Honeybees Learn Odour Mixtures via a Selection of Key Odorants

BACKGROUND The honeybee has to detect, process and learn numerous complex odours from her natural environment on a daily basis. Most of these odours are floral scents, which are mixtures of dozens of different odorants. To date, it is still unclear how the bee brain unravels the complex information contained in scent mixtures. METHODOLOGY/PRINCIPAL FINDINGS This study investigates learning of complex odour mixtures in honeybees using a simple olfactory conditioning procedure, the Proboscis-Extension-Reflex (PER) paradigm. Restrained honeybees were trained to three scent mixtures composed of 14 floral odorants each, and then tested with the individual odorants of each mixture. Bees did not respond to all odorants of a mixture equally: They responded well to a selection of key odorants, which were unique for each of the three scent mixtures. Bees showed less or very little response to the other odorants of the mixtures. The bees' response to mixtures composed of only the key odorants was as good as to the original mixtures of 14 odorants. A mixture composed of the other, non-key-odorants elicited a significantly lower response. Neither an odorant's volatility or molecular structure, nor learning efficiencies for individual odorants affected whether an odorant became a key odorant for a particular mixture. Odorant concentration had a positive effect, with odorants at high concentration likely to become key odorants. CONCLUSIONS/SIGNIFICANCE Our study suggests that the brain processes complex scent mixtures by predominantly learning information from selected key odorants. Our observations on key odorant learning lend significant support to previous work on olfactory learning and mixture processing in honeybees.This work was supported by a grant from the Commonwealth Scientific and Industrial Research Organisation Food Futures Flagship Collaborative Research Fund (CBR3_45865_9 W2003, http://www.csiro.au/org/FoodFuturesFlagship.html). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript

Odorants for surveillance and control of the Asian Citrus Psyllid (Diaphorina citri).

BackgroundThe Asian Citrus Psyllid (ACP), Diaphorina citri, can transmit the bacterium Candidatus Liberibacter while feeding on citrus flush shoots. This bacterium causes Huanglongbing (HLB), a major disease of citrus cultivation worldwide necessitating the development of new tools for ACP surveillance and control. The olfactory system of ACP is sensitive to variety of odorants released by citrus plants and offers an opportunity to develop new attractants and repellents.ResultsIn this study, we performed single-unit electrophysiology to identify odorants that are strong activators, inhibitors, and prolonged activators of ACP odorant receptor neurons (ORNs). We identified a suite of odorants that activated the ORNs with high specificity and sensitivity, which may be useful in eliciting behavior such as attraction. In separate experiments, we also identified odorants that evoked prolonged ORN responses and antagonistic odorants able to suppress neuronal responses to activators, both of which can be useful in lowering attraction to hosts. In field trials, we tested the electrophysiologically identified activating odorants and identified a 3-odor blend that enhances trap catches by ∼230%.ConclusionThese findings provide a set of odorants that can be used to develop affordable and safe odor-based surveillance and masking strategies for this dangerous pest insect

Lack of Pattern Separation in Sensory Inputs to the Olfactory Bulb during Perceptual Learning.

Recent studies revealed changes in odor representations in the olfactory bulb during active olfactory learning (Chu et al., 2016; Yamada et al., 2017). Specifically, mitral cell ensemble responses to very similar odorant mixtures sparsened and became more distinguishable as mice learned to discriminate the odorants over days (Chu et al., 2016). In this study, we explored whether changes in the sensory inputs to the bulb underlie the observed changes in mitral cell responses. Using two-photon calcium imaging to monitor the odor responses of the olfactory sensory neuron (OSN) axon terminals in the glomeruli of the olfactory bulb during a discrimination task, we found that OSN inputs to the bulb are stable during discrimination learning. During one week of training to discriminate between very similar odorant mixtures in a Go/No-go task, OSN responses did not show significant sparsening, and the responses to the trained similar odorants did not diverge throughout training. These results suggest that the adaptive changes of mitral cell responses during perceptual learning are ensured by mechanisms downstream of OSN input, possibly in local circuits within olfactory bulb

Odors: from chemical structures to gaseous plumes

We are immersed within an odorous sea of chemical currents that we parse into individual odors with complex structures. Odors have been posited as determined by the structural relation between the molecules that compose the chemical compounds and their interactions with the receptor site. But, naturally occurring smells are parsed from gaseous odor plumes. To give a comprehensive account of the nature of odors the chemosciences must account for these large distributed entities as well. We offer a focused review of what is known about the perception of odor plumes for olfactory navigation and tracking, which we then connect to what is known about the role odorants play as properties of the plume in determining odor identity with respect to odor quality. We end by motivating our central claim that more research needs to be conducted on the role that odorants play within the odor plume in determining odor identity

Short-term memory trace mediated by termination kinetics of olfactory receptor.

