Hostname: page-component-78c5997874-ndw9j Total loading time: 0 Render date: 2024-11-20T04:28:37.477Z Has data issue: false hasContentIssue false
  • English
  • Français

Mechanically adaptive nanocomposites for neural interfacing

Published online by Cambridge University Press:  08 June 2012

Jeffrey R. Capadona ,
Dustin J. Tyler ,
Christian A. Zorman ,
Stuart J. Rowan  and
Christoph Weder
Jeffrey R. Capadona
Affiliation:
Department of Biomedical Engineering, Case Western Reserve University, Cleveland, OH 44106, USA; jrc35@case.edu
Dustin J. Tyler
Affiliation:
Department of Biomedical Engineering, Case Western Reserve University, Cleveland, OH 44106, USA; dustin.tyler@case.edu
Christian A. Zorman
Affiliation:
Department of Electrical Engineering and Computer Science, Case Western Reserve University, Cleveland, OH 44106, USA; Christian.Zorman@case.edu
Stuart J. Rowan
Affiliation:
Department of Macromolecular Science and Engineering, Case Western Reserve University, Cleveland, OH 44106, USA; stuart.rowan@case.edu
Christoph Weder
Affiliation:
Adolphe Merkle Institute, University of Fribourg, Switzerland; christoph.weder@unifr.ch
Get access

Abstract

The recording of neural signals with microelectrodes that are implanted into the cortex of the brain is potentially useful for a range of clinical applications. However, the widespread use of such neural interfaces has so far been stifled because existing intracortical electrode systems rarely allow for consistent long-term recording of neural activity. This limitation is usually attributed to scar formation and neuron death near the surface of the implanted electrode. It has been proposed that the mechanical property mismatch between existing electrode materials and the brain tissue is a significant contributor to these events. To alleviate this problem, we utilized the architecture of the sea cucumber dermis as a blueprint to engineer a new class of mechanically adaptive materials as substrates for “smart” intracortical electrodes. We demonstrated that these originally rigid polymer nanocomposites soften considerably upon exposure to emulated physiological and in vivo conditions. The adaptive nature of these bioinspired materials makes them useful as a basis for electrodes that are sufficiently stiff to be easily implanted and subsequently soften to better match the stiffness of the brain. Initial histological evaluations suggest that mechanically adaptive neural prosthetics can more rapidly stabilize neural cell populations at the device interface than rigid systems, which bodes well for improving the functionality of intracortical devices.

Type
Research Article
Information
MRS Bulletin , Volume 37 , Issue 6: Materials for neural interfaces , June 2012 , pp. 581 - 589
Copyright
Copyright © Materials Research Society 2012

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.)

