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Recent advances in neural interfaces—Materials chemistry to clinical translation

Published online by Cambridge University Press:  10 August 2020

Christopher J. Bettinger ,
Melanie Ecker ,
Takashi Daniel Yoshida Kozai ,
George G. Malliaras ,
Ellis Meng  and
Walter Voit
Christopher J. Bettinger
Affiliation:
Department of Materials Science and Engineering, and Department of Biomedical Engineering, Carnegie Mellon University, USA; [email protected]
Melanie Ecker
Affiliation:
Department of Biomedical Engineering, University of North Texas, USA
Takashi Daniel Yoshida Kozai
Affiliation:
Department of Bioengineering, University of Pittsburgh, USA
George G. Malliaras
Affiliation:
University of Cambridge, UK; [email protected]
Ellis Meng
Affiliation:
Department of Electrical and Computer Engineering, University of Southern California, Los Angeles, USA
Walter Voit
Affiliation:
Department of Mechanical Engineering, The University of Texas at Dallas, USA
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Abstract

Implantable neural interfaces are important tools to accelerate neuroscience research and translate clinical neurotechnologies. The promise of a bidirectional communication link between the nervous system of humans and computers is compelling, yet important materials challenges must be first addressed to improve the reliability of implantable neural interfaces. This perspective highlights recent progress and challenges related to arguably two of the most common failure modes for implantable neural interfaces: (1) compromised barrier layers and packaging leading to failure of electronic components; (2) encapsulation and rejection of the implant due to injurious tissue–biomaterials interactions, which erode the quality and bandwidth of signals across the biology–technology interface. Innovative materials and device design concepts could address these failure modes to improve device performance and broaden the translational prospects of neural interfaces. A brief overview of contemporary neural interfaces is presented and followed by recent progress in chemistry, materials, and fabrication techniques to improve in vivo reliability, including novel barrier materials and harmonizing the various incongruences of the tissue–device interface. Challenges and opportunities related to the clinical translation of neural interfaces are also discussed.

Type
Technical Feature
Information
MRS Bulletin , Volume 45 , Issue 8: Organic Semiconductors for Brain-Inspired Computing , August 2020 , pp. 655 - 668
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Copyright
Copyright © Materials Research Society 2020

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Footnotes

This article is based on the Materials Research Society/Kavli Future of Materials workshop: Brain–Machine Interfaces: Materials to Clinical Translation, presented at the 2019 MRS Spring Meeting in Phoenix, Ariz.

