Real Space and Time Imaging of Collective Headgroup Dipole Motions in Zwitterionic Lipid Bilayers

Abstract

Lipid bilayers are supramolecular structures responsible for a range of processes, such as transmembrane transport of ions and solutes, and sorting and replication of genetic materials, to name just a few. Some of these processes are transient and currently, cannot be visualized in real space and time. Here, we developed an approach using 1D, 2D, and 3D Van Hove correlation functions to image collective headgroup dipole motions in zwitterionic phospholipid bilayers. We show that both 2D and 3D spatiotemporal images of headgroup dipoles are consistent with commonly understood dynamic features of fluids. However, analysis of the 1D Van Hove function reveals lateral transient and re-emergent collective dynamics of the headgroup dipoles—occurring at picosecond time scales—that transmit and dissipate heat at longer times, due to relaxation processes. At the same time, the headgroup dipoles also generate membrane surface undulations due a collective tilting of the headgroup dipoles. A continuous intensity band of headgroup dipole spatiotemporal correlations—at nanometer length and nanosecond time scales—indicates that dipoles undergo stretching and squeezing elastic deformations. Importantly, the above mentioned intrinsic headgroup dipole motions can be externally stimulated at GHz-frequency scale, enhancing their flexoelectric and piezoelectric capabilities (i.e., increased conversion efficiency of mechanical energy into electric energy). In conclusion, we discuss how lipid membranes can provide molecular-level insights about biological learning and memory, and as platforms for the development of the next generation of neuromorphic computers.

Cations Control Lipid Bilayer Memcapacitance Associated with Long-Term Potentiation

“…In other words, the membrane is intrinsically a piezoelectric supramolecular structure as a result of fluctuations in the form of membrane surface undulations (standing waves). These undulations then give rise to collective headgroup dipole motions, due to lipid tilting . Taken together, the various forces acting on the PC headgroups during the training period induce long-lived piezoelectric and flexoelectric responses.…”

Electric Fields at the Lipid Membrane Interface

“…Another interesting idea was recently suggested regarding dipoles in the polar headgroups of lipids. In the works [70,71], a new experimental system was used to detect changes in the bilayer capacitance after a special "learning" procedure by an external voltage applied to the membrane. Unexpectedly, these changes persist for a long time (tens of minutes).…”