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Cerebellar folding is initiated by mechanical constraints on a fluid-like layer without a cellular pre-pattern

Andrew K Lawton, Tyler Engstrom, Daniel Rohrbach, Masaaki Omura, Daniel H Turnbull, Jonathan Mamou, Teng Zhang, Jennifer M Schwarz, Alexandra L Joyner
doi: https://doi.org/10.1101/382887
Andrew K Lawton
1 Developmental Biology Program. Sloan Kettering Institute;
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  • For correspondence: lawtona@mskcc.org
Tyler Engstrom
2 Department of Physics Syracuse University;
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Daniel Rohrbach
3 Lizzi Center for Biomedical Engineering, Riverside Research;
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Masaaki Omura
4 Graduate School of Science and Engineering, Chiba University;
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Daniel H Turnbull
5 Skirball Institute of Biomolecular Medicine and Department of Radiology, NYU School of Medicine;
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Jonathan Mamou
3 Lizzi Center for Biomedical Engineering, Riverside Research;
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Teng Zhang
6 Department of Mechanical & Aerospace Engineering, Syracuse University;
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Jennifer M Schwarz
7 Department of Physics, Syracuse University
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Alexandra L Joyner
1 Developmental Biology Program. Sloan Kettering Institute;
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  • For correspondence: joynera@mskcc.org
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Abstract

Models based in differential expansion of elastic material, axonal constraints, directed growth, or multi-phasic combinations have all been proposed to explain brain folding. However, the cellular and physical processes at the time of folding have not been defined. We used the murine cerebellum to challenge the standard folding models with in vivo data from the time of folding initiation. We show that at folding initiation differential expansion is created by the outer layer of proliferating progenitors expanding faster than the core. However, the stiffness differential, compressive forces, and emergent thickness variations required by elastic material models are not present. We find that folding occurs without an obvious cellular pre-pattern, that the outer layer expansion is uniform and fluid-like, and that the cerebellum is under radial and circumferential constraints. Lastly, we find that a multi-phase model incorporating differential expansion of a fluid outer layer and radial and circumferential constraints approximates the in vivo shape evolution observed during initiation of cerebellar folding. We discuss how our findings provide a new mechanistic framework to understand brain folding.

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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 4.0 International license.
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Posted January 09, 2019.
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Cerebellar folding is initiated by mechanical constraints on a fluid-like layer without a cellular pre-pattern
Andrew K Lawton, Tyler Engstrom, Daniel Rohrbach, Masaaki Omura, Daniel H Turnbull, Jonathan Mamou, Teng Zhang, Jennifer M Schwarz, Alexandra L Joyner
bioRxiv 382887; doi: https://doi.org/10.1101/382887
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Cerebellar folding is initiated by mechanical constraints on a fluid-like layer without a cellular pre-pattern
Andrew K Lawton, Tyler Engstrom, Daniel Rohrbach, Masaaki Omura, Daniel H Turnbull, Jonathan Mamou, Teng Zhang, Jennifer M Schwarz, Alexandra L Joyner
bioRxiv 382887; doi: https://doi.org/10.1101/382887

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