Neural interfaces based on amorphous silicon carbide ultramicroelectrode arrays

Size and material considerations are important in the development of next-generation chronically reliable neural interface devices. In this review, we discuss the use of amorphous silicon carbide (a-SiC) for the fabrication of indwelling electrode arrays with ultrathin penetrating shanks for neural stimulation and recording. The a-SiC film is stable in saline environments and has a high intrinsic stiffness that allows fabrication of tissue-penetrating arrays with extremely small cross-sectional areas (<60 μm2). Present literature on arrays with extremely small shanks and/or ultramicroelectrode (UME) sites are reviewed. Properties of a-SiC films and their current biomedical applications are summarized. Reduced shank dimensions increase the flexibility of high Young's modulus a-SiC arrays. Iridium oxide-coated UMEs had electrochemical properties suitable for neural recording and stimulation, and recorded neural signals with high amplitudes and high signal-to-noise ratios. UMEs and a-SiC may provide a platform for next-generation high-density chronic neural interface devices.

[1]  Richard Everly,et al.  Demonstration of a Robust All-Silicon-Carbide Intracortical Neural Interface , 2018, Micromachines.

[2]  Hanlin Zhu,et al.  Nanofabricated Ultraflexible Electrode Arrays for High‐Density Intracortical Recording , 2018, Advanced science.

[3]  S. Cogan,et al.  Amorphous silicon carbide ultramicroelectrode arrays for neural stimulation and recording , 2018, Journal of neural engineering.

[4]  S. Cogan,et al.  Electrodeposited Iridium Oxide on Carbon Fiber Ultramicroelectrodes for Neural Recording and Stimulation , 2018 .

[5]  Stuart F Cogan,et al.  Thinking Small: Progress on Microscale Neurostimulation Technology , 2017, Neuromodulation : journal of the International Neuromodulation Society.

[6]  A. Iacopi,et al.  Superior Robust Ultrathin Single-Crystalline Silicon Carbide Membrane as a Versatile Platform for Biological Applications. , 2017, ACS applied materials & interfaces.

[7]  Sergey L. Gratiy,et al.  Fully integrated silicon probes for high-density recording of neural activity , 2017, Nature.

[8]  D. Raz-Prag,et al.  Electrical stimulation of different retinal components and the effect of asymmetric pulses , 2017, Journal of Neuroscience Methods.

[9]  Loredana Zollo,et al.  Invasive Intraneural Interfaces: Foreign Body Reaction Issues , 2017, Front. Neurosci..

[10]  J M Carmena,et al.  A silicon carbide array for electrocorticography and peripheral nerve recording , 2017, Journal of neural engineering.

[11]  B. Trafford Low-cost private schools , 2017 .

[12]  Khalil B. Ramadi,et al.  Characterization of Mechanically Matched Hydrogel Coatings to Improve the Biocompatibility of Neural Implants , 2017, Scientific Reports.

[13]  Francis R. Willett,et al.  Restoration of reaching and grasping in a person with tetraplegia through brain-controlled muscle stimulation: a proof-of-concept demonstration , 2017, The Lancet.

[14]  S. Cogan Conductive and Insulative Materials , 2017 .

[15]  Felix Deku,et al.  Carbon fiber on polyimide ultra-microelectrodes , 2017, bioRxiv.

[16]  A Cutrone,et al.  Long-term usability and bio-integration of polyimide-based intra-neural stimulating electrodes. , 2017, Biomaterials.

[17]  Jose M. Carmena,et al.  Emergence of Coordinated Neural Dynamics Underlies Neuroprosthetic Learning and Skillful Control , 2017, Neuron.

[18]  J. J. Siegel,et al.  Ultraflexible nanoelectronic probes form reliable, glial scar–free neural integration , 2017, Science Advances.

[19]  N. Ramsey,et al.  Fully Implanted Brain-Computer Interface in a Locked-In Patient with ALS. , 2016, The New England journal of medicine.

[20]  Leigh R. Hochberg,et al.  Retrospectively supervised click decoder calibration for self-calibrating point-and-click brain–computer interfaces , 2016, Journal of Physiology-Paris.

[21]  Eduardo Fernandez,et al.  Clinical applications of penetrating neural interfaces and Utah Electrode Array technologies , 2016, Journal of neural engineering.

[22]  Stephen T. Foldes,et al.  Intracortical microstimulation of human somatosensory cortex , 2016, Science Translational Medicine.

