Hostname: page-component-76c49bb84f-7l7zb Total loading time: 0 Render date: 2025-07-09T22:42:28.468Z Has data issue: false hasContentIssue false
  • English
  • Français

Towards biomimetic electronics that emulate cells

Published online by Cambridge University Press:  20 July 2020

Claudia Lubrano ,
Giovanni Maria Matrone ,
Csaba Forro ,
Zeinab Jahed ,
Andreas Offenhaeusser ,
Alberto Salleo ,
Bianxiao Cui  and
Francesca Santoro
Claudia Lubrano
Affiliation:
Tissue Electronics, Istituto Italiano di Tecnologia, Naples, Italy Dipartimento di Chimica, Materiali e Produzione Industriale, Università di Napoli Federico II, Naples, Italy
Giovanni Maria Matrone
Affiliation:
Tissue Electronics, Istituto Italiano di Tecnologia, Naples, Italy
Csaba Forro
Affiliation:
Tissue Electronics, Istituto Italiano di Tecnologia, Naples, Italy Department of Chemistry, Stanford University, Stanford, CA, USA
Zeinab Jahed
Affiliation:
Department of Chemistry, Stanford University, Stanford, CA, USA
Andreas Offenhaeusser
Affiliation:
Institute of Biological Information Processes (IBI-3), Bioelectronics, Forschungszentrum Jülich GmbH, Jülich, Germany
Alberto Salleo
Affiliation:
Department of Materials Science and Engineering, Stanford University, Stanford, CA, USA
Bianxiao Cui
Affiliation:
Department of Chemistry, Stanford University, Stanford, CA, USA
Francesca Santoro*
Affiliation:
Tissue Electronics, Istituto Italiano di Tecnologia, Naples, Italy
*
Address all correspondence to Francesca Santoro at francesca.santoro@iit.it
Get access

Abstract

Bioelectronics aims to design electronic devices which can be fully integrated within tissues to monitor or stimulate specific cell functions. The main challenge is the engineering of the cell–chip interface and diverse materials, and devices have been developed to recapitulate biological architectures and functionalities. In this Prospective article, the authors give an overview on how the bioelectronics community has exploited biomimetic approaches to emulate cell morphologies, interactions, and functions to design optimal electrical platforms to be coupled to living cells.

Information

Type
Prospective Articles
Information
MRS Communications , Volume 10 , Issue 3 , September 2020 , pp. 398 - 412
Check for updates
Copyright
Copyright © Materials Research Society, 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

Footnotes

†

These authors have equally contributed to this work.

References

Ott, J., Lazalde, M., and Gu, G.X.: Algorithmic-driven design of shark denticle bioinspired structures for superior aerodynamic properties. Bioinspir. Biomim. 15, 026001 (2020).CrossRefGoogle ScholarPubMed
Gu, G.X., Takaffoli, M., and Buehler, M.J.: Hierarchically enhanced impact resistance of bioinspired composites. Adv. Mater. 29, 1700060 (2017).CrossRefGoogle ScholarPubMed
Diesendruck, C.E., Sottos, N.R., Moore, J.S., and White, S.R.: Biomimetic self-healing. Angew. Chem. Int. Ed. 54, 10428–10447 (2015).CrossRefGoogle ScholarPubMed
Nakata, T., Liu, H., Tanaka, Y., Nishihashi, N., Wang, X., and Sato, A.: Aerodynamics of a bio-inspired flexible flapping-wing micro air vehicle. Bioinspir. Biomim. 6, 045002 (2011).CrossRefGoogle ScholarPubMed
