Changes in gaseous concentration of alkylpyrazine analogs affect mouse avoidance behavior

The Y-maze is often used to detect subtle differences between similar odor sources; however, very little information is available about the dispersion of odor plumes in the Y-maze. Using headspace solid-phase microextraction (HS-SPME) in conjunction with a GC-MS system, we quantified alkylpyrazine analogs in the Y-maze. Rapid extraction of volatile compounds in the vapor phase enabled accurate quantitative analysis of temporal changes in the levels of gaseous alkylpyrazine analogs at several locations in the Y-maze. We conducted behavioral tests of mice in response to these volatiles and identified a positive relationship between the rate of increase in gaseous concentration and the induced avoidance rate. Our results demonstrate that the Y-maze is a simple but reliable apparatus for behavioral studies of olfaction. Our findings show that the HS-SPME fast extraction method could quantify how gaseous concentrations of alkylpyrazine analogs change over time, and that temporal increases in alkylpyrazine concentration were correlated with induction of aversive behavior in mice.

Does the Ratio of Compounds in a Plant Volatiles Blend Remain Stable During Transmission by Wind?

For plant volatiles to mediate interactions in tritrophic systems, they must convey accurate and reliable information to insects. However, it is unknown whether the ratio of compounds in plant volatile blends remains stable during wind transmission. In this study, volatiles released from an odor source were collected at different points in a wind tunnel and analyzed. The variation in the amounts of volatiles collected at different points formed a rough cone shape. The amounts of volatiles collected tended to decrease with increasing distance from the odor source. Principal component analyses showed that the volatile profiles were dissimilar among different collection points. The profiles of volatiles collected nearest the odor source were the most similar to the released odor. Higher wind speed resulted in a clearer distinction of the spatial distribution of volatile compounds. Thus, variations in the ratios of compounds in odor plumes exist even during transport over short distances.

Plume Dynamics Structure the Spatiotemporal Activity of Mitral/Tufted Cell Networks in the Mouse Olfactory Bulb

Although mice locate resources using turbulent airborne odor plumes, the stochasticity and intermittency of fluctuating plumes create challenges for interpreting odor cues in natural environments. Population activity within the olfactory bulb (OB) is thought to process this complex spatial and temporal information, but how plume dynamics impact odor representation in this early stage of the mouse olfactory system is unknown. Limitations in odor detection technology have made it difficult to measure plume fluctuations while simultaneously recording from the mouse's brain. Thus, previous studies have measured OB activity following controlled odor pulses of varying profiles or frequencies, but this approach only captures a subset of features found within olfactory plumes. Adequately sampling this feature space is difficult given a lack of knowledge regarding which features the brain extracts during exposure to natural olfactory scenes. Here we measured OB responses to naturally fluctuating odor plumes using a miniature, adapted odor sensor combined with wide-field GCaMP6f signaling from the dendrites of mitral and tufted (MT) cells imaged in olfactory glomeruli of head-fixed mice. We precisely tracked plume dynamics and imaged glomerular responses to this fluctuating input, while varying flow conditions across a range of ethologically-relevant values. We found that a consistent portion of MT activity in glomeruli follows odor concentration dynamics, and the strongest responding glomeruli are the best at following fluctuations within odor plumes. Further, the reliability and average response magnitude of glomerular populations of MT cells are affected by the flow condition in which the animal samples the plume, with the fidelity of plume following by MT cells increasing in conditions of higher flow velocity where odor dynamics result in intermittent whiffs of stronger concentration. Thus, the flow environment in which an animal encounters an odor has a large-scale impact on the temporal representation of an odor plume in the OB. Additionally, across flow conditions odor dynamics are a major driver of activity in many glomerular networks. Taken together, these data demonstrate that plume dynamics structure olfactory representations in the first stage of odor processing in the mouse olfactory system.

