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Graphene-based thin film microelectrode technology for in vivo high resolution neural recording and stimulation

Damià Viana, Steven T. Walston, Xavier Illa, Jaume del Valle, Andrew Hayward, Abbie Dodd, Thomas Loret, Elisabet Prats-Alfonso, Natàlia de la Oliva, Marie Palma, Elena del Corro, Bruno Rodríguez-Meana, María del Pilar Bernicola, Elisa Rodríguez-Lucas, Thomas A. Gener, Jose Manuel de la Cruz, Miguel Torres-Miranda, Fikret Taygun Duvan, Nicola Ria, Justin Sperling, Sara Martí-Sánchez, Maria Chiara Spadaro, Clément Hébert, Eduard Masvidal-Codina, Sinead Savage, Jordi Arbiol, Anton Guimerà-Brunet, M. Victoria Puig, Xavier Navarro, Blaise Yvert, Kostas Kostarelos, Jose A. Garrido
doi: https://doi.org/10.1101/2022.11.16.515761
Damià Viana
1Catalan Institute of Nanoscience and Nanotechnology (ICN2), CSIC and BIST, Campus UAB, Bellaterra, Barcelona, Spain
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Steven T. Walston
1Catalan Institute of Nanoscience and Nanotechnology (ICN2), CSIC and BIST, Campus UAB, Bellaterra, Barcelona, Spain
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Xavier Illa
2Institut de Microelectrònica de Barcelona, IMB-CNM (CSIC), Campus UAB, Bellaterra, Spain
3Centro de Investigación Biomédica en Red en Bioingeniería, Biomateriales y Nanomedicina (CIBER-BBN), Madrid, Spain
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Jaume del Valle
4Institute of Neurosciences, Dept Cell Biology, Physiology and Immunology, Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas (CIBERNED), Universitat Autònoma de Barcelona, Barcelona, Spain
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Andrew Hayward
5Nanomedicine Lab, National Graphene Institute and Faculty of Biology, Medicine & Health, AV Hill Building, Manchester, M13 9PT, United Kingdom
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Abbie Dodd
5Nanomedicine Lab, National Graphene Institute and Faculty of Biology, Medicine & Health, AV Hill Building, Manchester, M13 9PT, United Kingdom
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Thomas Loret
5Nanomedicine Lab, National Graphene Institute and Faculty of Biology, Medicine & Health, AV Hill Building, Manchester, M13 9PT, United Kingdom
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Elisabet Prats-Alfonso
2Institut de Microelectrònica de Barcelona, IMB-CNM (CSIC), Campus UAB, Bellaterra, Spain
3Centro de Investigación Biomédica en Red en Bioingeniería, Biomateriales y Nanomedicina (CIBER-BBN), Madrid, Spain
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Natàlia de la Oliva
4Institute of Neurosciences, Dept Cell Biology, Physiology and Immunology, Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas (CIBERNED), Universitat Autònoma de Barcelona, Barcelona, Spain
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Marie Palma
6Inserm, University of Grenoble, Braintech-Lab U1205, Grenoble, France
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Elena del Corro
1Catalan Institute of Nanoscience and Nanotechnology (ICN2), CSIC and BIST, Campus UAB, Bellaterra, Barcelona, Spain
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Bruno Rodríguez-Meana
4Institute of Neurosciences, Dept Cell Biology, Physiology and Immunology, Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas (CIBERNED), Universitat Autònoma de Barcelona, Barcelona, Spain
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María del Pilar Bernicola
1Catalan Institute of Nanoscience and Nanotechnology (ICN2), CSIC and BIST, Campus UAB, Bellaterra, Barcelona, Spain
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Elisa Rodríguez-Lucas
1Catalan Institute of Nanoscience and Nanotechnology (ICN2), CSIC and BIST, Campus UAB, Bellaterra, Barcelona, Spain
7Institut Hospital del Mar d’Investigacions Mèdiques, Barcelona, Spain
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Thomas A. Gener
1Catalan Institute of Nanoscience and Nanotechnology (ICN2), CSIC and BIST, Campus UAB, Bellaterra, Barcelona, Spain
4Institute of Neurosciences, Dept Cell Biology, Physiology and Immunology, Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas (CIBERNED), Universitat Autònoma de Barcelona, Barcelona, Spain
7Institut Hospital del Mar d’Investigacions Mèdiques, Barcelona, Spain
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Jose Manuel de la Cruz
1Catalan Institute of Nanoscience and Nanotechnology (ICN2), CSIC and BIST, Campus UAB, Bellaterra, Barcelona, Spain
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Miguel Torres-Miranda
1Catalan Institute of Nanoscience and Nanotechnology (ICN2), CSIC and BIST, Campus UAB, Bellaterra, Barcelona, Spain
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Fikret Taygun Duvan
1Catalan Institute of Nanoscience and Nanotechnology (ICN2), CSIC and BIST, Campus UAB, Bellaterra, Barcelona, Spain
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Nicola Ria
1Catalan Institute of Nanoscience and Nanotechnology (ICN2), CSIC and BIST, Campus UAB, Bellaterra, Barcelona, Spain
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Justin Sperling
1Catalan Institute of Nanoscience and Nanotechnology (ICN2), CSIC and BIST, Campus UAB, Bellaterra, Barcelona, Spain
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Sara Martí-Sánchez
1Catalan Institute of Nanoscience and Nanotechnology (ICN2), CSIC and BIST, Campus UAB, Bellaterra, Barcelona, Spain
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Maria Chiara Spadaro
1Catalan Institute of Nanoscience and Nanotechnology (ICN2), CSIC and BIST, Campus UAB, Bellaterra, Barcelona, Spain
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Clément Hébert
1Catalan Institute of Nanoscience and Nanotechnology (ICN2), CSIC and BIST, Campus UAB, Bellaterra, Barcelona, Spain
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Eduard Masvidal-Codina
1Catalan Institute of Nanoscience and Nanotechnology (ICN2), CSIC and BIST, Campus UAB, Bellaterra, Barcelona, Spain
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Sinead Savage
5Nanomedicine Lab, National Graphene Institute and Faculty of Biology, Medicine & Health, AV Hill Building, Manchester, M13 9PT, United Kingdom
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Jordi Arbiol
1Catalan Institute of Nanoscience and Nanotechnology (ICN2), CSIC and BIST, Campus UAB, Bellaterra, Barcelona, Spain
8ICREA, Barcelona, Spain
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Anton Guimerà-Brunet
2Institut de Microelectrònica de Barcelona, IMB-CNM (CSIC), Campus UAB, Bellaterra, Spain
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M. Victoria Puig
1Catalan Institute of Nanoscience and Nanotechnology (ICN2), CSIC and BIST, Campus UAB, Bellaterra, Barcelona, Spain
4Institute of Neurosciences, Dept Cell Biology, Physiology and Immunology, Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas (CIBERNED), Universitat Autònoma de Barcelona, Barcelona, Spain
7Institut Hospital del Mar d’Investigacions Mèdiques, Barcelona, Spain
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Xavier Navarro
4Institute of Neurosciences, Dept Cell Biology, Physiology and Immunology, Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas (CIBERNED), Universitat Autònoma de Barcelona, Barcelona, Spain
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Blaise Yvert
6Inserm, University of Grenoble, Braintech-Lab U1205, Grenoble, France
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Kostas Kostarelos
1Catalan Institute of Nanoscience and Nanotechnology (ICN2), CSIC and BIST, Campus UAB, Bellaterra, Barcelona, Spain
5Nanomedicine Lab, National Graphene Institute and Faculty of Biology, Medicine & Health, AV Hill Building, Manchester, M13 9PT, United Kingdom
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  • For correspondence: joseantonio.garrido@icn2.cat kostas.kostarelos@manchester.ac.uk
Jose A. Garrido
1Catalan Institute of Nanoscience and Nanotechnology (ICN2), CSIC and BIST, Campus UAB, Bellaterra, Barcelona, Spain
8ICREA, Barcelona, Spain
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  • For correspondence: joseantonio.garrido@icn2.cat kostas.kostarelos@manchester.ac.uk
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Abstract