Barthelat, F. and Zhu, D.: A novel biomimetic material duplicating the structure and mechanics of natural nacre. J. Mater. Res. 26, 1203–1215 (2011).CrossRefGoogle Scholar
Eder, M., Amini, S., and Fratzl, P.: Biological composites—complex structures for functional diversity. Science 362, 543–547 (2018).CrossRefGoogle ScholarPubMed
Huebsch, N. and Mooney, D.J.: Inspiration and application in the evolution of biomaterials. Nature 462, 426–432 (2009).CrossRefGoogle ScholarPubMed
Sun, T. and Qing, G.: Biomimetic smart interface materials for biological applications. Adv. Mater. 23, H57–H77 (2011).CrossRefGoogle ScholarPubMed
Vunjak-Novakovic, G. and Scadden, D.T.: Biomimetic platforms for human stem cell research. CellStemCell 8, 252–261 (2011).Google ScholarPubMed
George, P.M., Oh, B., Dewi, R., Hua, T., Cai, L., Levinson, A., Liang, X., Krajina, B.A., Bliss, T.M., Heilshorn, S.C., and Steinberg, G.K.: Engineered stem cell mimics to enhance stroke recovery. Biomaterials 178, 63–72 (2018).CrossRefGoogle ScholarPubMed
Yoon, J., Shin, M., Lim, J., Kim, D.Y., Lee, T., and Choi, J.-W.: Nanobiohybrid material-based bioelectronic devices. Biotechnol. J. 15, 1900347 (2020).CrossRefGoogle ScholarPubMed
Jia, M. and Rolandi, M.: Soft and ion-conducting materials in bioelectronics: from conducting polymers to hydrogels. Adv. Healthc. Mater. 9, 1901372 (2020).CrossRefGoogle ScholarPubMed
Spira, M.E. and Hai, A.: Multi-electrode array technologies for neuroscience and cardiology. Nat. Nanotechnol. 8, 83–94 (2013).CrossRefGoogle ScholarPubMed
Hersel, U., Dahmen, C., and Kessler, H.: RGD modified polymers: biomaterials for stimulated cell adhesion and beyond. Biomaterials 24, 4385–4415 (2003).CrossRefGoogle ScholarPubMed
Sgarbi, N., Pisignano, D., Di Benedetto, F., Gigli, G., Cingolani, R., and Rinaldi, R.: Self-assembled extracellular matrix protein networks by microcontact printing. Biomaterials 25, 1349–1353 (2004).CrossRefGoogle ScholarPubMed
Offenhäusser, A., Böcker-Meffert, S., Decker, T., Helpenstein, R., Gasteier, P., Groll, J., Möller, M., Reska, A., Schäfer, S., Schulte, P., and Vogt-Eisele, A.: Microcontact printing of proteins for neuronal cell guidance. Soft Matter 3, 290–298 (2007).CrossRefGoogle ScholarPubMed
Włodarczyk-Biegun, M.K. and del Campo, A.: 3D bioprinting of structural proteins. Biomaterials 134, 180–201 (2017).CrossRefGoogle ScholarPubMed
Wrobel, G., Höller, M., Ingebrandt, S., Dieluweit, S., Sommerhage, F., Bochem, H.P., and Offenhäusser, A.: Transmission electron microscopy study of the cell–sensor interface. J. R. Soc. Interface 5, 213–222 (2008).CrossRefGoogle ScholarPubMed
Santoro, F., Zhao, W., Joubert, L.-M., Duan, L., Schnitker, J., van de Burgt, Y., Lou, H.-Y., Liu, B., Salleo, A., Cui, L., Cui, Y., and Cui, B.: Revealing the cell-material interface with nanometer resolution by FIB-SEM. ACS Nano 11, 8320–8328 (2017).CrossRefGoogle Scholar
Bauch, M., Toma, K., Toma, M., Zhang, Q., and Dostalek, J.: Plasmon-enhanced fluorescence biosensors: a review. Plasmonics 9, 781–799 (2014).CrossRefGoogle ScholarPubMed
Braun, D. and Fromherz, P.: Imaging neuronal seal resistance on silicon chip using fluorescent voltage-sensitive dye. Biophys. J. 87, 1351–1359 (2004).CrossRefGoogle ScholarPubMed
