Odor background increases pheromone coding efficiency in moth olfactory neurons

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Odor background increases pheromone coding efficiency in moth olfactory neurons

International audienc

Effects of an odor background on moth pheromone communication: constituent identity matters more than blend complexity

Olfaction allows insects to communicate with pheromones even in complex olfactory landscapes. It is generally admitted that, due to the binding selectivity of the receptors, general odorants should weakly interfere with pheromone detection. However, laboratory studies show that volatile plant compounds (VPCs) modulate responses to the pheromone in male moths. We used extracellular electrophysiology and calcium imaging to measure the responses to the pheromone of receptor and central neurons in males Agrotis ipsilon while exposed to simple or composite backgrounds of VPCs. Maps of activities were built using calcium-imaging to visualize which areas in antennal lobes (ALs) were affected by VPCs. To mimic a natural olfactory landscape short pheromone puffs were delivered over VPC backgrounds. We chose a panel of VPCs with different chemical structures and physicochemical properties representative of the odorant variety encountered by a moth. We evaluated the intrinsic activity of each VPC and compared the impact of VPC backgrounds at antenna and antennal lobe levels. Then, we prepared binary, ternary and quaternary combinations to determine whether blend activity could be deduced from that of its components. Our data confirm that a VPC background interfere with the moth pheromone system in a dose-dependent manner. Interference with the neuronal coding of pheromone signal starts at the periphery. VPCs showed differences in their capacity to elicit Phe-ORN firing response that cannot be explained by differences in stimulus intensities because we adjusted the source concentrations to vapor pressures. Thus, these differences must be attributed to the selectivity of ORs or any other olfactory proteins. The neuronal network in the ALs, which reformats the ORN-input, did not improve pheromone salience. We postulate that the AL network might have evolved to increase sensitivity and encode for fast changes over a wide range of concentrations, possibly at some cost for selectivity. Comparing three- or four-component blends to binary blends or single compound indicated that a blend showed the activity of its most active compound. Thus, although the diversity of a background might increase the probability of including a VPC interacting with the pheromone system, chemical diversity does not seem to be a prominent factor per se. Global warming is significantly affecting plant metabolism so that the emissions of VPCs and resulting odorscapes are modified. Increase in atmospheric mixing rates of VPCs will change olfactory landscapes which, as confirmed in our study, might impact pheromone communication

Effects of Multi-Component Backgrounds of Volatile Plant Compounds on Moth Pheromone Perception

International audienceThe volatile plant compounds (VPC) alter pheromone perception by insects but mixture effects inside insect olfactory landscapes are poorly understood. We measured the activity of receptor neurons tuned to Z7-12Ac (Z7-ORN), a pheromone component, in the antenna and central neurons in male Agrotis ipsilon while exposed to simple or composite backgrounds of a panel of VPCs representative of the odorant variety encountered by a moth. Maps of activities were built using calcium imaging to visualize which areas in antennal lobes (AL) were affected by VPCs. We compared the VPC activity and their impact as backgrounds at antenna and AL levels, individually or in blends. At periphery, VPCs showed differences in their capacity to elicit Z7-ORN firing response that cannot be explained by differences in stimulus intensities because we adjusted concentrations according to vapor pressures. The AL neuronal network, which reformats the ORN input, did not improve pheromone salience. We postulate that the AL network evolved to increase sensitivity and to encode for fast changes of pheromone at some cost for signal extraction. Comparing blends to single compounds indicated that a blend shows the activity of its most active component. VPC salience seems to be more important than background complexity

Response termination in insect olfactory receptor neurons can be fast and precise

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Using insect electroantennogram sensors on autonomous robots for olfactory searches

International audienceWe describe a protocol for using insect antennae in the form of electroantennograms (EAGs) on autonomous robots. Our experimental design allows stable recordings within a day and resolves individual odor patches up to 10 Hz. The efficiency of EAG sensors for olfactory searches is demonstrated in driving a robot toward an odor source

Stimulus duration encoding by moth olfactory receptor neurons

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Evidence for a role of oestrogen receptor-related receptor in the regulation of male sexual behaviour in the moth Agrotis ipsilon

