Fruit flies make their living on the fly in search of attractive food odors. To maintain forward flight, flies balance the strength of self-induced bilateral visual motion  and bilateral wind cues , but it is unknown whether they use bilateral olfactory cues to track odors in flight. Tracking an odor gradient requires comparisons across two spatially separated chemosensory organs and has been observed in several walking insects [3–5], including Drosophila . The olfactory antennae are separated by a fraction of a millimeter, and most sensory neurons project bilaterally and symmetrically activate the first-order olfactory relay [7, 8], both of which would seem to constrain the capacity for bilateral sensory comparisons. Are fruit flies nonetheless able to track an odor gradient during flight? Using a modified flight simulator that enables maneuvers in the yaw axis , we found that flies readily steer directly toward a laterally positioned odor plume. This capability is abolished by occluding sensory input to one antenna. Mechanosensory input from the Johnston’s organ and olfactory input from the third antennal segment cooperate to direct small angle yaw turns up the plume gradient. We additionally show that sensory signals from the left antenna contribute disproportionately more to odor tracking than the right, providing further evidence of sensory lateralization in invertebrates [10–13].
It has been clear for many years that insects use visual cues to stabilize their heading in a wind stream. Many animals track odors carried in the wind. As such, visual stabilization of upwind tracking directly aids in odor tracking. But do olfactory signals directly influence visual tracking behavior independently from wind cues? Also, the recent deluge of research on the neurophysiology and neurobehavioral genetics of olfaction in Drosophila has motivated ever more technically sophisticated and quantitative behavioral assays. Here, we modified a magnetic tether system originally devised for vision experiments by equipping the arena with narrow laminar flow odor plumes. A fly is glued to a small steel pin and suspended in a magnetic field that enables it to yaw freely. Small diameter food odor plumes are directed downward over the fly s head, eliciting stable tracking by a hungry fly. Here we focus on the critical mechanics of tethering, aligning the magnets, devising the odor plume, and confirming stable odor tracking.
Engineered tracking systems ‘fuse’ data from disparate sensor platforms, such as radar and video, to synthesize information that is more reliable than any single input. The mammalian brain registers visual and auditory inputs to directionally localize an interesting environmental feature. For a fly, sensory perception is challenged by the extreme performance demands of high speed flight. Yet even a fruit fly can robustly track a fragmented odor plume through varying visual environments, outperforming any human engineered robot. Flies integrate disparate modalities, such as vision and olfaction, which are neither related by spatiotemporal spectra nor processed by registered neural tissue maps. Thus, the fly is motivating new conceptual frameworks for how low-level multisensory circuits and functional algorithms produce high-performance motor control.
Turbulent fluid landscapes impose temporal patterning upon chemical signals, and the dynamical neuronal responses to patterned input vary across the olfactory receptor repertoire in flies, moths, and locusts. Sensory transformations exhibit low pass filtering that ultimately results in perceptual fusion of temporally transient sensory signals. For example, humans perceive a sufficiently fast flickering light as continuous, but the frequency threshold at which this fusion occurs varies with wavelength. Although the summed frequency sensitivity of the fly antenna has been examined to a considerable extent, it is unknown how intermittent odor signals are integrated to influence plume tracking behavior independent of wind cues, and whether temporal fusion for behavioral tracking might vary according to the odor encountered.
Here we have adopted a virtual reality flight simulator to study the dynamics of plume tracking under different experimental conditions. Flies tethered in a magnetic field actively track continuous (non-intermittent) plumes of vinegar, banana, or ethyl butyrate with equal precision. However, pulsing these plumes at varying frequency reveals that the threshold rate, above which flies track the plume as if it were continuous, is unique for each odorant tested. Thus, the capability of a fly to navigate an intermittent plume depends on the particular odorant being tracked during flight. Finally, we measured antennal field potential responses to an intermittent plume, found that receptor dynamics track the temporal pattern of the odor stimulus and therefore do not limit the observed behavioral temporal fusion limits.
