺-Dependent K⁺ Currents Modulates the Shape of Action Potentials in Neurosecretory Insect Neurons

¹Saxon Academy of Sciences, Department of Neurohormones, Jena; ²Institute of Physiology, Department of Neuroendocrinology, Philipps University Marburg, Marburg; and ³Max-Planck Institute of Neurobiology, Department of Systems and Computational Neurobiology, Martinsried, Germany

Submitted 30 August 2005; accepted in final form 18 September 2005

Influx of Ca²⁺ and Na⁺ ions during an action potential can strongly affect the repolarization and the fast afterhyperpolarization (fAHP) if a neuron expresses Ca²⁺- and Na⁺-dependent K⁺ currents (K_Ca and K_Na). This applies to cockroach abdominal dorsal unpaired median neurons (DUMs). Here the rapid activation of K_Ca depends mainly on the P/Q-type Ca²⁺ current. Adipokinetic hormones (AKHs)—insect counterparts to mammalian glucagon—mobilize energy reserves but also modulate neuronal activity and lead to enhanced locomotor activity. Cockroach AKH I accelerates spiking and enhances the fAHP of octopaminergic DUM neurons, and it is generally held that enhanced release of the biogenic amine from these and other neurons may lead to general arousal. AKH I modulates the voltage-gated Na⁺ and P/Q-type Ca²⁺ current and the background Ca²⁺ current. Upregulation of P/Q-type Ca²⁺ current increases the K_Ca current, whereas enhanced inactivation of Na⁺ current decreases the K_Na current. We quantified the hormone-induced changes in ion currents in terms of Hodgkin-Huxley models and simulated the resulting activity of DUM neurons. Upregulation of P/Q-type Ca²⁺ and K_Ca current enhanced the hyperpolarization but had a weak effect on spiking. Downregulation of Na⁺ and K_Na current decreased hyperpolarization and slightly accelerated spiking. Superposition of these modulations produced an increase in fAHP while the spike frequency remained unchanged. Only when the upregulation of the pacemaking Ca²⁺ background current was included in the simulated modulation the model reproduced the experimentally observed AKH-I-induced changes. The possible physiological relevance of this dual effect is discussed in respect to transmitter release and synaptic integration.

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