The long-distance flight behavior of Drosophila supports an agent-based model for wind-assisted dispersal in insects

Despite the ecological importance of long-distance dispersal in insects, its mechanistic basis is poorly understood in genetic model species, in which advanced molecular tools are readily available. One critical question is how insects interact with the wind to detect attractive odor plumes and increase their travel distance as they disperse. To gain insight into dispersal, we conducted release-and-recapture experiments in the Mojave Desert using the fruit fly, Drosophila melanogaster. We deployed chemically baited traps in a 1 km radius ring around the release site, equipped with cameras that captured the arrival times of flies as they landed. In each experiment, we released between 30,000 and 200,000 flies. By repeating the experiments under a variety of conditions, we were able to quantify the influence of wind on flies’ dispersal behavior. Our results confirm that even tiny fruit flies could disperse ∼12 km in a single flight in still air and might travel many times that distance in a moderate wind. The dispersal behavior of the flies is well explained by an agent-based model in which animals maintain a fixed body orientation relative to celestial cues, actively regulate groundspeed along their body axis, and allow the wind to advect them sideways. The model accounts for the observation that flies actively fan out in all directions in still air but are increasingly advected downwind as winds intensify. Our results suggest that dispersing insects may strike a balance between the need to cover large distances while still maintaining the chance of intercepting odor plumes from upwind sources.

Spatial odor discrimination in the hawkmoth, Manduca sexta (L.)

ABSTRACT Flying insects track turbulent odor plumes to find mates, food and egg-laying sites. To maintain contact with the plume, insects are thought to adapt their flight control according to the distribution of odor in the plume using the timing of odor onsets and intervals between odor encounters. Although timing cues are important, few studies have addressed whether insects are capable of deriving spatial information about odor distribution from bilateral comparisons between their antennae in flight. The proboscis extension reflex (PER) associative learning protocol, originally developed to study odor learning in honeybees, was used as a tool to ask if hawkmoths, Manduca sexta, can discriminate between odor stimuli arriving on either antenna. We show moths discriminated the odor arrival side with an accuracy of >70%. Information about spatial distribution of odor stimuli may be available to moths searching for odor sources, opening the possibility that they use both spatial and temporal odor information. This article has an associated First Person interview with the first author of the paper.

Spatial, but not temporal, aspects of orientation are controlled by the fine scale distribution of chemical cues in turbulent odor plumes

Orientation within turbulent odor plumes occurs across a vast range of spatial and temporal scales. From salmon homing across featureless oceans to microbes forming reproductive spores, the extraction of spatial and temporal information from chemical cues is a common sensory phenomenon. Yet, given the difficulty of quantifying chemical cues at the spatial and temporal scales used by organisms, discovering what aspects of chemical cues controls orientation behavior has remain elusive. In this study, we place electrochemical sensors on the carapace of orienting crayfish and measure, with fast temporal rates and small spatial scales, the concentration fluctuations arriving at the olfactory appendages during orientation. The results of these studies show that the spatial aspects of orientation (turning and heading angles) are controlled by the temporal aspects of odor cues.

Identification of Exploration and Exploitation Balance in the Silkmoth Olfactory Search Behavior by Information-Theoretic Modeling

Insects search for and find odor sources as their basic behaviors, such as when looking for food or a mate. This has motivated research to describe how they achieve such behavior under turbulent odor plumes with a small number of neurons. Among different insects, the silk moth has been studied owing to its clear motor response to olfactory input. In past studies, the “programmed behavior” of the silk moth has been modeled as the average duration of a sequence of maneuvers based on the duration of periods without odor hits. However, this model does not fully represent the fine variations in their behavior. In this study, we used silk moth olfactory search trajectories from an experimental virtual reality device. We achieved an accurate input by using optogenetic silk moths that react to blue light. We then modeled such trajectories as a probabilistic learning agent with a belief of possible source locations. We found that maneuvers mismatching the programmed behavior are related to larger entropy decrease, that is, they are more likely to increase the certainty of the belief. This implies that silkmoths include some stochasticity in their search policy to balance the exploration and exploitation of olfactory information by matching or mismatching the programmed behavior model. We believe that this information-theoretic representation of insect behavior is important for the future implementation of olfactory searches in artificial agents such as robots.

Navigation Along Windborne Plumes of Pheromone and Resource-Linked Odors

Many insects locate resources such as a mate, a host, or food by flying upwind along the odor plumes that these resources emit to their source. A windborne plume has a turbulent structure comprised of odor filaments interspersed with clean air. As it propagates downwind, the plume becomes more dispersed and dilute, but filaments with concentrations above the threshold required to elicit a behavioral response from receiving organisms can persist for long distances. Flying insects orient along plumes by steering upwind, triggered by the optomotor reaction. Sequential measurements of differences in odor concentration are unreliable indicators of distance to or direction of the odor source. Plume intermittency and the plume's fine-scale structure can play a role in setting an insect's upwind course. The prowess of insects in navigating to odor sources has spawned bioinspired virtual models and even odor-seeking robots, although some of these approaches use mechanisms that are unnecessarily complex and probably exceed an insect's processing capabilities.