Memristive Ion Channel-Doped Biomembranes as Synaptic Mimics

Najem, Joseph S.; Taylor, Graham J.; Weiss, Ryan J.; Hasan, Md Sakib; Rose, Garrett; Schuman, Catherine D.; Belianinov, Alex; Collier, C. Patrick; Sarles, Stephen A.

doi:10.1021/acsnano.8b01282

Title: Memristive Ion Channel-Doped Biomembranes as Synaptic Mimics

Journal Article · Mon Mar 26 00:00:00 EDT 2018 · ACS Nano

DOI:https://doi.org/10.1021/acsnano.8b01282· OSTI ID:1468075

^[1];

^[2]; Weiss, Ryan J. ^[3]; Hasan, Md Sakib ^[3]; Rose, Garrett ^[3];

^[4];

^[5];

^[5]; Sarles, Stephen A. ^[6]

Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Joint Institute for Biological Sciences; Univ. of Tennessee, Knoxville, TN (United States). Department of Mechanical, Aerospace and Biomedical Engineering
Univ. of Tennessee, Knoxville, TN (United States). Bredesen Center for Interdisciplinary Research and Department of Mechanical, Aerospace and Biomedical Engineering
Univ. of Tennessee, Knoxville, TN (United States). Department of Electrical Engineering and Computer Science
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Computer Science and Mathematics Division
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Center for Nanophase Materials Science (CNMS)
Univ. of Tennessee, Knoxville, TN (United States). Department of Mechanical, Aerospace and Biomedical Engineering

Solid-state neuromorphic systems based on transistors or memristors have yet to achieve the interconnectivity, performance, and energy efficiency of the brain due to excessive noise, undesirable material properties, and nonbiological switching mechanisms. Here in this work, we demonstrate that an alamethicin-doped, synthetic biomembrane exhibits memristive behavior, emulates key synaptic functions including paired-pulse facilitation and depression, and enables learning and computing. Unlike state-of-the-art devices, our two-terminal, biomolecular memristor features similar structure (biomembrane), switching mechanism (ion channels), and ionic transport modality as biological synapses while operating at considerably lower power. The reversible and volatile voltage-driven insertion of alamethicin peptides into an insulating lipid bilayer creates conductive pathways that exhibit pinched current–voltage hysteresis at potentials above their insertion threshold. Moreover, the synapse-like dynamic properties of the biomolecular memristor allow for simplified learning circuit implementations. Finally, low-power memristive devices based on stimuli-responsive biomolecules represent a major advance toward implementation of full synaptic functionality in neuromorphic hardware.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1468075

Journal Information:: ACS Nano, Vol. 12, Issue 5; ISSN 1936-0851

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 73 works

Citation information provided by
Web of Science

References (53)