References

Rousche, P.J., Normann, R.A., J. Neurosci. Methods 82, 1 (1998).10.1016/S0165-0270(98)00031-4CrossRefGoogle Scholar
Kollo, M., Racz, R., Hanna, M., Obaid, A., Angle, M.R., Wray, W., Kong, Y., Hierlemann, A., Müller, J., Melosh, N.A., Schaefer, A.T., bioRxiv 570069 (2019), https://doi.org/10.1101/570069.CrossRefGoogle Scholar
Jun, J.J., Steinmetz, N.A., Siegle, J.H., Denman, D.J., Bauza, M., Barbarits, B., Lee, A.K., Anastassiou, C.A., Andrei, A., Aydın, Ç., Barbic, M., Blanche, T.J., Bonin, V., Couto, J., Dutta, B., Gratiy, S.L., Gutnisky, D.A., Häusser, M., Karsh, B., Ledochowitsch, P., Lopez, C.M., Mitelut, C., Musa, S., Okun, M., Pachitariu, M., Putzeys, J., Rich, P.D., Rossant, C., Sun, W., Svoboda, K., Carandini, M., Harris, K.D., Koch, C., O'Keefe, J., Harris, T.D., Nature 551, 232 (2017).10.1038/nature24636CrossRefGoogle Scholar
Juavinett, A.L., Bekheet, G., Churchland, A.K., eLife 8, e47188 (2019).10.7554/eLife.47188CrossRefGoogle Scholar
Putzeys, J., Raducanu, B.C., Carton, A., De Ceulaer, J., Karsh, B., Siegle, J.H., Van Helleputte, N., Harris, T.D., Dutta, B., Musa, S., Lopez, C.M., IEEE Trans. Biomed. Circuits Syst. 13, 1 (2019).10.1109/TBCAS.2019.2943077CrossRefGoogle Scholar
Golabchi, A., Wu, B., Cao, B., Bettinger, C.J., Cui, X.T., Biomaterials 225, 119519 (2019).10.1016/j.biomaterials.2019.119519CrossRefGoogle Scholar
Polikov, V.S., Tresco, P.A., Reichert, W.M., J. Neurosci, Methods 148, 1 (2005).10.1016/j.jneumeth.2005.08.015CrossRefGoogle Scholar
Biran, R., Martin, D.C., Tresco, P.A., Exp. Neurol. 195, 115 (2005).10.1016/j.expneurol.2005.04.020CrossRefGoogle Scholar
Nolta, N.F., Christensen, M.B., Crane, P.D., Skousen, J.L., Tresco, P.A., Biomaterials 53, 753 (2015).10.1016/j.biomaterials.2015.02.081CrossRefGoogle Scholar
Patel, P.R., Na, K., Zhang, H., Kozai, T.D.Y., Kotov, N.A., Yoon, E., Chestek, C.A., J. Neural Eng. 12, 046009 (2015).10.1088/1741-2560/12/4/046009CrossRefGoogle Scholar
Lee, K., Singh, A., He, J., Massia, S., Kim, B., Raupp, G., Sens. Actuators B 102, 67 (2004).10.1016/j.snb.2003.10.018CrossRefGoogle Scholar
Mercanzini, A., Cheung, K., Buhl, D.L., Boers, M., Maillard, A., Colin, P., Bensadoun, J.-C., Bertsch, A., Renaud, P., Sens. Actuators A 143, 90 (2008).10.1016/j.sna.2007.07.027CrossRefGoogle Scholar
Castagnola, V., Descamps, E., Lecestre, A., Dahan, L., Remaud, J., Nowak, L.G., Bergaud, C., Biosens. Bioelectron. 67, 450 (2015).10.1016/j.bios.2014.09.004CrossRefGoogle Scholar
Hara, S.A., Kim, B.J., Kuo, J.T.W., Lee, C.D., Meng, E., Pikov, V., J. Neural Eng. 13, 066020 (2016).10.1088/1741-2560/13/6/066020CrossRefGoogle Scholar
Du, Z.J., Kolarcik, C.L., Kozai, T.D.Y., Luebben, S.D., Sapp, S.A., Zheng, X.S., Nabity, J.A., Cui, X.T., Acta Biomater. 53, 46 (2017).CrossRefGoogle Scholar
Xu, H., Hirschberg, A.W., Scholten, K., Berger, T.W., Song, D., Meng, E., J. Neural Eng. 15, 016017 (2018).10.1088/1741-2552/aa9451CrossRefGoogle Scholar
