Olfactory Navigation: Tempo is the key
Tracking odors is a matter of life or death for most organisms, and insects are no exception (Baker et al., 2018). Male moths can track the pheromones of their potential mating partners from hundreds of meters away, and even fruit flies successfully engage in long-range searches for food using their sense of smell. However, this task is far from easy. This is because the molecules that carry the odorous message are transported by turbulent wind, where they get mixed with other molecules and form complex structures (Murlis et al., 1992; Crimaldi and Koseff, 2001). As a result, the information about the origin of a scent is seemingly lost, hidden in the intricacies of the intermittent odor signal. Insects appear to be able to overcome this problem, but it is unclear how they extract information about the origin of the odor and translate it into behaviors that allow them to find the source.
A major hurdle in the way of understanding how animals track smells is the need to visualize odors and behaviors simultaneously. While tracking insect behaviors in the wild remains a daunting task, wind-tunnel experiments provide a way to collect high-throughput data in controlled situations (Álvarez-Salvado et al., 2018). However, the artificial environment still poses several challenges: for example, it is unclear whether naturally occurring stimuli can be reproduced, or if it is possible to visualize odor concentrations with sufficient resolution.
Now, in eLife, Thierry Emonet and co-workers from Yale University – including Mahmut Demir and Nirag Kadakia as first authors – report how the fruit fly Drosophila melanogaster behaves in response to an attractive smell while walking (Demir et al., 2020). Quite serendipitously, they discovered that starved flies are attracted to smoke, which can be easily visualized. By manipulating the airflow in a wind tunnel with lateral jets, they generated a stream of smoke with properties similar to the odor signals that flies encounter in the wild (Celani et al., 2014). In agreement with theoretical expectations, they found that, within the smoke, flies have brief, frequent and unpredictable encounters with the odor. But how do these encounters modulate flies’ behavior?
Demir et al. observed that the rich variety of movements exhibited by walking Drosophila could be summarized into just a few behavioral states relevant to olfactory navigation, echoing previous findings (Tao et al., 2019). They found the search process was inherently stochastic: periods of walking in a straight line would randomly be interrupted by rapid turning events or by stopping for longer extents of time.
By comparing the trajectories recorded with or without smoke, but always in presence of turbulent airflow, Demir et al. were able to identify which features of the flies’ movements were affected by encountering the smell. They found that the walking pace, the frequency and speed at which the flies made a turn, and the sharpness of the turns were not affected by the smoke. Conversely, when the smoke was present walks were on average longer and stops shorter. Most importantly, when the flies were turning, they were more likely to reorient upwind against the direction of the wind if they had already encountered the odor. But what are the specific characteristics of the odor that the fly perceives and responds to?
Demir et al. found that neither the concentration of the odor nor the amount of times flies were exposed to it played a significant role in the search process. Instead, the tempo of the flies’ encounters with the odor appeared to be the key determinant of the decision-making process. In a stopped fly, a single encounter was sufficient to initiate a walk, and several encounters close together shortened the duration of the stops. Walking times increased after an encounter, but further exposure to the odor shortly after did not lead to a cumulative effect. This modulation of walks and stops produces a bias that results in the fly visiting regions of space where it is more likely to encounter the smell. Further experiments showed that above a certain frequency of encounters flies were more likely to re-orientate themselves upwind. In fact, the combined effect of the odor on the frequency of walks and stops, as well as the direction of the turns, proved to be fundamental for the flies to find the origin of a smell (Figure 1).
![](https://iiif.elifesciences.org/lax/63385%2Felife-63385-fig1-v1.tif/full/617,/0/default.jpg)
How a walking fly navigates towards the source of an odor.
Flies that have been starved are attracted to smoke. In this schematic diagram of a wind tunnel experiment, the fly starts on the right, the source of the smoke is on the left, and the wind blows from left to right (black arrow). When far from the source (right box), the fly is less likely to encounter the odor, leading to frequent stops (red dots) and a similar number of upwind and downwind (green and blue dots) turns. Once the fly gets closer to the source (left box), it is more likely to encounter the odor, and the number of stops decrease, while the frequency of upwind turns increases.