A million spiking-neuron integrated circuit with a scalable communication network and interface Merolla, P. A.; Arthur, J. V.; Alvarez-Icaza, R. Science, Vol. 345, Issue 6197 https://doi.org/10.1126/science.1254642	journal	August 2014
Neurogrid: A Mixed-Analog-Digital Multichip System for Large-Scale Neural Simulations Benjamin, Ben Varkey; Gao, Peiran; McQuinn, Emmett Proceedings of the IEEE, Vol. 102, Issue 5 https://doi.org/10.1109/JPROC.2014.2313565	journal	May 2014
A 32 GBit/s communication SoC for a waferscale neuromorphic system Scholze, Stefan; Eisenreich, Holger; Höppner, Sebastian Integration, Vol. 45, Issue 1 https://doi.org/10.1016/j.vlsi.2011.05.003	journal	January 2012
The SpiNNaker Project Furber, Steve B.; Galluppi, Francesco; Temple, Steve Proceedings of the IEEE, Vol. 102, Issue 5 https://doi.org/10.1109/JPROC.2014.2304638	journal	May 2014
Synapses and Memory Storage Mayford, M.; Siegelbaum, S. A.; Kandel, E. R. Cold Spring Harbor Perspectives in Biology, Vol. 4, Issue 6 https://doi.org/10.1101/cshperspect.a005751	journal	April 2012
Spike Timing-Dependent Plasticity: From Synapse to Perception Dan, Yang; Poo, Mu-Ming Physiological Reviews, Vol. 86, Issue 3 https://doi.org/10.1152/physrev.00030.2005	journal	July 2006
Efficiency of Functional Brain Networks and Intellectual Performance van den Heuvel, M. P.; Stam, C. J.; Kahn, R. S. Journal of Neuroscience, Vol. 29, Issue 23 https://doi.org/10.1523/JNEUROSCI.1443-09.2009	journal	June 2009
Neuromorphic electronic systems Mead, C. Proceedings of the IEEE, Vol. 78, Issue 10 https://doi.org/10.1109/5.58356	journal	January 1990
A single-transistor silicon synapse Diorio, C.; Hasler, P.; Minch, A. IEEE Transactions on Electron Devices, Vol. 43, Issue 11 https://doi.org/10.1109/16.543035	journal	January 1996
The missing memristor found Strukov, Dmitri B.; Snider, Gregory S.; Stewart, Duncan R. Nature, Vol. 453, Issue 7191 https://doi.org/10.1038/nature06932	journal	May 2008
Two centuries of memristors Prodromakis, Themistoklis; Toumazou, Christofer; Chua, Leon Nature Materials, Vol. 11, Issue 6 https://doi.org/10.1038/nmat3338	journal	May 2012
Nanoscale Memristor Device as Synapse in Neuromorphic Systems Jo, Sung Hyun; Chang, Ting; Ebong, Idongesit Nano Letters, Vol. 10, Issue 4, p. 1297-1301 https://doi.org/10.1021/nl904092h	journal	April 2010
Training and operation of an integrated neuromorphic network based on metal-oxide memristors Prezioso, M.; Merrikh-Bayat, F.; Hoskins, B. D. Nature, Vol. 521, Issue 7550 https://doi.org/10.1038/nature14441	journal	May 2015
Sparse coding with memristor networks Sheridan, Patrick M.; Cai, Fuxi; Du, Chao Nature Nanotechnology, Vol. 12, Issue 8 https://doi.org/10.1038/nnano.2017.83	journal	May 2017
Memristor-The missing circuit element Chua, L. IEEE Transactions on Circuit Theory, Vol. 18, Issue 5 https://doi.org/10.1109/TCT.1971.1083337	journal	January 1971
How We Found The Missing Memristor Williams, R. IEEE Spectrum, Vol. 45, Issue 12 https://doi.org/10.1109/MSPEC.2008.4687366	journal	December 2008
Atomic structure of conducting nanofilaments in TiO2 resistive switching memory Kwon, Deok-Hwang; Kim, Kyung Min; Jang, Jae Hyuck Nature Nanotechnology, Vol. 5, Issue 2 https://doi.org/10.1038/nnano.2009.456	journal	January 2010
Nanoscale cation motion in TaOx, HfOx and TiOx memristive systems Wedig, Anja; Luebben, Michael; Cho, Deok-Yong Nature Nanotechnology, Vol. 11, Issue 1 https://doi.org/10.1038/nnano.2015.221	journal	September 2015
Experimental Demonstration of a Second-Order Memristor and Its Ability to Biorealistically Implement Synaptic Plasticity Kim, Sungho; Du, Chao; Sheridan, Patrick Nano Letters, Vol. 15, Issue 3 https://doi.org/10.1021/acs.nanolett.5b00697	journal	February 2015
