Neural electrode resilience against dielectric damage may be improved by use of highly doped silicon as a conductive material

BACKGROUND Dielectric damage occurring in vivo to neural electrodes, leading to conductive material exposure and impedance reduction over time, limits the functional lifetime and clinical viability of neuroprosthetics. We used silicon micromachined Utah Electrode Arrays (UEAs) with iridium oxide (IrOx) tip metallization and parylene C dielectric encapsulation to understand the factors affecting device resilience and drive improvements. NEW METHOD In vitro impedance measurements and finite element analyses were conducted to evaluate how exposed surface area of silicon and IrOx affect UEA properties. Through an aggressive in vitro reactive accelerated aging (RAA) protocol, in vivo parylene degradation was simulated on UEAs to explore agreement with our models. Electrochemical properties of silicon and other common electrode materials were compared to help inform material choice in future neural electrode designs. RESULTS Exposure of silicon on UEAs was found to primarily affect impedance at frequencies >1kHz, while characteristics at 1 kHz and below were largely unchanged. Post-RAA impedance reduction of UEAs was mitigated in cases where dielectric damage was more likely to expose silicon instead of IrOx. Silicon was found to have a per-area electrochemical impedance >10×higher than many common electrode materials regardless of doping level and resistivity, making it best suited for use as a low-shunting conductor. COMPARISON WITH EXISTING METHODS Non-semiconductor electrode materials commonly used in neural electrode design are more susceptible to shunting neural interface signals through dielectric defects, compared to highly doped silicon. CONCLUSION Strategic use of silicon and similar materials may increase neural electrode robustness against encapsulation failures.

[1]  S.F. Cogan,et al.  Sputtered iridium oxide films (SIROFs) for low-impedance neural stimulation and recording electrodes , 2004, The 26th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[2]  S. Cogan Neural stimulation and recording electrodes. , 2008, Annual review of biomedical engineering.

[3]  D. Robinson,et al.  The electrical properties of metal microelectrodes , 1968 .

[4]  Michael P. Hughes,et al.  Effects of electrode size on the performance of neural recording microelectrodes , 2000, 1st Annual International IEEE-EMBS Special Topic Conference on Microtechnologies in Medicine and Biology. Proceedings (Cat. No.00EX451).

[5]  Martin Han,et al.  A new chronic neural probe with electroplated iridium oxide microelectrodes , 2008, 2008 30th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[6]  Jeong Hun Kim,et al.  Soft implantable microelectrodes for future medicine: prosthetics, neural signal recording and neuromodulation. , 2016, Lab on a chip.

[7]  Patrick A. Tresco,et al.  Impedance characterization of microarray recording electrodes in vitro , 2005, IEEE Transactions on Biomedical Engineering.

[8]  E. Schmidt,et al.  Long-term implants of Parylene-C coated microelectrodes , 2006, Medical and Biological Engineering and Computing.

[9]  R. Stein,et al.  Selective stimulation of cat sciatic nerve using an array of varying-length microelectrodes. , 2001, Journal of neurophysiology.

[10]  P. Boddy Impedance measurements at the semiconductor-electrolyte interface☆ , 1969 .

[11]  F. Solzbacher,et al.  Characterization of a-SiC(x):H thin films as an encapsulation material for integrated silicon based neural interface devices. , 2007, Thin Solid Films.

[12]  Juan Aceros,et al.  Scanning electron microscopy of chronically implanted intracortical microelectrode arrays in non-human primates , 2016, Journal of neural engineering.

[13]  Sheryl R. Kane,et al.  Electrical Performance of Penetrating Microelectrodes Chronically Implanted in Cat Cortex , 2013, IEEE Transactions on Biomedical Engineering.

[14]  Rajmohan Bhandari,et al.  Long-term reliability of Al2O3 and Parylene C bilayer encapsulated Utah electrode array based neural interfaces for chronic implantation , 2014, Journal of neural engineering.

[15]  David C. Martin,et al.  Layered carbon nanotube-polyelectrolyte electrodes outperform traditional neural interface materials. , 2009, Nano letters.

[16]  David C. Martin,et al.  Chronic neural recordings using silicon microelectrode arrays electrochemically deposited with a poly(3,4-ethylenedioxythiophene) (PEDOT) film , 2006, Journal of neural engineering.

[17]  Michael D Joseph,et al.  Poly(3,4-ethylenedioxythiophene) (PEDOT) polymer coatings facilitate smaller neural recording electrodes , 2011, Journal of neural engineering.

