Neurological confirmation of periplanone-D exploitation as a primary sex pheromone and counteractions of other components in the smoky brown cockroach Periplaneta fuliginosa

The smoky brown cockroach, Periplaneta fuliginosa, is a peridomestic pest inhabiting broad regions of the world from temperate to subtropical zones. In common with other related species such as the American cockroach, Periplaneta americana, female-emitted sex pheromone components, named periplanones, are known to be key volatiles that elicit long-range attraction and courtship rituals in males. How periplanones are processed in the nervous system has been entirely unexplored in P. fuliginosa. By using pheromone compounds, periplanones A, B, C, and D, as stimulants to the antenna, we identified four distinct types of interneurons (projection neurons) that relay pheromonal signals from a single olfactory glomerulus of the first-order olfactory center (antennal lobe) to higher-order centers in the ipsilateral hemibrain. All glomeruli innervated by pheromone-responsive projection neurons clustered near the antennal nerve entrance of the antennal lobe. The projection neuron with dendrites in the largest glomerulus was tuned specifically to periplanone-D, and adding other components to periplanone-D counteracted the excitation elicited by periplanone-D alone. Likewise, the projection neuron with dendrites in the second largest glomerulus and that with dendrites in a medium-sized glomerulus were tuned to periplanone-A and periplanone-B, respectively. Our results are, therefore, consistent with behavioral findings that periplanone-D alone acts as a primary sex attractant and that other components act as potential behavioral antagonists. Moreover, a comparison of the glomeruli in P. fuliginosa and P. americana suggested that there are differences in the sizes of homologous glomeruli, as well as in the ligands they process.