The oestrogen receptor-related receptors (ERRs) are orphan nuclear receptors that were originally identified on the basis of their close homology to the oestrogen receptors. The three mammalian ERR genes participate in the regulation of vital physiological processes including reproduction, development and metabolic homeostasis. Although unique ERRs have been found in insects, data on the function and regulation of these receptors remain sparse. In the present study, a 2095-bp full-length cDNA encoding an ERR, termed AiERR, was isolated from males of the moth Agrotis ipsilon and deposited in the GenBank database under the accession number KT944662. The predicted AiERR protein shared an overall identity of 47–82% with other known insect and mammalian ERR homologues. AiERR exhibited a broad tissue expression pattern with the detection of one transcript of approximately 2 kb in the primary olfactory centres, the antennal lobes (AL). In adult males, the amount of AiERR mRNA in the AL increased concomitantly with age and responses to the female-emitted sex pheromone. Moreover, AiERR knockdown induced an inhibition in the sex pheromone-orientated flight of male. Using A. ipsilon as a model, our study demonstrates that the insect ERR is critical for the performance of male sexual behaviour, probably by acting on central pheromone processing

Bestrophin-encoded Ca²⁺-activated Cl⁻ channels underlie a current with properties similar to the native current in the moth Spodoptera littoralis olfactory receptor neurons

Responses of insect olfactory receptor neurons (ORNs) involve an entry of Ca2+ through olfactory heterodimeric receptor complexes. In moths, the termination of ORN responses was found to strongly depend on the external Ca2+ concentration through the activation of unknown Ca2+-dependent Cl- channels. We thus investigated the molecular identity of these Cl- channels. There is compelling evidence that bestrophins form Cl- channels when expressed in heterologous systems. Here we provide evidence that antennae of the moth Spodoptera littoralis express three transcripts encoding proteins with hallmarks of bestrophins. One of these transcripts, SlitBest1b, is expressed in ORNs. The heterologous expression of SlitBest1b protein in CHO-K1 cells yielded a Ca2+-activated Cl- current that shares electrophysiological properties with the native Ca2+-activated Cl- current of ORNs. Both currents are anionic, present similar dependence on the intracellular Ca2+ concentration, partly inactivate over time, have the same anion permeability sequence, the same sequence of inhibitory efficiency of blockers, the same almost linear I-V relationships and finally both currents do not depend on the cell volume. Therefore, our data suggest that SlitBest1b is a good candidate for being a molecular component of the olfactory Ca2+-activated Cl- channel and is likely to constitute part of the insect olfactory transduction pathway. A different function (e. g. regulation of other proteins, maintenance of the anionic homeostasis in the sensillar lymph) and a different role (e. g. involvement in the olfactory system development) cannot be excluded however

The insect HR38 nuclear receptor, a member of the NR4A subfamily, is a synchronizer of reproductive activity in a moth

International audienceIn the male moth, Agrotis ipsilon, the behavioural response and neuron sensitivity within the olfactory centres, the antennal lobes (ALs), to female sex pheromone increase with age, in correlation with the maturation of sex accessory glands (SAGs). By contrast, newly mated males cease to be attracted to sex pheromone and remate when their SAGs are refilled during the next night. The insect hormone receptor 38 (HR38), an ortholog of the vertebrate NR4A receptors, is a component of ecdysteroid signalling pathway which controls adult male physiology and behaviour. Here, we cloned the A. ipsilon HR38 (AiHR38) and explored its function in the coordination of reproductive events in the male. AiHR38 was detected in SAGs and ALs, and where its amount raised with age, in parallel with SAG protein content and sex pheromone responsiveness. By contrast, the AL and SAG AiHR38 expressions declined at 0–2 h after mating, in linking with depletion of SAG protein reserves and loss of sensitivity to sex pheromone. The increased AL and SAG AiHR38 expressions at 20–24 h postmating coincided with replenishing of SAGs and recovery of sensitivity to sex pheromone for a new mating. Moreover, AiHR38 knockdown resulted in reduction in SAG protein amount and disruption of sex pheromone‐orientated flight. These results show that the insect HR38 is essential both for SAG activity, probably by controlling the protein synthesis, and display of male sexual behaviour, and that the concomitant regulation of its expression within SAGs and olfactory centres contributes to synchronisation between fertility and sexual activity