Structural hierarchy confers error tolerance in biological tissues

Networks of elastic beams can deform either by stretching or bending of their members. The primary mode of deformation (bending or stretching) crucially depends on the specific details of the network architecture. In order to shed light on the relationship between microscopic geometry and macroscopic mechanics, we characterize the structural features of networks which deform uniformly, through the stretching of the beams only. We provide a convenient set of geometrical criter...

We study the micromechanics of collagen-I gel with the goal of bridging the gap between theory and experiment in the study of biopolymer networks. Three-dimensional images of fluorescently labeled collagen are obtained by confocal microscopy and the network geometry is extracted using a 3d network skeletonization algorithm. Each fiber is modeled as a worm-like-chain that resists stretching and bending, and each cross-link is modeled as torsional spring. The stress-strain curv...

The cells and tissues that make up our body juggle contradictory mechanical demands. It is crucial for their survival to be able to withstand large mechanical loads, but it is equally crucial for them to produce forces and actively change shape during biological processes such as tissue growth and repair. The mechanics of cell and tissues is determined by scaffolds of protein polymers known as the cytoskeleton and the extracellular matrix, respectively. Experiments on model s...

We study the elasticity of fibrous materials composed of generalized stiff polymers. It is shown that in contrast to cellular foam-like structures affine strain fields are generically unstable. Instead, a subtle interplay between the architecture of the network and the elastic properties of its building blocks leads to intriguing mechanical properties with intermediate asymptotic scaling regimes. We present exhaustive numerical studies based on a finite element method complem...

Motivated by recent experiments showing nonlinear elasticity of in vitro networks of the biopolymer actin cross-linked with filamin, we present an effective medium theory of flexibly cross-linked stiff polymer networks. We model such networks by randomly oriented elastic rods connected by flexible connectors to a surrounding elastic continuum, which self-consistently represents the behavior of the rest of the network. This model yields a crossover from a linear elastic regime...

Reinforced elastic sheets surround us in daily life, from concrete shell buildings to biological structures such as the arthropod exoskeleton or the venation network of dicotyledonous plant leaves. Natural structures are often highly optimized through evolution and natural selection, leading to the biologically and practically relevant problem of understanding and applying the principles of their design. Inspired by the hierarchically organized scaffolding networks found in p...

Cells actively probe and respond to the stiffness of their surroundings. Since mechanosensory cells in connective tissue are surrounded by a disordered network of biopolymers, their in vivo mechanical environment can be extremely heterogeneous. Here, we investigate how this heterogeneity impacts mechanosensing by modeling the cell as an idealized local stiffness sensor inside a disordered fiber network. For all types of networks we study, including experimentally-imaged colla...

We present a statistical mechanical study of stiff polymers, motivated by experiments on actin filaments and the considerable current interest in polymer networks. We obtain simple, approximate analytical forms for the force-extension relations and compare these with numerical treatments. We note the important role of boundary conditions in determining force-extension relations. The theoretical predictions presented here can be tested against single molecule experiments on ne...

Semiflexible biopolymer networks are commonly found in biological systems, from the cytoskeleton of cells to the extracellular matrix. Such networks often naturally occur as composites, in which various components interact to generate rich mechanical behaviours. In this work we examine the mechanics of composites formed when a single fibre inclusion is placed within discrete fibre networks of two distinct architectures. In particular, we computationally and theoretically inve...

Natural hard composites like human bone possess a combination of strength and toughness that exceeds that of their constituents and of many engineered composites. This augmentation is attributed to their complex hierarchical structure, spanning multiple length scales; in bone, characteristic dimensions range from nanoscale fibrils to microscale lamellae to mesoscale osteons and macroscale organs. The mechanical properties of bone have been studied, with the understanding that...