Massobrio, G., Martinoia, S., and Massobrio, P.: Equivalent circuit of the neuro-electronic junction for signal recordings from planar and engulfed micro-nano-electrodes. IEEE Trans. Biomed. Circuits Syst. 12, 3–12 (2018).CrossRefGoogle ScholarPubMed
Massobrio, P., Massobrio, G., and Martinoia, S.: Interfacing cultured neurons to microtransducers arrays: a review of the neuro-electronic junction models. Front. Neurosci. 10, 1–13 (2016).CrossRefGoogle ScholarPubMed
Chernomordik, L.V. and Kozlov, M.M.: Mechanics of membrane fusion. Nat. Struct. Mol. Biol. 15, 675–683 (2008).CrossRefGoogle ScholarPubMed
Lingler, S., Rubinstein, I., Knoll, W., and Offenhäusser, A.: Fusion of small unilamellar lipid vesicles to alkanethiol and thiolipid self-assembled monolayers on gold. Langmuir 13, 7085–7091 (1997).CrossRefGoogle Scholar
Schiller, S., Naumann, R., Lovejoy, K., Kunz, H., and Knoll, W.: Archaea analogue thiolipids for tethered bilayer lipid membranes on ultrasmooth gold surfaces. Angew. Chem. Int. Ed Engl. 42, 208–211 (2003).CrossRefGoogle ScholarPubMed
Choi, S.-E., Greben, K., Wördenweber, R., and Offenhäusser, A.: Positively charged supported lipid bilayer formation on gold surfaces for neuronal cell culture. Biointerphases 11, 021003 (2016).CrossRefGoogle Scholar
Koenig, B.W., Krueger, S., Orts, W.J., Majkrzak, C.F., Berk, N.F., Silverton, J.V., and Gawrisch, K.: Neutron reflectivity and atomic force microscopy studies of a lipid bilayer in water adsorbed to the surface of a silicon single crystal. Langmuir 12, 1343–1350 (1996).CrossRefGoogle Scholar
Haratake, M., Osei-Asante, S., Fuchigami, T., and Nakayama, M.: Fluorescence microscopic characterization of ionic polymer bead-supported phospholipid bilayer membrane systems. Colloids Surf. B Biointerfaces 100, 190–196 (2012).CrossRefGoogle ScholarPubMed
Oldfield, E. and Chapman, D.: Dynamics of lipids in membranes: heterogeneity and the role of cholesterol. FEBS Lett. 23, 285–297 (1972).CrossRefGoogle ScholarPubMed
Ghosh Moulick, R., Afanasenkau, D., Choi, S.-E., Albers, J., Lange, W., Maybeck, V., Utesch, T., and Offenhäusser, A.: Reconstitution of fusion proteins in supported lipid bilayers for the study of cell surface receptor-ligand interactions in cell-cell contact. Langmuir ACS J. Surf. Colloids 32, 3462–3469 (2016).CrossRefGoogle Scholar
Tabaei, S.R., Jackman, J.A., Kim, S.-O., Liedberg, B., Knoll, W., Parikh, A.N., and Cho, N.-J.: Formation of cholesterol-rich supported membranes using solvent-assisted lipid self-assembly. Langmuir 30, 13345–13352 (2014).CrossRefGoogle ScholarPubMed
Hao, W., Han, J., Chu, Y., Huang, L., Sun, J., Zhuang, Y., Li, X., Ma, H., Chen, Y., and Dai, J.: Lower fluidity of supported lipid bilayers promotes neuronal differentiation of neural stem cells by enhancing focal adhesion formation. Biomaterials 161, 106–116 (2018).CrossRefGoogle ScholarPubMed
Vafaei, S., Tabaei, S.R., and Cho, N.-J.: Optimizing the performance of supported lipid bilayers as cell culture platforms based on extracellular matrix functionalization. ACS Omega 2, 2395–2404 (2017).CrossRefGoogle ScholarPubMed
Vafaei, S., Tabaei, S.R., Biswas, K.H., Groves, J.T., and Cho, N.-J.: Dynamic cellular interactions with extracellular matrix triggered by biomechanical tuning of low-rigidity, supported lipid membranes. Adv. Healthc. Mater. 6, 1–8 (2017).Google ScholarPubMed