References

1.Hochberg, L.R., Serruya, M.D., Friehs, G.M., Mukand, J.A., Saleh, M., Caplan, A.H., Branner, A., Chen, D., Penn, R.D., Donoghue, J.P., Nature 442, 164 (2006).CrossRefGoogle Scholar
2.Velliste, M., Perel, S., Spalding, M.C., Whitford, A.S., Schwartz, A.B., Nature 453, 1098 (2008).CrossRefGoogle Scholar
3.Ward, M.P., Rajdev, P., Ellison, C., Irazoqui, P.P., Brain Res. 1282, 183 (2009).CrossRefGoogle Scholar
4.Daly, J.J., Wolpaw, J.R., Lancet Neurol. 7, 1032 (2008).CrossRefGoogle Scholar
5.Donoghue, J.P., Neuron 60, 511 (2008).CrossRefGoogle Scholar
6.Leach, J., Achyuta, A.K.H., Murthy, S.K., Front. Neuroeng. 2 (2010).CrossRefGoogle Scholar
7.Moritz, C.T., Perlmutter, S.I., Fetz, E.E., Nature 456, 639 (2008).CrossRefGoogle Scholar
8.Schwartz, A.B., Annu. Rev. Neurosci. 27, 487 (2004).CrossRefGoogle Scholar
9.Schwartz, A.B., Cui, X.T., Weber, D.J., Moran, D.W., Neuron 52, 205 (2006).CrossRefGoogle Scholar
10.Buzsáki, G., Nat. Neurosci. 7, 446 (2004).CrossRefGoogle Scholar
11.Nicolelis, M.A., Nature 409, 403 (2001).CrossRefGoogle Scholar
12.McConnell, G.C., Rees, H.D., Levey, A.I., Gutekunst, C., Gross, R.E., Bellamkonda, R.V., J. Neural Eng. 6, 56003 (2009).CrossRefGoogle Scholar
13.Polikov, V.S., Block, M.L., Fellous, J.M., Hong, J.S., Reichert, W.M., Biomaterials 27, 5368 (2006).CrossRefGoogle Scholar
14.Williams, J.C., Rennaker, R.L., Kipke, D.R., Brain Res. 4, 303 (1999).Google Scholar
15.Biran, R., Martin, D.C., Tresco, P.A., Exp. Neurol. 195, 115 (2005).CrossRefGoogle Scholar
16.Polikov, V.S., Tresco, P.A., Reichert, W.M., J. Neurosci. Methods 148, 1 (2005).CrossRefGoogle Scholar
17.Szarowski, D.H., Andersen, M.D., Retterer, S., Spence, A.J., Isaacson, M., Craighead, H.G., Turner, J.N., Shain, W., Brain Res. 983, 23 (2003).CrossRefGoogle Scholar
18.Johnson, M.D., Kao, O.E., Kipke, D.R., J. Neurosci. Methods 160, 276 (2007).CrossRefGoogle Scholar
19.Bjornsson, C.S., Oh, S.J., Al-Kofahi, Y.A., Lim, Y.J., Smith, K.L., Turner, J.N., De, S., Roysam, B., Shain, W., Kim, S.J., J. Neural Eng. 3, 196 (2006).CrossRefGoogle Scholar
20.Sharp, A.A., Panchawagh, H.V., Ortega, A., Artale, R., Richardson-Burns, S., Finch, D.S., Gall, K., Mahajan, R.L., Restrepo, D., J. Neural Eng. 3, L23 (2006).CrossRefGoogle Scholar
21.He, W., Bellamkonda, R.V., in Indwelling Neural Implants: Strategies for Contending with the In Vivo Environment, Reichert, W.M., Ed. (CRC Press, Boca Raton, FL, 2008).Google Scholar
22.Zhong, Y., Bellamkonda, R.V., J. R. Soc. Interface 5, 957 (2008).CrossRefGoogle Scholar
23.Tresco, P.A., Winslow, B.D., Crit. Rev. Biomed. Eng. 39, 29 (2011).CrossRefGoogle Scholar
24.Kim, Y.-T., Hitchcock, R.W., Bridge, M.J., Tresco, P.A., Biomaterials 25, 2229 (2004).CrossRefGoogle Scholar
25.Lee, H., Bellamkonda, R.V., Sun, W., Levenston, M.E., J. Neural Eng. 2, 81 (2005).CrossRefGoogle Scholar
26.McConnell, G.C., Schneider, T.M., Owens, D.J., Bellamkonda, R.V., IEEE Trans. Biomed. Eng. 54, 1097 (2007).CrossRefGoogle Scholar
