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Research Article

Flexible and biocompatible nanopaper-based electrode arrays for neural activity recording

Yichuan Guo1,2Zhiqiang Fang3Mingde Du1,2Long Yang4Leihou Shao1,2Xiaorui Zhang1,2Li Li1,2Jidong Shi1,2Jinsong Tao3Jinfen Wang1,2Hongbian Li1,2()Ying Fang1,2,5()
CAS Key Laboratory for Biomedical Effects of Nanomaterials and NanosafetyCAS Center for Excellence in NanoscienceNational Center for Nanoscience and TechnologyBeijing100190China
University of Chinese Academy of SciencesBeijing100049China
State Key Laboratory of Pulp and Paper EngineeringSouth China University of TechnologyGuangzhou510640China
Department of NeurobiologyDavid Geffen School of MedicineUniversity of CaliforniaLos AngelesLos AngelesCA90095USA
CAS Center for Excellence in Brain Science and Intelligence Technology320 Yue Yang RoadShanghai200031China
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Abstract

Advances in neural electrode technologies can have a significant impact on both fundamental and applied neuroscience. Here, we report the development of flexible and biocompatible neural electrode arrays based on a nanopaper substrate. Nanopaper has important advantages with respect to polymers such as hydrophilicity and water wettability, which result in significantly enhanced biocompatibility, as confirmed by both in vitro viability assays and in vivo histological analysis. In addition, nanopaper exhibits high flexibility and good shape stability. Hence, nanopaper-based neural electrode arrays can conform to the convoluted cortical surface of a rat brain and allow stable multisite recording of epileptiform activity in vivo. Our results show that nanopaper-based electrode arrays represent promising candidates for the flexible and biocompatible recording of the neural activity.

References

1

Perlmutter, J. S.; Mink, J. W. Deep brain stimulation. Annu. Rev. Neurosci. 2006, 29, 229–257.

2

Kipke, D. R.; Vetter, R. J.; Williams, J. C.; Hetke, J. F. Silicon-substrate intracortical microelectrode arrays for long-term recording of neuronal spike activity in cerebral cortex. IEEE Trans. Neural Syst. Rehabil. Eng. 2003, 11, 151–155.

3

Rousche, P. J.; Normann, R. A. Chronic recording capability of the Utah intracortical electrode array in cat sensory cortex. J. Neurosci. Methods 1998, 82, 1–15.

4

Polikov, V. S.; Tresco, P. A.; Reichert, W. M. Response of brain tissue to chronically implanted neural electrodes. J. Neurosci. Methods 2005, 148, 1–18.

5

Ward, M. P.; Rajdev, P.; Ellison, C.; Irazoqui, P. P. Toward a comparison of microelectrodes for acute and chronic recordings. Brain Res. 2009, 1282, 183–200.

6

Wolpaw, J. R.; McFarland, D. J. Control of a two-dimensional movement signal by a noninvasive brain-computer interface in humans. Proc. Nati. Acad. Sci. USA 2004, 101, 17849–17854.

7

Buzsáki, G.; Anastassiou, C. A.; Koch, C. The origin of extracellular fields and currents—EEG, ECoG, LFP and spikes. Nat. Rev. Neurosci. 2012, 13, 407–420.

8

Osorio, I.; Frei, M. G.; Giftakis, J.; Peters, T.; Ingram, J.; Turnbull, M.; Herzog, M.; Rise, M. T.; Schaffner, S.; Wennberg, R. A. et al. Performance reassessment of a real-time seizure-detection algorithm on long ECoG series. Epilepsia 2002, 43, 1522–1535.

9

Leuthardt, E. C.; Schalk, G.; Wolpaw, J. R.; Ojemann, J. G.; Moran, D. W. A brain-computer interface using electrocorticographic signals in humans. J. Neural Eng. 2004, 1, 63–71.

10

Yang, L.; Zhao, Y.; Xu, W. J.; Shi, E. Z.; Wei, W. J.; Li, X. M.; Cao, A. Y.; Cao, Y. P.; Fang, Y. Highly crumpled all-carbon transistors for brain activity recording. Nano. Lett. 2017, 17, 71–77.

11

Kotov, N. A.; Winter, J. O.; Clements, I. P.; Jan, E.; Timko, B. P.; Campidelli, S.; Pathak, S.; Mazzatenta, A.; Lieber, C. M.; Prato, M. et al. Nanomaterials for neural interfaces. Adv. Mater. 2009, 21, 3970–4004.

12

Thongpang, S.; Richner, T. J.; Brodnick, S. K.; Schendel, A.; Kim, J.; Wilson, J. A.; Hippensteel, J.; Krugner-Higby, L.; Moran, D.; Ahmed, A. S. et al. A microelectrocorticography platform and deployment strategies for chronic BCI applications. Clin. EEG Neursci. 2011, 42, 259–265.

