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Mechanically Adaptive Intracortical Implants Improve the Proximity of Neuronal Cell Bodies

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Mechanically Adaptive Intracortical Implants Improve the Proximity of Neuronal Cell Bodies Home Search Collections Journals About Contact us My IOPscience Mechanically adaptive intracortical implants improve the proximity of neuronal cell bodies This content has been downloaded from IOPscience. Please scroll down to see the full text. 2011 J. Neural Eng. 8 066011 (http://iopscience.iop.org/1741-2552/8/6/066011) View the table of contents for this issue, or go to the journal homepage for more Download details: IP Address: 137.99.31.134 This content was downloaded on 22/05/2015 at 14:26 Please note that terms and conditions apply. IOP PUBLISHING JOURNAL OF NEURAL ENGINEERING J. Neural Eng. 8 (2011) 066011 (13pp) doi:10.1088/1741-2560/8/6/066011 Mechanically adaptive intracortical implants improve the proximity of neuronal cell bodies J P Harris1,2, J R Capadona1,2, R H Miller3,BCHealy4,5, K Shanmuganathan6, S J Rowan1,2,6, C Weder6,7 and D J Tyler1,2,8 1 Department of Biomedical Engineering, CWRU, 2071 Martin Luther King Jr Drive, Wickenden Bldg, Cleveland, OH 44106, USA 2 Rehabilitation Research and Development, L Stokes Cleveland VA Medical Center, 10701 East Blvd Mail Stop 151 AW/APT, Cleveland, OH 44106-1702, USA 3 Department of Neurosciences, CWRU, 2109 Adelbert Road, Cleveland, OH 44106, USA 4 Department of Neurology, Brigham and Women’s Hospital, Partners MS Center, Harvard Medical School, 1 Brookline Place West, Suite 225, Boston, MA 02445, USA 5 Biostatistics Center, Massachusetts General Hospital, 50 Staniford St Suite 560, Boston, MA 02114, USA 6 Department of Macromolecular Science and Engineering, 2100 Adelbert Road, Kent Hale Smith Bldg, CWRU, Cleveland, OH 44106, USA 7 Adolphe Merkle Institute and Fribourg Center for Nanomaterials, University of Fribourg, Rte de l’Ancienne Papeterie/PO Box 209, CH-1723 Marly 1, Switzerland E-mail: [email protected] Received 6 March 2011 Accepted for publication 27 September 2011 Published 2 November 2011 Online at stacks.iop.org/JNE/8/066011 Abstract The hypothesis is that the mechanical mismatch between brain tissue and microelectrodes influences the inflammatory response. Our unique, mechanically adaptive polymer nanocomposite enabled this study within the cerebral cortex of rats. The initial tensile storage modulus of 5 GPa decreases to 12 MPa within 15 min under physiological conditions. The response to the nanocomposite was compared to surface-matched, stiffer implants of traditional wires (411 GPa) coated with the identical polymer substrate and implanted on the contralateral side. Both implants were tethered. Fluorescent immunohistochemistry labeling examined neurons, intermediate filaments, macrophages, microglia and proteoglycans. We demonstrate, for the first time, a system that decouples the mechanical and surface chemistry components of the neural response. The neuronal nuclei density within 100 μm of the device at four weeks post-implantation was greater for the compliant nanocomposite compared to the stiff wire. At eight weeks post-implantation, the neuronal nuclei density around the nanocomposite was maintained, but the density around the wire recovered to match that of the nanocomposite. The glial scar response to the compliant nanocomposite was less vigorous than it was to the stiffer wire. The results suggest that mechanically associated factors such as proteoglycans and intermediate filaments are important modulators of the response of the compliant nanocomposite. (Some figures in this article are in colour only in the electronic version) 8 Author to whom any correspondence should be addressed. 1741-2560/11/066011+13$33.00 1 © 2011 IOP Publishing Ltd Printed in the UK J. Neural Eng. 8 (2011) 066011 J P Harris et al 1. Introduction reactivity, measured through the expression of glial fibrillary acidic protein (GFAP) (Lu et al 2009). Despite increasing evidence for the importance of cellular Given the evidence for the contribution of mechanical mechanotransduction in tissue repair and homeostasis (Clark force to the glial scar from in vitro, in silico and in vivo et al 2007, Ingber 2006), the role of mechanical mismatch has experiments, we hypothesize that the in vivo glial scar not been fully elucidated in an in vivo study to explain the response is influenced by a chronic stiffness mismatch between interplay of chemical and mechanical factors that contribute the soft brain tissue and stiff intracortical implants. To to glial scarring surrounding intracortical implants. Previous create an in vivo device to characterize the importance of research in vitro and in silico has supported the importance mechanical compliance of intracortical implants in both the of mechanical signaling in several cell types in the brain. chronic inflammatory reaction and the long-term electrode Cultured astrocytes have been shown to respond to mechanical performance, we used our recently developed mechanically stimuli via calcium signaling (Ostrow and Sachs 2005). adaptive polymer nanocomposite (NC), previously described Investigations