This study explores the flies' ability to track odor plumes that are temporally intermittent. We were surprised to find that the perceptual critical fusion limit, determined behaviorally, is strongly dependent on odor identity. Antennal field potential recordings indicate that peripheral processing of temporal cues faithfully follow rapid odor transients above the rates that can be resolved behaviorally. These results indicate that (1) higher order circuits create a perceptually continuous signal from an intermittent sensory one, and that (2) this transformation varies with odorant rather than being constrained by sensory-motor integration, thus (3) offering an entry point for examining the mechanisms of rapid olfactory decision making in an ecological context.
Flying insects use visual cues to stabilize their heading in a wind stream. Many animals additionally track odors carried in the wind. As such, visual stabilization of upwind tracking directly aids in odor tracking. But do olfactory signals directly influence visual tracking behavior independently from wind cues? Additionally, recent advances in olfactory molecular genetics and neurophysiology have motivated novel quantitative behavioral analyses to assess the behavioral influence of (e.g.) genetically inactivating specific olfactory activation circuits. We modified a magnetic tether system originally devised for vision experiments by equipping the arena with narrow laminar flow odor plumes. Here we focus on experiments that can be performed after a fly is tethered and is able to navigate in the magnetic arena. We show how to acquire video images optimized for measuring body angle, how to judge stable odor tracking, and we illustrate two experiments to examine the influence of visual cues on odor tracking.
How can odor-guided behavior of numerous individual Drosophila be assessed
automatically with high temporal resolution? For this purpose we introduce the
automatic integrated tracking and odor-delivery system Flywalk. In fifteen
aligned small wind tunnels individual flies are exposed to repeated odor pulses,
well defined in concentration and timing. The flies' positions are visually tracked,
which allows quantification of the odor-evoked walking behavior with high temporal
resolution of up to 100 ms. As a demonstration of Flywalk we show that the
flies' behavior is odorant-specific; attractive odors elicit directed upwind
movements, while repellent odors evoke decreased activity, followed by downwind
movements. These changes in behavior differ between sexes. Furthermore our findings
show that flies can evaluate the sex of a conspecific and males can determine a
female's mating status based on olfactory cues. Consequently, Flywalk allows
automatic screening of individual flies for their olfactory preference and
Multimodal integration allows neural circuits to be activated in a behaviorally context-specific manner. In the case of odor plume tracking by Drosophila, an attractive odorant increases the influence of yaw-optic flow on steering behavior in flight, which enhances visual stability reflexes, resulting in straighter flight trajectories within an odor plume. However, it is not well understood whether context-specific changes in optomotor behavior are the result of an increased sensitivity to motion inputs (e.g., through increased visual attention) or direct scaling of motor outputs (i.e., increased steering gain). We address this question by examining the optomotor behavior of Drosophila melanogaster in a tethered flight assay and demonstrate that whereas olfactory cues decrease the gain of the optomotor response to sideslip optic flow, they concomitantly increase the gain of the yaw optomotor response by enhancing the animal's ability to follow transient visual perturbations. Furthermore, ablating the mushroom bodies (MBs) of the fly brain via larval hydroxyurea (HU) treatment results in a loss of olfaction-dependent increase in yaw optomotor fidelity. By expressing either tetanus toxin light chain or diphtheria toxin in gal4-defined neural circuits, we were able to replicate the loss of function observed in the HU treatment within the lines expressing broadly in the mushroom bodies, but not within specific mushroom body lobes. Finally, we were able to genetically separate the yaw responses and sideslip responses in our behavioral assay. Together, our results implicate the MBs in a fast-acting, memory-independent olfactory modification of a visual reflex that is critical for flight control.
Navigating toward (or away from) a remote odor source is a challenging problem that requires integrating olfactory information with visual and mechanosensory cues. Drosophila melanogaster is a useful organism for studying the neural mechanisms of these navigation behaviors. There is a wealth of genetic tools in this organism, as well as a history of inventive behavioral experiments. There is also a large and growing literature in Drosophila on the neural coding of olfactory, visual, and mechanosensory stimuli. Here we review recent progress in understanding how these stimulus modalities are encoded in the Drosophila nervous system. We also discuss what strategies a fly might use to navigate in a natural olfactory landscape while making use of all these sources of sensory information. We emphasize that Drosophila are likely to switch between multiple strategies for olfactory navigation, depending on the availability of various sensory cues. Finally, we highlight future research directions that will be important in understanding the neural circuits that underlie these behaviors.
