Simultaneously propagating voltage and pressure pulses in lipid monolayers of pork brain and synthetic lipids

Abstract

Hydrated interfaces are ubiquitous in biology and appear on all length scales from ions and individual molecules to membranes and cellular networks. In vivo, they comprise a high degree of self-organization and complex entanglement, which limits their experimental accessibility by smearing out the individual phenomenology. The Langmuir technique, however, allows the examination of defined interfaces, the controllable thermodynamic state of which enables one to explore the proper state diagrams. Here we demonstrate that voltage and pressure pulses simultaneously propagate along monolayers comprised of either native pork brain or synthetic lipids. The excitation of pulses is conducted by the application of small droplets of acetic acid and monitored subsequently employing time-resolved Wilhelmy plate and Kelvin probe measurements. The isothermal state diagrams of the monolayers for both lateral pressure and surface potential are experimentally recorded, enabling us to predict dynamic voltage pulse amplitudes of 0.1-3 mV based on the assumption of static mechanoelectrical coupling. We show that the underlying physics for such propagating pulses is the same for synthetic and natural extracted (pork brain) lipids and that the measured propagation velocities and pulse amplitudes depend on the compressibility of the interface. Given the ubiquitous presence of hydrated interfaces in biology, our experimental findings seem to support a fundamentally new mechanism for the propagation of signals and communication pathways in biology (signaling), which is based neither on protein-protein or receptor-ligand interaction nor diffusion.

Solitary electromechanical pulses in lobster neurons

“…Recently, there have been various reports, both theoretical and experimental, regarding the possibility of mechanical pulse propagation in artificial systems close to transitions and in nerves (14,16,17,21,22,(31)(32)(33). Heimburg and Jackson (14) argued that, close to the phase transitions found in biological tissue, electromechanical solitons with properties similar to those of the action potential can travel along the nerve axons.…”

“…They are rather different aspects of the same phenomenon as seen by different instrumentation. There exists clear evidence that electromechanical pulses can travel on lipid monolayers close to the LE-LC transition with velocities very close to those of non-myelinated nerves (21,22). However, there is a striking lack of experiments that actually demonstrate the mechanical nature of the nerve pulse.…”

Evidence for two-dimensional solitary sound waves in a lipid controlled interface and its implications for biological signalling

“…In our recent work, on opto-mechanical coupling [6], it was shown that Du/u DA/A DV/V in the transition region at the interface, where A and V are the surface area and surface potential respectively. Based on this correspondence, the solitary waves excited in the transition regime with a relative FRET amplitude Du/u of 1.2 units are estimated to measure approximately 200 mV in surface potential while sub-threshold pulses measured outside this region will correspond to a surface potential of approximately 5 mV [5]. The pulse shape varies strongly as a function of state near the transition and can be resolved further (electronic supplementary material, figure S2).…”

“…The shape of the solitary pulses in lipid monolayers and action potentials in cell membranes can be directly compared because fluorescence reports membrane potential in both cases [6,35,36]. There are several striking similarities between our results on lipid monolayers and the data on nerve pulses: (i) both systems support 'all-or-none' pulses which propagate as solitary waves and exist only in a narrow window bound by certain nonlinearities in their respective state diagrams [28,37,38], (ii) the pulses in both systems represent an adiabatic phenomenon [39,40] and are not only electrical but are also inseparably mechanical (deflection and volume), optical (polarization, chirality, fluorescence, turbidity) and thermal (temperature, enthalpy) pulses [5,6,36,37,39,[41][42][43][44][45][46].…”

“…For instance, heat capacity or compressibility of the interface [2][3][4] has been shown to regulate transmembrane current fluctuations or two-dimensional pulse propagation, during which all the variables of interface (pressure, temperature, surface potential, fluorescence, density, charge, etc.) are affected simultaneously as required by Maxwell's relations [3,5,6]. Such events derived from fundamental physical principles may imply certain biological functions (e.g.…”