have shown that higher strain rates for cultured in detail (Capadona et al 2007, 2008, 2009, Shanmuganathan astrocytes lead to an increased reactivity (Cullen et al 2007). et al 2010a, 2010b, 2009). Our previous work has Cell types have responded differently to substrate stiffness as demonstrated that the polymer NC can reduce its tensile well. Notably, the rate of astrocyte and neuron proliferation as storage modulus from 5 GPa to 12 MPa within 15 min upon well as oligodendrocyte spreading and neuronal branching was exposure to simulated physiological conditions in artificial influenced by substrate stiffness (Kippert et al 2009, Flanagan cerebral spinal fluid at 37 ◦C (Capadona et al 2007, 2008, 2009, et al 2002, Georges et al 2006). Substrate stiffness is also Shanmuganathan et al 2010a, 2010b, 2009). The polymer NC known to shift cell differentiation in mesenchymal stem cells has modest aqueous swelling of 60–75%, in comparison to the to be neurogenic, myogenic or osteogenic (Engler et al 2006). several hundred per cent exhibited by hydrogel approaches. In addition to the effect of substrate stiffness, in silico Here, we have created model electrodes from the adaptive modeling studies indicate that indwelling electrodes exert polymer NC material. We have demonstrated that the NC forces on local populations of cells (Lee et al 2005, Subbaroyan material performs similarly in vitro and in vivo (Harris et al 2005, McConnell et al 2007). Over time, the implanted et al 2011). While the previous work performed modest electrode is anchored to the tissue via the extracellular matrix histological analysis, this is a more complete histological (ECM) and neural inflammatory cells (including microglia and report on their use as cortical implants, demonstrating that astrocytes), resulting in cellular attachments to the electrode there are both foreign body elements and mechanical effects modifying the forces exerted on the brain tissue (McConnell contributing to the overall tissue response at the biotic–abiotic et al 2007). Micromotion associated with electrode movement interface. These components of the inflammatory response within the tissue and the mechanical properties of the electrode appear to be separate but intricately coupled to the neuronal dynamically change the level of exerted forces on the cortical response. tissue during scar maturation. This phenomenon can also be exacerbated as a result of mechanically tethering the electrodes 2. Materials and methods to the skull. In vivo studies which focus on the effects of electrode tethering have shown that untethered implants reduce 2.1. Implant fabrication and imaging the extent of the glial scar (Biran et al 2007,Kimet al 2004, Subbaroyan 2007). It has been suggested that a reduced glial Implants consisted of two types, referred to as nanocomposite scar results from the reduction in forces applied to the tissue. (NC) and wire. NC implants were created by casting Alternatively, it has been proposed that less scarring is the films from a dimethylformamide solution of poly(vinyl result of limited meningeal ingrowth in response to untethered acetate) (PVAc) and tunicate whiskers, as reported previously implants (Subbaroyan 2007). (Capadona et al 2008). The NC had a cellulose whisker To investigate the effects of mechanical mismatch content of 15% w/w. The resulting films were used to create between the electrodes and the cortical tissue, several groups sheets via a custom mold in a hot press (Carver, Wabash, IN). have developed electrode substrates and substrate coatings Sheets were used to create 3 mm long probes that measured from materials such as polyimide, polydimethylsiloxane 100 ± 5 μm in thickness and 203 ± 19 μm in width with and parylene, which are more compliant than materials an approximately 45 ± 3◦ angle tip (figure 1(a)) via a cutting traditionally used to create electrodes. However, these process. The cutting process created a NC with two types materials have had limited success in attenuating glial scar of surfaces: two pressed sides (figure 1(c)) and two cut sides formation. A limitation to many of these studies is that (figure 1(d)). Both implant types were single shank probes such materials still have moduli six orders of magnitude with nearly the same cross-sectional area, refer to Harris et al larger than those of the brain, while also introducing different 2011 for a characterization of implant mechanical properties surface chemistries that could confound the tissue–material of the NC material. interaction (Lee et al 2004, Nikles et al 2003, Takeuchi Wire implants consisted of 50 μm diameter tungsten et al 2004,Westeret al 2009, Takeuchi et al 2005) and wires (AM-Systems, Sequim, WA) from which the Teflon complicate the interpretation of these results. Of interest is insulation was mechanically stripped using cutting tweezers. that surface treatments of electrode materials with a poly(vinyl Wire implants (figure 1(b)) were dip-coated in a solution of alcohol)/poly(acrylic acid) hydrogel have reduced astrocyte PVAc (MW 113 000 g mol−1, density 1.19 g cm−3,Sigma 2 J. Neural Eng. 8 (2011) 066011 J P Harris et al (b) (a) (c) (d) (e) Figure 1.
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