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Brain capillary networks across species : a few simple organizational requirements are sufficient to reproduce both structure and function

Smith, Amy F. and Doyeux, Vincent and Berg, Maxime and Peyrounette, Myriam and Haft Javaheriam, Mohamad and Larue, Anne and Slater, John H. and Lauwers, Frédéric and Blinder, Pablo and Tsai, Philbert and Kleinfeld, David and Schaffer, Chris B. and Nishimura, Nozomi and Davit, Yohan and Lorthois, Sylvie Brain capillary networks across species : a few simple organizational requirements are sufficient to reproduce both structure and function. (2019) Frontiers in Physiology, 10 (233). 1-22. ISSN 1664-042X

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Official URL: https://doi.org/10.3389/fphys.2019.00233

Abstract

Despite the key role of the capillaries in neurovascular function, a thorough characterization of cerebral capillary network properties is currently lacking. Here, we define a range of metrics (geometrical, topological, flow, mass transfer, and robustness) for quantification of structural differences between brain areas, organs, species, or patient populations and, in parallel, digitally generate synthetic networks that replicate the key organizational features of anatomical networks (isotropy, connectedness, space-filling nature, convexity of tissue domains, characteristic size). To reach these objectives, we first construct a database of the defined metrics for healthy capillary networks obtained from imaging of mouse and human brains. Results show that anatomical networks are topologically equivalent between the two species and that geometrical metrics only differ in scaling. Based on these results, we then devise a method which employs constrained Voronoi diagrams to generate 3D model synthetic cerebral capillary networks that are locally randomized but homogeneous at the network-scale. With appropriate choice of scaling, these networks have equivalent properties to the anatomical data, demonstrated by comparison of the defined metrics. The ability to synthetically replicate cerebral capillary networks opens a broad range of applications, ranging from systematic computational studies of structure-function relationships in healthy capillary networks to detailed analysis of pathological structural degeneration, or even to the development of templates for fabrication of 3D biomimetic vascular networks embedded in tissue-engineered constructs.

Item Type:Article
Additional Information:Deux pdf : Article + supplément
HAL Id:hal-02135744
Audience (journal):International peer-reviewed journal
Uncontrolled Keywords:
Institution:French research institutions > Centre National de la Recherche Scientifique - CNRS (FRANCE)
Other partners > Cornell University (USA)
Université de Toulouse > Institut National Polytechnique de Toulouse - Toulouse INP (FRANCE)
French research institutions > Institut National de la Santé et de la Recherche Médicale - INSERM (FRANCE)
Université de Toulouse > Université Toulouse III - Paul Sabatier - UT3 (FRANCE)
Other partners > University of Delaware Newark - UDEL (USA)
Other partners > Tel Aviv University (ISRAEL)
Other partners > University of California - UC San Diego (USA)
Laboratory name:
Funders:
ERC BrainMicroFlow GA615102 - NIH NCI IMAT R21CA214299 - NIH NINDS R35 NS097265 - NIH NIMH R01 MH111438 - NSFCAREER Award 1751797 - CALMIP (Grant 2016-P1541)
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Deposited On:03 Apr 2019 15:07

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