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Connectomes across development reveal principles of brain maturation in C. elegans

View ORCID ProfileDaniel Witvliet, View ORCID ProfileBen Mulcahy, James K. Mitchell, Yaron Meirovitch, View ORCID ProfileDaniel R. Berger, Yuelong Wu, View ORCID ProfileYufang Liu, Wan Xian Koh, Rajeev Parvathala, Douglas Holmyard, Richard L. Schalek, Nir Shavit, View ORCID ProfileAndrew D. Chisholm, Jeff W. Lichtman, View ORCID ProfileAravinthan D.T. Samuel, View ORCID ProfileMei Zhen
doi: https://doi.org/10.1101/2020.04.30.066209
Daniel Witvliet
1Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, ON, Canada
2Department of Molecular Genetics, University of Toronto, Toronto, ON, Canada
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Ben Mulcahy
1Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, ON, Canada
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James K. Mitchell
3Department of Physics, Harvard University, Cambridge, MA
4Center for Brain Science, Harvard University, Cambridge, MA
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Yaron Meirovitch
4Center for Brain Science, Harvard University, Cambridge, MA
5Computer Science and Artificial Intelligence Laboratory, Massachusetts Institute of Technology, MA
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Daniel R. Berger
4Center for Brain Science, Harvard University, Cambridge, MA
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Yuelong Wu
4Center for Brain Science, Harvard University, Cambridge, MA
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Yufang Liu
1Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, ON, Canada
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Wan Xian Koh
1Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, ON, Canada
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Rajeev Parvathala
5Computer Science and Artificial Intelligence Laboratory, Massachusetts Institute of Technology, MA
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Douglas Holmyard
1Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, ON, Canada
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Richard L. Schalek
4Center for Brain Science, Harvard University, Cambridge, MA
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Nir Shavit
5Computer Science and Artificial Intelligence Laboratory, Massachusetts Institute of Technology, MA
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Andrew D. Chisholm
6Division of Biological Sciences, Section of Cell and Developmental Biology, University of California, San Diego, CA
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Jeff W. Lichtman
4Center for Brain Science, Harvard University, Cambridge, MA
7Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA
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  • For correspondence: jeff@mcb.harvard.edu samuel@physics.harvard.edu zhen@lunenfeld.ca
Aravinthan D.T. Samuel
3Department of Physics, Harvard University, Cambridge, MA
4Center for Brain Science, Harvard University, Cambridge, MA
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  • For correspondence: jeff@mcb.harvard.edu samuel@physics.harvard.edu zhen@lunenfeld.ca
Mei Zhen
1Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, ON, Canada
2Department of Molecular Genetics, University of Toronto, Toronto, ON, Canada
8Department of Physiology, University of Toronto, Toronto, ON, Canada
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  • For correspondence: jeff@mcb.harvard.edu samuel@physics.harvard.edu zhen@lunenfeld.ca
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Abstract

From birth to adulthood, an animal’s nervous system changes as its body grows and its behaviours mature. However, the extent of circuit remodelling across the connectome is poorly understood. Here, we used serial-section electron microscopy to reconstruct the brain of eight isogenic C. elegans individuals at different ages to learn how an entire wiring diagram changes with maturation. We found that the overall geometry of the nervous system is preserved from birth to adulthood, establishing a constant scaffold upon which synaptic change is built. We observed substantial connectivity differences among individuals that make each brain partly unique. We also observed developmental connectivity changes that are consistent between animals but different among neurons, altering the strengths of existing connections and creating additional connections. Collective synaptic changes alter information processing of the brain. Across maturation, the decision-making circuitry is maintained whereas sensory and motor pathways are substantially remodelled, and the brain becomes progressively more modular and feedforward. These synaptic changes reveal principles that underlie brain maturation.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Minor text changes throughout for clarity. Three supplementary panels were added to show that variability as defined by animals of the same ages supports the conclusions derived from variability defined across maturation. Statistics section was added to methods. Two new videos were added. Additional people were added to acknowledgements and additional funding sources were added.

  • http://nemanode.org/

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted May 22, 2020.
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Connectomes across development reveal principles of brain maturation in C. elegans
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 Shavit, Andrew D. Chisholm, Jeff W. Lichtman, Aravinthan D.T. Samuel, Mei Zhen
bioRxiv 2020.04.30.066209; doi: https://doi.org/10.1101/2020.04.30.066209
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Connectomes across development reveal principles of brain maturation in C. elegans
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 Shavit, Andrew D. Chisholm, Jeff W. Lichtman, Aravinthan D.T. Samuel, Mei Zhen
bioRxiv 2020.04.30.066209; doi: https://doi.org/10.1101/2020.04.30.066209

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