Dataset Information

Neural Substrates of Drosophila Larval Anemotaxis.

ABSTRACT: Animals use sensory information to move toward more favorable conditions. Drosophila larvae can move up or down gradients of odors (chemotax), light (phototax), and temperature (thermotax) by modulating the probability, direction, and size of turns based on sensory input. Whether larvae can anemotax in gradients of mechanosensory cues is unknown. Further, although many of the sensory neurons that mediate taxis have been described, the central circuits are not well understood. Here, we used high-throughput, quantitative behavioral assays to demonstrate Drosophila larvae anemotax in gradients of wind speeds and to characterize the behavioral strategies involved. We found that larvae modulate the probability, direction, and size of turns to move away from higher wind speeds. This suggests that similar central decision-making mechanisms underlie taxis in somatosensory and other sensory modalities. By silencing the activity of single or very few neuron types in a behavioral screen, we found two sensory (chordotonal and multidendritic class III) and six nerve cord neuron types involved in anemotaxis. We reconstructed the identified neurons in an electron microscopy volume that spans the entire larval nervous system and found they received direct input from the mechanosensory neurons or from each other. In this way, we identified local interneurons and first- and second-order subesophageal zone (SEZ) and brain projection neurons. Finally, silencing a dopaminergic brain neuron type impairs anemotaxis. These findings suggest that anemotaxis involves both nerve cord and brain circuits. The candidate neurons and circuitry identified in our study provide a basis for future detailed mechanistic understanding of the circuit principles of anemotaxis.

SUBMITTER: Jovanic T

PROVIDER: S-EPMC6380933 | biostudies-literature | 2019 Feb

REPOSITORIES: biostudies-literature

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Neural Substrates of Drosophila Larval Anemotaxis.

Jovanic Tihana T Winding Michael M Cardona Albert A Truman James W JW Gershow Marc M Zlatic Marta M

Current biology : CB 20190207 4

Animals use sensory information to move toward more favorable conditions. Drosophila larvae can move up or down gradients of odors (chemotax), light (phototax), and temperature (thermotax) by modulating the probability, direction, and size of turns based on sensory input. Whether larvae can anemotax in gradients of mechanosensory cues is unknown. Further, although many of the sensory neurons that mediate taxis have been described, the central circuits are not well understood. Here, we used high- ...[more]

PMID: 30744969

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Project description:Animals engaged in naturalistic behavior can exhibit a large degree of behavioral variability even under sensory invariant conditions. Such behavioral variability can include not only variations of the same behavior, but also variability across qualitatively different behaviors driven by divergent cognitive states, such as fight-or-flight decisions. However, the neural circuit mechanisms that generate such divergent behaviors across trials are not well understood. To investigate this question, here we studied the visual-evoked responses of larval zebrafish to moving objects of various sizes, which we found exhibited highly variable and divergent responses across repetitions of the same stimulus. Given that the neuronal circuits underlying such behaviors span sensory, motor, and other brain areas, we built a novel Fourier light field microscope which enables high-resolution, whole-brain imaging of larval zebrafish during behavior. This enabled us to screen for neural loci which exhibited activity patterns correlated with behavioral variability. We found that despite the highly variable activity of single neurons, visual stimuli were robustly encoded at the population level, and the visual-encoding dimensions of neural activity did not explain behavioral variability. This robustness despite apparent single neuron variability was due to the multi-dimensional geometry of the neuronal population dynamics: almost all neural dimensions that were variable across individual trials, i.e. the "noise" modes, were orthogonal to those encoding for sensory information. Investigating this neuronal variability further, we identified two sparsely-distributed, brain-wide neuronal populations whose pre-motor activity predicted whether the larva would respond to a stimulus and, if so, which direction it would turn on a single-trial level. These populations predicted single-trial behavior seconds before stimulus onset, indicating they encoded time-varying internal modulating behavior, perhaps organizing behavior over longer timescales or enabling flexible behavior routines dependent on the animal's internal state. Our results provide the first whole-brain confirmation that sensory, motor, and internal variables are encoded in a highly mixed fashion throughout the brain and demonstrate that de-mixing each of these components at the neuronal population level is critical to understanding the mechanisms underlying the brain's remarkable flexibility and robustness.

Dataset Information

Neural Substrates of Drosophila Larval Anemotaxis.

Publications

Neural Substrates of Drosophila Larval Anemotaxis.

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