Evidence for long-term potentiation in phospholipid membranes

Haden L. Scott, Dima Bolmatov, Peter T. Podar, Zening Liu, Jacob J. Kinnun, Benjamin Doughty, Ralph Lydic, Robert L. Sacci, C. Patrick Collier, John Katsaras

Research output: Contribution to journalArticlepeer-review

15 Scopus citations

Abstract

Biological supramolecular assemblies, such as phospholipid bilayer membranes, have been used to demonstrate signal processing via short-term synaptic plasticity (STP) in the form of paired pulse facilitation and depression, emulating the brain’s efficiency and flexible cognitive capabilities. However, STP memory in lipid bilayers is volatile and cannot be stored or accessed over relevant periods of time, a key requirement for learning. Using droplet interface bilayers (DIBs) composed of lipids, water and hexadecane, and an electrical stimulation training protocol featuring repetitive sinusoidal voltage cycling, we show that DIBs displaying memcapacitive properties can also exhibit persistent synaptic plasticity in the form of long-term potentiation (LTP) associated with capacitive energy storage in the phospholipid bilayer. The time scales for the physical changes associated with the LTP range between minutes and hours, and are substantially longer than previous STP studies, where stored energy dissipated after only a few seconds. STP behavior is the result of reversible changes in bilayer area and thickness. On the other hand, LTP is the result of additional molecular and structural changes to the zwitterionic lipid headgroups and the dielectric properties of the lipid bilayer that result from the buildup of an increasingly asymmetric charge distribution at the bilayer interfaces.

Original languageEnglish
Article numbere2212195119
JournalProceedings of the National Academy of Sciences of the United States of America
Volume119
Issue number50
DOIs
StatePublished - Dec 13 2022

Funding

J.Katsaras would like to thank Fyl Pincus (UC Santa Barbara) for useful discussions. H.L.S., Z.L., C.P.C., J. J. K. and J.Katsaras are supported through the Scientific User Facilities Division of the Department of Energy (DOE) Office of Science, sponsored by the Basic Energy Science (BES) Program, DOE Office of Science, under Contract No. DE-AC05-00OR22725. Data were collected and analyzed at the Center for Nanophase Materials Sciences (CNMS), a US DOE Office of Science User Facility. B.D. is supported by the U.S. Department of Energy, Office of Science, Basic Energy Sciences, Chemical Sciences, Geosciences, and Biosciences Division. R.L.S. was supported by the DOE, Office of Science, sponsored by BES, Materials Sciences and Engineering Division. D.B. is supported through the National Science Foundation, Division of Molecular and Cellular Biosciences (MCB), under contract no. 2219289. P.T.P. was supported by the U.S. DOE, Office of Science, under the Science Undergraduate Laboratory Internships (SULI) program. All samples were prepared at the Physical Characterization Labs,located at the Shull Wollan Center. We thank the editor and the reviewers for their critical reviews that improved the final manuscript. ACKNOWLEDGMENTS. J.Katsaras would like to thank Fyl Pincus (UC Santa Barbara) for useful discussions. H.L.S., Z.L., C.P.C., J. J. K. and J.Katsaras are supported through the Scientific User Facilities Division of the Department of Energy (DOE) Office of Science, sponsored by the Basic Energy Science (BES) Program, DOE Office of Science, under Contract No. DE-AC05-00OR22725. Data were collected and analyzed at the Center for Nanophase Materials Sciences (CNMS), a US DOE Office of Science User Facility. B.D. is supported by the U.S. Department of Energy, Office of Science, Basic Energy Sciences, Chemical Sciences, Geosciences, and Biosciences Division. R.L.S. was supported by the DOE, Office of Science, sponsored by BES, Materials Sciences and Engineering Division. D.B. is supported through the National Science Foundation, Division of Molecular and Cellular Biosciences (MCB), under contract no. 2219289.

FundersFunder number
Center for Nanophase Materials Sciences
Fyl Pincus
National Science Foundation
U.S. Department of Energy
Division of Molecular and Cellular Biosciences2219289
Office of ScienceDE-AC05-00OR22725
Basic Energy Sciences
University of California, Santa Barbara
Division of Materials Sciences and Engineering
Chemical Sciences, Geosciences, and Biosciences Division

    Keywords

    • droplet interface bilayers
    • lipid bilayers
    • long-term potentiation
    • neuromorphic
    • plasticity

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