Vascular adaptation model from force balance: Physarum polycephalum as a case study

Abstract

Understanding vascular adaptation, namely what drives veins to shrink or grow, is key for the self-organization of flow networks and their optimization. From the top-down principle of minimizing flow dissipation at a fixed metabolic cost within flow networks, flow shear rate resulting from the flows pervading veins is hypothesized to drive vein adaptation. Yet, there is no bottom-up derivation of how flow forces impact vein dynamics. From the physical principle of force balance, shear rate acts parallel to vein walls, and hence, naively shear rate could only stretch veins and not dilate or shrink them. We, here, resolve this paradox by theoretically investigating force balance on a vein wall in the context of the vascular network of the model organism P. polycephalum. We propose, based on previous mechanical studies of cross-linked gels, that shear induces a nonlinear, anisotropic response of the actomyosin gel, making up vein walls that can indeed drive vein dilatation. Furthermore, our force balance approach allows us to identify that shear feedback occurs with a typical timescale and with a typical target shear rate that are not universal properties of the material but instead depend smoothly on the location of the vein within the network. In particular, the target shear rate is related to the veins hydrostatic pressure, which highlights the role of pressure in vascular adaptation. Finally, since our derivation is based on force balance and fluid mechanics, we believe our approach can be extended to vascular adaptation in other organisms.