[23]  Huanan Zhang,et al.  Chronic in vivo stability assessment of carbon fiber microelectrode arrays , 2016, Journal of neural engineering.

[24]  L. Nathan Perkins,et al.  Unstable neurons underlie a stable learned behavior , 2016, Nature Neuroscience.

[25]  Ellis Meng,et al.  Flexible, Penetrating Brain Probes Enabled by Advances in Polymer Microfabrication , 2016, Micromachines.

[26]  Christopher L. Frewin,et al.  Invited) Silicon Carbide as a Robust Neural Interface , 2016 .

[27]  Stuart F. Cogan,et al.  In vivo Characterization of Amorphous Silicon Carbide As a Biomaterial for Chronic Neural Interfaces , 2016, Front. Neurosci..

[28]  Daniel Palanker,et al.  SiC protective coating for photovoltaic retinal prosthesis , 2016, Journal of neural engineering.

[29]  A. Jackson,et al.  Mechanical Flexibility Reduces the Foreign Body Response to Long-Term Implanted Microelectrodes in Rabbit Cortex , 2016, bioRxiv.

[30]  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.

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

[32]  S. Cogan,et al.  Amorphous Silicon Carbide for Neural Interface Applications , 2016 .

[33]  István Ulbert,et al.  A Multimodal, SU-8 - Platinum - Polyimide Microelectrode Array for Chronic In Vivo Neurophysiology , 2015, PloS one.

[34]  John P. Cunningham,et al.  Single-trial dynamics of motor cortex and their applications to brain-machine interfaces , 2015, Nature Communications.

[35]  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.

[36]  R. Andersen,et al.  Decoding motor imagery from the posterior parietal cortex of a tetraplegic human , 2015, Science.

[37]  J. Muthuswamy,et al.  Compliant intracortical implants reduce strains and strain rates in brain tissue in vivo , 2015, Journal of neural engineering.

[38]  Winnie Jensen,et al.  Subchronic stimulation performance of transverse intrafascicular multichannel electrodes in the median nerve of the Göttingen minipig. , 2015, Artificial organs.

[39]  D. S. Freedman,et al.  Chronic tissue response to untethered microelectrode implants in the rat brain and spinal cord , 2015, Journal of neural engineering.

[40]  X Tracy Cui,et al.  Effects of caspase-1 knockout on chronic neural recording quality and longevity: insight into cellular and molecular mechanisms of the reactive tissue response. , 2014, Biomaterials.

[41]  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.

[42]  G A Clark,et al.  The foreign body response to the Utah Slant Electrode Array in the cat sciatic nerve. , 2014, Acta biomaterialia.

[43]  Jessica K. Nguyen,et al.  Mechanically-compliant intracortical implants reduce the neuroinflammatory response , 2014, Journal of neural engineering.

[44]  R. Bellamkonda,et al.  The effect of inflammatory cell-derived MCP-1 loss on neuronal survival during chronic neuroinflammation. , 2014, Biomaterials.

[45]  S. Micera,et al.  Development, manufacturing and application of double-sided flexible implantable microelectrodes , 2014, Biomedical microdevices.

[46]  Thomas Stieglitz,et al.  Blood pressure control with selective vagal nerve stimulation and minimal side effects , 2014, Journal of neural engineering.

[47]  Stuart N. Baker,et al.  Newcastle University Eprints Date Deposited: 23 the Sinusoidal Probe: a New Approach to Improve Electrode Longevity , 2022 .

[48]  Srikanth Vasudevan,et al.  Thiol-ene/acrylate substrates for softening intracortical electrodes. , 2014, Journal of biomedical materials research. Part B, Applied biomaterials.

[49]  J. Donoghue,et al.  Failure mode analysis of silicon-based intracortical microelectrode arrays in non-human primates , 2013, Journal of neural engineering.

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

[51]  Mark L. Homer,et al.  Sensors and decoding for intracortical brain computer interfaces. , 2013, Annual review of biomedical engineering.

[52]  Garrett B Stanley,et al.  The impact of chronic blood-brain barrier breach on intracortical electrode function. , 2013, Biomaterials.

[53]  Brian J. Kim,et al.  3D Parylene sheath neural probe for chronic recordings , 2013, Journal of neural engineering.

[54]  Rosa Villa,et al.  SU-8 based microprobes for simultaneous neural depth recording and drug delivery in the brain. , 2013, Lab on a chip.