Smalley, E., Nat. Biotechnol. 37, 978 (2019).10.1038/s41587-019-0231-yCrossRefGoogle Scholar
Musk Neuralink, E., bioRxiv 703801 (2019), https://doi.org/10.1101/703801.CrossRefGoogle Scholar
Miocinovic, S., Somayajula, S., Chitnis, S., Vitek, J.L., JAMA Neurol. 70, 163 (2013).CrossRefGoogle Scholar
Wellman, S.M., Eles, J.R., Ludwig, K.A., Seymour, J.P., Michelson, N.J., McFadden, W.E., Vazquez, A.L., Kozai, T.D.Y., Adv. Funct. Mater. 28, 1701269 (2018).10.1002/adfm.201701269CrossRefGoogle Scholar
Wang, L., Ruan, C., Li, M., Zou, J., Tao, H., Peng, J., Xu, M., J. Mater. Chem. C 5, 4017 (2017).10.1039/C7TC00903HCrossRefGoogle Scholar
Yin, L., Farimani, A.B., Min, K., Vishal, N., Lam, J., Lee, Y.K., Aluru, N.R., Rogers, J.A., Adv. Mater. (2015), https://doi.org/10.1002/adma.201404579.Google Scholar
Fang, H., Zhao, J., Yu, K.J., Song, E., Farimani, A.B., Chiang, C.-H., Jin, X., Xue, Y., Xu, D., Du, W., Seo, K.J., Zhong, Y., Yang, Z., Won, S.M., Fang, G., Choi, S.W., Chaudhuri, S., Huang, Y., Alam, M.A., Viventi, J., Aluru, N.R., Rogers, J.A., Proc. Natl. Acad. Sci. U.S.A. 113, 11682 (2016).CrossRefGoogle Scholar
Song, E., Fang, H., Jin, X., Zhao, J., Jiang, C., Yu, K.J., Zhong, Y., Xu, D., Li, J., Fang, G., Du, H., Zhang, J., Park, J.M., Huang, Y., Alam, M.A., Mei, Y., Rogers, J.A., Adv. Electron. Mater. 3, 1700077 (2017).10.1002/aelm.201700077CrossRefGoogle Scholar
Cogan, S.F., Edell, D.J., Guzelian, A.A., Liu, Y.P., Edell, R., J. Biomed. Mater. Res. A 67A, 856 (2003).10.1002/jbm.a.10152CrossRefGoogle Scholar
Diaz-Botia, C.A., Luna, L.E., Chamanzar, M., Carraro, C., Sabes, P.N., Maboudian, R., Maharbiz, M.M., 8th Int. IEEE/EMBS Conf. Neural Engr. (NER) (2017), pp. 170–173.Google Scholar
Lee, B.H., Kang, L., Qi, W.-J., Nieh, R., Jeon, Y., Onishi, K., Lee, J.C., IEDM 1999, Tech. Dig. (Cat.N0.99CH36318) (1999), pp. 133–136.Google Scholar
Song, E., Lee, Y.K., Li, R., Li, J., Jin, X., Yu, K.J., Xie, Z., Fang, H., Zhong, Y., Du, H., Zhang, J., Fang, G., Kim, Y., Yoon, Y., Alam, M.A., Mei, Y., Huang, Y., Rogers, J.A., Adv. Funct. Mater. 28, 1702284 (2018).10.1002/adfm.201702284CrossRefGoogle Scholar
Chiang, C.-H., Won, S.M., Orsborn, A.L., Yu, K.J., Trumpis, M., Bent, B., Wang, C., Xue, Y., Min, S., Woods, V., Yu, C., Kim, B.H., Kim, S.B., Huq, R., Li, J., Seo, K.J., Vitale, F., Richardson, A., Fang, H., Huang, Y., Shepard, K., Pesaran, B., Rogers, J.A., Viventi, J., Sci. Transl. Med. 12, eaay4682 (2020).10.1126/scitranslmed.aay4682CrossRefGoogle Scholar
Roy, R.K., Lee, K.-R., J. Biomed. Mater. Res. B 83B, 72 (2007).10.1002/jbm.b.30768CrossRefGoogle Scholar
Ganesan, K., Garrett, D.J., Ahnood, A., Shivdasani, M.N., Tong, W., Turnley, A.M., Fox, K., Meffin, H., Prawer, S., Biomaterials 35, 908 (2014).10.1016/j.biomaterials.2013.10.040CrossRefGoogle Scholar
Alcaide, M., Taylor, A., Fjorback, M., Zachar, V., Pennisi, C.P., Front. Neurosci. 10 (2016), https://doi.org/10.3389/fnins.2016.00087.CrossRefGoogle Scholar
