Neural Substrates of Drosophila Larval Anemotaxis

Abstract

Graphical AbstractHighlights d Drosophila larvae perform negative anemotaxis d To anemotax, larvae modulate the turn rate, size, and direction as in other taxis d Chordotonal and multidendritic class III sensory neurons together mediate anemotaxis d The anemotactic circuitry involves both the nerve cord and the brain SUMMARY 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 highthroughput, 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 firstand 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. CATMAID https://catmaid.readthedocs.org/ [32] MATLAB http://www.mathworks.com [45, 69] Current Biology 29, 554-566.e1-e4, February 18, 2019 e1

Identifying neural substrates of competitive interactions and sequence transitions during mechanosensory responses in Drosophila

“…In the first two categories silencing of neurons results in significantly lower or higher probabilities of one or more actions compared to the control (Fig 2E, Fig 3B and Table, S7 Table), while in the third Behavioral probabilities for sensory lines driving UAS-TNT-e. A-B. Using our behavioral detection method we find that silencing chordotonals with tetanus-toxin using iav and R61D08 drivers results in significantly less Hunches and less Bends in response to air-puff compared to the control, as we have shown previously [10,21,38] as well as less Back-up. C. silencing of md class III sensory neurons results in less Hunches and less Back-ups D. Silencing of md III and subsets of chordotonals results in less Hunches E-G Phenotypic summaries for the hits from the behavioral screen.…”

“…In lines: R23D10, R77H11, R23A05, R29D11, R61A01 we were able to match some of the neurons from the multicolor flip-out images to the EM reconstruction images and analyze their connectivity to each other and to previously identified elements of the mechanosensory network [10,21,38] as well as nociceptive and pre-motor networks [21,30,39,41]. This is summarized and shown in Fig 8. and S6 Fig. In the R23D10 we were able to identify the T05t neuron in the EM volume [21] and found it receives input from LnA type interneurons and Basin neurons in the Hunch/Bend behavioral choice circuit [10] (Fig 8).…”

“…In another line (R88C11), we found two neurons that receive input from chordotonals. One is Jupiter (A08h2) that we previously shown was required for anemotaxis [38]. The second one is a long-range projection neuron A23j, that we reconstructed in the EM volume and named Hook-1.…”

“…When silencing chordotonal and multidendritic class III neurons expressing tetanus-toxin using NompC (a TRP channel that confers light touch sensitivity [36,37]), a GAL4 driver that drives in both md III neurons and subsets of chordotonals, the larvae showed an impaired response with significantly less Hunches, and slightly, although not significantly, less Bends and Back-up, a phenotype consistent with a strong impairment in sensing air-current. Interestingly our recent study on anemotaxis revealed that multidendritic class III neurons may act synergistically with chordotonal sensory neurons to mediate larval navigation a wind speed gradient [38].…”

“…We used multicolor flip-outs to morphologically characterize the neurons in the lines whose silencing resulted in more Hunches (i.e. R11A07, R88C11, R39H05) ( Fig In two previous studies we have identified both local interneurons and ascending projection neurons involved in mechanosensory behaviors that receive inputs from chordotonal or multidendritic sensory neurons [10,38]. In a circuit for the choice between Hunching and Bending, we described distinct types of inhibitory neurons: LnA type interneurons that inhibit Basin-2 neurons (that promotes Bending and inhibits Hunching) and disinhibit Basins-1 projection neuron (that promotes Hunching and Bending), while LnB interneurons inhibit Basin-1 and disinhibit Basin-2.…”