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Cations Control Lipid Bilayer Memcapacitance Associated with Long-Term Potentiation
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    Cations Control Lipid Bilayer Memcapacitance Associated with Long-Term Potentiation
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    ACS Applied Materials & Interfaces

    Cite this: ACS Appl. Mater. Interfaces 2023, 15, 37, 44533–44540
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    https://doi.org/10.1021/acsami.3c09056
    Published September 11, 2023
    Copyright © 2023 American Chemical Society

    Abstract

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    Phospholipid bilayers can be described as capacitors whose capacitance per unit area (specific capacitance, Cm) is determined by their thickness and dielectric constant─independent of applied voltage. It is also widely assumed that the Cm of membranes can be treated as a “biological constant”. Recently, using droplet interface bilayers (DIBs), it was shown that zwitterionic phosphatidylcholine (PC) lipid bilayers can act as voltage-dependent, nonlinear memory capacitors, or memcapacitors. When exposed to an electrical “training” stimulation protocol, capacitive energy storage in lipid membranes was enhanced in the form of long-term potentiation (LTP), which enables biological learning and long-term memory. LTP was the result of membrane restructuring and the progressive asymmetric distribution of ions across the lipid bilayer during training, which is analogous, for example, to exponential capacitive energy harvesting from self-powered nanogenerators. Here, we describe how LTP could be produced from a membrane that is continuously pumped into a nonequilibrium steady state, altering its dielectric properties. During this time, the membrane undergoes static and dynamic changes that are fed back to the system’s potential energy, ultimately resulting in a membrane whose modified molecular structure supports long-term memory storage and LTP. We also show that LTP is very sensitive to different salts (KCl, NaCl, LiCl, and TmCl3), with LiCl and TmCl3 having the most profound effect in depressing LTP, relative to KCl. This effect is related to how the different cations interact with the bilayer zwitterionic PC lipid headgroups primarily through electric-field-induced changes to the statistically averaged orientations of water dipoles at the bilayer headgroup interface.

    Copyright © 2023 American Chemical Society

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    Supporting Information

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    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acsami.3c09056.

    • Methods, vesicle preparation and droplet interface bilayer (DIB) formation, DIB electrical measurements, DIB data analysis, monolayer formation and SFG measurements, molecular dynamics simulations, phenomenological description of system total stored energy, evolution of time-dependent capacitances during training (PDF)

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    This article is cited by 10 publications.

    1. C. Patrick Collier, Dima Bolmatov, Ralph Lydic, John Katsaras. Neuronal Plasma Membranes as Supramolecular Assemblies for Biological Memory. Langmuir 2025, 41 (5) , 2973-2979. https://doi.org/10.1021/acs.langmuir.4c03375
    2. Maxim O. Lavrentovich, Jan-Michael Y. Carrillo, Charles Patrick Collier, John Katsaras, Dima Bolmatov. Curvature Memory in Electrically Stimulated Lipid Membranes. Langmuir 2025, 41 (5) , 3157-3165. https://doi.org/10.1021/acs.langmuir.4c03799
    3. Kenneth D. Judd, Sean W. Parsons, Tirthick Majumder, Jahan M. Dawlaty. Electrostatics, Hydration, and Chemical Equilibria at Charged Monolayers on Water. Chemical Reviews 2025, Article ASAP.
    4. Braydon Segars, Kyle Rosenberg, Sarita Shrestha, Joshua J. Maraj, Stephen A. Sarles, Eric Freeman. Neuron‐Inspired Biomolecular Memcapacitors Formed Using Droplet Interface Bilayer Networks. Advanced Electronic Materials 2025, 48 https://doi.org/10.1002/aelm.202400644
    5. Mohammad Amin Morsali, Hemayat Shekaari, Behrang Golmohammadi. Hydration behavior of L-proline in the presence of mono, bis, tris-(2-hydroxyethyl) ammonium acetate protic ionic liquids:  Thermophysical properties. Scientific Reports 2024, 14 (1) https://doi.org/10.1038/s41598-024-77341-6
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    7. Zening Liu, Lu Lin, Tianyu Li, Uvinduni I. Premadasa, Kunlun Hong, Ying-Zhong Ma, Robert L. Sacci, John Katsaras, Jan-Michael Carrillo, Benjamin Doughty, C. Patrick Collier. Physicochemical control of solvation and molecular assembly of charged amphiphilic oligomers at air-aqueous interfaces. Journal of Colloid and Interface Science 2024, 669 , 552-560. https://doi.org/10.1016/j.jcis.2024.05.008
    8. Dima Bolmatov, John Katsaras, C. Patrick Collier. Heterosynaptic plasticity in memristive and memcapacitive lipid bilayers: A snapshot review. MRS Advances 2024, 9 (9) , 565-573. https://doi.org/10.1557/s43580-024-00800-9
    9. Dima Bolmatov, C. Patrick Collier, John Katsaras, Maxim O. Lavrentovich. Physical insights into biological memory using phospholipid membranes. The European Physical Journal E 2024, 47 (1) https://doi.org/10.1140/epje/s10189-023-00391-7
    10. Yury Ermakov. Electric Fields at the Lipid Membrane Interface. Membranes 2023, 13 (11) , 883. https://doi.org/10.3390/membranes13110883

    ACS Applied Materials & Interfaces

    Cite this: ACS Appl. Mater. Interfaces 2023, 15, 37, 44533–44540
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acsami.3c09056
    Published September 11, 2023
    Copyright © 2023 American Chemical Society

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