Many animals utilize sex pheromone for detecting conspecific mates. Sex pheromone is usually a blend of two or more components with similar chemical compositions. The pheromone receivers are equipped with localized olfactory glomeruli in the first-order olfactory center for specifically processing these pheromone components. In the American cockroach, Periplaneta americana, either periplanone A or periplanone B emitted by virgin females evokes identical sexual behaviors in males. The antennal lobes of adult male cockroaches have enlarged, neighboring A- and B-glomeruli, which preferentially process periplanones A and B, respectively. By using intracellular recording and staining of neurons in the same preparations, we provide the first detailed projection maps of output neurons (projection neurons; PNs) from the A-glomerulus and the B-glomerulus. Although both PNs project to the mushroom body calyces and the lateral horn, their proximities in the two centers largely differ: in the calyces, the axon terminals of the A-PN were located more predominantly in the periphery compared with those of the B-PN, whereas axon terminals of both PNs were highly congruent in the anteromedial region of the lateral horn. These results suggest that pheromone component signals are dispersed in the mushroom body for specific odor discrimination but are integrated in the lateral horn for generating behaviors common to the pheromone components. Stimulation of the ipsilateral antenna with various odors showed that the odor specificity of A-PN is higher than that of B-PN. The different developmental lineages of A- and B-PNs suggested by these results are discussed. J. Comp. Neurol. 520:3428–3445, 2012. © 2012 Wiley Periodicals, Inc.