[55]  M. Stutzmann,et al.  Organic functionalization of 3C-SiC surfaces. , 2013, ACS applied materials & interfaces.

[56]  M. Spira,et al.  Multi-electrode array technologies for neuroscience and cardiology. , 2013, Nature nanotechnology.

[57]  Brian J. Kim,et al.  Novel flexible Parylene neural probe with 3D sheath structure for enhancing tissue integration. , 2013, Lab on a chip.

[58]  Xavier Navarro,et al.  Interfaces with the peripheral nerve for the control of neuroprostheses. , 2013, International review of neurobiology.

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

[60]  Joshua A. Smith,et al.  Role of pro-inflammatory cytokines released from microglia in neurodegenerative diseases , 2012, Brain Research Bulletin.

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

[62]  James P. Harris,et al.  Mechanically adaptive intracortical implants improve the proximity of neuronal cell bodies , 2011, Journal of neural engineering.

[63]  Hui-ji Shi,et al.  Mechanical Properties of Amorphous Silicon Carbide , 2011 .

[64]  K. Horch,et al.  Object Discrimination With an Artificial Hand Using Electrical Stimulation of Peripheral Tactile and Proprioceptive Pathways With Intrafascicular Electrodes , 2011, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[65]  James P. Harris,et al.  In vivo deployment of mechanically adaptive nanocomposites for intracortical microelectrodes , 2011, Journal of neural engineering.

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

[67]  Patrick A Tresco,et al.  Reducing surface area while maintaining implant penetrating profile lowers the brain foreign body response to chronically implanted planar silicon microelectrode arrays. , 2011, Progress in brain research.

[68]  D R Kipke,et al.  Reduction of neurovascular damage resulting from microelectrode insertion into the cerebral cortex using in vivo two-photon mapping , 2010, Journal of neural engineering.

[69]  Patrick A Tresco,et al.  Quantitative analysis of the tissue response to chronically implanted microwire electrodes in rat cortex. , 2010, Biomaterials.

[70]  C. Marin,et al.  Biocompatibility of Intracortical Microelectrodes: Current Status and Future Prospects , 2010, Front. Neuroeng..

[71]  A. Levey,et al.  Implanted neural electrodes cause chronic, local inflammation that is correlated with local neurodegeneration , 2009, Journal of neural engineering.

[72]  Y. Chen,et al.  Design and fabrication of a polyimide-based microelectrode array: Application in neural recording and repeatable electrolytic lesion in rat brain , 2009, Journal of Neuroscience Methods.

[73]  M. Ward,et al.  Toward a comparison of microelectrodes for acute and chronic recordings , 2009, Brain Research.

[74]  S. Cogan,et al.  Sputtered iridium oxide films for neural stimulation electrodes. , 2009, Journal of biomedical materials research. Part B, Applied biomaterials.

[75]  B A Wester,et al.  Development and characterization of in vivo flexible electrodes compatible with large tissue displacements , 2009, Journal of neural engineering.

[76]  P. Renaud,et al.  Demonstration of cortical recording using novel flexible polymer neural probes , 2008 .

[77]  Ciprian Iliescu,et al.  PECVD amorphous silicon carbide membranes for cell culturing , 2008 .

[78]  W. Reichert Indwelling Neural Implants : Strategies for Contending with the In Vivo Environment , 2007 .

[79]  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.

[80]  D. Kipke,et al.  Neural probe design for reduced tissue encapsulation in CNS. , 2007, Biomaterials.

[81]  J. Muthuswamy,et al.  Thin microelectrodes reduce GFAP expression in the implant site in rodent somatosensory cortex , 2007, Journal of neural engineering.

[82]  P. Turchi,et al.  Simulations of the mechanical properties of crystalline, nanocrystalline, and amorphous SiC and Si , 2007 .

[83]  K. Cheung Implantable microscale neural interfaces , 2007, Biomedical microdevices.

[84]  R. Wightman,et al.  Conical tungsten tips as substrates for the preparation of ultramicroelectrodes. , 2006, Langmuir : the ACS journal of surfaces and colloids.

[85]  S.F. Cogan In vivo and In vitro Differences in the Charge-injection and Electrochemical Properties of Iridium Oxide Electrodes , 2006, 2006 International Conference of the IEEE Engineering in Medicine and Biology Society.