[18]  M L Boninger,et al.  Ten-dimensional anthropomorphic arm control in a human brain−machine interface: difficulties, solutions, and limitations , 2015, Journal of neural engineering.

[19]  Victor Krauthamer,et al.  Rapid evaluation of the durability of cortical neural implants using accelerated aging with reactive oxygen species , 2015, Journal of neural engineering.

[20]  Justin C. Sanchez,et al.  Comprehensive characterization and failure modes of tungsten microwire arrays in chronic neural implants , 2012, Journal of neural engineering.

[21]  Christoph Weder,et al.  Progress towards biocompatible intracortical microelectrodes for neural interfacing applications , 2015, Journal of neural engineering.

[22]  Martin Stelzle,et al.  Biostability of micro-photodiode arrays for subretinal implantation. , 2002, Biomaterials.

[23]  Kevin J. Otto,et al.  Poly(3,4-ethylenedioxythiophene) as a Micro-Neural Interface Material for Electrostimulation , 2009, Front. Neuroeng..

[24]  Henry Markram,et al.  Substrate Arrays of Iridium Oxide Microelectrodes for in Vitro Neuronal Interfacing , 2008, Front. Neuroeng..

[25]  John D. Simeral,et al.  Prediction of Imagined Single-Joint Movements in a Person With High-Level Tetraplegia , 2012, IEEE Transactions on Biomedical Engineering.

[26]  S. Badwal,et al.  Equivalent Circuit Analysis of the Impedance Response of Semiconductor/Electrolyte/Counterelectrode Cells , 1982 .

[27]  Kip A Ludwig,et al.  Tissue damage thresholds during therapeutic electrical stimulation , 2016, Journal of neural engineering.

[28]  Justin C. Sanchez,et al.  Corrosion of tungsten microelectrodes used in neural recording applications , 2011, Journal of Neuroscience Methods.

[29]  Excimer-laser deinsulation of Parylene-C coated Utah electrode array tips , 2012 .

[30]  Justin C. Sanchez,et al.  Abiotic-biotic characterization of Pt/Ir microelectrode arrays in chronic implants , 2014, Front. Neuroeng..

[31]  L. Hihara,et al.  Galvanic Corrosion and Localized Degradation of Aluminum-Matrix Composites Reinforced with Silicon Particulates , 2008 .

[32]  Michael J. Black,et al.  Neural control of cursor trajectory and click by a human with tetraplegia 1000 days after implant of an intracortical microelectrode array , 2011 .

[33]  James D. Weiland,et al.  Chronic neural stimulation with thin-film, iridium oxide electrodes , 2000, IEEE Trans. Biomed. Eng..

[34]  Florian Solzbacher,et al.  Long-Term Bilayer Encapsulation Performance of Atomic Layer Deposited Al $_{\bf 2}$O$_{\bf 3}$ and Parylene C for Biomedical Implantable Devices , 2013, IEEE Transactions on Biomedical Engineering.

[35]  William A Liberti,et al.  A carbon-fiber electrode array for long-term neural recording , 2013, Journal of neural engineering.

[36]  Hyeon-Bong Pyo,et al.  Wafer-scale fabrication of polymer-based microdevices via injection molding and photolithographic micropatterning protocols. , 2005, Analytical chemistry.

[37]  R. Normann,et al.  Chronic recording capability of the Utah Intracortical Electrode Array in cat sensory cortex , 1998, Journal of Neuroscience Methods.

[38]  E. M. Schmidt,et al.  Long-term chronic recording from cortical neurons , 1976, Experimental Neurology.

[39]  Bradley Greger,et al.  Approaches to a cortical vision prosthesis: implications of electrode size and placement , 2016, Journal of neural engineering.

[40]  Daryl R Kipke,et al.  Theoretical analysis of intracortical microelectrode recordings , 2011, Journal of neural engineering.

[41]  P. Tresco,et al.  A new high-density (25 electrodes/mm2) penetrating microelectrode array for recording and stimulating sub-millimeter neuroanatomical structures , 2013, Journal of neural engineering.

[42]  Huanan Zhang,et al.  Insertion of linear 8.4 μm diameter 16 channel carbon fiber electrode arrays for single unit recordings , 2015, Journal of neural engineering.

[43]  Jeffrey D. Schall,et al.  Review of signal distortion through metal microelectrode recording circuits and filters , 2008, Journal of Neuroscience Methods.

[44]  Rajmohan Bhandari,et al.  Effect of sputtering pressure on pulsed-DC sputtered iridium oxide films , 2009 .

