Odor motion sensing enables complex plume navigation

Kadakia, Nirag; Demir, Mahmut; Bt, Michaelis; Reidenbach, Matthew A.; Da, Clark; Emonet, Thierry

doi:10.1101/2021.09.29.462473

Cited by 5 publications

(5 citation statements)

References 86 publications

(183 reference statements)

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“…It is possible that in high-intermittency plumes organisms might use frequency to track the edges of odor plumes or even execute offset responses, such as those detailed in Álvarez-Salvado et al, 2018 . Moreover, it has recently been shown that flies can use bilateral information to detect the direction of motion of odor signals ( Kadakia et al, 2021 ), and that this information is particularly relevant in turbulent environments. In more diffuse and smooth plumes, odor velocity is less well-defined, and might be of more limited use.…”

Section: Discussionmentioning

confidence: 99%

Sensing complementary temporal features of odor signals enhances navigation of diverse turbulent plumes

Jayaram

Kadakia

Emonet

2022

eLife

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We and others have shown that during odor plume navigation, walking Drosophila melanogaster bias their motion upwind in response to both the frequency of their encounters with the odor (Demir et al., 2020), and the intermittency of the odor signal, which we define to be the fraction of time the signal is above a detection threshold (Alvarez-Salvado et al., 2018). Here we combine and simplify previous mathematical models that recapitulated these data to investigate the benefits of sensing both of these temporal features, and how these benefits depend on the spatiotemporal statistics of the odor plume. Through agent-based simulations, we find that navigators that only use frequency or intermittency perform well in some environments - achieving maximal performance when gains are near those inferred from experiment - but fail in others. Robust performance across diverse environments requires both temporal modalities. However, we also find a steep tradeoff when using both sensors simultaneously, suggesting a strong benefit to modulating how much each sensor is weighted, rather than using both in a fixed combination across plumes. Finally, we show that the circuitry of the Drosophila olfactory periphery naturally enables simultaneous intermittency and frequency sensing, enhancing robust navigation through a diversity of odor environments. Together, our results suggest that the first stage of olfactory processing selects and encodes temporal features of odor signals critical to real-world navigation tasks.

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Section: Discussionmentioning

confidence: 99%

Sensing complementary temporal features of odor signals enhances navigation of diverse turbulent plumes

Jayaram

Kadakia

Emonet

2022

eLife

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“…The use of fictive CO 2 delivered optogenetically was critical for studying the internal state of the mosquito after these transient host cues. Delivery and removal of real CO 2 necessitates constant air flow, which is itself an important sensory cue for insects ( Alvarez-Salvado et al, 2018 ; Kadakia et al, 2021 ; Suver et al, 2019 ).…”

Section: Resultsmentioning

confidence: 99%

A persistent behavioral state enables sustained predation of humans by mosquitoes

Sorrells

Pandey

Rosas-Villegas

et al. 2022

eLife

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Predatory animals pursue prey in a noisy sensory landscape, deciding when to continue or abandon their chase. The mosquito Aedes aegypti is a micropredator that first detects humans at a distance through sensory cues such as carbon dioxide. As a mosquito nears its target it senses more proximal cues such as body heat that guide it to a meal of blood. How long the search for blood continues after initial detection of a human is not known. Here we show that a 5-second optogenetic pulse of fictive carbon dioxide induced a persistent behavioral state in female mosquitoes that lasted for more than 10 minutes. This state is highly specific to females searching for a blood meal and was not induced in recently blood-fed females or in males, who do not feed on blood. In males that lack the gene fruitless, which controls persistent social behaviors in other insects, fictive carbon dioxide induced a long-lasting behavior response resembling the predatory state of females. Finally, we show that the persistent state triggered by detection of fictive carbon dioxide enabled females to engorge on a blood meal mimic offered up to 14 minutes after the initial 5-second stimulus. Our results demonstrate that a persistent internal state allows female mosquitoes to integrate multiple human sensory cues over long timescales, an ability that is key to their success as an apex micropredator of humans.

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“…Further, the wealth of architectural insights emerging from the fly connectome may be used to constrain wiring motifs in artificial networks 72 . Modelling multiple antennae 36,73 , or more generally a biomechanical body, would enrich the interactions between the agent and the simulation environment 22,74 .…”

Section: Limitations and Future Workmentioning

confidence: 99%

Emergent behaviour and neural dynamics in artificial agents tracking odour plumes

et al. 2023

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Tracking an odour plume to locate its source under variable wind and plume statistics is a complex task. Flying insects routinely accomplish such tracking, often over long distances, in pursuit of food or mates. Several aspects of this remarkable behaviour and its underlying neural circuitry have been studied experimentally. Here we take a complementary in silico approach to develop an integrated understanding of their behaviour and neural computations. Specifically, we train artificial recurrent neural network agents using deep reinforcement learning to locate the source of simulated odour plumes that mimic features of plumes in a turbulent flow. Interestingly, the agents’ emergent behaviours resemble those of flying insects, and the recurrent neural networks learn to compute task-relevant variables with distinct dynamic structures in population activity. Our analyses put forward a testable behavioural hypothesis for tracking plumes in changing wind direction, and we provide key intuitions for memory requirements and neural dynamics in odour plume tracking.

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Odor motion sensing enables complex plume navigation

Cited by 5 publications

References 86 publications

Sensing complementary temporal features of odor signals enhances navigation of diverse turbulent plumes

Sensing complementary temporal features of odor signals enhances navigation of diverse turbulent plumes

A persistent behavioral state enables sustained predation of humans by mosquitoes

Emergent behaviour and neural dynamics in artificial agents tracking odour plumes

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