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 genereally 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. Up-regulation of P/Q-type Ca²⁺ current increases the K,Ca current while 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. Up-regulation of P/Q-type Ca²⁺ and K,Ca current enhanced the hyperpolarization but had a weak effect on spiking. Down-regulation 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 up-regulation 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.