Biorealistic Implementation of Synaptic Functions with Oxide Memristors through Internal Ionic Dynamics Du, Chao; Ma, Wen; Chang, Ting Advanced Functional Materials, Vol. 25, Issue 27 https://doi.org/10.1002/adfm.201501427	journal	June 2015
Memristors with diffusive dynamics as synaptic emulators for neuromorphic computing Wang, Zhongrui; Joshi, Saumil; Savel’ev, Sergey E. Nature Materials, Vol. 16, Issue 1 https://doi.org/10.1038/nmat4756	journal	September 2016
Fully memristive neural networks for pattern classification with unsupervised learning Wang, Zhongrui; Joshi, Saumil; Savel’ev, Sergey Nature Electronics, Vol. 1, Issue 2 https://doi.org/10.1038/s41928-018-0023-2	journal	February 2018
Optimization of an organic memristor as an adaptive memory element Berzina, Tatiana; Smerieri, Anteo; Bernabò, Marco Journal of Applied Physics, Vol. 105, Issue 12 https://doi.org/10.1063/1.3153944	journal	June 2009
Polymer memristor for information storage and neuromorphic applications Chen, Yu; Liu, Gang; Wang, Cheng Materials Horizons, Vol. 1, Issue 5 https://doi.org/10.1039/C4MH00067F	journal	January 2014
A non-volatile organic electrochemical device as a low-voltage artificial synapse for neuromorphic computing van de Burgt, Yoeri; Lubberman, Ewout; Fuller, Elliot J. Nature Materials, Vol. 16, Issue 4 https://doi.org/10.1038/nmat4856	journal	February 2017
A ferroelectric memristor Chanthbouala, André; Garcia, Vincent; Cherifi, Ryan O. Nature Materials, Vol. 11, Issue 10 https://doi.org/10.1038/nmat3415	journal	September 2012
Ferroelectric Tunnel Memristor Kim, D. J.; Lu, H.; Ryu, S. Nano Letters, Vol. 12, Issue 11 https://doi.org/10.1021/nl302912t	journal	October 2012
Analog Memristors Based on Thickening/Thinning of Ag Nanofilaments in Amorphous Manganite Thin Films Liu, Dongqing; Cheng, Haifeng; Zhu, Xuan ACS Applied Materials & Interfaces, Vol. 5, Issue 21 https://doi.org/10.1021/am403497y	journal	October 2013
Nanoscale electrochemical metallization memories based on amorphous (La, Sr)MnO ₃ using ultrathin porous alumina masks Liu, Dongqing; Zhang, Chaoyang; Wang, Guang Journal of Physics D: Applied Physics, Vol. 47, Issue 8 https://doi.org/10.1088/0022-3727/47/8/085108	journal	February 2014
Spintronic Memristor Through Spin-Torque-Induced Magnetization Motion IEEE Electron Device Letters, Vol. 30, Issue 3 https://doi.org/10.1109/LED.2008.2012270	journal	March 2009
The chips are down for Moore’s law Waldrop, M. Mitchell Nature, Vol. 530, Issue 7589 https://doi.org/10.1038/530144a	journal	February 2016
Analogue signal and image processing with large memristor crossbars Li, Can; Hu, Miao; Li, Yunning Nature Electronics, Vol. 1, Issue 1 https://doi.org/10.1038/s41928-017-0002-z	journal	December 2017
Regulated Attachment Method for Reconstituting Lipid Bilayers of Prescribed Size within Flexible Substrates Sarles, Stephen A.; Leo, Donald J. Analytical Chemistry, Vol. 82, Issue 3 https://doi.org/10.1021/ac902555z	journal	February 2010
Direct in situ measurement of specific capacitance, monolayer tension, and bilayer tension in a droplet interface bilayer Taylor, Graham J.; Venkatesan, Guru A.; Collier, C. Patrick Soft Matter, Vol. 11, Issue 38 https://doi.org/10.1039/C5SM01005E	journal	January 2015
Alamethicin: A Peptide Model for Voltage Gating and Protein-Membrane Interactions Cafiso, D. S. Annual Review of Biophysics and Biomolecular Structure, Vol. 23, Issue 1 https://doi.org/10.1146/annurev.bb.23.060194.001041	journal	June 1994
If it’s pinched it’s a memristor Chua, Leon Semiconductor Science and Technology, Vol. 29, Issue 10 https://doi.org/10.1088/0268-1242/29/10/104001	journal	September 2014