Zobel, K., Choi, S.E., Minakova, R., Gocyla, M., and Offenhäusser, A.: N-Cadherin modified lipid bilayers promote neural network formation and circuitry. Soft Matter 13, 8096–8107 (2017).CrossRefGoogle ScholarPubMed
Liu, H.-Y., Grant, H., Hsu, H.-L., Sorkin, R., Bošković, F., Wuite, G., and Daniel, S.: Supported planar mammalian membranes as models of in vivo cell surface architectures. ACS Appl. Mater. Interfaces 9, 35526–35538 (2017).CrossRefGoogle ScholarPubMed
Svetlova, A., Ellieroth, J., Milos, F., Maybeck, V., and Offenhäusser, A.: Composite lipid bilayers from cell membrane extracts and artificial mixes as a cell culture platform. Langmuir ACS J. Surf. Colloids 35, 8076–8084 (2019).CrossRefGoogle ScholarPubMed
Montis, C., Busatto, S., Valle, F., Zendrini, A., Salvatore, A., Gerelli, Y., Berti, D., and Bergese, P.: Biogenic supported lipid bilayers from nanosized extracellular vesicles. Adv. Biosyst. 2, 1700200 (2018).CrossRefGoogle Scholar
Richards, M.J., Hsia, C.-Y., Singh, R.R., Haider, H., Kumpf, J., Kawate, T., and Daniel, S.: Membrane protein mobility and orientation preserved in supported bilayers created directly from cell plasma membrane blebs. Langmuir 32, 2963–2974 (2016).CrossRefGoogle ScholarPubMed
Zhang, Y., Inal, S., Hsia, C.-Y., Ferro, M., Ferro, M., Daniel, S., and Owens, R.M.: Supported lipid bilayer assembly on PEDOT:PSS films and transistors. Adv. Funct. Mater. 26, 7304–7313 (2016).CrossRefGoogle Scholar
Jackman, J.A. and Cho, N.-J.: Supported lipid bilayer formation: beyond vesicle fusion. Langmuir ACS J. Surf. Colloids 36, 1387–1400 (2020).CrossRefGoogle ScholarPubMed
Su, H., Liu, H.-Y., Pappa, A.-M., Hidalgo, T.C., Cavassin, P., Inal, S., Owens, R.M., and Daniel, S.: Facile generation of biomimetic-supported lipid bilayers on conducting polymer surfaces for membrane biosensing. ACS Appl. Mater. Interfaces 11, 43799–43810 (2019).CrossRefGoogle ScholarPubMed
Lee, Y.K., Lee, H., and Nam, J.-M.: Lipid-nanostructure hybrids and their applications in nanobiotechnology. NPG Asia Mater. 5, e48 (2013).CrossRefGoogle Scholar
Moulick, R.G., Panaitov, G., Du, L., Mayer, D., and Offenhäusser, A.: Neuronal adhesion and growth on nanopatterned EA5-POPC synthetic membranes. Nanoscale 10, 5295–5301 (2018).CrossRefGoogle Scholar
Flemming, R.G., Murphy, C.J., Abrams, G.A., Goodman, S.L., and Nealey, P.F.: Effects of synthetic micro- and nano-structured surfaces on cell behavior. Biomaterials 20, 573–588 (1999).CrossRefGoogle ScholarPubMed
Yim, E.K.F. and Leong, K.W.: Significance of synthetic nanostructures in dictating cellular response. Nanomed. Nanotechnol. Biol. Med. 1, 10–21 (2005).CrossRefGoogle ScholarPubMed
Higgins, S.G., Becce, M., Belessiotis-Richards, A., Seong, H., Sero, J.E., and Stevens, M.M.: High-aspect-ratio nanostructured surfaces as biological metamaterials. Adv. Mater. 32, 1903862 (2020).CrossRefGoogle ScholarPubMed
Nguyen, A.T., Sathe, S.R., and Yim, E.K.F.: From nano to micro: topographical scale and its impact on cell adhesion, morphology and contact guidance. J. Phys. Condens. Matter Inst. Phys. J. 28, 183001 (2016).CrossRefGoogle ScholarPubMed
Dvir, T., Timko, B.P., Kohane, D.S., and Langer, R.: Nanotechnological strategies for engineering complex tissues. Nat. Nanotechnol. 6, 13–22 (2011).CrossRefGoogle ScholarPubMed
