  In a diversity of physiological contexts, eukaryotic cells adhere to an
extracellular matrix (ECM), a disordered network with complex nonlinear
mechanics. Such cells can perform mechanosensation: using local force probing
they can measure and respond to their substrate's mechanical properties. It
remains unclear, however, how the mechanical complexity of the ECM at the
cellular scale impacts mechanosensation. Here, we investigate the physical
limits of mechanosensation imposed by the inherent structural disorder and
nonlinear elastic response of the ECM. Using a theoretical framework for
disordered fiber networks, we find that the extreme mechanical heterogeneity
that cells can locally sense with small probing forces is strongly reduced with
increasing force. Specifically, we predict that the accuracy of
mechanosensation dramatically improves with force, following a universal power
law insensitive to constitutive details, which we quantitatively confirm using
microrheology experiments in collagen and fibrin gels. We provide conceptual
insights into this behavior by introducing a general model for nonlinear
mechanosensation, based on the idea of an emergent nonlinear length-scale
associated with fiber buckling. This force-dependent length-scale enhances the
range over which local mechanical measurements are performed, thereby averaging
the response of a disordered network over an enlarged region. We show with an
example how a cell can use this nonlinear mechanosensation to infer the
macroscopic mechanical properties of a disordered ECM using local measurements.
Together, our results demonstrate that cells can take advantage of the inherent
nonlinearity of fibrous networks to robustly sense, control, and respond to
their mechanical environment.
