Regenerative Electrode Interfaces for Neural Prostheses.

Neural prostheses are electrode arrays implanted in the nervous system that record or stimulate electrical activity in neurons. Rapid growth in the use of neural prostheses in research and clinical applications has occurred in recent years, but instability and poor patency in the tissue-electrode interface undermines the longevity and performance of these devices. The application of tissue engineering strategies to the device interface is a promising approach to improve connectivity and communication between implanted electrodes and local neurons, and several research groups have developed new and innovative modifications to neural prostheses with the goal of seamless device-tissue integration. These approaches can be broadly categorized based on the strategy used to maintain and regenerate neurons at the device interface: (1) redesign of the prosthesis architecture to include finer-scale geometries and/or provide topographical cues to guide regenerating neural outgrowth, (2) incorporation of material coatings and bioactive molecules on the prosthesis to improve neuronal growth, viability, and adhesion, and (3) inclusion of cellular grafts to replenish the local neuron population or provide a target site for reinnervation (biohybrid devices). In addition to stabilizing the contact between neurons and electrodes, the potential to selectively interface specific subpopulations of neurons with individual electrode sites is a key advantage of regenerative interfaces. In this study, we review the development of regenerative interfaces for applications in both the peripheral and central nervous system. Current and future development of regenerative interfaces has the potential to improve the stability and selectivity of neural prostheses, improving the patency and resolution of information transfer between neurons and implanted electrodes.

[1]  D J Weber,et al.  In vivo effects of L1 coating on inflammation and neuronal health at the electrode-tissue interface in rat spinal cord and dorsal root ganglion. , 2012, Acta biomaterialia.

[2]  J. Csicsvari,et al.  Intracellular features predicted by extracellular recordings in the hippocampus in vivo. , 2000, Journal of neurophysiology.

[3]  F. Cui,et al.  Layer-by-layer assembly of polyelectrolyte films improving cytocompatibility to neural cells. , 2007, Journal of biomedical materials research. Part A.

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

[5]  Luca Citi,et al.  Restoring Natural Sensory Feedback in Real-Time Bidirectional Hand Prostheses , 2014, Science Translational Medicine.

[6]  M. Hortsch,et al.  The L1 Family of Neural Cell Adhesion Molecules: Old Proteins Performing New Tricks , 1996, Neuron.

[7]  Daryl R. Kipke,et al.  Conducting-polymer nanotubes improve electrical properties, mechanical adhesion, neural attachment, and neurite outgrowth of neural electrodes. , 2010, Small.

[8]  B. Botterman,et al.  Carbon nanotube coating improves neuronal recordings. , 2008, Nature nanotechnology.

[9]  D. Thompson,et al.  Electrical stimulation of schwann cells promotes sustained increases in neurite outgrowth. , 2013, Tissue engineering. Part A.

[10]  R. Stein,et al.  Regeneration Electrode Units: Implants for Recording from Single Peripheral Nerve Fibers in Freely Moving Animals , 1974, Science.

[11]  David C. Martin,et al.  Effect of Immobilized Nerve Growth Factor on Conductive Polymers: Electrical Properties and Cellular Response , 2007 .

[12]  Gordon G Wallace,et al.  Polypyrrole-coated electrodes for the delivery of charge and neurotrophins to cochlear neurons. , 2009, Biomaterials.

[13]  W. Rutten,et al.  In vivo testing of a 3D bifurcating microchannel scaffold inducing separation of regenerating axon bundles in peripheral nerves , 2013, Journal of neural engineering.

[14]  Melanie G. Urbanchek,et al.  Electrically stimulated signals from a long-term Regenerative Peripheral Nerve Interface , 2014, 2014 36th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[15]  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.

[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]  Wei Liu,et al.  Conductive single-walled carbon nanotube substrates modulate neuronal growth. , 2009, Nano letters.