[45]  Jason Silver,et al.  Noise and impedance of the SIROF utah electrode array , 2016, 2016 IEEE SENSORS.

[46]  Piet Bergveld,et al.  On the impedance of the silicon dioxide/electrolyte interface , 1983 .

[47]  P. Tresco,et al.  Response of brain tissue to chronically implanted neural electrodes , 2005, Journal of Neuroscience Methods.

[48]  J. Nadol,et al.  Foreign Body Response to Silicone in Cochlear Implant Electrodes in the Human. , 2017, Otology & neurotology : official publication of the American Otological Society, American Neurotology Society [and] European Academy of Otology and Neurotology.

[49]  K. E. Jones,et al.  A glass/silicon composite intracortical electrode array , 2006, Annals of Biomedical Engineering.

[50]  David J. Warren,et al.  An automated system for measuring tip impedance and among-electrode shunting in high-electrode count microelectrode arrays , 2009, Journal of Neuroscience Methods.

[51]  M. Prato,et al.  Carbon nanotube substrates boost neuronal electrical signaling. , 2005, Nano letters.

[52]  Paras R. Patel,et al.  Ultrasmall implantable composite microelectrodes with bioactive surfaces for chronic neural interfaces. , 2012, Nature materials.

[53]  K. Lyons,et al.  The importance of testing deep brain stimulation lead impedances before final lead implantation , 2011, Surgical neurology international.

[54]  Stuart F Cogan,et al.  Electrical performance of penetrating microelectrodes chronically implanted in cat cortex , 2011, EMBC.

[55]  F Solzbacher,et al.  A Wafer-Scale Etching Technique for High Aspect Ratio Implantable MEMS Structures. , 2010, Sensors and actuators. A, Physical.

[56]  Daryl R. Kipke,et al.  Wireless implantable microsystems: high-density electronic interfaces to the nervous system , 2004, Proceedings of the IEEE.

[57]  David C. Martin,et al.  Electrochemical deposition and characterization of poly(3,4-ethylenedioxythiophene) on neural microelectrode arrays , 2003 .

[58]  C. Stoldt,et al.  Galvanically coupled gold/silicon-on-insulator microstructures in hydrofluoric acid electrolytes: finite element simulation and morphological analysis of electrochemical corrosion , 2010 .

[59]  Stuart F Cogan,et al.  Plasma-enhanced chemical vapor deposited silicon carbide as an implantable dielectric coating. , 2003, Journal of biomedical materials research. Part A.

[60]  David J. Warren,et al.  Using multiple high-count electrode arrays in human median and ulnar nerves to restore sensorimotor function after previous transradial amputation of the hand , 2014, 2014 36th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[61]  S. B. Brummer,et al.  Electrical Stimulation with Pt Electrodes: II-Estimation of Maximum Surface Redox (Theoretical Non-Gassing) Limits , 1977, IEEE Transactions on Biomedical Engineering.

[62]  J. Randles Kinetics of rapid electrode reactions , 1947 .

[63]  Florian Solzbacher,et al.  Analysis of Al2O3—parylene C bilayer coatings and impact of microelectrode topography on long term stability of implantable neural arrays , 2017, Journal of neural engineering.

[64]  Daryl R Kipke,et al.  The insulation performance of reactive parylene films in implantable electronic devices. , 2009, Biomaterials.

[65]  N. Voelcker,et al.  Biocompatibility of porous silicon , 2018 .

[66]  Cindy X. Wang,et al.  In Vivo Validation of Custom-Designed Silicon-Based Microelectrode Arrays for Long-Term Neural Recording and Stimulation , 2012, IEEE Transactions on Biomedical Engineering.

[67]  G A Clark,et al.  Restoring motor control and sensory feedback in people with upper extremity amputations using arrays of 96 microelectrodes implanted in the median and ulnar nerves , 2016, Journal of neural engineering.

[68]  J.P. Donoghue,et al.  Reliability of signals from a chronically implanted, silicon-based electrode array in non-human primate primary motor cortex , 2005, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[69]  Andrew B. Schwartz,et al.  Brain-Controlled Interfaces: Movement Restoration with Neural Prosthetics , 2006, Neuron.

[70]  Luciano Fadiga,et al.  Carbon nanotube composite coating of neural microelectrodes preferentially improves the multiunit signal-to-noise ratio , 2011, Journal of neural engineering.

[71]  J. W. Schultze,et al.  Passivation and corrosion of microelectrode arrays , 1999 .