Sensorimotor pathway controlling stopping behavior during chemotaxis in the Drosophila melanogaster larva

Tastekin, Ibrahim; Khandelwal, Avinash; Tadres, David; Fessner, Nico D.; Truman, James W.; Zlatic, Marta; Cardona, Albert; Louis, Matthieu

doi:10.7554/elife.38740

Cited by 70 publications

(88 citation statements)

References 113 publications

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“…Once Figure 2Diii). This result is consistent with the behavior of wild-type larvae in response to attractive odors (33). It establishes that PiVR can automatically detect and accurately track animal in real time.…”

Section: Benchmarking Pivr Performances By Eliciting Larval Chemotaxisupporting

confidence: 84%

“…For all experimental conditions, we found that the turn-triggered average of the sensory experience showed a decrease in stimulus intensity for several seconds preceding a stop (17,56,61) (Figure 5E). This characteristic decrease in stimulus has been shown to inhibit the activity of the olfactory sensory neurons, which in turn enhances the probability of interrupting forward peristalsis (17,33).…”

Section: Defining the Nature Of Taste-driven Responses In Adult Fliesmentioning

confidence: 99%

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PiVR: an affordable and versatile closed-loop platform to study unrestrained sensorimotor behavior

Tadres

Louis

2019

Preprint

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Tools enabling closed-loop experiments are crucial to delineate causal relationships between the activity of genetically-labeled neurons and specific behaviors. We developed the Raspberry Pi Virtual Reality system (PiVR) to conduct closed-loop optogenetic stimulation of neural functions in unrestrained animals. PiVR is an experimental platform that operates at hightemporal resolution (>50 Hz) with low latencies (~10 ms), while being affordable (<$500) and easy to build (<6 hours). This tool was designed to be accessible to a wide public, from highschool students to professional researchers studying systems neuroscience. We illustrate the functionality of PiVR by focusing on sensory navigation in response to gradients of chemicals (chemotaxis) and light (phototaxis). We show how Drosophila flies perform negative chemotaxis by modulating their locomotor speed to avoid locations associated with optogenetically-evoked bitter taste. In Drosophila larvae, we use innate positive chemotaxis to compare orientation behavior elicited by real-and virtual-odor gradients with static shapes as well as by turbulent virtual-odor plumes. Finally, we examine how positive phototaxis emerges in zebrafish larvae from the modulation of turning maneuvers during the ascent of virtual white-light gradients. Besides its application to study chemotaxis and phototaxis, PiVR is a versatile tool designed to bolster efforts to map and to functionally characterize neural circuits.

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Section: Benchmarking Pivr Performances By Eliciting Larval Chemotaxisupporting

confidence: 84%

Section: Defining the Nature Of Taste-driven Responses In Adult Fliesmentioning

confidence: 99%

PiVR: an affordable and versatile closed-loop platform to study unrestrained sensorimotor behavior

Tadres

Louis

2019

Preprint

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“…There is evidence that the transcription factor FoxP plays a role in valuebased decision making, implicating these mutants as possible targets for future studies [55]. Finally, encounter-elicited stopping might be unique to walking Drosophila and larvae [56], since remaining stationary is more difficult in flight. Still, the reflexive counterturns that flying Drosophila execute after losing a plume [19] do bear loose resemblance to the increased stop rates following a drop in encounter frequency, so these decisions may have a common origin, but a different behavioral response.…”

Section: Discussionmentioning

confidence: 99%

WalkingDrosophilanavigate complex plumes using stochastic decisions biased by the timing of odor encounters

Demir

Kadakia

Anderson

et al. 2020

Preprint

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Insects find food, mates, and egg-laying sites by tracking odor plumes swept by complex wind patterns. Previous studies have shown that moths and flies localize plumes by surging upwind at odor onset and turning cross-or downwind at odor offset. Less clear is how, once within the expanding cone of the odor plume, insects use their brief encounters with individual odor packets, whose location and timing are random, to progress towards the source. Experiments and theory have suggested that the timing of odor encounters might assist navigation, but connecting behaviors to individual encounters has been challenging. Here, we imaged complex odor plumes simultaneous with freely-walking flies, allowing us to quantify how behavior is shaped by individual odor encounters. Combining measurements, dynamical models, and statistical inference, we found that within the plume cone, individual encounters did not trigger reflexive surging, casting, or counterturning. Instead, flies turned stochastically with stereotyped saccades, whose direction was biased upwind by the timing of prior odor encounters, while the magnitude and rate of saccades remained constant. Odor encounters did not strongly affect walking speed. Instead, flies used encounter timing to modulate the rate of transitions between walks and stops. When stopped, flies initiated walks using information from multiple odor encounters, suggesting that integrating evidence without losing position was part of the strategy. These results indicate that once within the complex odor plume, where odor location and timing are unpredictable, animals navigate with biased random walks shaped by the entire sequence of encounters.

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“…Here, we were able to overcome these obstacles by using the tractable genetic model system of Drosophila melanogaster larva. In this system, we could combine: i) large-scale electron microscopy reconstruction of neural circuits due to the relatively small size of its brain (Jovanic et al, 2016;Ohyama et al, 2015); ii) targeted manipulation of uniquely identified neuron types (Jovanic et al, 2016;Ohyama et al, 2015;Tastekin et al, 2018), iii) and functional imaging of neural activity.…”

Section: Introductionmentioning

confidence: 99%

Circuits for integrating learnt and innate valences in the fly brain

Eschbach

Fushiki

Winding

et al. 2020

Preprint

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Animal behavior is shaped both by evolution and by individual experience. In many species parallel brain pathways are thought to encode innate and learnt behavior drives and as a result may link the same sensory cue to different actions if innate and learnt drives are in opposition. How these opposing drives are integrated into a single coherent action is not well understood. In insects, the Mushroom Body Output Neurons (MBONs) and the Lateral Horn Neurons (LHNs) are thought to provide the learnt and innate drives, respectively. However their patterns of convergence and the mechanisms by which their outputs are used to select actions are not well understood. We used electron microscopy reconstruction to comprehensively map the downstream targets of all MBONs in Drosophila larva and characterise their patterns of convergence with LHNs. We discovered convergence neurons that receive direct input from MBONs and LHNs and compare opposite behaviour drives. Functional imaging and optogenetic manipulation suggest these convergence neurons compute the overall predicted value of approaching or avoiding an odor and mediate action selection. Our study describes the circuit mechanisms allowing integration of opposing drives from parallel olfactory pathways.

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Sensorimotor pathway controlling stopping behavior during chemotaxis in the Drosophila melanogaster larva

Cited by 70 publications

References 113 publications

PiVR: an affordable and versatile closed-loop platform to study unrestrained sensorimotor behavior

PiVR: an affordable and versatile closed-loop platform to study unrestrained sensorimotor behavior

WalkingDrosophilanavigate complex plumes using stochastic decisions biased by the timing of odor encounters

Circuits for integrating learnt and innate valences in the fly brain

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