Hsu, J.-M., Rieth, L., Normann, R.A., Tathireddy, P., Solzbacher, F., IEEE Trans. Biomed. Eng. 56, 23 (2009).10.1109/TBME.2008.2002155CrossRefGoogle Scholar
Huang, H., Xu, Y., Low, H.Y., Polymer 46, 5949 (2005).CrossRefGoogle Scholar
Noh, H., Moon, Kyoung-sik, Cannon, A., Hesketh, P.J., Wong, C.P., Proc. 54th Electron. Comp. Technol. Conf. (IEEE Cat. N0.04CH37546) (Las Vegas, NV, 2004), pp. 924–930.Google Scholar
Hassler, C., von Metzen, R.P., Ruther, P., Stieglitz, T., J. Biomed. Mater. Res. B 93B, 266 (2010).Google Scholar
Chen, Y.-Y., Lai, H.-Y., Lin, S.-H., Cho, C.-W., Chao, W.-H., Liao, C.-H., Tsang, S., Chen, Y.-F., Lin, S.-Y., J. Neurosci. Methods 182, 6 (2009).CrossRefGoogle Scholar
Takeuchi, S., Suzuki, T., Mabuchi, K., Fujita, H., J. Micromech. Microeng. 14, 104 (2003).10.1088/0960-1317/14/1/014CrossRefGoogle Scholar
Stieglitz, T., Beutel, H., Schuettler, M., Meyer, J.-U., Biomed. Microdevices 2, 283 (2000).CrossRefGoogle Scholar
van Daal, R.J.J., Sun, J.-J., Ceyssens, F., Michon, F., Kraft, M., Puers, R., Kloosterman, F., J. Neural Eng. 17, 016046 (2020).10.1088/1741-2552/ab5e19CrossRefGoogle Scholar
Noh, H., Moon, K., Cannon, A., Hesketh, P.J., Wong, C.P., J. Micromech. Microeng. 14, 625 (2004).10.1088/0960-1317/14/4/025CrossRefGoogle Scholar
Huang, J., Cranford, R.J., Matsuura, T., Roy, C., J. Appl. Polym. Sci. 87, 2306 (2003).10.1002/app.11731CrossRefGoogle Scholar
Minev, I.R., Musienko, P., Hirsch, A., Barraud, Q., Wenger, N., Moraud, E.M., Gandar, J., Capogrosso, M., Milekovic, T., Asboth, L., Torres, R.F., Vachicouras, N., Liu, Q., Pavlova, N., Duis, S., Larmagnac, A., Vörös, J., Micera, S., Suo, Z., Courtine, G., Lacour, S.P., Science 347, 159 (2015).10.1126/science.1260318CrossRefGoogle Scholar
Vocke, C., Anttila, U., Seppälä, J., J. Appl. Polym. Sci. 72, 1443 (1999).10.1002/(SICI)1097-4628(19990613)72:11<1443::AID-APP7>3.0.CO;2-43.0.CO;2-4>CrossRefGoogle Scholar
Yam, K.L., The Wiley Encyclopedia of Packaging Technology (Wiley, New York, 2010).Google Scholar
Kolarcik, C.L., Luebben, S.D., Sapp, S.A., Hanner, J., Snyder, N., Kozai, T.D.Y., Chang, E., Nabity, J.A., Nabity, S.T., Lagenaur, C.F., Cui, X.T., Soft Matter 11, 4847 (2015).CrossRefGoogle Scholar
Granstrom, J., Swensen, J.S., Moon, J.S., Rowell, G., Yuen, J., Heeger, A.J., Appl. Phys. Lett. 93, 193304 (2008).10.1063/1.3006349CrossRefGoogle Scholar
Wu, H., Kustra, S., Gates, E.M., Bettinger, C.J., Org. Electron. 14, 1636 (2013).10.1016/j.orgel.2013.02.037CrossRefGoogle Scholar
Le Floch, P., Meixuanzi, S., Tang, J., Liu, J., Suo, Z., ACS Appl. Mater. Interfaces 10, 27333 (2018).10.1021/acsami.8b08910CrossRefGoogle Scholar
Kozai, T.D.Y., Vazquez, A.L., J. Mater. Chem. B 3, 4965 (2015).10.1039/C5TB00108KCrossRefGoogle Scholar
Kozai, T.D.Y., Jaquins-Gerstl, A.S., Vazquez, A.L., Michael, A.C., Cui, X.T., ACS Chem. Neurosci. 6, 48 (2015).CrossRefGoogle Scholar
Salatino, J.W., Ludwig, K.A., Kozai, T.D.Y., Purcell, E.K., Nat. Biomed. Eng. 1, 862 (2017).10.1038/s41551-017-0154-1CrossRefGoogle Scholar
