Dynamical nonlinear memory capacitance in biomimetic membranes

Joseph S Najem,Stephen A Sarles,R Stanley Williams,Garrett S Rose,C Patrick Collier,Graham J Taylor,Ryan J Weiss,Md Sakib Hasan

doi:10.1038/s41467-019-11223-8

Abstract

Two-terminal memory elements, or memelements, capable of co-locating signal processing and memory via history-dependent reconfigurability at the nanoscale are vital for next-generation computing materials striving to match the brain’s efficiency and flexible cognitive capabilities. While memory resistors, or memristors, have been widely reported, other types of memelements remain underexplored or undiscovered. Here we report the first example of a volatile, voltage-controlled memcapacitor in which capacitive memory arises from reversible and hysteretic geometrical changes in a lipid bilayer that mimics the composition and structure of biomembranes. We demonstrate that the nonlinear dynamics and memory are governed by two implicitly-coupled, voltage-dependent state variables—membrane radius and thickness. Further, our system is capable of tuneable signal processing and learning via synapse-like, short-term capacitive plasticity. These findings will accelerate the development of low-energy, biomolecular neuromorphic memelements, which, in turn, could also serve as models to study capacitive memory and signal processing in neuronal membranes.

Highlights

We recently demonstrated that a synthetic biomembrane doped with voltage-activated ion channels exhibits volatile memory resistance governed by two voltage-dependent state variables: the areal density of ion channels and the increase in membrane area due to electrowetting[16]
We have shown that the spike-rate-dependent plasticity (SRDP) exhibited by these two-terminal memristors enable them to function as resistive synapses for online learning in spike recurrent neural networks built from solid-state neurons[33,34]
Based on these findings we hypothesized that an insulating lipid bilayer, without conductive ion channels, may exhibit capacitive memory governed solely by voltage-dependent changes to the dimensions of the dielectric dominated by the hydrophobic core of the bilayer

Summary

Introduction

We recently demonstrated that a synthetic biomembrane (i.e., lipid bilayer) doped with voltage-activated ion channels exhibits volatile memory resistance governed by two voltage-dependent state variables: the areal density of ion channels and the increase in membrane area due to electrowetting[16]. We have shown that the spike-rate-dependent plasticity (SRDP) exhibited by these two-terminal memristors enable them to function as resistive synapses for online learning in spike recurrent neural networks built from solid-state neurons[33,34] Based on these findings we hypothesized that an insulating lipid bilayer, without conductive ion channels, may exhibit capacitive memory governed solely by voltage-dependent changes to the dimensions of the dielectric dominated by the hydrophobic core of the bilayer. We report that adhering, lipid-encased, aqueous droplets in oil yields an interfacial biomimetic membrane (3–5 nm thick) that exhibits volatile, analogue memcapacitance via voltagecontrolled geometric reconfigurability Pinched hysteresis in both the charge-voltage and capacitance-voltage planes result from dynamic changes in interfacial area and hydrophobic thickness, each of which are nonlinearly dependent on voltage. Our results forecast new classes of biomimetic, lowpower memelements based on soft, organic materials and biomolecules, which, in turn, will aid in exploring capacitive memory and susceptibility in neuronal membranes

Methods

Results

Conclusion