Crustaceans such as crabs, lobsters and crayfish use dispersing odorant molecules to determine the location of predators, prey, potential mates and habitat. Odorant molecules diffuse in turbulent flows and are sensed by the olfactory organs of these animals, often using a flicking motion of their antennules. These antennules contain both chemosensory and mechanosensory sensilla, which enable them to detect both flow and odorants during a flick. To determine how simultaneous flow and odorant sampling can aid in search behavior, a 3-dimensional numerical model for the near-bed flow environment was created. A stream of odorant concentration was released into the flow creating a turbulent plume, and both temporally and spatially fluctuating velocity and odorant concentration were quantified. The plume characteristics show close resemblance to experimental measurements within a large laboratory flume. Results show that mean odorant concentration and it's intermittency, computed as dc/dt, increase towards the plume source, but the temporal and spatial rate of this increase is slow and suggests that long measurement times would be necessary to be useful for chemosensory guidance. Odorant fluxes measured transverse to the mean flow direction, quantified as the product of the instantaneous fluctuation in concentration and velocity, v′c′, do show statistically distinct magnitude and directional information on either side of a plume centerline over integration times of <0.5 s. Aquatic animals typically have neural responses to odorant and velocity fields at rates between 50 and 500 ms, suggesting this simultaneous sampling of both flow and concentration in a turbulent plume can aid in source tracking on timescales relevant to aquatic animals.
plume; olfaction; turbulence; tracking; crustacean; odorants
Fruit flies (Drosophila melanogaster) rely on their olfactory system to process environmental information. This information has to be transmitted without system-relevant loss by the olfactory system to deeper brain areas for learning. Here we study the role of several parameters of the fly's olfactory system and the environment and how they influence olfactory information transmission. We have designed an abstract model of the antennal lobe, the mushroom body and the inhibitory circuitry. Mutual information between the olfactory environment, simulated in terms of different odor concentrations, and a sub-population of intrinsic mushroom body neurons (Kenyon cells) was calculated to quantify the efficiency of information transmission. With this method we study, on the one hand, the effect of different connectivity rates between olfactory projection neurons and firing thresholds of Kenyon cells. On the other hand, we analyze the influence of inhibition on mutual information between environment and mushroom body. Our simulations show an expected linear relation between the connectivity rate between the antennal lobe and the mushroom body and firing threshold of the Kenyon cells to obtain maximum mutual information for both low and high odor concentrations. However, contradicting all-day experiences, high odor concentrations cause a drastic, and unrealistic, decrease in mutual information for all connectivity rates compared to low concentration. But when inhibition on the mushroom body is included, mutual information remains at high levels independent of other system parameters. This finding points to a pivotal role of inhibition in fly information processing without which the system efficiency will be substantially reduced.
Drosophila; information theory; mutual information; system efficiency; inhibitory neurons; odor concentration
An animal navigating to an unseen odor source must accurately resolve the spatiotemporal distribution of that stimulus in order to express appropriate upwind flight behavior. Intermittency of natural odor plumes, caused by air turbulence, is critically important for many insects, including the hawkmoth, Manduca sexta, for odor-modulated search behavior to an odor source. When a moth's antennae receive intermittent odor stimulation, the projection neurons (PNs) in the primary olfactory centers (the antennal lobes), which are analogous to the olfactory bulbs of vertebrates, generate discrete bursts of action potentials separated by periods of inhibition, suggesting that the PNs may use the binary burst/non-burst neural patterns to resolve and enhance the intermittency of the stimulus encountered in the odor plume.
We tested this hypothesis first by establishing that bicuculline methiodide reliably and reversibly disrupted the ability of PNs to produce bursting response patterns. Behavioral studies, in turn, demonstrated that after injecting this drug into the antennal lobe at the effective concentration used in the physiological experiments animals could no longer efficiently locate the odor source, even though they had detected the odor signal.
