Compressive Instabilities Enable Cell-Induced Extreme Densification Patterns in the Fibrous Extracellular Matrix: Discrete Model Predictions

Abstract: Through modelling and simulations we show that material instabilities play a dominant role in the mechanical behavior of the fibrous collagen Extracellular Matrix (ECM), as observed when the ECM is deformed by contractile biological cells. We compare two families of fiber network models, Family 1 with stable and Family 2 with unstable force-stretch response of individual fibers in compression. The latter is a characteristic of post-buckling of beams with hierarchical structure. Our simulations reveal different compression instabilities at play in each family, namely, fiber collapse (buckling) in Family 2 and fiber element collapse (snap-through) in Family 1. These result in highly localized densification zones consisting of strongly aligned fibers emanating from individual contractile cells or joining neighbouring cells, as observed in experiments. Despite substantial differences in the response of the two families, our work underscores the importance of buckling/compression instabilities in the behavior of fibrous biological tissues, with implications in cancer invasion and metastasis.