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1.  Spatial memory-based behaviors for locating sources of odor plumes 
Movement Ecology  2015;3(1):11.
Many animals must locate odorant point sources during key behaviors such as reproduction, foraging and habitat selection. Cues from such sources are typically distributed as air- or water-borne chemical plumes, characterized by high intermittency due to environmental turbulence and episodically rapid changes in position and orientation during wind or current shifts. Well-known examples of such behaviors include male moths, which have physiological and behavioral specializations for locating the sources of pheromone plumes emitted by females. Male moths and many other plume-following organisms exhibit “counter-turning” behavior, in which they execute a pre-planned sequence of cross-stream movements spanning all or part of an odorant plume, combined with upstream movements towards the source. Despite its ubiquity and ecological importance, theoretical investigation of counter-turning has so far been limited to a small subset of plausible behavioral algorithms based largely on classical biased random walk gradient-climbing or oscillator models.
We derive a model of plume-tracking behavior that assumes a simple spatially-explicit memory of previous encounters with odorant, an explicit statistical model of uncertainty about the plume’s position and extent, and the ability to improve estimates of plume characteristics over sequential encounters using Bayesian updating. The model implements spatial memory and effective cognitive strategies with minimal neural processing. We show that laboratory flight tracks of Manduca sexta moths are consistent with predictions of our spatial memory-based model. We assess plume-following performance of the spatial memory-based algorithm in terms of success and efficiency metrics, and in the context of “contests” in which the winner is the first among multiple simulated moths to locate the source.
Even rudimentary spatial memory can greatly enhance plume-following. In particular, spatial memory can maintain source-seeking success even when plumes are so intermittent that no pheromone is detected in most cross-wind transits. Performance metrics reflect trade-offs between “risk-averse” strategies (wide cross-wind movements, slow upwind advances) that reliably but slowly locate odor sources, and “risk-tolerant” strategies (narrow cross-wind movements, fast upwind advances) that often fail to locate a source but are fast when successful. Success in contests of risk-averse vs. risk-tolerant behaviors varies strongly with the number of competitors, suggesting empirically testable predictions for diverse plume-following taxa. More generally, spatial memory-based models provide tractable, explicit theoretical linkages between sensory biomechanics, neurophysiology and behavior, and ecological and evolutionary dynamics operating at much larger spatio-temporal scales.
Electronic supplementary material
The online version of this article (doi:10.1186/s40462-015-0037-6) contains supplementary material, which is available to authorized users.
PMCID: PMC4424511  PMID: 25960875
Bayesian estimation; Gaussian puff model; odor source location; moth behavior; Manduca sexta
2.  Projection neurons in Drosophila antennal lobes signal the acceleration of odor concentrations 
eLife  null;4:e06651.
Temporal experience of odor gradients is important in spatial orientation of animals. The fruit fly Drosophila melanogaster exhibits robust odor-guided behaviors in an odor gradient field. In order to investigate how early olfactory circuits process temporal variation of olfactory stimuli, we subjected flies to precisely defined odor concentration waveforms and examined spike patterns of olfactory sensory neurons (OSNs) and projection neurons (PNs). We found a significant temporal transformation between OSN and PN spike patterns, manifested by the PN output strongly signaling the OSN spike rate and its rate of change. A simple two-dimensional model admitting the OSN spike rate and its rate of change as inputs closely predicted the PN output. When cascaded with the rate-of-change encoding by OSNs, PNs primarily signal the acceleration and the rate of change of dynamic odor stimuli to higher brain centers, thereby enabling animals to reliably respond to the onsets of odor concentrations.
eLife digest
Fruit flies are attracted to the smell of rotting fruit, and use it to guide them to nearby food sources. However, this task is made more challenging by the fact that the distribution of scent or odor molecules in the air is constantly changing. Fruit flies therefore need to cope with, and exploit, this variation if they are to use odors as cues.
Odor molecules bind to receptors on the surface of nerve cells called olfactory sensory neurons, and trigger nerve impulses that travel along these cells. The olfactory sensory neurons are connected to other cells called projection neurons that in turn relay information to the higher centers of the brain. While many studies have investigated how fruit flies can distinguish between different odors, less is known about how animals can use variation in the strength of an odor to guide them towards its source.
Kim et al. have now addressed this question by devising a method for delivering precise quantities of odors in controlled patterns to fruit flies, and then measuring the responses of olfactory sensory neurons and projection neurons. These experiments revealed that olfactory sensory neurons—which are found mainly in the flies' antennae—responded most strongly whenever an odor changed rapidly in strength, and showed relatively little response to constant odors. An independent study by Schulze, Gomez-Marin et al. found that olfactory sensory neurons in fruit fly larvae also respond in a similar way.
Kim et al. also found that the response of the projection neurons depended on both the rate of nerve impulses in the olfactory sensory neurons and on how quickly this rate was changing. But, unlike the olfactory sensory neurons, projection neurons showed their strongest responses immediately after an odor first appeared.