McGuire, A.F., Santoro, F., and Cui, B.: Interfacing cells with vertical nanoscale devices: applications and characterization. Annu. Rev. Anal. Chem. 11, 101–126 (2018).CrossRefGoogle ScholarPubMed
Zhao, W., Hanson, L., Lou, H.-Y., Akamatsu, M., Chowdary, P.D., Santoro, F., Marks, J.R., Grassart, A., Drubin, D.G., Cui, Y., and Cui, B.: Nanoscale manipulation of membrane curvature for probing endocytosis in live cells. Nat. Nanotechnol. 12, 750–756 (2017).CrossRefGoogle ScholarPubMed
Amin, H., Dipalo, M., De Angelis, F., and Berdondini, L.: Biofunctionalized 3D nanopillar arrays fostering cell guidance and promoting synapse stability and neuronal activity in networks. ACS Appl. Mater. Interfaces 10, 15207–15215 (2018).CrossRefGoogle ScholarPubMed
Desbiolles, B.X.E., de Coulon, E., Bertsch, A., Rohr, S., and Renaud, P.: Intracellular recording of cardiomyocyte action potentials with nanopatterned volcano-shaped microelectrode arrays. Nano Lett. 19, 6173–6181 (2019).CrossRefGoogle ScholarPubMed
Capozza, R., Caprettini, V., Gonano, C.A., Bosca, A., Moia, F., Santoro, F., and De Angelis, F.: Cell membrane disruption by vertical micro-/nanopillars: role of membrane bending and traction forces. ACS Appl. Mater. Interfaces 10, 29107–29114 (2018).CrossRefGoogle ScholarPubMed
Hai, A., Shappir, J., and Spira, M.E.: In-cell recordings by extracellular microelectrodes. Nat. Methods 7, 200–202 (2010).CrossRefGoogle ScholarPubMed
Dipalo, M., Caprettini, V., Bruno, G., Caliendo, F., Garma, L.D., Melle, G., Dukhinova, M., Siciliano, V., Santoro, F., and De Angelis, F.: Membrane poration mechanisms at the cell–nanostructure interface. Adv. Biosyst. 3, 1900148 (2019).CrossRefGoogle ScholarPubMed
Chiappini, C., Martinez, J.O., De Rosa, E., Almeida, C.S., Tasciotti, E., and Stevens, M.M.: Biodegradable nanoneedles for localized delivery of nanoparticles in vivo: exploring the biointerface. ACS Nano 9, 5500–5509 (2015).CrossRefGoogle ScholarPubMed
Chiappini, C., De Rosa, E., Martinez, J.O., Liu, X., Steele, J., Stevens, M.M., and Tasciotti, E.: Biodegradable silicon nanoneedles delivering nucleic acids intracellularly induce localized in vivo neovascularization. Nat. Mater. 14, 532–539 (2015).CrossRefGoogle ScholarPubMed
Santoro, F., Dasgupta, S., Schnitker, J., Auth, T., Neumann, E., Panaitov, G., Gompper, G., and Offenhäusser, A.: Interfacing electrogenic cells with 3D nanoelectrodes: position, shape, and size matter. ACS Nano 8, 6713–6723 (2014).CrossRefGoogle ScholarPubMed
Hong, G., Yang, X., Zhou, T., and Lieber, C.M.: Mesh electronics: a new paradigm for tissue-like brain probes. Curr. Opin. Neurobiol. 50, 33–41 (2018).CrossRefGoogle ScholarPubMed
Gross, G.W., Rhoades, B.K., Azzazy, H.M.E., and Wu, M.-C.: The use of neuronal networks on multielectrode arrays as biosensors. Biosens. Bioelectron. 10, 553–567 (1995).CrossRefGoogle ScholarPubMed
Maynard, E.M., Nordhausen, C.T., and Normann, R.A.: The Utah intracortical electrode array: a recording structure for potential brain-computer interfaces. Electroencephalogr. Clin. Neurophysiol 102, 228–239 (1997).CrossRefGoogle ScholarPubMed
Tybrandt, K., Khodagholy, D., Dielacher, B., Stauffer, F., Renz, A.F., Buzsáki, G., and Vörös, J.: High-density stretchable electrode grids for chronic neural recording. Adv. Mater. 30, e1706520 (2018).CrossRefGoogle ScholarPubMed
