The lateral accessory lobe (LAL) and the ventral protocerebrum (VPC) are a pair of symmetrical neural structures in the insect brain. The LAL-VPC is regarded as the major target of olfactory responding neurons as well as the control center for olfactory-evoked sequential zigzag turns. Previous studies of the silkworm moth Bombyx mori showed that these turns are controlled by long-lasting anti-phasic activities of the flip-flopping descending neurons with dendrites in the LAL-VPC. To elucidate the neural mechanisms underlying the generation of this alternating activity between the LAL-VPC units of both hemispheres, we first analyzed the detailed neural architecture of the LAL-VPC and identified five subregions. We then investigated the morphology and physiological responses of the LAL-VPC neurons by intracellular recording and staining and morphologically identified three types of bilateral neurons and three types of unilateral neurons. Bilateral neurons showed either brief or cyclic long-lasting responses. At least some neurons of the latter type produced γ-aminobutyric acid (GABA). Unilateral neurons linking the LAL and VPC, in contrast, showed long-lasting or quick alternating activity. Timing analysis of the activity onset of each neural type suggests that quick reciprocal neural transmission between unilateral neurons would be responsible for the generation of long-lasting activity in one LAL-VPC unit, which lasts for up to a few seconds. Reciprocal inhibition and excitation by the bilateral neurons with long-lasting activities would mediate the alternating long-lasting activity between both LAL-VPC units, which might last for up to 20 seconds. J. Comp. Neurol. 518:366–388, 2010. © 2009 Wiley-Liss, Inc.