Moths use a sophisticated olfactory navigation strategy for resource localization. Here we investigate the neuronal circuits involved in sensory processing to generate locomotor commands for pheromone-source orientation in the moth. We identify a candidate pathway for pheromone processing in the protocerebrum using a mass-staining technique. Our intracellular recordings of pheromone responsiveness detect four major circuits, including a newly identified unstructured neuropil, the superior medial protocerebrum, which supplies output to the lateral accessory lobe (LAL), the premotor centre for walking commands. Interneurons innervating the lower division of the LAL elicited longer responses than those innervating the upper division. Descending interneurons innervating the lower division of the LAL showed a state-dependent flip-flop response. In contrast, input from other visual areas in the protocerebrum mostly converge onto the upper division of the LAL. These results reveal the basic organization of the LAL: the upper division is identified as a protocerebral hub that receives inputs from various areas, while the lower division generates long-lasting activity for locomotor command.