27.Lebedev, M.A., Nicolelis, M.A., Trends Neurosci. 29, 536 (2006).CrossRefGoogle Scholar
28.Gilletti, A., Muthuswamy, J., J. Neural Eng. 3, 189 (2006).CrossRefGoogle Scholar
29.Subbaroyan, J., Martin, D.C., Kipke, D.R., J. Neural Eng. 2, 103 (2005).CrossRefGoogle Scholar
30.Biran, R., Martin, D.C., Tresco, P.A., J. Biomed. Mater. Res. Part A 82, 169 (2007).CrossRefGoogle Scholar
31.Williams, J.C., Hippensteel, J.A., Dilgen, J., Shain, W., Kipke, D.R., J. Neural Eng. 4, 410 (2007).CrossRefGoogle Scholar
32.Kim, D.H., Martin, D.C., Biomaterials 27, 3031 (2006).CrossRefGoogle Scholar
33.Shain, W., Spataro, L., Dilgen, J., Haverstick, K., Retterer, S., Isaacson, M., Saltzman, M., Turner, J.N., IEEE Trans. Neural Syst. Rehabil. Eng. 11, 186 (2003).CrossRefGoogle Scholar
34.Wadhwa, R., Lagenaur, C.F., Cui, X.T., J. Controlled Release 110, 531 (2006).CrossRefGoogle ScholarPubMed
35.Zhong, Y., Bellamkonda, R.V., Brain Res. 1148, 15 (2007).CrossRefGoogle Scholar
36.Spataro, L., Dilgen, J., Retterer, S., Spence, A.J., Isaacson, M., Turner, J.N., Shain, W., Exp. Neurol. 194, 289 (2005).CrossRefGoogle Scholar
37.Rennaker, R.L., Miller, J., Tang, H., Wilson, D.A., J. Neural Eng. 4, L1 (2007).CrossRefGoogle Scholar
38.Caruso, C., Mohn, C., Karara, A.L., Rettori, V., Watanobe, H., Schioth, H.B., Seilicovich, A., Lasaga, M., Neuroendocrinology 79, 278 (2004).CrossRefGoogle Scholar
39.He, W., McConnell, G., Schneider, T., Bellamkonda, R., Adv. Mater. 19, 3529 (2007).CrossRefGoogle Scholar
40.Rousche, P.J., Pellinen, D.S., Pivin, D.P., Williams, J.C., Vetter, R.J., Kipke, D.R., IEEE Trans. Biomed. Eng. 48, 361 (2001).CrossRefGoogle Scholar
41.Subbaroyan, J., Kipke, D.R., Conf. Proc. IEEE Eng. Med. Biol. Soc. 1, 3588 (2006).CrossRefGoogle Scholar
42.Takeuchi, S., Ziegler, D., Yoshida, Y., Mabuchi, K., Suzuki, T., Lab Chip 5, 519 (2005).CrossRefGoogle Scholar
43.Wester, B.A., Lee, R.H., LaPlaca, M.C., J. Neural Eng. 6, 024002 (2009).CrossRefGoogle Scholar
44.Fernandez, L.J., Altuna, A., Tijero, M., Gabriel, G., Villa, R., Rodrıguez, M.J., Batlle, M., Vilares, R., Berganzo, J., Blanco, F.J., J. Micromech. Microeng. 19, 025007 (2009).CrossRefGoogle Scholar
45.Mercanzini, A., Colin, P., Bensadoun, J.C., Bertsch, A., Renaud, P., IEEE Trans. Biomed. Eng. 56, 1909 (2009).CrossRefGoogle Scholar
46.Lu, Y., Shoichet, M.S., Biomaterials 30, 4143 (2009).CrossRefGoogle Scholar
47.Lee, K., He, J., Clement, R., Massia, S., Kim, B., Biosens. Bioelectron. 20, 404 (2004).CrossRefGoogle Scholar
48.Nikles, S.A., Pellinen, D.S., Kitagawa, J., Bradley, R.M., Kipke, D.R., Najafi, K., Engineering in Medicine and Biology Society, 2003. Proceedings of the 25th Annual International Conference of the IEEE, vol. 4, 3340 (2003).Google Scholar
49.Takeuchi, S., Suzuki, T., Mabuchi, K., Fujita, H., J. Micromech. Microeng. 14, 104 (2004).CrossRefGoogle Scholar
50.Kozai, T.D., Kipke, D.R., J. Neurosci. Methods 184, 2 (2009).CrossRefGoogle Scholar
