Mechanically Robust, Softening Shape Memory Polymer Probes for Intracortical Recording
Abstract
:1. Introduction
2. Materials and Methods
2.1. Polymer Preparation and Device Fabrication
2.2. Surgical Implantation
2.3. Electrophysiological Recordings and Electrochemistry
2.4. Behavioral Testing
2.5. Immunohistochemistry and Analysis
2.6. Device Physical Robustness
2.7. Statistics
3. Results
3.1. Single Unit Recordings and In Vivo Electrochemistry
3.2. Device Physical Robustness
3.3. Immunohistochemistry
3.4. Pilot Behavioral Deficit Data
4. Discussion
5. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
- Ferguson, M.; Sharma, D.; Ross, D.; Zhao, F. A critical review of microelectrode arrays and strategies for improving neural interfaces. Adv. Healthc. Mater. 2019, 8. [Google Scholar] [CrossRef]
- Guo, L. Principles of functional neural mapping using an intracortical ultra-density microelectrode array (ultra-density MEA). J. Neural Eng. 2020. [Google Scholar] [CrossRef]
- Hochberg, L.R.; Bacher, D.; Jarosiewicz, B.; Masse, N.Y.; Simeral, J.D.; Vogel, J.; Haddadin, S.; Liu, J.; Cash, S.S.; van der Smagt, P.; et al. Reach and grasp by people with tetraplegia using a neurally controlled robotic arm. Nature 2012, 485, 372–375. [Google Scholar] [CrossRef] [Green Version]
- Tsu, A.P.; Burish, M.J.; GodLove, J.; Ganguly, K. Cortical neuroprosthetics from a clinical perspective. Neurobiol. Dis. 2015, 83, 154–160. [Google Scholar] [CrossRef] [Green Version]
- Lebedev, M.A.; Nicolelis, M.A.L. Brain-machine interfaces: Past, present and future. Trends Neurosci. 2006, 29, 536–546. [Google Scholar] [CrossRef]
- Goss-Varley, M.; Dona, K.R.; McMahon, J.A.; Shoffstall, A.J.; Ereifej, E.S.; Lindner, S.C.; Capadona, J.R. Microelectrode implantation in motor cortex causes fine motor deficit: Implications on potential considerations to Brain Computer Interfacing and Human Augmentation. Sci. Rep. 2017, 7. [Google Scholar] [CrossRef] [Green Version]
- Du, J.; Roukes, M.L.; Masmanidis, S.C. Dual-side and three-dimensional microelectrode arrays fabricated from ultra-thin silicon substrates. J. Micromech. Microeng. 2009, 19. [Google Scholar] [CrossRef]
- Schjetnan, A.G.P.; Luczak, A. Recording large-scale neuronal ensembles with silicon probes in the anesthetized rat. J. Vis. Exp. 2011, 56, 3282. [Google Scholar] [CrossRef]
- Grand, L.B. Development, Testing and Application of Laminar Multielectrodes and Biocompatible Coatings for Intracortical Applications. Ph.D. Thesis, Pazmany Peter Catholic University, Budapest, Hungary, 2007. [Google Scholar]
- Kozai, T.D.Y.; Catt, K.; Li, X.; Gugel, Z.V.; Olafsson, V.T.; Vazquez, A.L.; Cui, X.T. Mechanical failure modes of chronically implanted planar silicon-based neural probes for laminar recording. Biomaterials 2015, 37, 25–39. [Google Scholar] [CrossRef] [Green Version]
- Gilletti, A.; Muthuswamy, J. Brain micromotion around implants in the rodent somatosensory cortex. J. Neural Eng. 2006, 3, 189–195. [Google Scholar] [CrossRef]
- Lee, H.; Bellamkonda, R.V.; Sun, W.; Levenston, M.E. Biomechanical analysis of silicon microelectrode-induced strain in the brain. J. Neural Eng. 2005, 2, 81–89. [Google Scholar] [CrossRef] [PubMed]
- Sridharan, A.; Nguyen, J.K.; Capadona, J.R.; Muthuswamy, J. Compliant intracortical implants reduce strains and strain rates in brain tissue in vivo. J. Neural Eng. 2015, 12. [Google Scholar] [CrossRef] [Green Version]
- Subbaroyan, J.; Martin, D.C.; Kipke, D.R. A finite-element model of the mechanical effects of implantable microelectrodes in the cerebral cortex. J. Neural Eng. 2005, 2, 103–113. [Google Scholar] [CrossRef] [PubMed]
- Luan, L.; Wei, X.; Zhao, Z.; Siegel, J.J.; Potnis, O.; Tuppen, C.A.; Lin, S.; Kazmi, S.; Fowler, R.A.; Holloway, S.; et al. Ultraflexible nanoelectronic probes form reliable, glial scar–free neural integration. Sci. Adv. 2017, 3. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lo, M.C.; Wang, S.; Singh, S.; Damodaran, V.B.; Kaplan, H.M.; Kohn, J.; Shreiber, D.I.; Zahn, J.D. Coating flexible probes with an ultra fast degrading polymer to aid in tissue insertion. Biomed. Microdevices 2015, 17, 34–45. [Google Scholar] [CrossRef] [Green Version]
- Jeon, M.; Cho, J.; Kim, Y.K.; Jung, D.; Yoon, E.-S.; Shin, S.; Cho, I.-J. Partially flexible MEMS neural probe composed of polyimide and sucrose gel for reducing brain damage during and after implantation. J. Micromech. Microeng. 2014, 24. [Google Scholar] [CrossRef]