Neuroprosthetic technology aims to restore nervous system functionality in cases of severe damage or degeneration by recording and stimulating the electrical activity of the neural tissue. One of the key factors determining the quality of the neuroprostheses is the electrode material used to establish electrical communication with the neural tissue, which is subject to strict electrical, electrochemical, and mechanical specifications as well as biological and microfabrication compatibility requirements. This work presents a nanoporous graphene-based thin film technology and its engineering to form flexible neural implants. Bench measurements show that the developed microelectrodes offer low impedance and high charge injection capacity throughout millions of pulses. In vivo electrode performance was assessed in rodents both from brain surface and intracortically showing high-fidelity recording performance, while stimulation performance was assessed with an intrafascicular implant that demonstrated low current thresholds and high selectivity for activating subsets of axons within the sciatic nerve. Furthermore, the tissue biocompatibility of the devices was validated by chronic epicortical and intraneural implantation. Overall, this works describes a novel graphene-based thin film microelectrode technology and demonstrates its potential for high-precision neural interfacing in both recording and stimulation applications.

Competing Interest Statement

D.V., A.G., K.K. and J.A.G. would like to declare that they hold interest in INBRAIN Neuroelectronics that has licensed the technology described in this manuscript.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Graphene-based thin film microelectrode technology for in vivo high resolution neural recording and stimulation
Damià Viana, Steven T. Walston, Xavier Illa, Jaume del Valle, Andrew Hayward, Abbie Dodd, Thomas Loret, Elisabet Prats-Alfonso, Natàlia de la Oliva, Marie Palma, Elena del Corro, Bruno Rodríguez-Meana, María del Pilar Bernicola, Elisa Rodríguez-Lucas, Thomas A. Gener, Jose Manuel de la Cruz, Miguel Torres-Miranda, Fikret Taygun Duvan, Nicola Ria, Justin Sperling, Sara Martí-Sánchez, Maria Chiara Spadaro, Clément Hébert, Eduard Masvidal-Codina, Sinead Savage, Jordi Arbiol, Anton Guimerà-Brunet, M. Victoria Puig, Xavier Navarro, Blaise Yvert, Kostas Kostarelos, Jose A. Garrido
bioRxiv 2022.11.16.515761; doi: https://doi.org/10.1101/2022.11.16.515761
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Graphene-based thin film microelectrode technology for in vivo high resolution neural recording and stimulation
Damià Viana, Steven T. Walston, Xavier Illa, Jaume del Valle, Andrew Hayward, Abbie Dodd, Thomas Loret, Elisabet Prats-Alfonso, Natàlia de la Oliva, Marie Palma, Elena del Corro, Bruno Rodríguez-Meana, María del Pilar Bernicola, Elisa Rodríguez-Lucas, Thomas A. Gener, Jose Manuel de la Cruz, Miguel Torres-Miranda, Fikret Taygun Duvan, Nicola Ria, Justin Sperling, Sara Martí-Sánchez, Maria Chiara Spadaro, Clément Hébert, Eduard Masvidal-Codina, Sinead Savage, Jordi Arbiol, Anton Guimerà-Brunet, M. Victoria Puig, Xavier Navarro, Blaise Yvert, Kostas Kostarelos, Jose A. Garrido
bioRxiv 2022.11.16.515761; doi: https://doi.org/10.1101/2022.11.16.515761

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