Biran, R., Martin, D.C., Tresco, P.A., Exp. Neurol. 195, 115 (2005).CrossRefGoogle Scholar
Michelson, N.J., Vazquez, A.L., Eles, J.R., Salatino, J.W., Purcell, E.K., Williams, J.J., Cui, X.T., Kozai, T.D.Y., J. Neural Eng. 15, 033001 (2018).CrossRefGoogle Scholar
Wellman, S.M., Kozai, T.D.Y., Biomaterials 164, 121 (2018).10.1016/j.biomaterials.2018.02.037CrossRefGoogle Scholar
Kozai, T.D.Y., Marzullo, T.C., Hooi, F., Langhals, N.B., Majewska, A.K., Brown, E.B., Kipke, D.R., J. Neural Eng. 7, 046011 (2010).CrossRefGoogle Scholar
McCreery, D., Cogan, S., Kane, S., Pikov, V., J. Neural Eng. 13, 036012 (2016).10.1088/1741-2560/13/3/036012CrossRefGoogle Scholar
Kozai, T.D.Y., Li, X., Bodily, L.M., Caparosa, E.M., Zenonos, G.A., Carlisle, D.L., Friedlander, R.M., Cui, X.T., Biomaterials 35, 9620 (2014).10.1016/j.biomaterials.2014.08.006CrossRefGoogle Scholar
Wellman, S.M., Li, L., Yaxiaer, Y., McNamara, I., Kozai, T.D.Y., Front. Neurosci. 13 (2019), https://doi.org/10.3389/fnins.2019.00493.CrossRefGoogle Scholar
Merrill, D.R., Bikson, M., Jefferys, J.G.R., J. Neurosci. Methods 141, 171 (2005).CrossRefGoogle Scholar
Romo, R., Hernández, A., Zainos, A., Salinas, E., Nature 392, 387 (1998).10.1038/32891CrossRefGoogle Scholar
Gittis, A., Science 361, 462 (2018).Google Scholar
Armenta Salas, M., Bashford, L., Kellis, S., Jafari, M., Jo, H., Kramer, D., Shanfield, K., Pejsa, K., Lee, B., Liu, C.Y., Andersen, R.A., eLife 7, e32904 (2018).CrossRefGoogle Scholar
Callier, T., Brantly, N.W., Caravelli, A., Bensmaia, S.J., Proc. Natl. Acad. Sci. U.S.A. 117, 1191 (2020).CrossRefGoogle Scholar
Eles, J.R., Kozai, T.D.Y., Biomaterials 234, 119767 (2020).CrossRefGoogle Scholar
Eles, J.R., Vazquez, A.L., Kozai, T.D.Y., Cui, X.T., Biomaterials 174, 79 (2018).10.1016/j.biomaterials.2018.04.043CrossRefGoogle Scholar
Damasio, H., Grabowski, T., Frank, R., Galaburda, A.M., Damasio, A.R., Science 264, 1102 (1994).10.1126/science.8178168CrossRefGoogle Scholar
Stocking, K.C., Vazquez, A.L., Kozai, T.D.Y., IEEE Trans. Biomed. Eng. 66, 2402 (2019).10.1109/TBME.2018.2889832CrossRefGoogle Scholar
Eles, J.R., Vazquez, A.L., Snyder, N.R., Lagenaur, C., Murphy, M.C., Kozai, T.D.Y., Cui, X.T., Biomaterials 113, 279 (2017).10.1016/j.biomaterials.2016.10.054CrossRefGoogle Scholar
Ferguson, M., Sharma, D., Ross, D., Zhao, F., Adv. Healthc. Mater. 8, 1900558 (2019).CrossRefGoogle Scholar
Ecker, M., Joshi-Imre, A., Modi, R., Frewin, C.L., Garcia-Sandoval, A., Maeng, J., Gutierrez-Heredia, G., Pancrazio, J.J., Voit, W.E., Multifunct. Mater. 2, 012001 (2018).10.1088/2399-7532/aaed58CrossRefGoogle Scholar
Stiller, A.M., Usoro, J., Frewin, C.L., Danda, V.R., Ecker, M., Joshi-Imre, A., Musselman, K.C., Voit, W., Modi, R., Pancrazio, J.J., Black, B.J., Micromachines 9, 500 (2018).CrossRefGoogle Scholar
Shoffstall, A.J., Ecker, M., Danda, V., Joshi-Imre, A., Stiller, A., Yu, M., Paiz, J.E., Mancuso, E., Bedell, H.W., Voit, W.E., Pancrazio, J.J., Capadona, J.R., Micromachines 9, 486 (2018).10.3390/mi9100486CrossRefGoogle Scholar