Hodgkin–Huxley axon is made of Memristors Chua, Leon; Sbitnev, Valery; Kim, Hyongsuk International Journal of Bifurcation and Chaos, Vol. 22, Issue 03 https://doi.org/10.1142/S021812741230011X	journal	March 2012
Short-Term Synaptic Plasticity Zucker, Robert S.; Regehr, Wade G. Annual Review of Physiology, Vol. 64, Issue 1 https://doi.org/10.1146/annurev.physiol.64.092501.114547	journal	March 2002
A Carbon Nanotube Synapse with Dynamic Logic and Learning Kim, Kyunghyun; Chen, Chia-Ling; Truong, Quyen Advanced Materials, Vol. 25, Issue 12 https://doi.org/10.1002/adma.201203116	journal	December 2012
Memristor-Based Nonvolatile Random Access Memory: Hybrid Architecture for Low Power Compact Memory Design Sarwar, Syed Shakib; Saqueb, Syed An Nazmus; Quaiyum, Farhan IEEE Access, Vol. 1 https://doi.org/10.1109/ACCESS.2013.2259891	journal	January 2013
Vesicle and bilayer formation of diphytanoylphosphatidylcholine (DPhPC) and diphytanoylphosphatidylethanolamine (DPhPE) mixtures and their bilayers’ electrical stability Andersson, Martin; Jackman, Joshua; Wilson, Danyell Colloids and Surfaces B: Biointerfaces, Vol. 82, Issue 2 https://doi.org/10.1016/j.colsurfb.2010.10.017	journal	February 2011
Amyloid β Ion Channels in a Membrane Comprising Brain Total Lipid Extracts Lee, Joon; Kim, Young Hun; T. Arce, Fernando ACS Chemical Neuroscience, Vol. 8, Issue 6 https://doi.org/10.1021/acschemneuro.7b00006	journal	February 2017
Emulsions: basic principles Bibette, J.; Calderon, F. Leal; Poulin, P. Reports on Progress in Physics, Vol. 62, Issue 6 https://doi.org/10.1088/0034-4885/62/6/203	journal	January 1999
From the stochasticity of molecular processes to the variability of synaptic transmission Ribrault, Claire; Sekimoto, Ken; Triller, Antoine Nature Reviews Neuroscience, Vol. 12, Issue 7 https://doi.org/10.1038/nrn3025	journal	June 2011
Hydrodynamic trapping for rapid assembly and in situ electrical characterization of droplet interface bilayer arrays Nguyen, Mary-Anne; Srijanto, Bernadeta; Collier, C. Patrick Lab on a Chip, Vol. 16, Issue 18 https://doi.org/10.1039/C6LC00810K	journal	January 2016
Heating-Enabled Formation of Droplet Interface Bilayers Using Escherichia coli Total Lipid Extract Taylor, Graham J.; Sarles, Stephen A. Langmuir, Vol. 31, Issue 1 https://doi.org/10.1021/la503471m	journal	December 2014
Chemical Nature of Synaptic Transmission in Vertebrates Krnjević, K. Physiological Reviews, Vol. 54, Issue 2 https://doi.org/10.1152/physrev.1974.54.2.418	journal	April 1974
Channel kinetics determine the time course of NMDA receptor-mediated synaptic currents Lester, Robin A. J.; Clements, John D.; Westbrook, Gary L. Nature, Vol. 346, Issue 6284 https://doi.org/10.1038/346565a0	journal	August 1990
Calcium-channel number critically influences synaptic strength and plasticity at the active zone Sheng, Jiansong; He, Liming; Zheng, Hongwei Nature Neuroscience, Vol. 15, Issue 7 https://doi.org/10.1038/nn.3129	journal	June 2012
Facilitation and depression at single central synapses Stevens, Charles F.; Wang, Yanyan Neuron, Vol. 14, Issue 4 https://doi.org/10.1016/0896-6273(95)90223-6	journal	April 1995
Ion Channels of Alamethicin Dimer N-Terminally Linked by Disulfide Bond Okazaki, Takashi; Sakoh, Machiko; Nagaoka, Yasuo Biophysical Journal, Vol. 85, Issue 1 https://doi.org/10.1016/S0006-3495(03)74472-5	journal	July 2003
A Tissue-Like Printed Material Villar, Gabriel; Graham, Alexander D.; Bayley, Hagan Science, Vol. 340, Issue 6128 https://doi.org/10.1126/science.1229495	journal	April 2013
Capacitive Detection of Low-Enthalpy, Higher-Order Phase Transitions in Synthetic and Natural Composition Lipid Membranes Taylor, Graham J.; Heberle, Frederick A.; Seinfeld, Jason S. Langmuir, Vol. 33, Issue 38 https://doi.org/10.1021/acs.langmuir.7b02022	journal	August 2017

