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

Abstract

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.

Plant odour stimuli reshape pheromonal representation in neurons of the antennal lobe macroglomerular complex of a male moth

“…Optical imaging studies have also shown that the input of pheromone information to the AL is reduced when adding plant odours (Deisig et al, 2012). Although plant odours down-modulate pheromone detection at the peripheral level (Deisig et al, 2012), the response in most MGC neurons to heptanal observed in this study indicates that input through independent information channels reaches the AL, and that the AL network must be involved in the mixture interactions observed in AL output neurons. We assume that the suppression of the pheromone response upon stimulation with the mixture in the AL is caused by GABAergic inhibition via LNs, but the precise mechanisms still need to be unveiled.…”

“…Evidence for inhibitory effects of plant compounds on pheromone responses in antennal sensilla responding exclusively to pheromone compounds has been found in several moth species (e.g. Pophof and van der Goes van Naters, 2002;Party et al, 2009), including A. ipsilon, using single sensillum recordings (Deisig et al, 2012). Optical imaging studies have also shown that the input of pheromone information to the AL is reduced when adding plant odours (Deisig et al, 2012).…”

“…Pophof and van der Goes van Naters, 2002;Party et al, 2009), including A. ipsilon, using single sensillum recordings (Deisig et al, 2012). Optical imaging studies have also shown that the input of pheromone information to the AL is reduced when adding plant odours (Deisig et al, 2012). Although plant odours down-modulate pheromone detection at the peripheral level (Deisig et al, 2012), the response in most MGC neurons to heptanal observed in this study indicates that input through independent information channels reaches the AL, and that the AL network must be involved in the mixture interactions observed in AL output neurons.…”

Compound valence is conserved in binary odor mixtures in Drosophila melanogaster

“…Components of odor mixtures have been shown to influence each other's reception on the level of OSNs (Deisig et al, 2012;Hillier and Vickers, 2011;Münch et al, 2013;Pregitzer et al, 2012;Schuckel et al, 2009;Su et al, 2011;Su et al, 2012). Furthermore, olfactory information is significantly modulated by a dense network of local neurons in the first olfactory center of the insect brain, the antennal lobe (AL) (reviewed in Galizia and Rössler, 2010;Masse et al, 2009;Wilson, 2013;Wilson and Mainen, 2006).…”

Concurrent modulation of neuronal and behavioural olfactory responses to sex and host plant cues in a male moth

“…Mating-induced downregulation of male attraction to sex pheromone has been investigated in the parasitoid wasp, Spalangia endius, and the noctuid moth, Agrotis ipsilon [6,7]. In A. ipsilon males, this behavioural inhibition is correlated with a decreased sensitivity of antennal lobe (AL) neurons to the conspecific sex pheromone [7][8][9] and an increased response to a plant odour [9,10]. Available data also suggest that mating-induced changes in the olfactory response are distinct for pheromone and non-pheromone coding pathways [9].…”