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      Drosophila melanogaster foraging regulates a nociceptive-like escape behavior through a developmentally plastic sensory circuit

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          Abstract

          Painful or threatening experiences trigger escape responses that are guided by nociceptive neuronal circuitry. Although some components of this circuitry are known and conserved across animals, how this circuitry is regulated at the genetic and developmental levels is mostly unknown. To escape noxious stimuli, such as parasitoid wasp attacks, Drosophila melanogaster larvae generate a curling and rolling response. Rover and sitter allelic variants of the Drosophila foraging ( for) gene differ in parasitoid wasp susceptibility, suggesting a link between for and nociception. By optogenetically activating cells associated with each of for’s promoters (pr1–pr4), we show that pr1 cells regulate larval escape behavior. In accordance with rover and sitter differences in parasitoid wasp susceptibility, we found that rovers have higher pr1 expression and increased sensitivity to nociception relative to sitters. The for null mutants display impaired responses to thermal nociception, which are rescued by restoring for expression in pr1 cells. Conversely, knockdown of for in pr1 cells phenocopies the for null mutant. To gain insight into the circuitry underlying this response, we used an intersectional approach and activity-dependent GFP reconstitution across synaptic partners (GRASP) to show that pr1 cells in the ventral nerve cord (VNC) are required for the nociceptive response, and that multidendritic sensory nociceptive neurons synapse onto pr1 neurons in the VNC. Finally, we show that activation of the pr1 circuit during development suppresses the escape response. Our data demonstrate a role of for in larval nociceptive behavior. This function is specific to for pr1 neurons in the VNC, guiding a developmentally plastic escape response circuit.

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          Most cited references42

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          Genetic mosaic with dual binary transcriptional systems in Drosophila.

          MARCM (mosaic analysis with a repressible cell marker) involves specific labeling of GAL80-minus and GAL4-positive homozygous cells in otherwise heterozygous tissues. Here we demonstrate how the concurrent use of two independent binary transcriptional systems may facilitate complex MARCM studies in the Drosophila nervous system. By fusing LexA with the VP16 acidic activation domain (VP16) or the GAL4 activation domain (GAD), we obtained both GAL80-insensitive and GAL80-suppressible transcriptional factors. LexA::VP16 can mediate MARCM-independent binary transgene induction in mosaic organisms. The incorporation of LexA::GAD into MARCM, which we call dual-expression-control MARCM, permits the induction of distinct transgenes in different patterns among GAL80-minus cells in mosaic tissues. Lineage analysis with dual-expression-control MARCM suggested the presence of neuroglioblasts in the developing optic lobes but did not indicate the production of glia by postembryonic mushroom body neuronal precursors. In addition, dual-expression-control MARCM with a ubiquitous LexA::GAD driver revealed many unidentified cells in the GAL4-GH146-positive projection neuron lineages.
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            Discovery of brainwide neural-behavioral maps via multiscale unsupervised structure learning.

            A single nervous system can generate many distinct motor patterns. Identifying which neurons and circuits control which behaviors has been a laborious piecemeal process, usually for one observer-defined behavior at a time. We present a fundamentally different approach to neuron-behavior mapping. We optogenetically activated 1054 identified neuron lines in Drosophila larvae and tracked the behavioral responses from 37,780 animals. Application of multiscale unsupervised structure learning methods to the behavioral data enabled us to identify 29 discrete, statistically distinguishable, observer-unbiased behavioral phenotypes. Mapping the neural lines to the behavior(s) they evoke provides a behavioral reference atlas for neuron subsets covering a large fraction of larval neurons. This atlas is a starting point for connectivity- and activity-mapping studies to further investigate the mechanisms by which neurons mediate diverse behaviors.
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              Sex-specific control and tuning of the pattern generator for courtship song in Drosophila.

              The differentially spliced transcription factors encoded by the fruitless (fru) gene are key determinants of sexual behavior in Drosophila. They are expressed in a minority of neurons with limited dimorphisms and regulate neural processes that remain largely unknown. Here, we use light-activated ion channels to stimulate fru-expressing neurons in the thoracic-abdominal ganglia, enabling direct functional comparisons of homologous circuitry between sexes. Optical stimulation of males or females initiates the unilateral wing vibrations that normally generate the male courtship song. The pattern-generating circuit operates differently in the two sexes, producing wing movement and sound in both but authentic songs only in males and in females expressing male fru product. A song-like motor program is thus present in females but lies dormant because the neural commands required for song initiation are absent. Supplying such commands artificially reveals fru-specific differences in the internal dynamics of the song generator and sets the stage for exploring their physiological basis.
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                Author and article information

                Journal
                Proceedings of the National Academy of Sciences
                Proc Natl Acad Sci USA
                Proceedings of the National Academy of Sciences
                0027-8424
                1091-6490
                June 18 2019
                : 201820840
                Article
                10.1073/pnas.1820840116
                7519308
                31213548
                ba35553d-cc8b-4db4-9680-de304a27ed45
                © 2019

                Free to read

                https://www.pnas.org/site/aboutpnas/licenses.xhtml

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