Three-Dimensional Thermal Noise Imaging of Collagen Networks

Abstract

Extracellular biopolymer networks show interesting mechanical properties that are essential for living organisms. In particular, a highly nonlinear elastic response to strain is seen, which gives biopolymer networks the ability to comply with small stresses but to resist large ones. The macroscopic mechanical properties have their origin in the properties of the individual filaments and the properties of the network that they form, like their cross-linking geometry and pore size distribution. While the macroscopic properties of biopolymer networks have been extensively studied, there has been a lack of experimental techniques that can simultaneously determine mechanical and architectural properties of the network in situ with single filament resolution. Thermal Noise Imaging is a scanning probe technique that utilizes the confined thermal motion of an optically trapped particle as a three-dimensional, noninvasive scanner for soft, biological material. It achieves nanometer precision in probe position detection with MHz bandwidth. Thermal noise imaging visualizes single biopolymer filaments as nanoscale channels and allows for the quantification of their mechanical properties from their transversal fluctuations. using feedback control, we have recorded micrometer scale thermal noise images inside a collagen network for the first time. We extract quantitative information about cross-linking geometry and fiber elasticity from the data. These results pave the way for an investigation of force distributions inside biopolymer networks on the single filament level.