Odorants activate receptors in the peripheral olfactory neurons, which sends information to higher brain centers where behavioral valence is determined. Movement and airflow continuously change what odor plumes an animal encounters and little is known about the effect one plume has on the detection of another. Using the simple Drosophila melanogaster larval model to study this relationship we identify an unexpected phenomenon: response to an attractant can be selectively blocked by previous exposure to some odorants that activates the same receptor. At a mechanistic level, we find that exposure to this type of odorant causes prolonged tonic responses from a receptor (Or42b), which can block subsequent detection of a strong activator of that same receptor. We identify naturally occurring odorants with prolonged tonic responses for other odorant receptors (Ors) as well, suggesting that termination-kinetics is a factor for olfactory coding mechanisms. This mechanism has implications for odor-coding in any system and for designing applications to modify odor-driven behaviors

Perceiving Smellscapes

We perceive smells as perduring complex entities within a distal array that might be conceived of as smellscapes. However, the philosophical orthodoxy of Odor Theories has been to deny that smells are perceived as having a distal location. Recent challenges have been mounted to Odor Theories’ veracity in handling the timescale of olfactory perception, how it individuates odors as a distal entities, and their claim that olfactory perception is not spatial. The paper does not aim to dispute these criticisms. Rather, what will be shown is that Molecular Structure Theory, a refinement of Odor Theory, can be further developed to handle these challenges. The theory is further refined by focusing on distal perception that requires considering the perceptual object as mereologically complex persisting odor against a background scene conceived of as a smellscape. What will be offered is an expansion of Molecular Structure Theory to account for distal smell perception within natural environments

Stimulation of electro-olfactogram responses in the main olfactory epithelia by airflow depends on the type 3 adenylyl cyclase

Cilia of olfactory sensory neurons are the primary sensory organelles for olfaction. The detection of odorants by the main olfactory epithelium (MOE) depends on coupling of odorant receptors to the type 3 adenylyl cyclase (AC3) in olfactory cilia. We monitored the effect of airflow on electro-olfactogram (EOG) responses and found that the MOE of mice can sense mechanical forces generated by airflow. The airflow-sensitive EOG response in the MOE was attenuated when cAMP was increased by odorants or by forskolin suggesting a common mechanism for airflow and odorant detection. In addition, the sensitivity to airflow was significantly impaired in the MOE from AC3−/− mice. We conclude that AC3 in the MOE is required for detecting the mechanical force of airflow, which in turn may regulate odorant perception during sniffing

Conservation of Olfactory Avoidance in Drosophila Species and Identification of Repellents for Drosophila suzukii.

Flying insects use olfaction to navigate towards fruits in complex odor environments with remarkable accuracy. Some fruits change odor profiles substantially during ripening and related species can prefer different stages. In Drosophila species attractive odorants have been studied extensively, but little is understood about the role of avoidance pathways. In order to examine the role of the avoidance cue CO2 emitted from fruit on behavior of two species with different ripening stage preferences, we investigated the CO2-detection pathway in Drosophila melanogaster and Drosophila suzukii, a harmful pest of fruits. Avoidance to CO2 is not conserved in D. suzukii suggesting a behavioral adaptation that could facilitate attraction to younger fruit with higher CO2 emission levels. We investigated known innate avoidance pathways from five species at different evolutionary distances: D. melanogaster, D. yakuba, D. suzukii, D. pseudoobscura and D. virilis. Surprisingly, only DEET shows strong repellency across all species, whereas CO2, citronellal and ethyl 3-hydroxybutyrate show only limited conservation. These findings guide us to test recently discovered safe DEET substitutes, and we identify one that protects fruits from D. suzukii thus providing a new behavioral strategy for controlling agricultural pests