51.Kee-Keun, L., He, J., Singh, A., Kim, B., Proceedings of the International Conference on MEMS, NANO and Smart Systems 2003 (2003), p. 418.CrossRefGoogle Scholar
52.Kee-Keun, L., He, J., Singh, A., Massia, S., Ehteshami, G., Kim, B., Raupp, G., J. Micromech. Microeng. 14, 32 (2004).Google Scholar
53.Potter, K., Gui, B., Capadona, J.R., in Biomimetics—Innovation Thru Mimicking Natures Inventions, Bar-Cohen, Y., Ed. (CRC Press, Boca Raton, FL, 2011), vol. 2, pp. 95–129.Google Scholar
54.Lu, Y.B., Franze, K., Seifert, G., Steinhauser, C., Kirchhoff, F., Wolburg, H., Guck, J., Janmey, P., Wei, E.Q., Kas, J., Reichenbach, A., Proc. Natl. Acad. Sci. U.S.A. 103, 17759 (2006).CrossRefGoogle Scholar
55.Seymour, J.P., Kipke, D.R., Biomaterials 28, 3594 (2007).CrossRefGoogle Scholar
56.Lee, K., Singh, A., He, J., Massia, S., Sens. Actuators, B 102, 67 (2004).CrossRefGoogle Scholar
57.Lewitus, D., Smith, K.L., Shain, W., Kohn, J., Acta Biomater. 7, 2483 (2011).CrossRefGoogle Scholar
58.Ludwig, K.A., Uram, J.D., Yang, J., Martin, D.C., Kipke, D.R., J. Neural Eng. 3, 59 (2006).CrossRefGoogle Scholar
59.Kim, D.H., Wiler, J.A., Anderson, D.J., Kipke, D.R., Martin, D.C., ActaBiomater. 6, 57 (2010).Google Scholar
60.Cui, X.T., Martin, D.C., Sens. Actuators, B 89, 92 (2003).CrossRefGoogle Scholar
61.Xiao, Y.H., Cui, X., Hancock, J.M., Bouguettaya, M., Reynolds, J.R., Martin, D.C., Sens. Actuators, B 99, 437 (2004).CrossRefGoogle Scholar
62.Cui, X.T., Zhou, D.D., IEEE Trans. Neural Syst. Rehabil. Eng. 15, 502 (2007).CrossRefGoogle Scholar
63.Xiao, Y.H., Martin, D.C., Cui, X.T., Shenai, M., Appl. Biochem. Biotechnol. 128, 117 (2006).CrossRefGoogle Scholar
64.Kim, D.H., Abidian, M., Martin, D.C., J. Biomed. Mater. Res. Part A 71, 577 (2004).CrossRefGoogle Scholar
65.Yang, J., Kim, D.H., Hendricks, J.L., Leach, M., Northey, R., Martin, D.C., ActaBiomater. 1, 125 (2005).Google Scholar
66.Cui, X.T., Hetke, J.F., Wiler, J.A., Anderson, A.J., Martin, D.C., Sens. Actuators, A 93, 8 (2001).CrossRefGoogle Scholar
67.Cui, X.T., Lee, V.A., Raphael, Y., Wiler, J.A., Hetke, J.F., Anderson, D.J., Martin, D.C., J. Biomed. Mater. Res. 56, 261 (2001).3.0.CO;2-I>CrossRefGoogle Scholar
68.Capadona, J.R., Shanmuganathan, K., Tyler, D.J., Rowan, S.J., Weder, C., Science 319, 1370 (2008).CrossRefGoogle Scholar
69.Capadona, J.R., Shanmuganathan, K., Trittschuh, S., Seidel, S., Rowan, S.J., Weder, C., Biomacromolecules 10, 712 (2009).CrossRefGoogle Scholar
70.Capadona, J.R., van den Berg, O., Capadona, L.A., Schroeter, M., Rowan, S.J., Tyler, D.J., Weder, C., Nat. Nano 2, 765 (2007).CrossRefGoogle Scholar
71.Shanmuganathan, K., Capadona, J.R., Rowan, S.J., Weder, C., Prog. Polym. Sci. 35, 212 (2010).CrossRefGoogle Scholar
72.Shanmuganathan, K., Capadona, J.R., Rowan, S.J., Weder, C., J. Mater. Chem. 20, 180 (2010).CrossRefGoogle Scholar
73.Shanmuganathan, K., Capadona, J.R., Rowan, S.J., Weder, C., ACS Appl. Mater. Interfaces 2, 165 (2009).CrossRefGoogle Scholar