Obaid, A., Hanna, M.-E., Wu, Y.-W., Kollo, M., Racz, R., Angle, M.R., Müller, J., Brackbill, N., Wray, W., Franke, F., Chichilnisky, E.J., Hierlemann, A., Ding, J.B., Schaefer, A.T., and Melosh, N.A.: Massively parallel microwire arrays integrated with CMOS chips for neural recording. Sci. Adv. 6, eaay2789 (2020).CrossRefGoogle ScholarPubMed
Yang, X., Zhou, T., Zwang, T.J., Hong, G., Zhao, Y., Viveros, R.D., Fu, T.-M., Gao, T., and Lieber, C.M.: Bioinspired neuron-like electronics. Nat. Mater. 18, 510–517 (2019).CrossRefGoogle ScholarPubMed
Feiner, R., Engel, L., Fleischer, S., Malki, M., Gal, I., Shapira, A., Shacham-Diamand, Y., and Dvir, T.: Engineered hybrid cardiac patches with multifunctional electronics for online monitoring and regulation of tissue function. Nat. Mater. 15, 679–685 (2016).CrossRefGoogle ScholarPubMed
Acarón Ledesma, H., Li, X., Carvalho-de-Souza, J.L., Wei, W., Bezanilla, F., and Tian, B.: An atlas of nano-enabled neural interfaces. Nat. Nanotechnol. 14, 645–657 (2019).CrossRefGoogle ScholarPubMed
Pennacchio, F.A., Garma, L.D., Matino, L., and Santoro, F.: Bioelectronics goes 3D: new trends in cell–chip interface engineering. J. Mater. Chem. B (2018). doi:10.1039/C8TB01737A.CrossRefGoogle ScholarPubMed
Li, P., Anwar Ali, H.P., Cheng, W., Yang, J., and Tee, B.C.K.: Bioinspired prosthetic interfaces. Adv. Mater. Technol. 5, 1900856 (2020).CrossRefGoogle Scholar
James, C.D., Aimone, J.B., Miner, N.E., Vineyard, C.M., Rothganger, F.H., Carlson, K.D., Mulder, S.A., Draelos, T.J., Faust, A., Marinella, M.J., Naegle, J.H., and Plimpton, S.J.: A historical survey of algorithms and hardware architectures for neural-inspired and neuromorphic computing applications. Biol. Inspired Cogn. Archit. 19, 49–64 (2017).Google Scholar
van de Burgt, Y., Melianas, A., Keene, S.T., Malliaras, G., and Salleo, A.: Organic electronics for neuromorphic computing. Nat. Electron. 1, 386–397 (2018).CrossRefGoogle Scholar
Markram, H.: A history of spike-timing-dependent plasticity. Front. Synaptic Neurosci. 3, 1–24 (2011).CrossRefGoogle ScholarPubMed
Abbott, L.F. and Regehr, W.G.: Synaptic computation. Nature 431, 796–803 (2004).CrossRefGoogle ScholarPubMed
Minch, B.A., Hasler, P.E., Diorio, C., and Mead, C.: A silicon axon. In Adv. Neural Inf. Process. Syst. 7, edited by Tesauro, G., Touretzky, D.S., and Leen, T.K. (MIT Press, Cambridge, 1995) pp. 739–746. http://papers.nips.cc/paper/903-a-silicon-axon.pdf.Google Scholar
Diorio, C., Hasler, P., Minch, A., and Mead, C.A.: A single-transistor silicon synapse. IEEE Trans. Electron Devices 43, 1972–1980 (1996).CrossRefGoogle Scholar
Indiveri, G., Linares-Barranco, B., Hamilton, T.J., van Schaik, A., Etienne-Cummings, R., Delbruck, T., Liu, S.-C., Dudek, P., Häfliger, P., Renaud, S., Schemmel, J., Cauwenberghs, G., Arthur, J., Hynna, K., Folowosele, F., Saïghi, S., Serrano-Gotarredona, T., Wijekoon, J., Wang, Y., and Boahen, K.: Neuromorphic silicon neuron circuits. Front. Neurosci. 5, 1–23 (2011).CrossRefGoogle ScholarPubMed
Wang, Z., Wang, L., Nagai, M., Xie, L., Yi, M., and Huang, W.: Nanoionics-enabled memristive devices: strategies and materials for neuromorphic applications. Adv. Electron. Mater. 3, 1600510 (2017).CrossRefGoogle Scholar
