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. 2022 Mar:13:191-213.
doi: 10.1146/annurev-conmatphys-031720-032754. Epub 2021 Nov 8.

Olfactory Sensing and Navigation in Turbulent Environments

Gautam Reddy  1 , Venkatesh N Murthy  2   3 , Massimo Vergassola  4   5
Affiliations

Olfactory Sensing and Navigation in Turbulent Environments

Gautam Reddy et al. Annu Rev Condens Matter Phys. 2022 Mar.

Abstract

Fluid turbulence is a double-edged sword for the navigation of macroscopic animals, such as birds, insects, and rodents. On the one hand, turbulence enables pheromone communication among mates and the possibility of locating food by their odors from long distances. Molecular diffusion would indeed be unable to spread odors over relevant distances in natural conditions. On the other hand, turbulent flows are hard to predict, and learning effective maneuvers to navigate them is challenging, as we discuss in this review. We first provide a summary of the olfactory organs that sense airborne or surface-bound odors, as well as the computational tasks that animals face when extracting information useful for navigation from an olfactory signal. A compendium of the dynamics of turbulent transport emphasizes those aspects that directly impact animals' behavior. The state of the art on navigational strategies is discussed, followed by a concluding section dedicated to future challenges in the field.

Keywords: biological navigation; fluid turbulence; neurobiology; odor transport; olfaction.

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Figures

Figure 1
Figure 1
Odor landscapes and search strategies. The following schematic illustrates how the physics of chemical transport dictates the frequency and smoothness of stimulus encounters by navigating animals. (a) At microscopic scales, molecular diffusion generates smooth changes in concentrations of chemicals, allowing for gradient ascent. (b) In flow regimes close (tens of centimeters) to typical naturalistic sources, even if large fluctuations are present, odor concentration changes are still smooth, and an animal receives some signal most of the time. Gradient ascent strategies, or variants that approximate them, are still sufficient. (c) At distances on the order of meters or larger, odors are significantly dispersed such that an animal encounters stimuli infrequently and intermittently. Because local gradients are largely random in relation to the source direction at the relevant time scales, simple gradient ascent is not feasible for navigation. (d) Trail tracking is unique in that the stimulus is relatively stationary but spatially sparse. How animals combine ground and airborne cues by alternately sampling sniffs from the ground and in the air remains by and large unexplored.
Figure 2
Figure 2
Scheme of neural architectures that sense and process olfactory stimuli. (a) Schematic of the nasal cavity and the neural components involved in olfaction in mice (sagittal plane). Airflow brings odors over the olfactory epithelium during inhalation. OSNs are electrically activated by odors and signal to the brain through their axons converging on glomeruli in the OB (light blue). Processed information is carried from the OB to multiple brain areas by MTCs. (b) Schematic of the Drosophila olfactory system. OSNs are housed inside structures called sensilla in the antennae (OSN shown outside sensilla for clarity) and project to the AL. PNs receive sensory input and project to multiple brain structures including the mushroom body. (c) Common neural circuit motif in rodents and insects. OSNs expressing a particular receptor type out of a large repertoire (indicated by like colors) converge selectively in individual glomeruli in the OB, making connections with MTCs or PNs. Local circuit elements in the OB or AL include inhibitory neurons (shown as a black circle) that receive excitation from MTCs/PNs and reciprocally inhibit them. MTCs/PNs project to multiple brain regions, including the piriform cortex/mushroom body, where they are thought to make dispersed, random, and sparse connections (shown as intersecting wires, with connections denoted by small circles). Abbreviations: AL, antennal lobe; MTCs, mitral/tufted cells; OB, olfactory bulb; OSNs, olfactory sensory neurons; PN, principal neuron.
Figure 3
Figure 3
A concentration time series of duration 16 min (the y axis reports the raw signal from the detector): Data are continuous from the top panel to the bottom one, with each panel exhibiting 4 min of data. The time series was measured on the mean-plume centerline at a distance of 50 m from a source of propylene placed at a height of 2.5 m above the ground under near-neutral stability conditions. The graphs provide a vivid illustration of intermittency and clustering of odor detections at long distances from a source, with periods of no detection that can last tens of seconds. Figure adapted with permission from Reference .
Figure 4
Figure 4
Two separate sources of fluorescein (green) and rhodamine (red) are injected on the axis of a turbulent water jet (blue), in its downstream far field. The image shows a two-dimensional cut through the two instantaneous concentration fields, which illustrates the complexity of concentration fields generated by turbulent transport as compared with those generated by diffusive processes. Figure adapted from Reference with permission of AIP Publishing.
Figure 5
Figure 5
Tracks of male gypsy moths approaching a source releasing sex pheromone together with bubbles (that can be visualized and provide a sense of the distribution of odor stimuli) (127). Panels a and b show two typical tracks, with thick/thin parts referring to periods within/outside the bubbles, i.e., likely associated with high-frequency/absence of odor detection. Thick parts are known as surge, as they show consistent progression up the wind (indicated by arrows). Conversely, thin lines show crosswind motion and are known as casting. The portion of a track in panel c shows that a change in wind direction is reflected in the orientation of behavioral moves. Figure adapted with permission from Reference .
Figure 6
Figure 6
A sample trajectory of a POMDP searcher attempting to locate a source of chemicals that are dispersed by a turbulent environment. Note the sequence of an upwind surge followed by crosswind casts triggered upon a single detection. (a) The initial position of the searcher is ~50 units downwind from the source. The darkened area shows the conical average plume with nonzero probability of detecting an odor signal. The size of the blue dots shows the probability of the searcher’s location relative to the source, which is initially uniform and transforms to a cone upon the first odor detection (indicated by crosses). (b) Close to the source, the searcher exhibits a trial-and-error greedy strategy. Abbreviation: POMDP, partially observable Markov decision process.
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