74.van den Berg, O., Capadona, J.R., Weder, C., Biomacromolecules 8, 1353 (2007).CrossRefGoogle Scholar
75.Trotter, J.A., Koob, T.J., J. Exp. Biol. 198, 1951 (1995).CrossRefGoogle Scholar
76.Koob, T.J., Koob-Emunds, M.M., Trotter, J.A., J. Exp. Biol. 202, 2291 (1999).CrossRefGoogle Scholar
77.Trotter, J.A., Tipper, J., Lyons-Levy, G., Chino, K., Heuer, A.H., Liu, Z., Mrksich, M., Hodneland, C., Shannon-Dillmore, W., Koob, T.J., Koob-Emunds, M.M., Kadler, K., Holmes, D., Biochem. Soc. Trans. 28, 357 (2000).CrossRefGoogle Scholar
78.Motokawa, T., Comput. Biochem. Physiol. 70, 41 (1981).Google Scholar
79.Wilkie, I.C., J. Exp. Biol. 205, 159 (2002).CrossRefGoogle Scholar
80.Wilkie, I.C., Echinoderm Stud. 5, 61 (1996).Google Scholar
81.Szulgit, G.K.A.S., Shadwick, R.E., J. Exp. Biol. 203, 1539 (2000).CrossRefGoogle Scholar
82.Hsu, L., Rowan, S.J., Weder, C., J. Mater. Chem. 21, 2812 (2011).CrossRefGoogle Scholar
83.Eichhorn, S.J., Dufresne, A., Aranguren, M., Capadona, J.R., Rowan, S.J., Weder, C., Thielemans, W., Roman, M., Renneckar, S., Gindl, W., Weigel, S., Yano, H., Abe, K., Nogi, M., Mangalam, A., Simonsen, J., Benight, A.D., Bismarck, A., Berglund, L.A., J. Mater. Sci. 45, 1 (2010).CrossRefGoogle Scholar
84.Sturcova, A., Davies, G.R., Eichorn, S.J., Biomacromolecules 6, 1055 (2005).CrossRefGoogle Scholar
85.Rusli, R., Eichhorn, S.J., Appl. Phys. Lett. 93, 033111 (2008).CrossRefGoogle Scholar
86.Hsieh, Y.C., Yano, H., Nogi, M., Eichhorn, S.J., Cellulose 15, 507 (2008).CrossRefGoogle Scholar
87.Schroers, M., Kokil, A., Weder, C., J. Appl. Polym. Sci. 93, 2883 (2004).CrossRefGoogle Scholar
88.Takayanagi, M., Uemura, S., Minami, S., J. Polym. Sci. C 5, 113 (1964).CrossRefGoogle Scholar
89.Ouali, N., Cavaillé, J.Y., Pérez, J., Plast. Rubber Compos. Process. Appl. 16, 55 (1991).Google Scholar
90.Rusli, R., Shanmuganathan, K., Rowan, S.J., Weder, C., Eichhorn, S.J., Biomacromolecules 11, 762 (2010).CrossRefGoogle Scholar
91.Rusli, R., Shanmuganathan, K., Rowan, S.J., Weder, C., Eichhorn, S.J., Biomacromolecules 12, 1363 (2011).CrossRefGoogle Scholar
92.Rusli, R., Eichhorn, S.J., Appl. Phys. Lett. 93, 033111 (2008).CrossRefGoogle Scholar
93.Mendez, J., Annamalai, P.K., Eichhorn, S.J., Rusli, R., Rowan, S.J., Foster, E.J., Weder, C., Macromolecules 44, 6827 (2011).CrossRefGoogle Scholar
94.Harris, J.P., Hess, A.E., Rowan, S.J., Weder, C., Zorman, C.A., Tyler, D.J., Capadona, J.R., J. Neural Eng. 8, 046010 (2011).CrossRefGoogle Scholar
95.Hess, A., Capadona, J.R., Shanmuganathan, K., Hsu, L., Rowan, S.J., Weder, C., Tyler, D.J., Zorman, C.A., J. Micromech. Microeng. 21, 54009 (2011).CrossRefGoogle Scholar
96.Harris, J.P., Capadona, J.R., Miller, R.H., Healy, B.C., Shanmuganathan, K., Rowan, S.J., Weder, C., Tyler, D.J., J. Neural Eng. 8, 066011 (2011).CrossRefGoogle Scholar
97.Loane, D.J., Byrnes, K.R., Neurotherapeutics 7, 366 (2010).CrossRefGoogle Scholar