Differential Interactions of Sex Pheromone and Plant Odour in the Olfactory Pathway of a Male Moth

et al. (2012) Differential Interactions of Sex Pheromone and Plant Odour in the Olfactory Pathway of a Male Moth. PLoS ONE 7(3): e33159. doi:10.1371/journal.pone.0033159 Differential Interactions of Sex Pheromone and Plant Odour in the Olfactory Pathway of a Male Moth Nina Deisig 0 1 Jan Kropf 0 1 Simon Vitecek 0 1 Delphine Pevergne 0 1 Angela Rouyar 0 1 Jean-Christophe 0 1 Sandoz 0 1 Philippe Lucas 0 1 Christophe Gadenne 0 1 Sylvia Anton 0 1 Romina Barrozo 0 1 Matthieu Louis, Center for Genomic Regulation, Spain 0 a Current address: Behavioral Physiology and Sociobiology, University of Wuerzburg, Wuerzburg, Germany b Current address: Laboratory of Evolution , Genomes, Speciation , CNRS UPR 9034, Gif-sur-Yvette, France c Current address: Laboratoire Re cepteurs et Canaux Ioniques Membranaires, UPRES-EA 2647 USC INRA 1330, Universite d'Angers, Angers, France d Current address: Department of Biodiversity and Experimental Biology, FCEyN, University of Buenos Aires , Ciudad Universitaria, Buenos Aires , Argentina 1 1 UMR 1272 Physiologie de l'Insecte: Signalisation et Communication, INRA, Route de Saint-Cyr , Versailles, France , Universite Pierre et Marie Curie , 7 Quai Saint Bernard, Paris, France, 2 CNRS, UMR 5169 , Universite Paul Sabatier, Research Center for Animal Cognition , Toulouse , France Most animals rely on olfaction to find sexual partners, food or a habitat. The olfactory system faces the challenge of extracting meaningful information from a noisy odorous environment. In most moth species, males respond to sex pheromone emitted by females in an environment with abundant plant volatiles. Plant odours could either facilitate the localization of females (females calling on host plants), mask the female pheromone or they could be neutral without any effect on the pheromone. Here we studied how mixtures of a behaviourally-attractive floral odour, heptanal, and the sex pheromone are encoded at different levels of the olfactory pathway in males of the noctuid moth Agrotis ipsilon. In addition, we asked how interactions between the two odorants change as a function of the males' mating status. We investigated mixture detection in both the pheromone-specific and in the general odorant pathway. We used a) recordings from individual sensilla to study responses of olfactory receptor neurons, b) in vivo calcium imaging with a bath-applied dye to characterize the global input response in the primary olfactory centre, the antennal lobe and c) intracellular recordings of antennal lobe output neurons, projection neurons, in virgin and newly-mated males. Our results show that heptanal reduces pheromone sensitivity at the peripheral and central olfactory level independently of the mating status. Contrarily, heptanal-responding olfactory receptor neurons are not influenced by pheromone in a mixture, although some post-mating modulation occurs at the input of the sexually isomorphic ordinary glomeruli, where general odours are processed within the antennal lobe. The results are discussed in the context of mate localization. - . These authors contributed equally to this work. Most animals rely on olfactory cues to find their mating partner, food and shelter. For reproduction, the olfactory system faces the challenge of extracting salient odorant information emitted by sexual partners (pheromones) from an abundant background of general odorants. In the moths natural environment, males are attracted by a female-emitted sex pheromone blend (containing several components), and could either ignore or use background general odours as additional cues to locate a potential mate. Indeed, in several moth species, the behavioural response of males to sex pheromones is enhanced by host plant odours [1]. This seems to reflect a strategy to optimize mating, since females often call when situated on a host plant. The simultaneous presence of a pheromone and a plant odour may result in interactions between these odour classes, which can either lead to suppression (masking) or enhancing (synergy) of the response to one odour by the other. Detection of sex pheromones and general odours in animals is usually accomplished by two distinct olfactory pathways. In mammals, pheromone information is mainly processed by the accessory olfactory system, while the main olfactory system codes more general odours, e.g. food or shelter related odours [2]. In insects, such as moths, pheromone information is transmitted by specialized olfactory receptor neurons (ORNs) to the macroglomerular complex (MGC), a male-specific part of the primary olfactory processing centre, the antennal lobe (AL). Plant odour information is transferred by general ORNs to sexually isomorphic ordinary glomeruli (OG) [3]. Whereas in mammals both subsystems seem to participate in mate recognition [2], very little is known about how both sub-systems contribute to pheromone and plant odour recognition in moths. Pheromone-plant odour interactions may occur at different processing levels in the olfactory system. Olfactory mixture perception has already been studied at the peripheral level (vertebrates: e.g. [4,5]; invertebrates: e.g. [611]) and at the central level (vertebrates: e.g. [12,13]; invertebrates: e.g. [1418]). However, most of these studies investigated coding of mixtures composed of odorants from the same contextual origin (i.e. mixtures of either general odorants or single pheromone components). Very few studies have focussed on the coding of mixtures of pheromones (reproduction cues) and general odours (i.e. food, predator, social, host cues) in the central nervous system (e.g. vertebrates [19,20], and invertebrates [21,22]). As for vertebrates, the coding of these two types of odour cues was generally believed to occur in two separate pathways of the insect olfactory system. However, unusual representations of plant odours and pheromones were recently observed in tortricid moths: in Grapholita molesta, pheromone processing seems to occur in OG rather than in the MGC [23] and in Cydia pomonella there is no clear segregation between the pheromone and the general odour sub-systems in the AL, both odour classes being represented in both the MGC and in OG [24]. In males of the noctuid moth Agrotis ipsilon, a transient postmating inhibition of behavioural and central nervous responses to sex pheromone has been observed [21,25]. This plasticity prevents newly-mated males from orientating towards females and mating until the next night, allowing them to refill their sex glands for a potential new ejaculate. After mating, a strong decrease in sex pheromone sensitivity is observed up to the MGC [26]. Plant-odour processing, on the other hand, is much less affected by mating status. Behavioural responses to plant odours, such as a linden flower extract, observed in wind tunnel experiments remain stable after mating. Further, response thresholds of peripheral and central OG neurons to heptanal, a behaviourally attractive comp (...truncated)