Do, D.-H., Ecker, M., Voit, W.E., ACS Omega 2, 4604 (2017).10.1021/acsomega.7b00834CrossRefGoogle Scholar
Ware, T., Simon, D., Liu, C., Musa, T., Vasudevan, S., Sloan, A., Keefer, E.W., Rennaker, R.L., Voit, W., J. Biomed. Mater. Res. B 102, 1 (2014).CrossRefGoogle Scholar
Simon, D.M., Charkhkar, H., John, C.S., Rajendran, S., Kang, T., Reit, R., Arreaga-Salas, D., McHail, D.G., Knaack, G.L., Sloan, A., Grasse, D., Dumas, T.C., Rennaker, R.L., Pancrazio, J.J., Voit, W.E., J. Biomed. Mater. Res. A 105, 159 (2017).10.1002/jbm.a.35896CrossRefGoogle Scholar
Hosseini, S.M., Voit, W.E., Ecker, M., J. Vis. Exp. e59209 (2019), https://doi.org/10.3791/59209.Google Scholar
Hosseini, S.M., Rihani, R., Batchelor, B., Stiller, A.M., Pancrazio, J.J., Voit, W.E., Ecker, M., Front. Mater. 5 (2018), https://doi.org/10.3389/fmats.2018.00066.CrossRefGoogle Scholar
Lee, H.C., Ejserholm, F., Gaire, J., Currlin, S., Schouenborg, J., Wallman, L., Bengtsson, M., Park, K., Otto, K.J., J. Neural Eng. 14, 036026 (2017).10.1088/1741-2552/aa68f0CrossRefGoogle Scholar
Bettinger, J., Bao, Z., Adv. Mater. 22, 651 (2010).10.1002/adma.200902322CrossRefGoogle Scholar
Bettinger, C.J., Bao, Z., Polym. Int. 59, 563 (2010).Google Scholar
Bettinger, C.J., Bruggeman, J.P., Borenstein, J.T., Langer, R.S., Biomaterials 29, 2315 (2008).CrossRefGoogle Scholar
Bruggeman, J.P., de Bruin, B.-J., Bettinger, C.J., Langer, R., Biomaterials 29, 4726 (2008).CrossRefGoogle Scholar
Bettinger, C.J., Macromol. Biosci. 11, 467 (2011).10.1002/mabi.201000397CrossRefGoogle Scholar
Bettinger, C.J., Bruggeman, J.P., Borenstein, J.T., Langer, R., J. Biomed. Mater. Res. A 91A, 1077 (2009).10.1002/jbm.a.32306CrossRefGoogle Scholar
Bruggeman, J.P., Bettinger, C.J., Langer, R., J. Biomed. Mater. Res. A 95A, 92 (2010).CrossRefGoogle Scholar
Ninh, C., Bettinger, C.J., Biomacromolecules 14, 2162 (2013).10.1021/bm4002602CrossRefGoogle Scholar
Engelmayr, G.C., Cheng, M., Bettinger, C.J., Borenstein, J.T., Langer, R., Freed, L.E., Nat. Mater. 7, 1003 (2008).CrossRefGoogle Scholar
Nijst, C.L.E., Bruggeman, J.P., Karp, J.M., Ferreira, L., Zumbuehl, A., Bettinger, C.J., Langer, R., Biomacromolecules 8, 3067 (2007).CrossRefGoogle Scholar
Bettinger, C.J., Orrick, B., Misra, A., Langer, R., Borenstein, J.T., Biomaterials 27, 2558 (2006).10.1016/j.biomaterials.2005.11.029CrossRefGoogle Scholar
Bettinger, C.J., Kulig, K.M., Vacanti, J.P., Langer, R., Borenstein, J.T., Tissue Eng. A 15, 1321 (2008).10.1089/ten.tea.2008.0134CrossRefGoogle Scholar
Zhu, C., Kustra, S.R., Bettinger, C.J., Acta Biomater. 9, 7362 (2013).CrossRefGoogle Scholar
Huang, W.-C., Ali, F., Zhao, J., Rhee, K., Mou, C., Bettinger, C.J., Biomacromolecules 18, 1162 (2017).10.1021/acs.biomac.6b01841CrossRefGoogle Scholar
Mou, C., Ali, F., Malaviya, A., Bettinger, C.J., J. Mater. Chem. B 7, 1690 (2019).CrossRefGoogle Scholar
Wu, H., Sariola, V., Zhu, C., Zhao, J., Sitti, M., Bettinger, C.J., Adv. Mater. 27, 3398 (2015).CrossRefGoogle Scholar
