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

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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  • Authors+Show Affiliations

    ,

    Department of Cell & Systems Biology, University of Toronto, Toronto, ON M5S 3B2, Canada; jeffrey.dason@uwindsor.ca marla.sokolowski@utoronto.ca. Department of Biological Sciences, University of Windsor, Windsor, ON N9B 3P4, Canada.

    ,

    Department of Ecology & Evolutionary Biology, University of Toronto, Toronto, ON M5S 3B2, Canada.

    ,

    Department of Ecology & Evolutionary Biology, University of Toronto, Toronto, ON M5S 3B2, Canada. Child and Brain Development Program, Canadian Institute for Advanced Research, Toronto, ON M5G 1M1, Canada.

    ,

    Department of Biological Sciences, University of Windsor, Windsor, ON N9B 3P4, Canada.

    ,

    Department of Cell & Systems Biology, University of Toronto, Toronto, ON M5S 3B2, Canada.

    Department of Cell & Systems Biology, University of Toronto, Toronto, ON M5S 3B2, Canada; jeffrey.dason@uwindsor.ca marla.sokolowski@utoronto.ca. Department of Ecology & Evolutionary Biology, University of Toronto, Toronto, ON M5S 3B2, Canada. Child and Brain Development Program, Canadian Institute for Advanced Research, Toronto, ON M5G 1M1, Canada.

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    Pub Type(s)

    Journal Article

    Language

    eng

    PubMed ID

    31213548

    Citation

    Dason, Jeffrey S., et al. "Drosophila Melanogaster Foraging Regulates a Nociceptive-like Escape Behavior Through a Developmentally Plastic Sensory Circuit." Proceedings of the National Academy of Sciences of the United States of America, 2019.
    Dason JS, Cheung A, Anreiter I, et al. Drosophila melanogaster foraging regulates a nociceptive-like escape behavior through a developmentally plastic sensory circuit. Proc Natl Acad Sci USA. 2019.
    Dason, J. S., Cheung, A., Anreiter, I., Montemurri, V. A., Allen, A. M., & Sokolowski, M. B. (2019). Drosophila melanogaster foraging regulates a nociceptive-like escape behavior through a developmentally plastic sensory circuit. Proceedings of the National Academy of Sciences of the United States of America, doi:10.1073/pnas.1820840116.
    Dason JS, et al. Drosophila Melanogaster Foraging Regulates a Nociceptive-like Escape Behavior Through a Developmentally Plastic Sensory Circuit. Proc Natl Acad Sci USA. 2019 Jun 18; PubMed PMID: 31213548.
    * Article titles in AMA citation format should be in sentence-case
    TY - JOUR T1 - Drosophila melanogaster foraging regulates a nociceptive-like escape behavior through a developmentally plastic sensory circuit. AU - Dason,Jeffrey S, AU - Cheung,Amanda, AU - Anreiter,Ina, AU - Montemurri,Vanessa A, AU - Allen,Aaron M, AU - Sokolowski,Marla B, Y1 - 2019/06/18/ PY - 2019/6/20/entrez KW - Drosophila KW - genetic variation KW - nociception KW - optogenetics KW - plasticity JF - Proceedings of the National Academy of Sciences of the United States of America JO - Proc. Natl. Acad. Sci. U.S.A. N2 - 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. SN - 1091-6490 UR - https://www.unboundmedicine.com/medline/citation/31213548/Drosophila_melanogaster_foraging_regulates_a_nociceptive-like_escape_behavior_through_a_developmentally_plastic_sensory_circuit L2 - http://www.pnas.org/cgi/pmidlookup?view=long&pmid=31213548 DB - PRIME DP - Unbound Medicine ER -