Thus, in contrast to organisms such as bacteria and worms, which are highly sensitive to the local concentration gradients of odors, fruit flies instead appear to be more responsive to the sudden appearance of an odor in their environment. Kim et al. suggest that this difference may reflect the fact that for ground-based organisms, local gradients are generally reliable predictors of the location of an odor source. However, for flying insects, continually changing air currents mean that predictable local gradients are less common. Therefore, the ability to detect a hint of an odor before the wind changes is a more useful skill.
PMCID: PMC4466247  PMID: 25974217
olfactory sensory neurons; projection neurons; temporal processing; acceleration encoding; two-dimensional linear-nonlinear model; antennal lobes; D. melanogaster
3.  Contrast enhancement of stimulus intermittency in a primary olfactory network and its behavioral significance 
Journal of Biology  2009;8(2):21.
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.
PMCID: PMC2687775  PMID: 19232128
4.  Flies require bilateral sensory input to track odor gradients in flight 
Current biology : CB  2009;19(15):1301-1307.
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 [1] and bilateral wind cues [2], 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 [6]. 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 [9], 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].
PMCID: PMC2726901  PMID: 19576769
5.  Olfactory Neuromodulation of Motion Vision Circuitry in Drosophila 
Current Biology  2015;25(4):467-472.
It is well established that perception is largely multisensory [1]; often served by modalities such as touch, vision, and hearing that detect stimuli emanating from a common point in space [2, 3]; and processed by brain tissue maps that are spatially aligned [4]. However, the neural interactions among modalities that share no spatial stimulus domain yet are essential for robust perception within noisy environments remain uncharacterized. Drosophila melanogaster makes its living navigating food odor plumes. Odor acts to increase the strength of gaze-stabilizing optomotor reflexes [5] to keep the animal aligned within an invisible plume, facilitating odor localization in free flight [6–8]. Here, we investigate the cellular mechanism for cross-modal behavioral interactions. We characterize a wide-field motion-selective interneuron of the lobula plate that shares anatomical and physiological similarities with the “Hx” neuron identified in larger flies [9, 10]. Drosophila Hx exhibits cross-modal enhancement of visual responses by paired odor, and presynaptic inputs to the lobula plate are required for behavioral odor tracking but are not themselves the target of odor modulation, nor is the neighboring wide-field “HSE” neuron [11]. Octopaminergic neurons mediating increased visual responses upon flight initiation [12] also show odor-evoked calcium modulations and form connections with Hx dendrites. Finally, restoring synaptic vesicle trafficking within the octopaminergic neurons of animals carrying a null mutation for all aminergic signaling [13] is sufficient to restore odor-tracking behavior. These results are the first to demonstrate cellular mechanisms underlying visual-olfactory integration required for odor localization in fruit flies, which may be representative of adaptive multisensory interactions across taxa.
•Small-field motion detection neurons are required for odor-tracking behavior•Responses of a directional wide-field interneuron (Hx) increase with paired odor•Odor activates octopaminergic (OA) neurons that innervate the visual system•OA cells contact Hx; OA vesicle trafficking is required for odor-tracking behavior
Wasserman et al. report that a directionally selective wide-field motion-detecting neuron (Hx) in the fly increases response gain with paired odor. This multimodal interaction is dependent upon vesicle trafficking from octopaminergic neurons, which are themselves responsive to odor and make cell-cell contact with Hx.
PMCID: PMC4331282  PMID: 25619767
6.  Odor Detection in Manduca sexta Is Optimized when Odor Stimuli Are Pulsed at a Frequency Matching the Wing Beat during Flight 
PLoS ONE  2013;8(11):e81863.
Sensory systems sample the external world actively, within the context of self-motion induced disturbances. Mammals sample olfactory cues within the context of respiratory cycles and have adapted to process olfactory information within the time frame of a single sniff cycle. In plume tracking insects, it remains unknown whether olfactory processing is adapted to wing beating, which causes similar physical effects as sniffing. To explore this we first characterized the physical properties of our odor delivery system using hotwire anemometry and photo ionization detection, which confirmed that odor stimuli were temporally structured. Electroantennograms confirmed that pulse trains were tracked physiologically. Next, we quantified odor detection in moths in a series of psychophysical experiments to determine whether pulsing odor affected acuity. Moths were first conditioned to respond to a target odorant using Pavlovian olfactory conditioning. At 24 and 48 h after conditioning, moths were tested with a dilution series of the conditioned odor. On separate days odor was presented either continuously or as 20 Hz pulse trains to simulate wing beating effects. We varied pulse train duty cycle, olfactometer outflow velocity, pulsing method, and odor. Results of these studies, established that detection was enhanced when odors were pulsed. Higher velocity and briefer pulses also enhanced detection. Post hoc analysis indicated enhanced detection was the result of a significantly lower behavioral response to blank stimuli when presented as pulse trains. Since blank responses are a measure of false positive responses, this suggests that the olfactory system makes fewer errors (i.e. is more reliable) when odors are experienced as pulse trains. We therefore postulate that the olfactory system of Manduca sexta may have evolved mechanisms to enhance odor detection during flight, where the effects of wing beating represent the norm. This system may even exploit temporal structure in a manner similar to sniffing.