Cited By (14)

Improvement of analogue switching characteristics of MoS ₂ memristors through plasma treatment Li, Da; Ryu, Byunghoon; Yoon, JeongSeop Journal of Physics D: Applied Physics, Vol. 53, Issue 13 https://doi.org/10.1088/1361-6463/ab6572	journal	January 2020
On the Application of a Diffusive Memristor Compact Model to Neuromorphic Circuits Cisternas Ferri, Agustín; Rapoport, Alan; Fierens, Pablo I. Materials, Vol. 12, Issue 14 https://doi.org/10.3390/ma12142260	journal	July 2019
Artificial water channels enable fast and selective water permeation through water-wire networks Song, Woochul; Joshi, Himanshu; Chowdhury, Ratul Nature Nanotechnology, Vol. 15, Issue 1 https://doi.org/10.1038/s41565-019-0586-8	journal	December 2019
A flexible conformable artificial organ-damage memory system towards hazardous gas leakage based on a single organic transistor Song, Zhiqi; Tong, Yanhong; Zhao, Xiaoli Materials Horizons, Vol. 6, Issue 4 https://doi.org/10.1039/c8mh01577e	journal	January 2019
Overview of Resistive Random Access Memory (RRAM): Materials, Filament Mechanisms, Performance Optimization, and Prospects Wang, Hong; Yan, Xiaobing physica status solidi (RRL) – Rapid Research Letters, Vol. 13, Issue 9 https://doi.org/10.1002/pssr.201900073	journal	May 2019
Ultrathin TiO _x Interface‐Mediated ZnO‐Nanowire Memristive Devices Emulating Synaptic Behaviors Xiao, Ming; Yeow, Travis; Nguyen, Viet Huong Advanced Electronic Materials, Vol. 5, Issue 6 https://doi.org/10.1002/aelm.201900142	journal	May 2019
Regulating firing rates in a neural circuit by activating memristive synapse with magnetic coupling Wu, Fuqiang; Zhang, Yin; Zhang, Xinjing Nonlinear Dynamics, Vol. 98, Issue 2 https://doi.org/10.1007/s11071-019-05239-4	journal	September 2019
Bio-inspired protonic memristor devices based on metal complexes with proton-coupled electron transfer Hiruma, Yusuke; Yoshikawa, Kai; Haga, Masa-aki Faraday Discussions, Vol. 213 https://doi.org/10.1039/c8fd00098k	journal	January 2019
Memristive plasticity in artificial electrical synapses via geometrically reconfigurable, gramicidin-doped biomembranes Koner, Subhadeep; Najem, Joseph S.; Hasan, Md Sakib Nanoscale, Vol. 11, Issue 40 https://doi.org/10.1039/c9nr07288h	journal	January 2019
Memristive Synapses and Neurons for Bioinspired Computing Yang, Rui; Huang, He‐Ming; Guo, Xin Advanced Electronic Materials, Vol. 5, Issue 9 https://doi.org/10.1002/aelm.201900287	journal	November 2018
Threshold Switching in Single Metal‐Oxide Nanobelt Devices Emulating an Artificial Nociceptor Xiao, Ming; Shen, Daozhi; Futscher, Moritz H. Advanced Electronic Materials, Vol. 6, Issue 1 https://doi.org/10.1002/aelm.201900595	journal	November 2019
Dynamical nonlinear memory capacitance in biomimetic membranes Najem, Joseph S.; Hasan, Md Sakib; Williams, R. Stanley Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-11223-8	journal	July 2019
Memristive synapses with high reproducibility for flexible neuromorphic networks based on biological nanocomposites Ge, Jun; Li, Dongyuan; Huang, Changqiao Nanoscale, Vol. 12, Issue 2 https://doi.org/10.1039/c9nr08001e	journal	January 2020
Bridging Biological and Artificial Neural Networks with Emerging Neuromorphic Devices: Fundamentals, Progress, and Challenges Tang, Jianshi; Yuan, Fang; Shen, Xinke Advanced Materials, Vol. 31, Issue 49 https://doi.org/10.1002/adma.201902761	journal	September 2019

Similar Records

Response of a Memristive Biomembrane and Demonstration of Potential Use in Online Learning

Conference · Tue Jan 01 00:00:00 EST 2019 · OSTI ID:1468075

Hasan, Md Sakib; Najem, Joseph S.; Weiss, Ryan; +5 more

Biomimetic, Soft-Material Synapse for Neuromorphic Computing: from Device to Network

Conference · Tue Jan 01 00:00:00 EST 2019 · OSTI ID:1468075

Sakib hasan, Md; Schuman, Catherine; Najem, Joseph S.; +6 more

Assembly and Characterization of Biomolecular Memristors Consisting of Ion Channel-doped Lipid Membranes

Journal Article · Tue Jan 01 00:00:00 EST 2019 · Journal of Visualized Experiments · OSTI ID:1468075

Najem, Joseph S.; Taylor, Graham J.; Armendarez, Nick; +7 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
36 MATERIALS SCIENCE
42 ENGINEERING
alamethicin
biomembrane
biomolecular memristor
ion channel
lipid bilayer
memristor
neuromorphic computing

Title: Memristive Ion Channel-Doped Biomembranes as Synaptic Mimics

Citation Formats

References (53)

Cited By (14)

Similar Records

Related Subjects