Huang, W.-C., Ong, X.C., Kwon, I.S., Gopinath, C., Fisher, L.E., Wu, H., Fedder, G.K., Gaunt, R.A., Bettinger, C.J., Adv. Funct. Mater. 28, 1801059 (2018).CrossRefGoogle Scholar
Ong, X.C., Huang, W., Kwon, I.S., Gopinath, C., Wu, H., Fisher, L.E., Gaunt, R.A., Bettinger, C.J., Fedder, G.K., presented at the 31st International Conference on Micro Electro Mechanical Systems (MEMS), Belfast, Ireland, 2018, pp. 376–379.Google Scholar
Angle, M.R., Kong, Y., “Neural-Interface Probe and Methods of Packaging the Same,” US Patent 10327655B2, (2019).Google Scholar
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., Melosh, N.A., Sci. Adv. 6, eaay2789 (2020).10.1126/sciadv.aay2789CrossRefGoogle Scholar
Kozai, T.D.Y., Langhals, N.B., Patel, P.R., Deng, X., Zhang, H., Smith, K.L., Lahann, J., Kotov, N.A., Kipke, D.R., Nat. Mater. 11, 1065 (2012).CrossRefGoogle Scholar
Musk, E., J. Med. Internet Res. 21 (2019), https://doi.org/10.2196/16194.CrossRefGoogle Scholar
Driller, J., Hilal, S.K., Michelsen, W.J., Sollish, B., Katz, B., Konig, W., Med. Res. Eng. 8, 11 (1969).Google Scholar
Oxley, T.J., Opie, N.L., John, S.E., Rind, G.S., Ronayne, S.M., Wheeler, T.L., Judy, J.W., McDonald, A.J., Dornom, A., Lovell, T.J.H., Steward, C., Garrett, D.J., Moffat, B.A., Lui, E.H., Yassi, N., Campbell, B.C.V., Wong, Y.T., Fox, K.E., Nurse, E.S., Bennett, I.E., Bauquier, S.H., Liyanage, K.A., van der Nagel, N.R., Perucca, P., Ahnood, A., Gill, K.P., Yan, B., Churilov, L., French, C.R., Desmond, P.M., Horne, M.K., Kiers, L., Prawer, S., Davis, S.M., Burkitt, A.N., Mitchell, P.J., Grayden, D.B., May, C.N., O'Brien, T.J., Nat. Biotechnol. 34, 320 (2016).CrossRefGoogle Scholar
Opie, N.L., van der Nagel, N.R., John, S.E., Vessey, K., Rind, G.S., Ronayne, S.M., Fletcher, E.L., May, C.N., O'Brien, T.J., Oxley, T.J., IEEE Trans. Biomed. Eng. 64, 928 (2017).CrossRefGoogle Scholar
DiMilia, T., “Synchron Achieves First Successful Human Implantation of Brain Computer Interface,” Synchron (2019), https://www.synchronmed.com/media/2019/09/synchron-achieves-first-successful-human-implantation-of-brain-computer-interface (accessed April 9, 2020).Google Scholar
Hof, R.D., “Lessons from Sematech,” MIT Technology Review (2011), https://www.technologyreview.com/2011/07/25/192832/lessons-from-sematech (accessed April 9, 2020).Google Scholar
Khodagholy, D., Gelinas, J.N., Thesen, T., Doyle, W., Devinsky, O., Malliaras, G.G., Buzsáki, G., Nat. Neurosci. 18, 310 (2015).CrossRefGoogle Scholar
Martin, D.C., Malliaras, G.G., ChemElectroChem 3, 686 (2016).CrossRefGoogle Scholar
Khodagholy, D., Doublet, T., Gurfinkel, M., Quilichini, P., Ismailova, E., Leleux, P., Herve, T., Sanaur, S., Bernard, C., Malliaras, G.G., Adv. Mater. 23, H268 (2011).10.1002/adma.201102378CrossRefGoogle Scholar
Khodagholy, D., Gelinas, J.N., Zhao, Z., Yeh, M., Long, M., Greenlee, J.D., Doyle, W., Devinsky, O., Buzsáki, G., Sci. Adv. 2, e1601027 (2016).CrossRefGoogle Scholar