PMCID: PMC3836951  PMID: 24278463
7.  Mechanisms Underlying Population Response Dynamics in Inhibitory Interneurons of the Drosophila Antennal Lobe 
The Journal of Neuroscience  2016;36(15):4325-4338.
Local inhibitory neurons control the timing of neural activity in many circuits. To understand how inhibition controls timing, it is important to understand the dynamics of activity in populations of local inhibitory interneurons, as well as the mechanisms that underlie these dynamics. Here we describe the in vivo response dynamics of a large population of inhibitory local neurons (LNs) in the Drosophila melanogaster antennal lobe, the analog of the vertebrate olfactory bulb, and we dissect the network and intrinsic mechanisms that give rise to these dynamics. Some LNs respond to odor onsets (“ON” cells) and others to offsets (“OFF” cells), whereas still others respond at both times. Moreover, different LNs signal odor concentration fluctuations on different timescales. Some respond rapidly, and can track rapid concentration fluctuations. Others respond slowly, and are best at tracking slow fluctuations. We found a continuous spectrum of preferred stimulation timescales among LNs, as well as a continuum of ON–OFF behavior. Using in vivo whole-cell recordings, we show that the timing of an LN′s response (ON vs OFF) can be predicted from the interplay of excitatory and inhibitory synaptic currents that it receives. Meanwhile, the preferred timescale of an LN is related to its intrinsic properties. These results illustrate how a population of inhibitory interneurons can collectively encode bidirectional changes in stimulus intensity on multiple timescales, and how this can arise via an interaction between synaptic and intrinsic mechanisms.
SIGNIFICANCE STATEMENT Most neural circuits contain diverse populations of inhibitory interneurons. The way inhibition shapes network activity will depend on the spiking dynamics of the interneuron population. Here we describe the dynamics of activity in a large population of inhibitory interneurons in the first brain relay of the fruit fly olfactory system. Because odor plumes fluctuate on multiple timescales, the drive to this circuit can vary over a range of frequencies. We show how synaptic and cellular mechanisms interact to recruit different interneurons at different times, and in response to different temporal features of odor stimuli. As a result, inhibition is recruited over a range of conditions, and there is the potential to tune the timing of inhibition as the environment changes.
PMCID: PMC4829653  PMID: 27076428
Drosophila antennal lobe; inhibitory interneurons; intrinsic conductances; network dynamics; olfaction; synaptic dynamics
8.  Neural encoding of odors during active sampling and in turbulent plumes 
Neuron  2015;88(2):403-418.
Sensory inputs are often fluctuating and intermittent, yet animals reliably utilize them to direct behavior. Here we ask how natural stimulus fluctuations influence the dynamic neural encoding of odors. Using the locust olfactory system, we isolated two main causes of odor intermittency: chaotic odor plumes and active sampling behaviors. Despite their irregularity, chaotic odor plumes still drove dynamic neural response features including the synchronization, temporal patterning, and short-term plasticity of spiking in projection neurons, enabling classifier-based stimulus identification and activating downstream decoders (Kenyon cells). Locusts can also impose odor intermittency through active sampling movements with their unrestrained antennae. Odors triggered immediate, spatially-targeted antennal scanning that, paradoxically, weakened individual neural responses. However, these frequent but weaker responses were highly informative about stimulus location. Thus, not only are odor-elicited dynamic neural responses compatible with natural stimulus fluctuations and important for stimulus identification, but locusts actively increase intermittency, possibly to improve stimulus localization.
PMCID: PMC4742573  PMID: 26456047
9.  Simultaneous Sampling of Flow and Odorants by Crustaceans can Aid Searches within a Turbulent Plume 
Sensors (Basel, Switzerland)  2013;13(12):16591-16610.
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.
PMCID: PMC3892349  PMID: 24300599
plume; olfaction; turbulence; tracking; crustacean; odorants
10.  A Magnetic Tether System to Investigate Visual and Olfactory Mediated Flight Control in Drosophila 
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.
PMCID: PMC2953965  PMID: 19066526
11.  Neurally Encoding Time for Olfactory Navigation 
PLoS Computational Biology  2016;12(1):e1004682.
Accurately encoding time is one of the fundamental challenges faced by the nervous system in mediating behavior. We recently reported that some animals have a specialized population of rhythmically active neurons in their olfactory organs with the potential to peripherally encode temporal information about odor encounters. If these neurons do indeed encode the timing of odor arrivals, it should be possible to demonstrate that this capacity has some functional significance. Here we show how this sensory input can profoundly influence an animal’s ability to locate the source of odor cues in realistic turbulent environments—a common task faced by species that rely on olfactory cues for navigation. Using detailed data from a turbulent plume created in the laboratory, we reconstruct the spatiotemporal behavior of a real odor field. We use recurrence theory to show that information about position relative to the source of the odor plume is embedded in the timing between odor pulses. Then, using a parameterized computational model, we show how an animal can use populations of rhythmically active neurons to capture and encode this temporal information in real time, and use it to efficiently navigate to an odor source. Our results demonstrate that the capacity to accurately encode temporal information about sensory cues may be crucial for efficient olfactory navigation. More generally, our results suggest a mechanism for extracting and encoding temporal information from the sensory environment that could have broad utility for neural information processing.