13

Khodagholy, D.; Doublet, T.; Gurfinkel, M.; Quilichini, P.; Ismailova, E.; Leleux, P.; Herve, T.; Sanaur, S.; Bernard, C.; Malliaras, G. G. Highly conformable conducting polymer electrodes for in vivo recordings. Adv. Mater. 2011, 23, H268–H272.

14

Kunori, N.; Takashima, I. A transparent epidural electrode array for use in conjunction with optical imaging. J. Neurosci. Methods 2015, 251, 130–137.

15

Zhang, Y. Z.; Wang, Y.; Cheng, T.; Lai, W. Y.; Pang, H.; Huang, W. Flexible supercapacitors based on paper substrates: A new paradigm for low-cost energy storage. Chem. Soc. Rev. 2015, 44, 5181–5199.

16

Weng, M. C.; Zhou, P. D.; Chen, L. Z.; Zhang, L. L.; Zhang, W.; Huang, Z. G.; Liu, C. H.; Fan, S. S. Multiresponsive bidirectional bending actuators fabricated by a pencil-onpaper method. Adv. Funct. Mater. 2016, 26, 7244–7253.

17

Barr, M. C.; Rowehl, J. A.; Lunt, R. R.; Xu, J. J.; Wang, A. N.; Boyce, C. M.; Im, S. G.; Bulović, V.; Gleason, K. K. Direct monolithic integration of organic photovoltaic circuits on unmodified paper. Adv. Mater. 2011, 23, 3500–3505.

18

Siegel, A. C.; Phillips, S. T.; Wiley, B. J.; Whitesides, G. M. Thin, lightweight, foldable thermochromic displays on paper. Lab Chip 2009, 9, 2775–2781.

19

Martins, R.; Nathan, A.; Barros, R.; Pereira, L.; Barquinha, P.; Correia, N.; Costa, R.; Ahnood, A.; Ferreira, I.; Fortunato, E. Complementary metal oxide semiconductor technology with and on paper. Adv. Mater. 2011, 23, 4491–4496.

20

Martinez, A. W.; Phillips, S. T.; Butte, M. J.; Whitesides, G. M. Patterned paper as a platform for inexpensive, lowvolume, portable bioassays. Angew. Chem., Int. Ed. 2007, 46, 1318–1320.

21

Güder, F.; Ainla, A.; Redston, J.; Mosadegh, B.; Glavan, A.; Martin, T. J.; Whitesides, G. M. Paper-based electrical respiration sensor. Angew. Chem., Int. Ed. 2016, 55, 5727–5732.

22

Tobjörk, D.; Österbacka, R. Paper electronics. Adv. Mater. 2011, 23, 1935–1961.

23

Zhu, H. L.; Narakathu, B. B.; Fang, Z. Q.; Aijazi, A. T.; Joyce, M.; Atashbar, M.; Hu, L. B. A gravure printed antenna on shape-stable transparent nanopaper. Nanoscale 2014, 6, 9110–9115.

24

Klemm, D.; Kramer, F.; Moritz, S.; Lindström, T.; Ankerfors, M.; Gray, D.; Dorris, A. Nanocelluloses: A new family of nature-based materials. Angew. Chem., Int. Ed. 2011, 50, 5438–5466.

25

Zhu, H. L.; Luo, W.; Ciesielski, P. N.; Fang, Z. Q.; Zhu, J. Y.; Henriksson, G.; Himmel, M. E.; Hu, L. B. Wood-derived materials for green electronics, biological devices, and energy applications. Chem. Rev. 2016, 116, 9305–9374.

26

Kang, W. B.; Lin, M. F.; Chen, J. W.; Lee, P. S. Highly transparent conducting nanopaper for solid state foldable electrochromic devices. Small 2016, 12, 6370–6377.

27

Zhang, Q.; Bao, W. Z.; Gong, A.; Gong, T.; Ma, D. K.; Wan, J. Y.; Dai, J. Q.; Munday, J. N.; He, J. H.; Hu, L. B. et al. A highly sensitive, highly transparent, gel-gated MoS2 phototransistor on biodegradable nanopaper. Nanoscale 2016, 8, 14237–14242.

28

Huang, J.; Zhu, H. L.; Chen, Y. C.; Preston, C.; Rohrbach, K.; Cumings, J.; Hu, L. B. Highly transparent and flexible nanopaper transistors. ACS Nano 2013, 7, 2106–2113.

29

Zhu, H. L.; Xiao, Z. G.; Liu, D. T.; Li, Y. Y.; Weadock, N. J.; Fang, Z. Q.; Huang, J. S.; Hu, L. B. Biodegradable transparent substrates for flexible organic-light-emitting diodes. Energy Environ. Sci. 2013, 6, 2105–2111.