Gupta, I., Serb, A., Khiat, A., Zeitler, R., Vassanelli, S., and Prodromakis, T.: Real-time encoding and compression of neuronal spikes by metal-oxide memristors. Nat. Commun. 7, 1–9 (2016).CrossRefGoogle ScholarPubMed
Lanza, M., Wong, H.-S.P., Pop, E., Ielmini, D., Strukov, D., Regan, B.C., Larcher, L., Villena, M.A., Yang, J.J., Goux, L., Belmonte, A., Yang, Y., Puglisi, F.M., Kang, J., Magyari-Köpe, B., Yalon, E., Kenyon, A., Buckwell, M., Mehonic, A., Shluger, A., Li, H., Hou, T.-H., Hudec, B., Akinwande, D., Ge, R., Ambrogio, S., Roldan, J.B., Miranda, E., Suñe, J., Pey, K.L., Wu, X., Raghavan, N., Wu, E., Lu, W.D., Navarro, G., Zhang, W., Wu, H., Li, R., Holleitner, A., Wurstbauer, U., Lemme, M.C., Liu, M., Long, S., Liu, Q., Lv, H., Padovani, A., Pavan, P., Valov, I., Jing, X., Han, T., Zhu, K., Chen, S., Hui, F., and Shi, Y.: Recommended methods to study resistive switching devices. Adv. Electron. Mater. 5, 1800143 (2019).CrossRefGoogle Scholar
Zhang, X., Zhuo, Y., Luo, Q., Wu, Z., Midya, R., Wang, Z., Song, W., Wang, R., Upadhyay, N.K., Fang, Y., Kiani, F., Rao, M., Yang, Y., Xia, Q., Liu, Q., Liu, M., and Yang, J.J.: An artificial spiking afferent nerve based on Mott memristors for neurorobotics. Nat. Commun. 11, 1–9 (2020).Google ScholarPubMed
Fuller, E.J., Gabaly, F.E., Léonard, F., Agarwal, S., Plimpton, S.J., Jacobs-Gedrim, R.B., James, C.D., Marinella, M.J., and Talin, A.A.: Li-ion synaptic transistor for low power analog computing. Adv. Mater. 29, 1–8 (2017).CrossRefGoogle ScholarPubMed
Gupta, I., Serb, A., Khiat, A., Zeitler, R., Vassanelli, S., and Prodromakis, T.: Sub 100 nW volatile nano-metal-oxide memristor as synaptic-like encoder of neuronal spikes. IEEE Trans. Biomed. Circuits Syst. 12, 351–359 (2018).CrossRefGoogle ScholarPubMed
Abu-Hassan, K., Taylor, J.D., Morris, P.G., Donati, E., Bortolotto, Z.A., Indiveri, G., Paton, J.F.R., and Nogaret, A.: Optimal solid state neurons. Nat. Commun. 10, 1–13 (2019).CrossRefGoogle ScholarPubMed
Serb, A., Corna, A., George, R., Khiat, A., Rocchi, F., Reato, M., Maschietto, M., Mayr, C., Indiveri, G., Vassanelli, S., and Prodromakis, T.: Memristive synapses connect brain and silicon spiking neurons. Sci. Rep. 10, 1–7 (2020).Google ScholarPubMed
Juzekaeva, E., Nasretdinov, A., Battistoni, S., Berzina, T., Iannotta, S., Khazipov, R., Erokhin, V., and Mukhtarov, M.: Coupling cortical neurons through electronic memristive synapse. Adv. Mater. Technol. 4, 1800350 (2019).CrossRefGoogle Scholar
Battistoni, S., Erokhin, V., and Iannotta, S.: Frequency driven organic memristive devices for neuromorphic short term and long term plasticity. Org. Electron. 65, 434–438 (2019).CrossRefGoogle Scholar
Fidanovski, K. and Mawad, D.: Conjugated polymers in bioelectronics: addressing the interface challenge. Adv. Healthc. Mater. 8, 1900053 (2019).CrossRefGoogle ScholarPubMed
Simon, D.T., Gabrielsson, E.O., Tybrandt, K., and Berggren, M.: Organic bioelectronics: bridging the signaling gap between biology and technology. Chem. Rev. 116, 13009–13041 (2016).CrossRefGoogle ScholarPubMed