Author Summary
Many animals navigate turbulent environments using odor cues, a behavior known as olfactory search. We propose a neural mechanism for olfactory search based on evidence that a functional subset of olfactory receptor neurons (ORNs) called bursting ORNs or bORNs can encode the time intervals between successive encounters with odor. We show that these time intervals are estimators of the recurrence time, an information-rich statistic of the turbulent flow. Using a computational model parameterized with data from an actual turbulent plume, we demonstrate that a searcher can locate an odor source efficiently using only input from bORNs. These findings provide scientific evidence that the most important navigational information captured by the olfactory system may come in the form of measurements of time.
PMCID: PMC4711578  PMID: 26730727
12.  Multisensory integration for odor tracking by flying Drosophila 
Many see fruit flies as an annoyance, invading our homes with a nagging persistence and efficiency. Yet from a scientific perspective, these tiny animals are a wonder of multisensory integration, capable of tracking fragmented odor plumes amidst turbulent winds and constantly varying visual conditions. The peripheral olfactory, mechanosensory, and visual systems of the fruit fly, Drosophila melanogaster, have been studied in great detail;1–4 however, the mechanisms by which fly brains integrate information from multiple sensory modalities to facilitate robust odor tracking remain elusive. Our studies on olfactory orientation by flying flies reveal that these animals do not simply follow their “nose“; rather, fruit flies require mechanosensory and visual input to track odors in flight.5,6 Collectively, these results shed light on the neural circuits involved in odor localization by fruit flies in the wild and illuminate the elegant complexity underlying a behavior to which the annoyed and amazed are familiar.
PMCID: PMC2881244  PMID: 20539786
vision; olfaction; mechanosensory; antennae; visual processing; motor control; insect behavior; behavioral neuroscience; neuroethology; sensory ecology
13.  Starvation promotes concerted modulation of appetitive olfactory behavior via parallel neuromodulatory circuits 
eLife  null;4:e08298.
The internal state of an organism influences its perception of attractive or aversive stimuli and thus promotes adaptive behaviors that increase its likelihood of survival. The mechanisms underlying these perceptual shifts are critical to our understanding of how neural circuits support animal cognition and behavior. Starved flies exhibit enhanced sensitivity to attractive odors and reduced sensitivity to aversive odors. Here, we show that a functional remodeling of the olfactory map is mediated by two parallel neuromodulatory systems that act in opposing directions on olfactory attraction and aversion at the level of the first synapse. Short neuropeptide F sensitizes an antennal lobe glomerulus wired for attraction, while tachykinin (DTK) suppresses activity of a glomerulus wired for aversion. Thus we show parallel neuromodulatory systems functionally reconfigure early olfactory processing to optimize detection of nutrients at the risk of ignoring potentially toxic food resources.
eLife digest
Animals typically need to forage for their food, but doing so is not without risk. Foraging can expose an animal to predators and harmful toxins. Many animals use odors and other chemical signals to help them locate food or to avoid harm. In some animals, such as fruit flies, different parts of the nervous system are hardwired to encourage individuals to move towards attractive odors or away from unpleasant ones.
Fruit flies feed on the yeast that grows on decaying fruit. They do so by ignoring fresh fruits (which have very little yeast) and avoiding overly-rotten fruits (which might contain toxic chemicals). To determine ripeness, flies use a fruit's vinegar levels: fresh fruits contain low levels of vinegar, while fermented fruits have high levels. Previous studies using low levels of vinegar have shown that well-fed flies largely ignore the scent, while starving flies are attracted to it.
Ko et al. have built on the results of previous studies and now report that starving fruit flies are much less sensitive to unfavorable odors in high levels of vinegar and much more sensitive to favorable odors in low levels of vinegar. This behavior is due to two neuropeptides (molecules that carry signals between neurons) that have opposite effects on different parts of the fly's nervous system. One of the neuropeptides made the groups of neurons that respond to attractive odors more responsive, while the other suppressed the activity of neurons that normally respond to unpleasant odors. Together these changes could encourage the animals to take more risks when they are hungry, by suppressing of their ability to recognize noxious or harmful chemicals in favor of their ability to perceive attractive odors.
The effect of both neuropeptides is triggered by the insulin hormone, which carries information about the metabolic state (for example, whether it is starving or well-fed) throughout the whole animal. Thus, individual neurons may read the same metabolic signals and then respond in different ways to fine-tune the activity of nearby circuits of neurons to alter foraging behavior in a coordinated manner. Furthermore, it is almost certain that similar changes to the sensory system could affect an animal's appetite for food. One of the next challenges will be to attempt to understand if and how appetite in humans might be controlled in a similar way.
