Treffer: Structural and developmental principles of neuropil assembly in C. elegans.
Title:
Structural and developmental principles of neuropil assembly in C. elegans.
Authors:
Moyle MW; Department of Neuroscience and Department of Cell Biology, Yale University School of Medicine, New Haven, CT, USA., Barnes KM; Developmental Biology Program, Sloan Kettering Institute, New York, NY, USA., Kuchroo M; Department of Genetics, Yale University School of Medicine, New Haven, CT, USA., Gonopolskiy A; Department of Genetics, Yale University School of Medicine, New Haven, CT, USA., Duncan LH; Department of Neuroscience and Department of Cell Biology, Yale University School of Medicine, New Haven, CT, USA., Sengupta T; Department of Neuroscience and Department of Cell Biology, Yale University School of Medicine, New Haven, CT, USA., Shao L; Department of Neuroscience and Department of Cell Biology, Yale University School of Medicine, New Haven, CT, USA., Guo M; Laboratory of High Resolution Optical Imaging, National Institute of Biomedical Imaging and Bioengineering, National Institutes of Health, Bethesda, MD, USA., Santella A; Developmental Biology Program, Sloan Kettering Institute, New York, NY, USA., Christensen R; Laboratory of High Resolution Optical Imaging, National Institute of Biomedical Imaging and Bioengineering, National Institutes of Health, Bethesda, MD, USA., Kumar A; Marine Biological Laboratory, Woods Hole, MA, USA., Wu Y; Laboratory of High Resolution Optical Imaging, National Institute of Biomedical Imaging and Bioengineering, National Institutes of Health, Bethesda, MD, USA., Moon KR; Department of Mathematics and Statistics, Utah State University, Logan, UT, USA., Wolf G; Department of Mathematics and Statistics, Université de Montréal, Montreal, Quebec, Canada., Krishnaswamy S; Department of Genetics, Yale University School of Medicine, New Haven, CT, USA., Bao Z; Developmental Biology Program, Sloan Kettering Institute, New York, NY, USA., Shroff H; Laboratory of High Resolution Optical Imaging, National Institute of Biomedical Imaging and Bioengineering, National Institutes of Health, Bethesda, MD, USA.; Marine Biological Laboratory, Woods Hole, MA, USA., Mohler WA; Department of Genetics and Genome Sciences and Center for Cell Analysis and Modeling, University of Connecticut Health Center, Farmington, CT, USA., Colón-Ramos DA; Department of Neuroscience and Department of Cell Biology, Yale University School of Medicine, New Haven, CT, USA. daniel.colon-ramos@yale.edu.; Marine Biological Laboratory, Woods Hole, MA, USA. daniel.colon-ramos@yale.edu.; Instituto de Neurobiología, Recinto de Ciencias Médicas, Universidad de Puerto Rico, San Juan, Puerto Rico. daniel.colon-ramos@yale.edu.
Source:
Nature [Nature] 2021 Mar; Vol. 591 (7848), pp. 99-104. Date of Electronic Publication: 2021 Feb 24.
Publication Type:
Journal Article; Research Support, N.I.H., Extramural; Research Support, N.I.H., Intramural; Research Support, Non-U.S. Gov't
Language:
English
Journal Info:
Publisher: Nature Publishing Group Country of Publication: England NLM ID: 0410462 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1476-4687 (Electronic) Linking ISSN: 00280836 NLM ISO Abbreviation: Nature Subsets: MEDLINE
Imprint Name(s):
Publication: Basingstoke : Nature Publishing Group
Original Publication: London, Macmillan Journals ltd.
Original Publication: London, Macmillan Journals ltd.
MeSH Terms:
Caenorhabditis elegans/*embryology , Caenorhabditis elegans/*metabolism , Neuropil/*chemistry , Neuropil/*metabolism, Algorithms ; Animals ; Brain/cytology ; Brain/embryology ; Caenorhabditis elegans/chemistry ; Caenorhabditis elegans/cytology ; Cell Movement ; Diffusion ; Interneurons/metabolism ; Motor Neurons/metabolism ; Neurites/metabolism ; Neuropil/cytology ; Sensory Receptor Cells/metabolism
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Brittin, C. A., Cook, S. J., Hall, D. H., Emmons, S. W. & Cohen, N. Volumetric reconstruction of main Caenorhabditis elegans neuropil at two different time points. Preprint at https://doi.org/10.1101/485771 (2018).
