Responses to Pheromones in a Complex Odor World: Sensory Processing and Behavior

Insects communicating with pheromones, be it sex- or aggregation pheromones, are confronted with an olfactory environment rich in a diversity of volatile organic compounds of which plants are the main releaser. Certain of these volatiles can represent behaviorally relevant information, such as indications about host- or non-host plants; others will provide essentially a rich odor background out of which the behaviorally relevant information needs to be extracted. In an attempt to disentangle mechanisms of pheromone communication in a rich olfactory environment, which might underlie interactions between intraspecific signals and a background, we will summarize recent literature on pheromone/plant volatile interactions. Starting from molecular mechanisms, describing the peripheral detection and central nervous integration of pheromone-plant volatile mixtures, we will end with behavioral output in response to such mixtures and its plasticity

Elemental and configural olfactory coding by antennal lobe neurons of the honeybee (Apis mellifera)

When smelling an odorant mixture, olfactory systems can be analytical (i.e. extract information about the mixture elements) or synthetic (i.e. creating a configural percept of the mixture). Here, we studied elemental and configural mixture coding in olfactory neurons of the honeybee antennal lobe, local neurons in particular. We conducted intracellular recordings and stimulated with monomolecular odorants and their coherent or incoherent binary mixtures to reproduce a temporally dynamic environment. We found that about half of the neurons responded as ‘elemental neurons’, i.e. responses evoked by mixtures reflected the underlying feature information from one of the components. The other half responded as ‘configural neurons’, i.e. responses to mixtures were clearly different from responses to their single components. Elemental neurons divided in late responders (above 60 ms) and early responder neurons (below 60 ms), whereas responses of configural coding neurons concentrated in-between these divisions. Latencies of neurons with configural responses express a tendency to be faster for coherent stimuli which implies employment in different processing circuits

Low doses of a neonicotinoid insecticide modify pheromone response thresholds of central but not peripheral olfactory neurons in a pest insect

Insect pest management relies mainly on neurotoxic insecticides, including neonicotinoids, leaving residues in the environment. There is now evidence that low doses of insecticides can have positive effects on pest insects by enhancing various life traits. Because pest insects often rely on sex pheromones for reproduction, and olfactory synaptic transmission is cholinergic, neonicotinoid residues could modify chemical communication. We recently showed that treatments with different sublethal doses of clothianidin could either enhance or decrease behavioural sex pheromone responses in the male moth, Agrotis ipsilon. We investigated now effects of the behaviourally active clothianidin doses on the sensitivity of the peripheral and central olfactory system. We show with extracellular recordings that both tested clothianidin doses do not influence pheromone responses in olfactory receptor neurons. Similarly, in vivo optical imaging does not reveal any changes in glomerular response intensities to the sex pheromone after clothianidin treatments. The sensitivity of intracellularly recorded antennal lobe output neurons, however, is upregulated by a lethal dose 20 times and downregulated by a dose 10 times lower than the lethal dose 0. This correlates with the changes of behavioural responses after clothianidin treatment and suggests the antennal lobe as neural substrate involved in clothianidin-induced behavioural changes

Prediction Models for the Pleasantness of Binary Mixtures in Olfaction

Whereas the rules underlying the perceived intensity of binary mixtures have been investigated, minimal efforts have been directed at elucidating the rules underlying the perceived pleasantness of such mixtures. To address this, 84 subjects ranked the pleasantness and intensity of 5 distinct binary mixtures (15 pairs, inter-stimulus interval = 4 s, inter-trial interval = 30 s, flow = 6 l/min, pulse = 2 s) constructed from different ratios (0:100%, 25:75%, 50:50%, 75:25%, and 100:0%, olfactometer-generated vapor phase). We found that in the majority of cases, the pleasantness of the mixture fell between the pleasantness values of its separated constituents and that it was strongly influenced by the relative intensities of the constituents. Based on these results, we proposed a prediction paradigm for the pleasantness of binary mixtures from the pleasantness of their separated constituents weighted by their respective perceived intensities. The uniqueness of the proposed paradigm is that it neither requires presetting an interaction constant between the mixture components nor require any factorization of the pleasantness weights. It does, nonetheless, require solid psychophysical data on the separated components at their different concentrations, and currently it can only explain the behavior of intermediate pleasantness of mixtures

A biophysical model of the early olfactory system of honeybees

Experimental measurements often can only provide limited data from an animal’s sensory system. In addition, they exhibit large trial-to-trial and animal-to-animal variability. These limitations pose challenges to building mathematical models intended to make biologically relevant predictions. Here, we present a mathematical model of the early olfactory system of honeybees aiming to overcome these limitations. The model generates olfactory response patterns which conform to the statistics derived from experimental data for a variety of their properties. This allows considering the full dimensionality of the sensory input space as well as avoiding overfitting the underlying data sets. Several known biological mechanisms, including processes of chemical binding and activation of receptors, and spike generation and transmission in the antennal lobe network, are incorporated in the model at a minimal level. It can therefore be used to study how experimentally observed phenomena are shaped by these underlying biophysical processes. We verified that our model can replicate some key experimental findings that were not used when building it. Given appropriate data, our model can be generalized to the early olfactory systems of other insects. It hence provides a possible framework for future numerical and analytical studies of olfactory processing in insects

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

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

Generalization Mediates Sensitivity to Complex Odor Features in the Honeybee

Animals use odors as signals for mate, kin, and food recognition, a strategy which appears ubiquitous and successful despite the high intrinsic variability of naturally-occurring odor quantities. Stimulus generalization, or the ability to decide that two objects, though readily distinguishable, are similar enough to afford the same consequence [1], could help animals adjust to variation in odor signals without losing sensitivity to key inter-stimulus differences. The present study was designed to investigate whether an animal's ability to generalize learned associations to novel odors can be influenced by the nature of the associated outcome. We use a classical conditioning paradigm for studying olfactory learning in honeybees [2] to show that honeybees conditioned on either a fixed- or variable-proportion binary odor mixture generalize learned responses to novel proportions of the same mixture even when inter-odor differences are substantial. We also show that the resulting olfactory generalization gradients depend critically on both the nature of the stimulus-reward paradigm and the intrinsic variability of the conditioned stimulus. The reward dependency we observe must be cognitive rather than perceptual in nature, and we argue that outcome-dependent generalization is necessary for maintaining sensitivity to inter-odor differences in complex olfactory scenes