PMCID: PMC4531282  PMID: 26208339
olfaction; sNPF; insulin; RNA-seq; two-photon imaging; substance P; D. melanogaster
14.  Antennal lobe representations are optimized when olfactory stimuli are periodically structured to simulate natural wing beat effects 
Animals use behaviors to actively sample the environment across a broad spectrum of sensory domains. These behaviors discretize the sensory experience into unique spatiotemporal moments, minimize sensory adaptation, and enhance perception. In olfaction, behaviors such as sniffing, antennal flicking, and wing beating all act to periodically expose olfactory epithelium. In mammals, it is thought that sniffing enhances neural representations; however, the effects of insect wing beating on representations remain unknown. To determine how well the antennal lobe (AL) produces odor dependent representations when wing beating effects are simulated, we used extracellular methods to record neural units and local field potentials (LFPs) from moth AL. We recorded responses to odors presented as prolonged continuous stimuli or periodically as 20 and 25 Hz pulse trains designed to simulate the oscillating effects of wing beating around the antennae during odor guided flight. Using spectral analyses, we show that ~25% of all recorded units were able to entrain to “pulsed stimuli”; this includes pulsed blanks, which elicited the strongest overall entrainment. The strength of entrainment to pulse train stimuli was dependent on molecular features of the odorants, odor concentration, and pulse train duration. Moreover, units showing pulse tracking responses were highly phase locked to LFPs during odor stimulation, indicating that unit-LFP phase relationships are stimulus-driven. Finally, a Euclidean distance-based population vector analysis established that AL odor representations are more robust, peak more quickly, and do not show adaptation when odors were presented at the natural wing beat frequency as opposed to prolonged continuous stimulation. These results suggest a general strategy for optimizing olfactory representations, which exploits the natural rhythmicity of wing beating by integrating mechanosensory and olfactory cues at the level of the AL.
PMCID: PMC4053783  PMID: 24971052
olfaction; temporal coding; oscillations; synchrony; active sensing; sniffing; odor representation
15.  A Spatial Model of Mosquito Host-Seeking Behavior 
PLoS Computational Biology  2012;8(5):e1002500.
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.
Author Summary
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.
PMCID: PMC3355069  PMID: 22615546
16.  Learned odor discrimination in Drosophila without distinct combinatorial odor maps in the antennal lobe 
Current biology : CB  2008;18(21):1668-1674.
A unifying feature of mammalian and insect olfactory systems is that olfactory sensory neurons (OSNs) expressing the same unique odorant receptor gene converge onto the same glomeruli in the brain (1–7). Most odorants activate a combination of receptors and thus distinct patterns of glomeruli, forming a proposed combinatorial spatial code that could support discrimination between a large number of odorants (8–11). OSNs also exhibit odor-evoked responses with complex temporal dynamics (11), but the contribution of this activity to behavioral odor discrimination has received little attention (12). Here we investigated the importance of spatial encoding in the relatively simple Drosophila antennal lobe. We show that Drosophila can learn to discriminate between two odorants with one functional class of Or83b-expressing OSNs. Furthermore, these flies encode one odorant from a mixture, and cross-adapt to odorants that activate the relevant OSN class, demonstrating that they discriminate odorants using the same OSNs. Lastly, flies with a single class of Or83b-expressing OSNs recognize a specific odorant across a range of concentration indicating that they encode odorant identity. Therefore flies can distinguish odorants without discrete spatial codes in the antennal lobe, implying an important role for odorant-evoked temporal dynamics in behavioral odorant discrimination.
PMCID: PMC2602956  PMID: 18951022
17.  Physical Processes and Real-Time Chemical Measurement of the Insect Olfactory Environment 
Journal of chemical ecology  2008;34(7):837-853.
Odor-mediated insect navigation in airborne chemical plumes is vital to many ecological interactions, including mate finding, flower nectaring, and host locating (where disease transmission or herbivory may begin). After emission, volatile chemicals become rapidly mixed and diluted through physical processes that create a dynamic olfactory environment. This review examines those physical processes and some of the analytical technologies available to characterize those behavior-inducing chemical signals at temporal scales equivalent to the olfactory processing in insects. In particular, we focus on two areas of research that together may further our understanding of olfactory signal dynamics and its processing and perception by insects. First, measurement of physical atmospheric processes in the field can provide insight into the spatiotemporal dynamics of the odor signal available to insects. Field measurements in turn permit aspects of the physical environment to be simulated in the laboratory, thereby allowing careful investigation into the links between odor signal dynamics and insect behavior. Second, emerging analytical technologies with high recording frequencies and field-friendly inlet systems may offer new opportunities to characterize natural odors at spatiotemporal scales relevant to insect perception and behavior. Characterization of the chemical signal environment allows the determination of when and where olfactory-mediated behaviors may control ecological interactions. Finally, we argue that coupling of these two research areas will foster increased understanding of the physicochemical environment and enable researchers to determine how olfactory environments shape insect behaviors and sensory systems.
PMCID: PMC2778261  PMID: 18548311
Odor plume; Insect behavior; Odor-plume tracking; PTRMS; Mass spectrometry; Gas chromatography; Odor landscape
18.  Computations underlying Drosophila photo-taxis, odor-taxis, and multi-sensory integration 
eLife  null;4:e06229.
