Structural and developmental principles of neuropil assembly in C. elegans

Mark W. Moyle, Kristopher M. Barnes, Manik Kuchroo, Alex Gonopolskiy, Leighton H. Duncan, Titas Sengupta, Lin Shao, Min Guo, Anthony Santella, Ryan Christensen, Abhishek Kumar, Yicong Wu, Kevin R. Moon, Guy Wolf, Smita Krishnaswamy, Zhirong Bao, Hari Shroff, William A. Mohler and Daniel A. Colón-Ramos ()
Additional contact information
Mark W. Moyle: Yale University School of Medicine
Kristopher M. Barnes: Sloan Kettering Institute
Manik Kuchroo: Yale University School of Medicine
Alex Gonopolskiy: Yale University School of Medicine
Leighton H. Duncan: Yale University School of Medicine
Titas Sengupta: Yale University School of Medicine
Lin Shao: Yale University School of Medicine
Min Guo: National Institutes of Health
Anthony Santella: Sloan Kettering Institute
Ryan Christensen: National Institutes of Health
Abhishek Kumar: Marine Biological Laboratory
Yicong Wu: National Institutes of Health
Kevin R. Moon: Utah State University
Guy Wolf: Université de Montréal, Montreal
Smita Krishnaswamy: Yale University School of Medicine
Zhirong Bao: Sloan Kettering Institute
Hari Shroff: National Institutes of Health
William A. Mohler: University of Connecticut Health Center
Daniel A. Colón-Ramos: Yale University School of Medicine

Nature, 2021, vol. 591, issue 7848, 99-104

Abstract: Abstract Neuropil is a fundamental form of tissue organization within the brain1, in which densely packed neurons synaptically interconnect into precise circuit architecture2,3. However, the structural and developmental principles that govern this nanoscale precision remain largely unknown4,5. Here we use an iterative data coarse-graining algorithm termed ‘diffusion condensation’6 to identify nested circuit structures within the Caenorhabditis elegans neuropil, which is known as the nerve ring. We show that the nerve ring neuropil is largely organized into four strata that are composed of related behavioural circuits. The stratified architecture of the neuropil is a geometrical representation of the functional segregation of sensory information and motor outputs, with specific sensory organs and muscle quadrants mapping onto particular neuropil strata. We identify groups of neurons with unique morphologies that integrate information across strata and that create neural structures that cage the strata within the nerve ring. We use high resolution light-sheet microscopy7,8 coupled with lineage-tracing and cell-tracking algorithms9,10 to resolve the developmental sequence and reveal principles of cell position, migration and outgrowth that guide stratified neuropil organization. Our results uncover conserved structural design principles that underlie the architecture and function of the nerve ring neuropil, and reveal a temporal progression of outgrowth—based on pioneer neurons—that guides the hierarchical development of the layered neuropil. Our findings provide a systematic blueprint for using structural and developmental approaches to understand neuropil organization within the brain.

Date: 2021
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DOI: 10.1038/s41586-020-03169-5

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