Our results establish a direct link between the bursting response pattern of PNs and the odor-tracking behavior of the moth, demonstrating the behavioral significance of resolving the dynamics of a natural odor stimulus in antennal lobe circuits.
Carbon dioxide (CO2) elicits an attractive host-seeking response from mosquitos [1–3] yet is innately aversive to Drosophila melanogaster [4, 5] despite being a plentiful byproduct of attractive fermenting food sources. Prior studies used walking flies exclusively, yet adults track distant food sources on the wing . Here we show that a fly tethered within a magnetic field allowing free rotation about the yaw axis  actively seeks a narrow CO2 plume during flight. Genetic disruption of the canonical CO2-sensing olfactory neurons does not alter in-flight attraction to CO2; however, antennal ablation and genetic disruption of the Ir64a acid sensor do. Surprisingly, mutation of the obligate olfactory coreceptor (Orco ) does not abolish CO2 aversion during walking  yet eliminates CO2 tracking in flight. The biogenic amine octopamine regulates critical physiological processes during flight [9–11], and blocking synaptic output from octopamine neurons inverts the valence assigned to CO2 and elicits an aversive response in flight. Combined, our results suggest that a novel Orco-mediated olfactory pathway that gains sensitivity to CO2 in flight via changes in octopamine levels, along with Ir64a, quickly switches the valence of a key environmental stimulus in a behavioral-state-dependent manner.
In Drosophila the fruit fly, coincident exposure to an odor and an aversive electric shock can produce robust behavioral memory. This behavioral memory is thought to be regulated by cellular memory traces within the central nervous system of the fly. These molecular, physiological or structural changes in neurons, induced by pairing odor and shock, regulate behavior by altering the neurons’ response to the learned environment. Recently, novel in vivo functional imaging techniques have allowed researchers to observe cellular memory traces in intact animals. These investigations have revealed interesting temporal and spatial dynamics of cellular memory traces. First, a short-term cellular memory trace was discovered that exists in the antennal lobe, an early site of olfactory processing. This trace represents the recruitment of new synaptic activity into the odor representation and forms for only a short period of time just after training. Second, an intermediate-term cellular memory trace was found in the dorsal paired medial neuron, a neuron thought to play a role in stabilizing olfactory memories. Finally, a long-term protein synthesis-dependent cellular memory trace was discovered in the mushroom bodies, a structure long implicated in olfactory learning and memory. Therefore, it appears that aversive olfactory associations are encoded by multiple cellular memory traces that occur in different regions of the brain with different temporal domains.
Drosophila; mushroom body; olfactory learning; memory trace
Drosophila melanogaster has an olfactory organ called the maxillary palp. It is smaller and numerically simpler than the antenna, and its specific role in behavior has long been unclear. Because of its proximity to the mouthparts, I explored the possibility of a role in taste behavior. Maxillary palp was tuned to mediate odor-induced taste enhancement: a sucrose solution was more appealing when simultaneously presented with the odorant 4-methylphenol. The same result was observed with other odors that stimulate other types of olfactory receptor neuron in the maxillary palp. When an antennal olfactory receptor was genetically introduced in the maxillary palp, the fly interpreted a new odor as a sweet-enhancing smell. These results all point to taste enhancement as a function of the maxillary palp. It also opens the door for studying integration of multiple senses in a model organism.
