Abstract
Recognition of intra-specific olfactory signals within a complex environment of plant-related volatiles is crucial for reproduction in male moths. Sex pheromone information is detected by specific olfactory receptor neurons (Phe-ORNs), highly abundant on the male antenna. The information is then transmitted to the pheromone processing macroglomerular complex (MGC) within the primary olfactory center, the antennal lobe, where it is processed by local interneurons and projection neurons. Ultimately a behavioral response, orientation toward the pheromone source, is elicited. Volatile plant compounds (VPCs) are detected by other functional types of olfactory receptor neurons (ORNs) projecting in another area of the antennal lobe. However, Phe-ORNs also respond to some VPCs. Female-produced sex pheromones are emitted within a rich environment of VPCs, some of which have been shown to interfere with the detection and processing of sex pheromone information. As interference between the different odor sources might depend on the spatial and temporal features of the two types of stimuli, we investigated here behavioral and neuronal responses to a brief sex pheromone blend pulse in a VPC background as compared to a control background in the male noctuid moth Agrotis ipsilon. We observed male orientation behavior in a wind tunnel and recorded responses of Phe-ORNs and MGC neurons to a brief sex pheromone pulse within a background of individual VPCs. We also recorded the global input signal to the MGC using in vivo calcium imaging with the same stimulation protocol. We found that VPCs eliciting a response in Phe-ORNs and MGC neurons masked responses to the pheromone and decreased the contrast between background odor and the sex pheromone at both levels, whereas α-pinene did not interfere with first order processing. The calcium signal produced in response to a VPC background was tonic, lasting longer than the VPC stimulus duration, and masked entirely the pheromone response. One percent heptanal and linalool, in addition to the masking effect, caused a clear delay in responses of MGC neurons to the sex pheromone. Upwind flight toward the pheromone in a wind tunnel was also delayed but otherwise not altered by different doses of heptanal.
Highlights
Olfaction is essential for insects to find a mate, a food source or an oviposition site
Male moths’ flight behavior in response to the pheromone blend alone or in a background of heptanal was observed in a Plexiglas wind tunnel measuring 190 cm length × 75 cm width × 75 cm height (VT Plastics, Genevilliers, France)
The Phe-olfactory receptor neurons (ORNs) of A. ipsilon responded to short pulses of the pheromone blend (Z7-12:OAc, Z9-14:OAc, and Z11-16:OAc in a 4:1:4 ratio) at the low (10 ng) and high (100 ng) doses by a fast and phasic increase of the firing (Figures 2A, 3)
Summary
Olfaction is essential for insects to find a mate, a food source or an oviposition site. The mixing ratios of volatile plant compounds (VPCs) in air are typically in the range of several ppb (Kesselmeier et al, 2000; Wiedenmyer et al, 2011) The effects of such large amounts of VPCs in the atmosphere on the perception of specific olfactory signals that are often released in much lower concentrations are still not fully understood. It is important to understand how insect olfactory systems code specific signals in an odor background, and challenging the moth pheromone system by VPCs provides an excellent study model. In the present paper, using electrophysiological recordings and in vivo calcium imaging, we studied how a background of plant volatiles modifies the detection and early coding of the sex pheromone signal in Phe-ORNs and the macroglomerular complex (MGC), pheromone-specific part of the ALs, in the noctuid moth Agrotis ipsilon. To determine if effects found for pheromone responses in a heptanal background are specific to this plant component, we tested responses to the pheromone in backgrounds of two other plant volatiles
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