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The dynamic assembly and disassembly of the cytoskeleton can create waves and oscillations that are critical to cell migration and other important cell behaviors. Chemical signals have been found to trigger and steer these waves, facilitating the guidance e.g. of immune cells to their target. Here we consider the role of these cytoskeletal dynamics in sensing of the physical microenvironment. We demonstrate that cytoskeletal waves are directly involved in sensing both the microscopic texture of the surrounding, and local DC electric fields. In turn, these cytoskeletal dynamics drive signaling pathways, reversing the typical hierarchy where signals drive biomechanics. Finally, we characterize cytoskeletal dynamics in cells and cell groups with intrinsic electrical activity, networks of neural cells.