Ionotropic glutamate receptors (iGluRs) are a highly conserved family of ligand-gated ion channels present in animals, plants, and bacteria, which are best characterized for their roles in synaptic communication in vertebrate nervous systems. A variant subfamily of iGluRs, the Ionotropic Receptors (IRs), was recently identified as a new class of olfactory receptors in the fruit fly, Drosophila melanogaster, hinting at a broader function of this ion channel family in detection of environmental, as well as intercellular, chemical signals. Here, we investigate the origin and evolution of IRs by comprehensive evolutionary genomics and in situ expression analysis. In marked contrast to the insect-specific Odorant Receptor family, we show that IRs are expressed in olfactory organs across Protostomia—a major branch of the animal kingdom that encompasses arthropods, nematodes, and molluscs—indicating that they represent an ancestral protostome chemosensory receptor family. Two subfamilies of IRs are distinguished: conserved “antennal IRs,” which likely define the first olfactory receptor family of insects, and species-specific “divergent IRs,” which are expressed in peripheral and internal gustatory neurons, implicating this family in taste and food assessment. Comparative analysis of drosophilid IRs reveals the selective forces that have shaped the repertoires in flies with distinct chemosensory preferences. Examination of IR gene structure and genomic distribution suggests both non-allelic homologous recombination and retroposition contributed to the expansion of this multigene family. Together, these findings lay a foundation for functional analysis of these receptors in both neurobiological and evolutionary studies. Furthermore, this work identifies novel targets for manipulating chemosensory-driven behaviours of agricultural pests and disease vectors.
Ionotropic glutamate receptors (iGluRs) are a family of cell surface proteins best known for their role in allowing neurons to communicate with each other in the brain. We recently discovered a variant class of iGluRs in the fruit fly (Drosophila melanogaster), named Ionotropic Receptors (IRs), which function as olfactory receptors in its “nose,” prompting us to ask whether iGluR/IRs might have a more general function in detection of environmental chemicals. Here, we have identified families of IRs in olfactory and taste sensory organs throughout protostomes, one of the principal branches of animal life that includes snails, worms, crustaceans, and insects. Our findings suggest that this receptor family has an evolutionary ancient function in detecting odors and tastants in the external world. By comparing the repertoires of these chemosensory IRs among both closely- and distantly-related species, we have observed dynamic patterns of expansion and divergence of these receptor families in organisms occupying very different ecological niches. Notably, many of the receptors we have identified are in insects that are of significant harm to human health, such as the malaria mosquito. These proteins represent attractive targets for novel types of insect repellents to control the host-seeking behaviors of such pest species.
Drosophila larvae with a single sense organ locate a source of odor as well as larvae with two.
Do animals require bilateral input to track odors? A recent study reveals that fruit fly larvae can localize odor sources using unilateral inputs from a single functional sensory neuron, but that an enhanced signal-to-noise ratio provided by dual inputs is helpful in more challenging environments.
Using functional optical imaging in vivo, we demonstrate that the γ mushroom body (MB) neurons of Drosophila melanogaster respond with axonal calcium influx when odors or electric shock stimuli are presented to the fly. Pairing of odor and electric shock stimuli in a single training trial or multiple, massed training trials failed to modify the odor-evoked calcium signal when flies were tested at several different times after training. In contrast, animals that received multiple but spaced odor-shock pairings exhibited a robust increase in calcium influx into the MB axons when tested between 18 and 48 hr after training. This time window for the γ neuron memory trace is displaced relative to the modifications that occur between 9 and 24 hr after training in the α branch of the α/β MB neurons. The α/β and the γ neuron long-term memory traces were both blocked by expressing a repressor of the transcription factor Creb or a CaMKII hairpin RNA. These results demonstrate that behavioral long-term olfactory memory is encoded as modifications of calcium influx into distinct MB neurons during overlapping but different windows of time after training.
Drosophila; mushroom body; olfactory learning; memory trace; gamma neurons
Mosquito host-seeking behavior and heterogeneity in host distribution are important factors in predicting the transmission dynamics of mosquito-borne infections such as dengue fever, malaria, chikungunya, and West Nile virus. We develop and analyze a new mathematical model to describe the effect of spatial heterogeneity on the contact rate between mosquito vectors and hosts. The model includes odor plumes generated by spatially distributed hosts, wind velocity, and mosquito behavior based on both the prevailing wind and the odor plume. On a spatial scale of meters and a time scale of minutes, we compare the effectiveness of different plume-finding and plume-tracking strategies that mosquitoes could use to locate a host. The results show that two different models of chemotaxis are capable of producing comparable results given appropriate parameter choices and that host finding is optimized by a strategy of flying across the wind until the odor plume is intercepted. We also assess the impact of changing the level of host aggregation on mosquito host-finding success near the end of the host-seeking flight. When clusters of hosts are more tightly associated on smaller patches, the odor plume is narrower and the biting rate per host is decreased. For two host groups of unequal number but equal spatial density, the biting rate per host is lower in the group with more individuals, indicative of an attack abatement effect of host aggregation. We discuss how this approach could assist parameter choices in compartmental models that do not explicitly model the spatial arrangement of individuals and how the model could address larger spatial scales and other probability models for mosquito behavior, such as Lévy distributions.