Benfenati, V., Toffanin, S., Bonetti, S., Turatti, G., Pistone, A., Chiappalone, M., Sagnella, A., Stefani, A., Generali, G., Ruani, G., Saguatti, D., Zamboni, R., and Muccini, M.: A transparent organic transistor structure for bidirectional stimulation and recording of primary neurons. Nat. Mater. 12, 672–680 (2013).CrossRefGoogle ScholarPubMed
Castagnola, E., Maiolo, L., Maggiolini, E., Minotti, A., Marrani, M., Maita, F., Pecora, A., Angotzi, G.N., Ansaldo, A., Boffini, M., Fadiga, L., Fortunato, G., and Ricci, D.: PEDOT-CNT-coated low-impedance, ultra-flexible, and brain-conformable micro-ECoG arrays. IEEE Trans. Neural Syst. Rehabil. Eng. 23, 342–350 (2015).CrossRefGoogle ScholarPubMed
Khodagholy, D., Doublet, T., Quilichini, P., Gurfinkel, M., Leleux, P., Ghestem, A., Ismailova, E., Hervé, T., Sanaur, S., Bernard, C., and Malliaras, G.G.: In vivo recordings of brain activity using organic transistors. Nat. Commun. 4, 1–7 (2013).CrossRefGoogle ScholarPubMed
Cui, X., Lee, V.A., Raphael, Y., Wiler, J.A., Hetke, J.F., Anderson, D.J., and Martin, D.C.: Surface modification of neural recording electrodes with conducting polymer/biomolecule blends. J. Biomed. Mater. Res. 56, 261–272 (2001).3.0.CO;2-I>CrossRefGoogle ScholarPubMed
Ling, H., Koutsouras, D.A., Kazemzadeh, S., van de Burgt, Y., Yan, F., and Gkoupidenis, P.: Electrolyte-gated transistors for synaptic electronics, neuromorphic computing, and adaptable biointerfacing. Appl. Phys. Rev. 7, 011307 (2020).CrossRefGoogle Scholar
Gkoupidenis, P., Schaefer, N., Garlan, B., and Malliaras, G.G.: Neuromorphic functions in PEDOT:PSS organic electrochemical transistors. Adv. Mater. 27, 7176–7180 (2015).CrossRefGoogle ScholarPubMed
van de Burgt, Y., Lubberman, E., Fuller, E.J., Keene, S.T., Faria, G.C., Agarwal, S., Marinella, M.J., Alec Talin, A., and Salleo, A.: A non-volatile organic electrochemical device as a low-voltage artificial synapse for neuromorphic computing. Nat. Mater. 16, 414–418 (2017).CrossRefGoogle ScholarPubMed
Keene, S.T., Melianas, A., Fuller, E.J., Burgt, Y.v.d., Talin, A.A., and Salleo, A.: Optimized pulsed write schemes improve linearity and write speed for low-power organic neuromorphic devices. J. Phys. Appl. Phys. 51, 224002 (2018).CrossRefGoogle Scholar
Keene, S.T., Melianas, A., van de Burgt, Y., and Salleo, A.: Mechanisms for enhanced state retention and stability in redox-gated organic neuromorphic devices. Adv. Electron. Mater. 5, 1800686 (2019).CrossRefGoogle Scholar
Gkoupidenis, P., Schaefer, N., Strakosas, X., Fairfield, J.A., and Malliaras, G.G.: Synaptic plasticity functions in an organic electrochemical transistor. Appl. Phys. Lett. 107, 263302 (2015).CrossRefGoogle Scholar
Simon, D., di Lauro, M., Stefano, C., David, G., Silvia, T., Barbalinardo, M., Kyndiah, A., Mauro, M., Cramer, T., Fabio, B., and Dominique, V.: Electrolyte-gated organic synapse transistor interfaced with neurons. Org. Electron. 38, 21–28 (2016).Google Scholar
Keene, S.T., Lubrano, C., Kazemzadeh, S., Melianas, A., Tuchman, Y., Polino, G., Scognamiglio, P., Cinà, L., Salleo, A., van de Burgt, Y., and Santoro, F.: A biohybrid synapse with neurotransmitter-mediated plasticity. Nat. Mater (2020). doi:10.1038/s41563-020-0703-y.CrossRefGoogle ScholarPubMed
Rivnay, J., Inal, S., Salleo, A., Owens, R.M., Berggren, M., and Malliaras, G.G.: Organic electrochemical transistors. Nat. Rev. Mater. 3, 1–14 (2018).CrossRefGoogle Scholar