Spatiotemporal dynamics of ionic reorganization near biological membrane interfaces

Abstract

Electrical signals in excitable cells involve spatially localized ionic fluxes through ion channels and pumps on cellular lipid membranes. Common approaches to understand how these localized fluxes spread assume that the membrane and the surrounding electrolyte comprise an equivalent circuit of capacitors and resistors, which ignores the localized nature of transmembrane ion transport, the resulting ionic gradients and electric fields, and their spatiotemporal relaxation. Here, we consider a model of localized ion pumping across a lipid membrane, and use theory and simulation to investigate how the electrochemical signal propagates spatiotemporally in- and out-of-plane along the membrane. The localized pumping generates long-ranged electric fields with three distinct scaling regimes along the membrane: a constant potential near-field region, an intermediate "monopolar" region, and a far-field "dipolar" region. Upon sustained pumping, the monopolar region expands radially in-plane with a steady speed that is enhanced by the dielectric mismatch and the finite thickness of the lipid membrane. For unmyelinated lipid membranes in physiological settings, we find remarkably fast propagation speeds of $\sim\!40 \, \mathrm{m/s}$, allowing faster ionic reorganization compared to bare diffusion. Together, our work shows that transmembrane ionic fluxes induce transient long-ranged electric fields in electrolyte solutions, which may play hitherto unappreciated roles in biological signaling.