Mosquito-borne diseases can spread when a mosquito bites a vertebrate host to obtain a blood meal for egg-laying. The first step in the transmission process consists of the mosquitoes seeking and finding a host. Mosquitoes use the wind direction and odors, such as carbon dioxide, emitted by the hosts in order to locate a host to bite. We present a spatial computational model of the host-seeking process in a region where hosts are heterogeneously distributed in clusters. The model is used to analyze the success in finding hosts once the mosquitoes are close to the host. We show that the number of mosquito-host contacts increases as hosts become more widely spaced within their clusters; that mosquito flight perpendicular to the wind leads to greater success in locating a host; and that the number of bites per host decreases when hosts aggregate into larger clusters.
In this paper, the design of a real-time image acquisition system for tracking the movement of Drosophila in three-dimensional space is presented. The system uses three calibrated and synchronized cameras to detect multiple flies and integrates the detected fly silhouettes to construct the three-dimensional visual hull models of each fly. We used an extended Kalman filter to estimate the state of each fly, given past positions from the reconstructed fly visual hulls. The results show that our approach constructs the three-dimensional visual hull of each fly from the detected image silhouettes and robustly tracks them at real-time rates. The system is suitable for a more detailed analysis of fly behaviour.
real-time three-dimensional tracking; Drosophila activity monitoring; visual hull construction; extended Kalman filtering
How is behaviour organised across sensory modalities? Specifically, we ask concerning the fruit fly Drosophila melanogaster how visual context affects olfactory learning and recall and whether information about visual context is getting integrated into olfactory memory. We find that changing visual context between training and test does not deteriorate olfactory memory scores, suggesting that these olfactory memories can drive behaviour despite a mismatch of visual context between training and test. Rather, both the establishment and the recall of olfactory memory are generally facilitated by light. In a follow-up experiment, we find no evidence for learning about combinations of odours and visual context as predictors for reinforcement even after explicit training in a so-called biconditional discrimination task. Thus, a ‘true’ interaction between visual and olfactory modalities is not evident; instead, light seems to influence olfactory learning and recall unspecifically, for example by altering motor activity, alertness or olfactory acuity.
Olfaction; Vision; Learning; Context; Biconditional discrimination
The nervous functions of an organism are primarily reflected in the behavior it is capable of. Measuring behavior quantitatively, at high-resolution and in an automated fashion provides valuable information about the underlying neural circuit computation. Accordingly, computer-vision applications for animal tracking are becoming a key complementary toolkit to genetic, molecular and electrophysiological characterization in systems neuroscience.
We present Sensory Orientation Software (SOS) to measure behavior and infer sensory experience correlates. SOS is a simple and versatile system to track body posture and motion of single animals in two-dimensional environments. In the presence of a sensory landscape, tracking the trajectory of the animal's sensors and its postural evolution provides a quantitative framework to study sensorimotor integration. To illustrate the utility of SOS, we examine the orientation behavior of fruit fly larvae in response to odor, temperature and light gradients. We show that SOS is suitable to carry out high-resolution behavioral tracking for a wide range of organisms including flatworms, fishes and mice.
Our work contributes to the growing repertoire of behavioral analysis tools for collecting rich and fine-grained data to draw and test hypothesis about the functioning of the nervous system. By providing open-access to our code and documenting the software design, we aim to encourage the adaptation of SOS by a wide community of non-specialists to their particular model organism and questions of interest.