To better understand how organisms make decisions on the basis of temporally varying multi-sensory input, we identified computations made by Drosophila larvae responding to visual and optogenetically induced fictive olfactory stimuli. We modeled the larva's navigational decision to initiate turns as the output of a Linear-Nonlinear-Poisson cascade. We used reverse-correlation to fit parameters to this model; the parameterized model predicted larvae's responses to novel stimulus patterns. For multi-modal inputs, we found that larvae linearly combine olfactory and visual signals upstream of the decision to turn. We verified this prediction by measuring larvae's responses to coordinated changes in odor and light. We studied other navigational decisions and found that larvae integrated odor and light according to the same rule in all cases. These results suggest that photo-taxis and odor-taxis are mediated by a shared computational pathway.
eLife digest
Living organisms can sense cues from their surroundings and respond in appropriate ways. For example, animals will often move towards the smell of food or away from potential threats, such as predators. However, it is not fully understood how an animal's nervous system is set up to allow sensory information to control how the animal navigates its environment. It is also not clear how animals ‘decide’ what to do when they receive conflicting information from different senses.
Optogenetics is a technique that allows neuroscientists to control the activities of individual nerve cells simply by shining light on to them. Fruit fly larvae have a simple but well-studied nervous system, and they are nearly transparent, so scientists can use optogenetics to activate nerve cells in freely moving larvae.
Fruit fly larvae move in a series of forward ‘runs’ and direction-changing ‘turns’ and use sensory cues to decide when to turn, how large of a turn to make, and whether to turn left or right. Gepner, Mihovilovic Skanata et al. used optogenetics to stimulate different combinations of sensory nerve cells in larvae, while tracking the larvae's movements to discover exactly what information they used to make these decisions. An independent study by Hernandez-Nunez et al. also used a similar approach.
Fruit fly larvae are attracted towards scents from rotting fruit and are repelled by light—in particular, larvae are most sensitive to blue light but cannot detect red light. Therefore, Gepner, Mihovilovic Skanata et al. could expose the larvae to blue light to activate light-sensing nerve cells as normal, and use red light to activate odor-sensing nerve cells via optogenetics. These experiments showed that larvae changed direction more often when the level of blue light was increased or when the level of red light (which simulated the detection of odors from rotting fruits) was decreased.
Analysis of the data from these experiments revealed that larvae essentially assign negative values to the blue light and positive values to the ‘odor-mimicking’ red light. The larvae then use the sum of these two values to dictate their next move. This suggests that navigation in response to both light and odors is supported by the same pathways in a larva's nervous system.
The approach of using optogenetics in combination with quantitative analysis, as used in these two independent studies, is now opening the door to a more complete understanding of the connections between the activities of sensory nerve cells and perception and behavior.
PMCID: PMC4466338  PMID: 25945916
olfaction; vision; multi-sensory integration; optogenetics; reverse-correlation; D. melanogaster
19.  Dynamical feature extraction at the sensory periphery guides chemotaxis 
eLife  null;4:e06694.
Behavioral strategies employed for chemotaxis have been described across phyla, but the sensorimotor basis of this phenomenon has seldom been studied in naturalistic contexts. Here, we examine how signals experienced during free olfactory behaviors are processed by first-order olfactory sensory neurons (OSNs) of the Drosophila larva. We find that OSNs can act as differentiators that transiently normalize stimulus intensity—a property potentially derived from a combination of integral feedback and feed-forward regulation of olfactory transduction. In olfactory virtual reality experiments, we report that high activity levels of the OSN suppress turning, whereas low activity levels facilitate turning. Using a generalized linear model, we explain how peripheral encoding of olfactory stimuli modulates the probability of switching from a run to a turn. Our work clarifies the link between computations carried out at the sensory periphery and action selection underlying navigation in odor gradients.
eLife digest
Fruit flies are attracted to the smell of rotting fruit, and use it to guide them to nearby food sources. However, this task is made more challenging by the fact that the distribution of scent or odor molecules in the air is constantly changing. Fruit flies therefore need to cope with, and exploit, this variation if they are to use odors as cues.
Odor molecules bind to receptors on the surface of nerve cells called olfactory sensory neurons, and trigger nerve impulses that travel along these cells. While many studies have investigated how fruit flies can distinguish between different odors, less is known about how animals can use variation in the strength of an odor to guide them towards its source.
Optogenetics is a technique that allows neuroscientists to control the activities of individual nerve cells, simply by shining light on to them. Because fruit fly larvae are almost transparent, optogenetics can be used on freely moving animals. Now, Schulze, Gomez-Marin et al. have used optogenetics in these larvae to trigger patterns of activity in individual olfactory sensory neurons that mimic the activity patterns elicited by real odors. These virtual realities were then used to study, in detail, some of the principles that control the sensory navigation of a larva—as it moves using a series of forward ‘runs’ and direction-changing ‘turns’.
