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Olfaction is a crucial sensory modality in insects and is underpinned by odor-sensitive sensory neurons expressing odorant receptors that function in the dendrites as odorant-gated ion channels. Along with expression, trafficking, and receptor complexing, the regulation of odorant receptor function is paramount to ensure the extraordinary sensory abilities of insects. However, the full extent of regulation of sensory neuron activity remains to be elucidated. For instance, our understanding of the intracellular effectors that mediate signaling pathways within antennal cells is incomplete within the context of olfaction in vivo. Here, with the use of optical and electrophysiological techniques in live antennal tissue, we investigate whether nitric oxide signaling occurs in the sensory periphery of Drosophila. To answer this, we first query antennal transcriptomic datasets to demonstrate the presence of nitric oxide signaling machinery in antennal tissue. Next, by applying various modulators of the NO-cGMP pathway in open antennal preparations, we show that olfactory responses are unaffected by a wide panel of NO-cGMP pathway inhibitors and activators over short and long timescales. We further examine the action of cAMP and cGMP, cyclic nucleotides previously linked to olfactory processes as intracellular potentiators of receptor functioning, and find that both long-term and short-term applications or microinjections of cGMP have no effect on olfactory responses in vivo as measured by calcium imaging and single sensillum recording. The absence of the effect of cGMP is shown in contrast to cAMP, which elicits increased responses when perfused shortly before olfactory responses in OSNs. Taken together, the apparent absence of nitric oxide signaling in olfactory neurons indicates that this gaseous messenger may play no role as a regulator of olfactory transduction in insects, though may play other physiological roles at the sensory periphery of the antenna.

The mechanisms of insect odor transduction are still controversial. Insect odorant receptors (ORs) are 7TM receptors with inverted membrane topology. They colocalize with a conserved coreceptor (Orco) with chaperone and ion channel function. Some studies suggest that insects employ exclusively ionotropic odor transduction via OR-Orco heteromers. Other studies provide evidence for different metabotropic odor transduction cascades, which employ second messenger-gated ion channel families for odor transduction. The hawkmoth Manduca sexta is an established model organism for studies of insect olfaction, also due to the availability of the hawkmoth-specific pheromone blend with its main component bombykal. Previous patch-clamp studies on primary cell cultures of M. sexta olfactory receptor neurons provided evidence for a pheromone-dependent activation of a phospholipase Cβ. Pheromone application elicited a sequence of one rapid, apparently IP3-dependent, transient and two slower Ca(2+)-dependent inward currents. It remains unknown whether additionally an ionotropic pheromone-transduction mechanism is employed. If indeed an OR-Orco ion channel complex underlies an ionotropic mechanism, then Orco agonist-dependent opening of the OR-Orco channel pore should add up to pheromone-dependent opening of the pore. Here, in tip-recordings from intact pheromone-sensitive sensilla, perfusion with the Orco agonist VUAA1 did not increase pheromone-responses within the first 1000 ms. However, VUAA1 increased spontaneous activity of olfactory receptor neurons Zeitgebertime- and dose-dependently. We conclude that we find no evidence for an Orco-dependent ionotropic pheromone transduction cascade in M. sexta. Instead, in M. sexta Orco appears to be a slower, second messenger-dependent pacemaker channel which affects kinetics and threshold of pheromone-detection via changes of intracellular Ca(2+) baseline concentrations.

To perceive environmental chemical compounds and to convert these external signals into an intracellular message might be the oldest way for a living being to get information from the outside world. Chemoreceptors are proteins or protein complexes that detect molecules from the outside world either at distance (olfaction) or at close range (gustation). Chemoreceptors can operate as ionotropic or as metabotropic receptors. Ionotropic receptors form ion channels that are activated via ligand binding. Activation of a metabotropic receptor initiates an intracellular signaling cascade that could include a change of enzymatic activity, production of second messenger or activation of ion channels. The receptor performance has to be fine-tuned according to the actual physiological requirements and the presentation of the chemical signal. This Research Topic collects reports and reviews on structure and function of chemoreceptors in the animal kingdom, and how these receptors are regulated.