[86]  E. Chichilnisky,et al.  Electrical stimulation of mammalian retinal ganglion cells with multielectrode arrays. , 2006, Journal of neurophysiology.

[87]  Winnie Jensen,et al.  In-vivo implant mechanics of flexible, silicon-based ACREO microelectrode arrays in rat cerebral cortex , 2006, IEEE Transactions on Biomedical Engineering.

[88]  G.S. Dhillon,et al.  Direct neural sensory feedback and control of a prosthetic arm , 2005, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

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

[90]  David C. Martin,et al.  A finite-element model of the mechanical effects of implantable microelectrodes in the cerebral cortex , 2005, Journal of neural engineering.

[91]  David C. Martin,et al.  Neuronal cell loss accompanies the brain tissue response to chronically implanted silicon microelectrode arrays , 2005, Experimental Neurology.

[92]  K. Mabuchi,et al.  Parylene flexible neural probes integrated with microfluidic channels. , 2005, Lab on a chip.

[93]  K. Horch,et al.  Residual function in peripheral nerve stumps of amputees: implications for neural control of artificial limbs. , 2004, The Journal of hand surgery.

[94]  P. Renaud,et al.  Flexible polyimide probes with microelectrodes and embedded microfluidic channels for simultaneous drug delivery and multi-channel monitoring of bioelectric activity. , 2004, Biosensors & bioelectronics.

[95]  G. Buzsáki Large-scale recording of neuronal ensembles , 2004, Nature Neuroscience.

[96]  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.

[97]  P. Hugenholtz,et al.  Silicon carbide‐coated stents in patients with acute coronary syndrome , 2003, Catheterization and cardiovascular interventions : official journal of the Society for Cardiac Angiography & Interventions.

[98]  D. Szarowski,et al.  Brain responses to micro-machined silicon devices , 2003, Brain Research.

[99]  Joseph F Rizzo,et al.  Thresholds for activation of rabbit retinal ganglion cells with an ultrafine, extracellular microelectrode. , 2003, Investigative ophthalmology & visual science.

[100]  James D. Weiland,et al.  In vitro electrical properties for iridium oxide versus titanium nitride stimulating electrodes , 2002, IEEE Transactions on Biomedical Engineering.

[101]  S.F. Cogan,et al.  Electrodeposited iridium oxide for neural stimulation and recording electrodes , 2001, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[102]  Justin C. Williams,et al.  Flexible polyimide-based intracortical electrode arrays with bioactive capability , 2001, IEEE Transactions on Biomedical Engineering.

[103]  J. Rizzo,et al.  Multi-electrode stimulation and recording in the isolated retina , 2000, Journal of Neuroscience Methods.

[104]  E. Zrenner,et al.  Electrical multisite stimulation of the isolated chicken retina , 2000, Vision Research.

[105]  Mehran Mehregany,et al.  SiC MEMS: Opportunities and challenges for applications in harsh environments , 1999 .

[106]  E. Zrenner,et al.  Can subretinal microphotodiodes successfully replace degenerated photoreceptors? , 1999, Vision Research.

[107]  Chang Liu,et al.  Re-configurable fluid circuits by PDMS elastomer micromachining , 1999, Technical Digest. IEEE International MEMS 99 Conference. Twelfth IEEE International Conference on Micro Electro Mechanical Systems (Cat. No.99CH36291).

[108]  E. Gat,et al.  Characterization of the elastic properties of amorphous silicon carbide thin films by acoustic microscopy , 1997 .

[109]  J. Kieffer,et al.  Hardness and Young’s modulus of amorphous a-SiC thin films determined by nanoindentation and bulge tests , 1994 .

[110]  J. Heinze Ultramicroelectrodes in Electrochemistry , 1993 .

[111]  K. Horch,et al.  Muscle recruitment with intrafascicular electrodes , 1991, IEEE Transactions on Biomedical Engineering.

[112]  M. Fleischmann,et al.  The application of microelectrodes to the study of homogeneous processes coupled to electrode reactions: Part I. EC′ and CE reactions , 1984 .

[113]  Microvoltammetric electrodes. , 1981, Analytical chemistry.

[114]  W. Dawson,et al.  Evaluation of Microelectrodes Chronically Implanted on the Retina , 1977 .

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

[116]  W. Pitt,et al.  The effect of the beta-adrenergic antagonist propranolol on rabbit atrial cells with the use of the ultramicroelectrode technique. , 1968, American heart journal.