Olfactory sensory neurons responded most strongly whenever light levels changed rapidly in strength (which simulated a rapid change in odor concentration). On the other hand, these neurons showed relatively little response to constant light levels (i.e., constant odors). This indicates that the activity of olfactory sensory neurons typically represents the rate of change in the concentration of an odor. An independent study by Kim et al. found that olfactory sensory neurons in adult fruit flies also respond in a similar way.
Schulze, Gomez-Marin et al. went on to show that the signals processed by a single type of olfactory sensory neuron could be used to predict a larva's behavior. Larvae tended to turn less when their olfactory sensory neurons were highly active. Low levels and inhibition of activity in the olfactory sensory neurons had the opposite effect; this promoted turning. It remains to be determined how this relatively simple control principle is implemented by the neural circuits that connect sensory neurons to the parts of a larva's nervous system that are involved with movement.
PMCID: PMC4468351  PMID: 26077825
chemotaxis; olfaction; optogenetics; electrophysiology; sensorimotor control; computational modeling; D. melanogaster
20.  A Challenge for a Male Noctuid Moth? Discerning the Female Sex Pheromone against the Background of Plant Volatiles 
Finding a partner is an essential task for members of all species. Like many insects, females of the noctuid moth Heliothis virescens release chemical cues consisting of a species-specific pheromone blend to attract conspecific males. While tracking these blends, male moths are also continuously confronted with a wide range of other odor molecules, many of which are plant volatiles. Therefore, we analyzed how background plant odors influence the degree of male moth attraction to pheromones. In order to mimic a natural situation, we tracked pheromone-guided behavior when males were presented with the headspaces of each of two host plants in addition to the female pheromone blend. Since volatile emissions are also dependent on the physiological state of the plant, we compared pheromone attraction in the background of both damaged and intact plants. Surprisingly, our results show that a natural odor bouquet does not influence flight behavior at all, although previous studies had shown a suppressive effect at the sensory level. We also chose different concentrations of single plant-emitted volatiles, which have previously been shown to be neurophysiologically relevant, and compared their influence on pheromone attraction. We observed that pheromone attraction in male moths was significantly impaired in a concentration-dependent manner when single plant volatiles were added. Finally, we quantified the amounts of volatile emission in our experiments using gas chromatography. Notably, when the natural emissions of host plants were compared with those of the tested single plant compounds, we found that host plants do not release volatiles at concentrations that impact pheromone-guided flight behavior of the moth. Hence, our results lead to the conclusion that pheromone-plant interactions in Heliothis virescens might be an effect of stimulation with supra-natural plant odor concentrations, whereas under more natural conditions the olfactory system of the male moth appears to be well adapted to follow the female pheromone plume without interference from plant-emitted odors.
PMCID: PMC4843018  PMID: 27199761
Heliothis virescens; pheromone-guided flight behavior; plant volatiles; wind tunnel; GC-MS
21.  A carboxylesterase, Esterase-6, modulates sensory physiological and behavioral response dynamics to pheromone in Drosophila 
BMC Biology  2012;10:56.
Insects respond to the spatial and temporal dynamics of a pheromone plume, which implies not only a strong response to 'odor on', but also to 'odor off'. This requires mechanisms geared toward a fast signal termination. Several mechanisms may contribute to signal termination, among which odorant-degrading enzymes. These enzymes putatively play a role in signal dynamics by a rapid inactivation of odorants in the vicinity of the sensory receptors, although direct in vivo experimental evidences are lacking. Here we verified the role of an extracellular carboxylesterase, esterase-6 (Est-6), in the sensory physiological and behavioral dynamics of Drosophila melanogaster response to its pheromone, cis-vaccenyl acetate (cVA). Est-6 was previously linked to post-mating effects in the reproductive system of females. As Est-6 is also known to hydrolyze cVA in vitro and is expressed in the main olfactory organ, the antenna, we tested here its role in olfaction as a putative odorant-degrading enzyme.
We first confirm that Est-6 is highly expressed in olfactory sensilla, including cVA-sensitive sensilla, and we show that expression is likely associated with non-neuronal cells. Our electrophysiological approaches show that the dynamics of olfactory receptor neuron (ORN) responses is strongly influenced by Est-6, as in Est-6° null mutants (lacking the Est-6 gene) cVA-sensitive ORN showed increased firing rate and prolonged activity in response to cVA. Est-6° mutant males had a lower threshold of behavioral response to cVA, as revealed by the analysis of two cVA-induced behaviors. In particular, mutant males exhibited a strong decrease of male-male courtship, in association with a delay in courtship initiation.
Our study presents evidence that Est-6 plays a role in the physiological and behavioral dynamics of sex pheromone response in Drosophila males and supports a role of Est-6 as an odorant-degrading enzyme (ODE) in male antennae. Our results also expand the role of Est-6 in Drosophila biology, from reproduction to olfaction, and highlight the role of ODEs in insect olfaction.
PMCID: PMC3414785  PMID: 22715942
carboxylesterase; esterase 6; olfaction; pheromone; signal termination
22.  Intermittency Coding in the Primary Olfactory System: A Neural Substrate for Olfactory Scene Analysis 
The Journal of Neuroscience  2014;34(3):941-952.
