Heterogeneity and nonaffinity of cell-induced matrix displacements

Cell contractile forces deform and reorganize the surrounding matrix, but the relationship between the forces and the resulting displacements is complicated by the fact that the fibrous structure brings about a complex set of mechanical properties. Many studies have quantified nonlinear and time-dependent properties at macroscopic scales, but it is unclear whether macroscopic properties apply to the scale of a cell, where the matrix is composed of a heterogeneous network of fibers. To address this question, we mimicked the contraction of a cell embedded within a fibrous collagen matrix and quantified the resulting displacements. The data revealed displacements that were heterogeneous and nonaffine. The heterogeneity was reproducible during cyclic loading, and it decreased with decreasing fiber length. Both the experiments and a fiber network model showed that the heterogeneous displacements decayed over distance at a rate no faster than the average displacement field, indicating no transition to homogeneous continuum behavior. Experiments with cells fully embedded in collagen matrices revealed the presence of heterogeneous displacements as well, exposing the dramatic heterogeneity in matrix reorganization that is induced by cells at different positions within the same fibrous matrix.