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Sabrin, K. M., Wei, Y., van den Heuvel, M. P. & Dovrolis, C. The hourglass organization of the Caenorhabditis elegans connectome. PLoS Comput. Biol. 16, e1007526 (2020). (PMID: 32027645702987510.1371/journal.pcbi.1007526)
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Rapti, G., Li, C., Shan, A., Lu, Y. & Shaham, S. Glia initiate brain assembly through noncanonical Chimaerin–Furin axon guidance in C. elegans. Nat. Neurosci. 20, 1350–1360 (2017). (PMID: 28846083561485810.1038/nn.4630)
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Newman, M. E. Modularity and community structure in networks. Proc. Natl Acad. Sci. USA 103, 8577–8582 (2006). (PMID: 1672339810.1073/pnas.0601602103)
Millard, S. S. & Pecot, M. Y. Strategies for assembling columns and layers in the Drosophila visual system. Neural Dev. 13, 11 (2018). (PMID: 29875010599142710.1186/s13064-018-0106-9)
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Ward, S., Thomson, N., White, J. G. & Brenner, S. Electron microscopical reconstruction of the anterior sensory anatomy of the nematode Caenorhabditis elegans. J. Comp. Neurol. 160, 313–337 (1975). (PMID: 111292710.1002/cne.901600305)
Riddle, D. L., Blumenthal, T., Meyer, B. J. & Priess, J. R. (eds) C. elegans II 2nd edn (Cold Spring Harbor Lab. Press, 1997).
White, J. Clues to basis of exploratory behaviour of the C. elegans snout from head somatotropy. Phil. Trans. R. Soc. Lond. B 373, (2018).
Groh, J. M. Making Space: How The Brain Knows Where Things Are (Harvard Univ. Press, 2014).
Kaas, J. H. Topographic maps are fundamental to sensory processing. Brain Res. Bull. 44, 107–112 (1997). (PMID: 929219810.1016/S0361-9230(97)00094-4)
Sasakura, H. & Mori, I. Behavioral plasticity, learning, and memory in C. elegans. Curr. Opin. Neurobiol. 23, 92–99 (2013). (PMID: 2306329610.1016/j.conb.2012.09.005)
Chalfie, M. et al. The neural circuit for touch sensitivity in Caenorhabditis elegans. J. Neurosci. 5, 956–964 (1985). (PMID: 3981252656500810.1523/JNEUROSCI.05-04-00956.1985)
Gray, J. M., Hill, J. J. & Bargmann, C. I. A circuit for navigation in Caenorhabditis elegans. Proc. Natl Acad. Sci. USA 102, 3184–3191 (2005). (PMID: 1568940010.1073/pnas.0409009101)
Lockery, S. R. Neuroscience: A social hub for worms. Nature 458, 1124–1125 (2009). (PMID: 1940779210.1038/4581124a)
Macosko, E. Z. et al. A hub-and-spoke circuit drives pheromone attraction and social behaviour in C. elegans. Nature 458, 1171–1175 (2009). (PMID: 19349961276049510.1038/nature07886)
White, J. G., Southgate, E., Thomson, J. N. & Brenner, S. Factors that determine connectivity in the nervous system of Caenorhabditis elegans. Cold Spring Harb. Symp. Quant. Biol. 48, 633–640 (1983). (PMID: 658638010.1101/SQB.1983.048.01.067)
Wakabayashi, T., Kitagawa, I. & Shingai, R. Neurons regulating the duration of forward locomotion in Caenorhabditis elegans. Neurosci. Res. 50, 103–111 (2004). (PMID: 1528850310.1016/j.neures.2004.06.005)
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Grant Information:
R24 OD016474 United States OD NIH HHS; OD010943 United States NH NIH HHS; P40 OD010440 United States OD NIH HHS; UL1 TR001863 United States TR NCATS NIH HHS; R01 NS076558 United States NS NINDS NIH HHS; P30 CA008748 United States CA NCI NIH HHS; R01 GM135929 United States GM NIGMS NIH HHS; F32 NS098616 United States NS NINDS NIH HHS; R01 GM097576 United States GM NIGMS NIH HHS; DP1 NS111778 United States NS NINDS NIH HHS
Entry Date(s):
Date Created: 20210225 Date Completed: 20210408 Latest Revision: 20230129
Update Code:
20250114
PubMed Central ID:
PMC8385650
DOI:
10.1038/s41586-020-03169-5
PMID:
33627875
Database:
MEDLINE
Weitere Informationen
Neuropil is a fundamental form of tissue organization within the brain <sup>1</sup> , in which densely packed neurons synaptically interconnect into precise circuit architecture <sup>2,3</sup> . However, the structural and developmental principles that govern this nanoscale precision remain largely unknown <sup>4,5</sup> . Here we use an iterative data coarse-graining algorithm termed 'diffusion condensation' <sup>6</sup> 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 microscopy <sup>7,8</sup> coupled with lineage-tracing and cell-tracking algorithms <sup>9,10</sup> 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.