The spatial and temporal characteristics of the visual and acoustic sensory input are indispensable attributes for animals to perform scene analysis. In contrast, research in olfaction has focused almost exclusively on how the nervous system analyzes the quality and quantity of the sensory signal and largely ignored the spatiotemporal dimension especially in longer time scales. Yet, detailed analyses of the turbulent, intermittent structure of water- and air-borne odor plumes strongly suggest that spatio-temporal information in longer time scales can provide major cues for olfactory scene analysis for animals. We show that a bursting subset of primary olfactory receptor neurons (bORNs) in lobster has the unexpected capacity to encode the temporal properties of intermittent odor signals. Each bORN is tuned to a specific range of stimulus intervals, and collectively bORNs can instantaneously encode a wide spectrum of intermittencies. Our theory argues for the existence of a novel peripheral mechanism for encoding the temporal pattern of odor that potentially serves as a neural substrate for olfactory scene analysis.
PMCID: PMC3891969  PMID: 24431452
bursting olfactory receptor neuron; interval estimation; neural coding; olfactory scene analysis; point process; uncoupled oscillators
23.  Visually Mediated Odor Tracking During Flight in Drosophila 
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.
PMCID: PMC2781825  PMID: 19229181
24.  Decoding odor quality and intensity in the Drosophila brain 
eLife  null;3:e04147.
To internally reflect the sensory environment, animals create neural maps encoding the external stimulus space. From that primary neural code relevant information has to be extracted for accurate navigation. We analyzed how different odor features such as hedonic valence and intensity are functionally integrated in the lateral horn (LH) of the vinegar fly, Drosophila melanogaster. We characterized an olfactory-processing pathway, comprised of inhibitory projection neurons (iPNs) that target the LH exclusively, at morphological, functional and behavioral levels. We demonstrate that iPNs are subdivided into two morphological groups encoding positive hedonic valence or intensity information and conveying these features into separate domains in the LH. Silencing iPNs severely diminished flies' attraction behavior. Moreover, functional imaging disclosed a LH region tuned to repulsive odors comprised exclusively of third-order neurons. We provide evidence for a feature-based map in the LH, and elucidate its role as the center for integrating behaviorally relevant olfactory information.
eLife digest
Organisms need to sense and adapt to their environment in order to survive. Senses such as vision and smell allow an organism to absorb information about the external environment and translate it into a meaningful internal image. This internal image helps the organism to remember incidents and act accordingly when they encounter similar situations again. A typical example is when organisms are repeatedly attracted to odors that are essential for survival, such as food and pheromones, and are repulsed by odors that threaten survival.
Strutz et al. addressed how attractiveness or repulsiveness of a smell, and also the strength of a smell, are processed by a part of the olfactory system called the lateral horn in fruit flies. This involved mapping the neuronal patterns that were generated in the lateral horn when a fly was exposed to particular odors.
Strutz et al. found that a subset of neurons called inhibitory projection neurons processes information about whether the odor is attractive or repulsive, and that a second subset of these neurons process information about the intensity of the odor. Other insects, such as honey bees and hawk moths, have olfactory systems with a similar architecture and might also employ a similar spatial approach to encode information regarding the intensity and identity of odors. Locusts, on the other hand, employ a temporal approach to encoding information about odors.
The work of Strutz et al. shows that certain qualities of odors are contained in a spatial map in a specific brain region of the fly. This opens up the question of how the information in this spatial map influences decisions made by the fly.
PMCID: PMC4270039  PMID: 25512254
olfaction; neural circuit; lateral horn; antennal lobe; odor processing; functional imaging; D. melanogaster
25.  Reef Odor: A Wake Up Call for Navigation in Reef Fish Larvae 
PLoS ONE  2013;8(8):e72808.
The behavior of reef fish larvae, equipped with a complex toolbox of sensory apparatus, has become a central issue in understanding their transport in the ocean. In this study pelagic reef fish larvae were monitored using an unmanned open-ocean tracking device, the drifting in-situ chamber (DISC), deployed sequentially in oceanic waters and in reef-born odor plumes propagating offshore with the ebb flow. A total of 83 larvae of two taxonomic groups of the families Pomacentridae and Apogonidae were observed in the two water masses around One Tree Island, southern Great Barrier Reef. The study provides the first in-situ evidence that pelagic reef fish larvae discriminate reef odor and respond by changing their swimming speed and direction. It concludes that reef fish larvae smell the presence of coral reefs from several kilometers offshore and this odor is a primary component of their navigational system and activates other directional sensory cues. The two families expressed differences in their response that could be adapted to maintain a position close to the reef. In particular, damselfish larvae embedded in the odor plume detected the location of the reef crest and swam westward and parallel to shore on both sides of the island. This study underlines the critical importance of in situ Lagrangian observations to provide unique information on larval fish behavioral decisions. From an ecological perspective the central role of olfactory signals in marine population connectivity raises concerns about the effects of pollution and acidification of oceans, which can alter chemical cues and olfactory responses.
PMCID: PMC3755995  PMID: 24015278

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