The functional organization of descending sensory-motor pathways in Drosophila
In most animals, the brain controls the body via a set of descending neurons (DNs) that traverse the neck. DN activity activates, maintains or modulates locomotion and other behaviors. Individual DNs have been well-studied in species from insects to primates, but little is known about overall connectivity patterns across the DN population. We systematically investigated DN anatomy in Drosophila melanogaster and created over 100 transgenic lines targeting individual cell types. We identified roughly half of all Drosophila DNs and comprehensively map connectivity between sensory and motor neuropils in the brain and nerve cord, respectively. We find the nerve cord is a layered system of neuropils reflecting the fly's capability for two largely independent means of locomotion -- walking and flight -- using distinct sets of appendages. Our results reveal the basic functional map of descending pathways in flies and provide tools for systematic interrogation of neural circuits.
© 2018 Namiki et al. This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited. Received: 12 December 2017; Accepted: 09 May 2018; Published: 26 June 2018. We are grateful to Gerald Rubin and Barry Dickson for providing GAL4 lines, Barett Pfeiffer and Gerry Rubin for constructs used to make the PA-GFP reagent, Julie Simpson, Heather Dionne and Teri Ngo for genetic reagents, Rob Court for initial help setting up the VNC aligner at Janelia and Hideo Otsuna for optimization of the VNC aligner and processing of VNC data, Jana Boerner for segmentation data of VNC bundles. The Janelia Fly facility (Amanda Cavallaro, Todd Laverty, Karen Hibbard, Jui-Chun Kao and others) helped in fly husbandry, and the FlyLight Project Team (https://www.janelia.org/project-team/flylight, Rebecca Johnston, Oz Malkesman, Nirmala Iyer, Kevin Zeng, Kelley Salvesen, Nick Abel, Phuson Hulamm, Reeham Motaher, Susana Tae, Rebecca Vorimo) performed brain dissections, histological preparations, and confocal imaging. We also thank Kei Ito and Masayoshi Ito for sharing information on clonal units, Jens Goldammer and Masayoshi Ito for comments on an early version of the manuscript, and Jim Truman and David Shepherd for helpful discussions on VNC anatomy. We are grateful to the FlyCircuit database from the NCHC (National Center for High-performance Computing) and NTHU (National Tsing Hua University), and to the FLYBRAIN neuron database in the University of Tokyo. This research was partially funded by the Descending Interneuron Project Team (https://www.janelia.org/project-team/fly-descending-interneuron) and the Visiting Scientist Program at The Janelia Research Campus. Funding: Howard Hughes Medical Institute. The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication. Author contributions: Shigehiro Namiki, Conceptualization, Data curation, Software, Formal analysis, Investigation, Visualization, Methodology, Writing—original draft, Writing—review and editing; Michael H Dickinson, Conceptualization, Visualization, Methodology, Writing—original draft, Writing—review and editing; Allan M Wong, Investigation, Methodology, Data acquisition; Wyatt Korff, Conceptualization, Data curation, Funding acquisition, Visualization, Methodology, Writing—original draft, Project administration, Writing—review and editing; Gwyneth M Card, Conceptualization, Data curation, Supervision, Funding acquisition, Visualization, Methodology, Writing—original draft, Project administration, Writing—review and editing.
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