30

Nogi, M.; Komoda, N.; Otsuka, K.; Suganuma, K. Foldable nanopaper antennas for origami electronics. Nanoscale 2013, 5, 4395–4399.

31

Zhu, H. L.; Fang, Z. Q.; Wang, Z.; Dai, J. Q.; Yao, Y. G.; Shen, F.; Preston, C.; Wu, W. X.; Peng, P.; Jang, N. et al. Extreme light management in mesoporous wood cellulose paper for optoelectronics. ACS Nano 2016, 10, 1369–1377.

32

Jung, Y. H.; Chang, T. H.; Zhang, H. L.; Yao, C. H.; Zheng, Q. F.; Yang, V. W.; Mi, H. Y.; Kim, M.; Cho, S. J.; Park, D. W. et al. High-performance green flexible electronics based on biodegradable cellulose nanofibril paper. Nat. Commun. 2015, 6, 7170.

33

de Nooy, A. E. J.; Besemer, A. C.; van Bekkum, H. Highly selective nitroxyl radical-mediated oxidation of primary alcohol groups in water-soluble glucans. Carbohydr. Res. 1995, 269, 89–98.

34

Toivonen, M. S.; Kaskela, A.; Rojas, O. J.; Kauppinen, E. I.; Ikkala, O. Ambient-dried cellulose nanofibril aerogel membranes with high tensile strength and their use for aerosol collection and templates for transparent, flexible devices. Adv. Funct. Mater. 2015, 25, 6618–6626.

35

Daniele, M. A.; Knight, A. J.; Roberts, S. A.; Radom, K.; Erickson, J. S. Sweet substrate: A polysaccharide nanocomposite for conformal electronic decals. Adv. Mater. 2015, 27, 1600–1606.

36

Lacour, S. P.; Wagner, S.; Huang, Z. Y.; Suo, Z. Stretchable gold conductors on elastomeric substrates. Appl. Phys. Lett. 2003, 82, 2404–2406.

37

Müller, F. A.; Müller, L.; Hofmann, I.; Greil, P.; Wenzel, M. M.; Staudenmaier, R. Cellulose-based scaffold materials for cartilage tissue engineering. Biomaterials 2006, 27, 3955–3963.

38

Fundueanu, G.; Constantin, M.; Esposito, E.; Cortesi, R.; Nastruzzi, C.; Menegatti, E. Cellulose acetate butyrate microcapsules containing dextran ion-exchange resins as self-propelled drug release system. Biomaterials 2005, 26, 4337–4347.

39

Cullen, B.; Watt, P. W.; Lundqvist, C.; Silcock, D.; Schmidt, R. J.; Bogan, D.; Light, N. D. The role of oxidised regenerated cellulose/collagen in chronic wound repair and its potential mechanism of action. Int. J. Biochem. Cell Biol. 2002, 34, 1544–1556.

40

Xing, Q.; Zhao, F.; Chen, S.; McNamara, J.; DeCoster, M. A.; Lvov, Y. M. Porous biocompatible three-dimensional scaffolds of cellulose microfiber/gelatin composites for cell culture. Acta Biomater. 2010, 6, 2132–2139.

41

Liu, J.; Fu, T. M.; Cheng, Z. G.; Hong, G. S.; Zhou, T.; Jin, L. H.; Duvvuri, M.; Jiang, Z.; Kruskal, P.; Xie, C. et al. Syringe-injectable electronics. Nat. Nanotechnol. 2015, 10, 629–636.

42

Penfield, W.; Jasper, H. Epilepsy and the Functional Anatomy of the Human Brain; Little Brown & Co. : Boston, 1954.

43

Canan, S.; Ankarali, S.; Marangoz, C. Detailed spectral profile analysis of penicillin-induced epileptiform activity in anesthetized rats. Epilepsy Res. 2008, 82, 7–14.

44

Abidin, I.; Yildirim, M.; Aydin-Abidin, S.; Kalay, E.; Cansu, A.; Akca, M.; Mittmann, T. Penicillin induced epileptiform activity and EEG spectrum analysis of BDNF heterozygous mice: An in vivo electrophysiological study. Brain Res. Bull. 2011, 86, 159–164.

45

Pinto, D. J.; Patrick, S. L.; Huang, W. C.; Connors, B. W. Initiation, propagation, and termination of epileptiform activity in rodent neocortex in vitro involve distinct mechanisms. J. Neurosci. 2005, 25, 8131–8140.

Nano Research
Pages 5604-5614
Cite this article:
Guo Y, Fang Z, Du M, et al. Flexible and biocompatible nanopaper-based electrode arrays for neural activity recording. Nano Research, 2018, 11(10): 5604-5614. https://doi.org/10.1007/s12274-018-2005-0
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