Adipokinetic Hormone (AKH) peptides in insects serve the endocrine control of energy supply. They produce, however, also neuronal, vegetative and motor effects, suggesting that AKHs orchestrate adaptive behavior by multiple actions. We have cloned, for Periplaneta americana, the AKH receptor to determine its localization and, based on current measurements in neurons and heterologous expression systems, the mechanisms of AKH actions. Apart from fat body various neurons express the AKH receptor, among them abdominal dorsal unpaired median (DUM) neurons, which release the biogenic amine octopamine. They are part of the arousal system and are involved in the control of circulation and respiration. Both the two Periplaneta AKHs activate the G_s pathway, and AKH I also potently activates G_q. AKH I and - with much less efficacy - AKH II accelerate spiking of DUM neurons via an increase of the pacemaking Ca²⁺ current. Since the AKHs are released from the corpora cardiaca into the hemolymph, they must penetrate the blood brain barrier for acting on neurons. That this happens was demonstrated electrophysiologically by applying AKH I to an intact ganglion. Systemically injected AKH I stimulates locomotion potently in striking contrast to AKH II. This behavioral difference can be traced back conclusively to the different effectiveness of the AKHs on the level of G-proteins. Our findings also demonstrate that AKHs act via the same basic mechanisms on neuronal and non-neuronal cells, and they support an integration of metabolic and neuronal effects in homoeostatic mechanisms.