- Lecomte, A.; Castagnola, V.; Descamps, E.; Dahan, L.; Blatché, M.C.; Dinis, T.M.; Leclerc, E.; Egles, C.; Bergaud, C. Silk and PEG as means to stiffen a parylene probe for insertion in the brain: Toward a double time-scale tool for local drug delivery. J. Micromech. Microeng. 2015, 25. [Google Scholar] [CrossRef]
- Levental, I.; Georges, P.C.; Janmey, P.A. Soft biological materials and their impact on cell function. Soft Matter 2007, 3, 299–306. [Google Scholar] [CrossRef]
- Gefen, A.; Gefen, N.; Zhu, Q.; Raghupathi, R.; Margulies, S.S. Age-dependent changes in material properties of the brain and braincase of the rat. J. Neurotrauma 2003, 20, 1163–1177. [Google Scholar] [CrossRef]
- Stiller, A.; Usoro, J.; Frewin, C.; Danda, V.; Ecker, M.; Joshi-Imre, A.; Musselman, K.; Voit, W.; Modi, R.; Pancrazio, J.; et al. Chronic intracortical recording and electrochemical stability of Thiol-ene/acrylate shape memory polymer electrode arrays. Micromachines 2018, 9, 500. [Google Scholar] [CrossRef] [Green Version]
- Mather, P.T.; Luo, X.; Rousseau, I.A. Shape memory polymer research. Annu. Rev. Mater. Res. 2009, 39, 445–471. [Google Scholar] [CrossRef]
- Wang, K.; Strandman, S.; Zhu, X.X. A mini review: Shape memory polymers for biomedical applications. Front. Chem. Sci. Eng. 2017, 11. [Google Scholar] [CrossRef]
- Leng, J.; Lan, X.; Liu, Y.; Du, S. Shape-memory polymers and their composites: Stimulus methods and applications. Prog. Mater. Sci. 2011, 56, 1077–1135. [Google Scholar] [CrossRef]
- Black, B.J.; Ecker, M.; Stiller, A.; Rihani, R.; Danda, V.R.; Reed, I.; Voit, W.E.; Pancrazio, J.J. In vitro compatibility testing of thiol-ene/acrylate-based shape memory polymers for use in implantable neural interfaces. J. Biomed. Mater. Res. Part A 2018, 106, 2891–2898. [Google Scholar] [CrossRef]
- Schönfeld, L.M.; Dooley, D.; Jahanshahi, A.; Temel, Y.; Hendrix, S. Evaluating rodent motor functions: Which tests to choose? Neurosci. Biobehav. Rev. 2017, 83, 298–312. [Google Scholar] [CrossRef]
- Schönfeld, L.M.; Jahanshahi, A.; Lemmens, E.; Schipper, S.; Dooley, D.; Joosten, E.; Temel, Y.; Hendrix, S. Long-term motor deficits after controlled cortical impact in rats can be detected by fine motor skill tests but not by automated gait analysis. J. Neurotrauma 2017, 34, 505–516. [Google Scholar] [CrossRef]
- Schneider, C.A.; Rasband, W.S.; Eliceiri, K.W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 2012, 9, 671–675. [Google Scholar] [CrossRef]
- Schindelin, J.; Arganda-Carreras, I.; Frise, E.; Kaynig, V.; Longair, M.; Pietzsch, T.; Preibisch, S.; Rueden, C.; Saalfeld, S.; Schmid, B.; et al. Fiji: An open-source platform for biological-image analysis. Nat. Methods 2012, 9, 676–682. [Google Scholar] [CrossRef] [Green Version]
- Stiller, A.; Black, B.; Kung, C.; Ashok, A.; Cogan, S.; Varner, V.; Pancrazio, J. A meta-analysis of intracortical device stiffness and its correlation with histological outcomes. Micromachines 2018, 9, 443. [Google Scholar] [CrossRef] [Green Version]
- Hosseini, S.M.; Rihani, R.; Batchelor, B.; Stiller, A.M.; Pancrazio, J.J.; Voit, W.E.; Ecker, M. Softening shape memory polymer substrates for bioelectronic devices with improved hydrolytic stability. Front. Mater. 2018, 5. [Google Scholar] [CrossRef]
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Stiller, A.M.; Usoro, J.O.; Lawson, J.; Araya, B.; González-González, M.A.; Danda, V.R.; Voit, W.E.; Black, B.J.; Pancrazio, J.J. Mechanically Robust, Softening Shape Memory Polymer Probes for Intracortical Recording. Micromachines 2020, 11, 619. https://doi.org/10.3390/mi11060619
Stiller AM, Usoro JO, Lawson J, Araya B, González-González MA, Danda VR, Voit WE, Black BJ, Pancrazio JJ. Mechanically Robust, Softening Shape Memory Polymer Probes for Intracortical Recording. Micromachines. 2020; 11(6):619. https://doi.org/10.3390/mi11060619
Chicago/Turabian StyleStiller, Allison M., Joshua O. Usoro, Jennifer Lawson, Betsiti Araya, María Alejandra González-González, Vindhya R. Danda, Walter E. Voit, Bryan J. Black, and Joseph J. Pancrazio. 2020. "Mechanically Robust, Softening Shape Memory Polymer Probes for Intracortical Recording" Micromachines 11, no. 6: 619. https://doi.org/10.3390/mi11060619