The fruit fly Drosophila melanogaster has a sophisticated visual system and exhibits complex visual behaviors. Visual responses, vision processing and higher cognitive processes in Drosophila have been studied extensively. However, little is known about whether the retinal location of visual stimuli can affect fruit fly performance in various visual tasks. We tested the response of wild-type Berlin flies to visual stimuli at several vertical locations. Three paradigms were used in our study: visual operant conditioning, visual object fixation and optomotor response. We observed an acute zone for visual feature memorization in the upper visual field when visual patterns were presented with a black background. However, when a white background was used, the acute zone was in the lower visual field. Similar to visual feature memorization, the best locations for visual object fixation and optomotor response to a single moving stripe were in the lower visual field with a white background and the upper visual field with a black background. The preferred location for the optomotor response to moving gratings was around the equator of the visual field. Our results suggest that different visual processing pathways are involved in different visual tasks and that there is a certain degree of overlap between the pathways for visual feature memorization, visual object fixation and optomotor response.
Most odors are perceived to have the same quality over a large concentration range, but the neural mechanisms that permit concentration-invariant olfactory perception are unknown. In larvae of the vinegar fly Drosophila melanogaster, odors are sensed by an array of 25 odorant receptors expressed in 21 olfactory sensory neurons (OSNs). We investigated how subsets of larval OSNs with overlapping but distinct response properties cooperate to mediate perception of a given odorant across a range of concentrations.
Using calcium imaging, we found that ethyl butyrate, an ester perceived by humans as fruity, activated three OSNs with response thresholds that varied across three orders of magnitude. Whereas wild-type larvae were strongly attracted by this odor across a 500-fold range of concentration, individuals with only a single functional OSN showed attraction across a narrower concentration range corresponding to the sensitivity of each ethyl butyrate-tuned OSN. To clarify how the information carried by different OSNs is integrated by the olfactory system, we characterized the response properties of local inhibitory interneurons and projection neurons in the antennal lobe. Local interneurons only responded to high ethyl butyrate concentrations upon summed activation of at least two OSNs. Projection neurons showed a reduced response to odors when summed input from two OSNs impinged on the circuit compared to when there was only a single functional OSN.
Our results show that increasing odor concentrations induce progressive activation of concentration-tuned olfactory sensory neurons and concomitant recruitment of inhibitory local interneurons. We propose that the interplay of combinatorial OSN input and local interneuron activation allows animals to remain sensitive to odors across a large range of stimulus intensities.
Animals' behaviour towards odours depends on both odour quality and odour intensity. While neuronal coding of odour quality is fairly well studied, how odour intensity is treated by olfactory systems is less clear. Here we study odour intensity processing at the behavioural level, using the fruit fly Drosophila melanogaster. We trained flies by pairing a MEDIUM intensity of an odour with electric shock, and then, at a following test phase, measured flies' conditioned avoidance of either this previously trained MEDIUM intensity or a LOWer or a HIGHer intensity. With respect to 3-octanol, n-amylacetate and 4-methylcyclohexanol, we found that conditioned avoidance is strongest when training and test intensities match, speaking for intensity-specific memories. With respect to a fourth odour, benzaldehyde, on the other hand, we found no such intensity specificity. These results form the basis for further studies of odour intensity processing at the behavioural, neuronal and molecular level.
fruit fly; olfaction; odour intensity; associative learning; recognition; benzaldehyde
Cancer cells and non-cancer cells differ in their metabolism and they emit distinct volatile compound profiles, allowing to recognise cancer cells by their scent. Insect odorant receptors are excellent chemosensors with high sensitivity and a broad receptive range unmatched by current gas sensors. We thus investigated the potential of utilising the fruit fly's olfactory system to detect cancer cells. Using in vivo calcium imaging, we recorded an array of olfactory receptor neurons on the fruit fly's antenna. We performed multidimensional analysis of antenna responses, finding that cell volatiles from different cell types lead to characteristic response vectors. The distances between these response vectors are conserved across flies and can be used to discriminate healthy mammary epithelial cells from different types of breast cancer cells. This may expand the repertoire of clinical diagnostics, and it is the first step towards electronic noses equipped with biological sensors, integrating artificial and biological olfaction.