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

Amy Smith (1) , Vincent Doyeux (1) , Maxime Berg (1) , Myriam Peyrounette (1) , Mohamad Haft Javaheriam (2) , Anne Larue (1) , John H. Slater (3) , Frédéric Lauwers (4, 5) , Pablo Blinder (6) , Philbert Tsai (7) , David Kleinfeld (7) , Chris B. Schaffer (2) , Nozomi Nishimura (2) , Yohan Davit (1) , Sylvie Lorthois (1, 2) , Amy Smith (1) , Vincent And Doyeux (1) , Peyrounette And Berg (1) , Haft Javaheriam (2) , Anne Slater , John H And Lauwers , David Schaffer (2) , Chris B And Nishimura (2) , Yohan Lorthois (1)

1 IMFT - Institut de mécanique des fluides de Toulouse
2 Cornell University [New York]
3 University of Delaware [Newark]
4 ToNIC - Toulouse NeuroImaging Center
5 UT3 - Université Toulouse III - Paul Sabatier
6 TAU - Tel Aviv University
7 UC San Diego - University of California [San Diego]

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.

Mots clés: Cerebral cortex; Capillary network; Capillary loop; Capillary network model; Biomimetic network

Domaines: Mécanique des fluides [physics.class-ph]

Amy Smith, Vincent Doyeux, Maxime Berg, Myriam Peyrounette, Mohamad Haft Javaheriam, et al.. Brain capillary networks across species : a few simple organizational requirements are sufficient to reproduce both structure and function. Frontiers in Physiology, 2019, 10 (233), pp.1-22. ⟨10.3389/fphys.2019.00233⟩. ⟨hal-02135744⟩