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Connectomes across development reveal principles of brain maturation

Author

Listed:
  • Daniel Witvliet

    (Mount Sinai Hospital
    University of Toronto)

  • Ben Mulcahy

    (Mount Sinai Hospital)

  • James K. Mitchell

    (Harvard University
    Harvard University)

  • Yaron Meirovitch

    (Harvard University
    Massachusetts Institute of Technology)

  • Daniel R. Berger

    (Harvard University)

  • Yuelong Wu

    (Harvard University)

  • Yufang Liu

    (Mount Sinai Hospital)

  • Wan Xian Koh

    (Mount Sinai Hospital)

  • Rajeev Parvathala

    (Massachusetts Institute of Technology)

  • Douglas Holmyard

    (Mount Sinai Hospital)

  • Richard L. Schalek

    (Harvard University)

  • Nir Shavit

    (Massachusetts Institute of Technology)

  • Andrew D. Chisholm

    (University of California, San Diego)

  • Jeff W. Lichtman

    (Harvard University
    Harvard University)

  • Aravinthan D. T. Samuel

    (Harvard University
    Harvard University)

  • Mei Zhen

    (Mount Sinai Hospital
    University of Toronto
    University of Toronto)

Abstract

An animal’s nervous system changes as its body grows from birth to adulthood and its behaviours mature1–8. The form and extent of circuit remodelling across the connectome is unknown3,9–15. Here we used serial-section electron microscopy to reconstruct the full brain of eight isogenic Caenorhabditis elegans individuals across postnatal stages to investigate how it changes with age. The overall geometry of the brain is preserved from birth to adulthood, but substantial changes in chemical synaptic connectivity emerge on this consistent scaffold. Comparing connectomes between individuals reveals substantial differences in connectivity that make each brain partly unique. Comparing connectomes across maturation reveals consistent wiring changes between different neurons. These changes alter the strength of existing connections and create new connections. Collective changes in the network alter information processing. During development, the central decision-making circuitry is maintained, whereas sensory and motor pathways substantially remodel. With age, the brain becomes progressively more feedforward and discernibly modular. Thus developmental connectomics reveals principles that underlie brain maturation.

Suggested Citation

  • Daniel Witvliet & Ben Mulcahy & James K. Mitchell & Yaron Meirovitch & Daniel R. Berger & Yuelong Wu & Yufang Liu & Wan Xian Koh & Rajeev Parvathala & Douglas Holmyard & Richard L. Schalek & Nir Shavi, 2021. "Connectomes across development reveal principles of brain maturation," Nature, Nature, vol. 596(7871), pages 257-261, August.
  • Handle: RePEc:nat:nature:v:596:y:2021:i:7871:d:10.1038_s41586-021-03778-8
    DOI: 10.1038/s41586-021-03778-8
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    Citations

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    Cited by:

    1. 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.
    2. Dániel L. Barabási & Taliesin Beynon & Ádám Katona & Nicolas Perez-Nieves, 2023. "Complex computation from developmental priors," Nature Communications, Nature, vol. 14(1), pages 1-8, December.
    3. 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.
    4. Zhongyu Chen & Yuguo Yu & Xiangyang Xue, 2023. "A Connectome-Based Digital Twin Caenorhabditis elegans Capable of Intelligent Sensorimotor Behavior," Mathematics, MDPI, vol. 11(11), pages 1-23, May.
    5. 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.
    6. 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.
    7. Kate L. Laskowski & David Bierbach & Jolle W. Jolles & Carolina Doran & Max Wolf, 2022. "The emergence and development of behavioral individuality in clonal fish," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    8. Francesca Coraggio & Mahak Bhushan & Spyridon Roumeliotis & Francesca Caroti & Carlo Bevilacqua & Robert Prevedel & Georgia Rapti, 2024. "Age-progressive interplay of HSP-proteostasis, ECM-cell junctions and biomechanics ensures C. elegans astroglial architecture," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    9. Wendy Xueyi Wang & Julie L. Lefebvre, 2022. "Morphological pseudotime ordering and fate mapping reveal diversification of cerebellar inhibitory interneurons," Nature Communications, Nature, vol. 13(1), pages 1-21, December.

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