Mechanosensitive Remodeling Sustains Rigidity Homeostasis in Actin Cortex Models

The actin cortex is a dynamic biopolymer network whose mechanical rigidity, while relying critically on tensioned filaments, is robustly sustained amid constant architectural changes through the assembly and disassembly of filaments and crosslinkers. Yet the role of such remodeling processes in rigidity homeostasis remains essentially unexplored in computational models. As a result, we still lack proper understanding of the biological rationale for remodeling, which is energetically expensive, or of the microscopic mechanisms through which collective rigidity is maintained. To address this, we develop two complementary elastic network models in which rigidity homeostasis with complete turnover emerges as a result of mechanosensitive dynamics of filaments (edges) and crosslinkers (nodes), respectively. Both models require the following minimal ingredients: (1) preferential disassembly of edges or nodes under small tension or force, (2) a small but nonzero rate of random disassembly, and (3) energy injection upon assembly. Our models are robust to variations in random disassembly rates and can recover from drastic structural disruption. Remarkably, nodes and edges undergo diffusion even while elastic moduli and structural correlations reach steady states, showing that the models display representational drift similar to that found in neuronal activities and physical learning circuits. We propose that the cortex is an example of “tunable matter,” i.e ., its mechanosensitive remodeling dynamics tune its edges and nodes so that the cortex as a whole can maintain robust but flexible rigidity in fluctuating mechanical environments, creating survival advantages that justify its energy consumption.