There are tantalizing similarities between the olfactory-search strategies of walking flies and other insects, but also significant differences (Mafra-Neto and Cardé, 1994; Budick and Dickinson, 2006). In any event, irrespective of their sizes and behaviors, different species must overcome the same challenges posed by the transport of odor molecules by the turbulent airflow, pointing to the existence of general underlying principles. Perhaps, in the future, more studies like this one will pave the way towards a more fundamental understanding of long-range olfactory navigation.
References
-
Algorithms for olfactory search across speciesThe Journal of Neuroscience 38:9383–9389.https://doi.org/10.1523/JNEUROSCI.1668-18.2018
-
Free-flight responses of Drosophila melanogaster to attractive odorsJournal of Experimental Biology 209:3001–3017.https://doi.org/10.1242/jeb.02305
-
Odor landscapes in turbulent environmentsPhysical Review X 4:041015.https://doi.org/10.1103/PhysRevX.4.041015
-
Odor plumes and how insects use themAnnual Review of Entomology 37:505–532.https://doi.org/10.1146/annurev.en.37.010192.002445
Article and author information
Author details
Publication history
Copyright
© 2020, Celani
This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 1,205
- views
-
- 99
- downloads
-
- 5
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Further reading
-
- Neuroscience
We used light-sensitive drugs to identify the brain region-specific role of mGlu5 metabotropic glutamate receptors in the control of pain. Optical activation of systemic JF-NP-26, a caged, normally inactive, negative allosteric modulator (NAM) of mGlu5 receptors, in cingulate, prelimbic, and infralimbic cortices and thalamus inhibited neuropathic pain hypersensitivity. Systemic treatment of alloswitch-1, an intrinsically active mGlu5 receptor NAM, caused analgesia, and the effect was reversed by light-induced drug inactivation in the prelimbic and infralimbic cortices, and thalamus. This demonstrates that mGlu5 receptor blockade in the medial prefrontal cortex and thalamus is both sufficient and necessary for the analgesic activity of mGlu5 receptor antagonists. Surprisingly, when the light was delivered in the basolateral amygdala, local activation of systemic JF-NP-26 reduced pain thresholds, whereas inactivation of alloswitch-1 enhanced analgesia. Electrophysiological analysis showed that alloswitch-1 increased excitatory synaptic responses in prelimbic pyramidal neurons evoked by stimulation of presumed BLA input, and decreased BLA-driven feedforward inhibition of amygdala output neurons. Both effects were reversed by optical silencing and reinstated by optical reactivation of alloswitch-1. These findings demonstrate for the first time that the action of mGlu5 receptors in the pain neuraxis is not homogenous, and suggest that blockade of mGlu5 receptors in the BLA may limit the overall analgesic activity of mGlu5 receptor antagonists. This could explain the suboptimal effect of mGlu5 NAMs on pain in human studies and validate photopharmacology as an important tool to determine ideal target sites for systemic drugs.
-
- Neuroscience
Categorical sensory representations are critical for many behaviors, including speech perception. In the auditory system, categorical information is thought to arise hierarchically, becoming increasingly prominent in higher-order cortical regions. The neural mechanisms that support this robust and flexible computation remain poorly understood. Here, we studied sound representations in the ferret primary and non-primary auditory cortex while animals engaged in a challenging sound discrimination task. Population-level decoding of simultaneously recorded single neurons revealed that task engagement caused categorical sound representations to emerge in non-primary auditory cortex. In primary auditory cortex, task engagement caused a general enhancement of sound decoding that was not specific to task-relevant categories. These findings are consistent with mixed selectivity models of neural disentanglement, in which early sensory regions build an overcomplete representation of the world and allow neurons in downstream brain regions to flexibly and selectively read out behaviorally relevant, categorical information.