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Whole-animal connectomes of both Caenorhabditis elegans sexes

Author

Listed:
  • Steven J. Cook

    (Albert Einstein College of Medicine)

  • Travis A. Jarrell

    (Albert Einstein College of Medicine)

  • Christopher A. Brittin

    (Albert Einstein College of Medicine)

  • Yi Wang

    (Albert Einstein College of Medicine)

  • Adam E. Bloniarz

    (Google)

  • Maksim A. Yakovlev

    (Albert Einstein College of Medicine)

  • Ken C. Q. Nguyen

    (Albert Einstein College of Medicine)

  • Leo T.-H. Tang

    (Albert Einstein College of Medicine)

  • Emily A. Bayer

    (Columbia University)

  • Janet S. Duerr

    (Ohio University)

  • Hannes E. Bülow

    (Albert Einstein College of Medicine
    Albert Einstein College of Medicine)

  • Oliver Hobert

    (Columbia University
    Columbia University)

  • David H. Hall

    (Albert Einstein College of Medicine)

  • Scott W. Emmons

    (Albert Einstein College of Medicine
    Albert Einstein College of Medicine)

Abstract

Knowledge of connectivity in the nervous system is essential to understanding its function. Here we describe connectomes for both adult sexes of the nematode Caenorhabditis elegans, an important model organism for neuroscience research. We present quantitative connectivity matrices that encompass all connections from sensory input to end-organ output across the entire animal, information that is necessary to model behaviour. Serial electron microscopy reconstructions that are based on the analysis of both new and previously published electron micrographs update previous results and include data on the male head. The nervous system differs between sexes at multiple levels. Several sex-shared neurons that function in circuits for sexual behaviour are sexually dimorphic in structure and connectivity. Inputs from sex-specific circuitry to central circuitry reveal points at which sexual and non-sexual pathways converge. In sex-shared central pathways, a substantial number of connections differ in strength between the sexes. Quantitative connectomes that include all connections serve as the basis for understanding how complex, adaptive behavior is generated.

Suggested Citation

  • Steven J. Cook & Travis A. Jarrell & Christopher A. Brittin & Yi Wang & Adam E. Bloniarz & Maksim A. Yakovlev & Ken C. Q. Nguyen & Leo T.-H. Tang & Emily A. Bayer & Janet S. Duerr & Hannes E. Bülow & , 2019. "Whole-animal connectomes of both Caenorhabditis elegans sexes," Nature, Nature, vol. 571(7763), pages 63-71, July.
    • Handle: RePEc:nat:nature:v:571:y:2019:i:7763:d:10.1038_s41586-019-1352-7
    DOI: 10.1038/s41586-019-1352-7
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    Cited by:

    1. Yongbin Li & Siyu Chen & Weihong Liu & Di Zhao & Yimeng Gao & Shipeng Hu & Hanyu Liu & Yuanyuan Li & Lei Qu & Xiao Liu, 2024. "A full-body transcription factor expression atlas with completely resolved cell identities in C. elegans," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    2. Robert Jankowski & Antoine Allard & Marián Boguñá & M. Ángeles Serrano, 2023. "The D-Mercator method for the multidimensional hyperbolic embedding of real networks," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    3. Chenxi Lin & Yuxin Shan & Zhongyi Wang & Hui Peng & Rong Li & Pingzhou Wang & Junyan He & Weiwei Shen & Zhengxing Wu & Min Guo, 2024. "Molecular and circuit mechanisms underlying avoidance of rapid cooling stimuli in C. elegans," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    4. Hagar Setty & Yehuda Salzberg & Shadi Karimi & Elisheva Berent-Barzel & Michael Krieg & Meital Oren-Suissa, 2022. "Sexually dimorphic architecture and function of a mechanosensory circuit in C. elegans," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    5. Noa Deshe & Yifat Eliezer & Lihi Hoch & Eyal Itskovits & Eduard Bokman & Shachaf Ben-Ezra & Alon Zaslaver, 2023. "Inheritance of associative memories and acquired cellular changes in C. elegans," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    6. Zhihao Zheng & Christopher S. Own & Adrian A. Wanner & Randal A. Koene & Eric W. Hammerschmith & William M. Silversmith & Nico Kemnitz & Ran Lu & David W. Tank & H. Sebastian Seung, 2024. "Fast imaging of millimeter-scale areas with beam deflection transmission electron microscopy," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    7. Charles Murphy & Vincent Thibeault & Antoine Allard & Patrick Desrosiers, 2024. "Duality between predictability and reconstructability in complex systems," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    8. Hyunsoo Yim & Daniel T. Choe & J. Alexander Bae & Myung-kyu Choi & Hae-Mook Kang & Ken C. Q. Nguyen & Soungyub Ahn & Sang-kyu Bahn & Heeseung Yang & David H. Hall & Jinseop S. Kim & Junho Lee, 2024. "Comparative connectomics of dauer reveals developmental plasticity," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    9. Xu Zhan & Chao Chen & Longgang Niu & Xinran Du & Ying Lei & Rui Dan & Zhao-Wen Wang & Ping Liu, 2023. "Locomotion modulates olfactory learning through proprioception in C. elegans," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    10. Ichiro Aoki & Luca Golinelli & Eva Dunkel & Shripriya Bhat & Erschad Bassam & Isabel Beets & Alexander Gottschalk, 2024. "Hierarchical regulation of functionally antagonistic neuropeptides expressed in a single neuron pair," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    11. Alexandra Segref & Kavya L. Vakkayil & Tsimafei Padvitski & Qiaochu Li & Virginia Kroef & Jakob Lormann & Lioba Körner & Fabian Finger & Thorsten Hoppe, 2022. "Thermosensation in Caenorhabditis elegans is linked to ubiquitin-dependent protein turnover via insulin and calcineurin signalling," Nature Communications, Nature, vol. 13(1), pages 1-17, December.

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