[18]  U. Namgung.  The Role of Schwann Cell-Axon Interaction in Peripheral Nerve Regeneration , 2015, Cells Tissues Organs.

[19]  Jummi Laishram,et al.  Carbon Nanotube Scaffolds Tune Synaptic Strength in Cultured Neural Circuits: Novel Frontiers in Nanomaterial–Tissue Interactions , 2011, The Journal of Neuroscience.

[20]  Nicolas Y. Masse,et al.  Reach and grasp by people with tetraplegia using a neurally controlled robotic arm , 2012, Nature.

[21]  Danielle R. Bogdanowicz,et al.  Single-walled carbon nanotubes alter Schwann cell behavior differentially within 2D and 3D environments. , 2011, Journal of biomedical materials research. Part A.

[22]  Nicholas B Langhals,et al.  Regenerative Peripheral Nerve Interface Viability and Signal Transduction with an Implanted Electrode , 2014, Plastic and reconstructive surgery.

[23]  T. Stieglitz,et al.  A biohybrid system to interface peripheral nerves after traumatic lesions: design of a high channel sieve electrode. , 2002, Biosensors & bioelectronics.

[24]  P. Kennedy,et al.  Neurotrophic electrode: Method of assembly and implantation into human motor speech cortex , 2008, Journal of Neuroscience Methods.

[25]  Stéphanie P. Lacour,et al.  Microchannels as Axonal Amplifiers , 2008, IEEE Transactions on Biomedical Engineering.

[26]  Gerhard Friehs,et al.  Intra-day signal instabilities affect decoding performance in an intracortical neural interface system , 2013, Journal of neural engineering.

[27]  M. Morrell.  Responsive cortical stimulation for the treatment of medically intractable partial epilepsy , 2011, Neurology.

[28]  S. Haber,et al.  Closed-Loop Deep Brain Stimulation Is Superior in Ameliorating Parkinsonism , 2011, Neuron.

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

[30]  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.

[31]  N. Lago,et al.  Long term assessment of axonal regeneration through polyimide regenerative electrodes to interface the peripheral nerve. , 2005, Biomaterials.

[32]  P. Kennedy,et al.  Activity of single action potentials in monkey motor cortex during long-term task learning , 1997, Brain Research.

[33]  Daniel J Chew,et al.  High sensitivity recording of afferent nerve activity using ultra-compliant microchannel electrodes: an acute in vivo validation , 2012, Journal of neural engineering.

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

[35]  Erdrin Azemi,et al.  Seeding neural progenitor cells on silicon-based neural probes. , 2010, Journal of neurosurgery.

[36]  Daryl R. Kipke,et al.  Flavopiridol reduces the impedance of neural prostheses in vivo without affecting recording quality , 2009, Journal of Neuroscience Methods.

[37]  Carl F. Lagenaur,et al.  The surface immobilization of the neural adhesion molecule L1 on neural probes and its effect on neuronal density and gliosis at the probe/tissue interface. , 2011, Biomaterials.

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

[39]  Stephen O'Leary,et al.  The effect of polypyrrole with incorporated neurotrophin-3 on the promotion of neurite outgrowth from auditory neurons. , 2007, Biomaterials.

[40]  Nigel H Lovell,et al.  Impact of co-incorporating laminin peptide dopants and neurotrophic growth factors on conducting polymer properties. , 2010, Acta biomaterialia.

[41]  Daryl R Kipke,et al.  Alginate composition effects on a neural stem cell-seeded scaffold. , 2009, Tissue engineering. Part C, Methods.

[42]  Xavier Navarro,et al.  Neurobiological Assessment of Regenerative Electrodes for Bidirectional Interfacing Injured Peripheral Nerves , 2007, IEEE Transactions on Biomedical Engineering.

[43]  M. Abidian,et al.  Conducting‐Polymer Nanotubes for Controlled Drug Release , 2006, Advanced materials.

[44]  Liang Guo,et al.  Regenerative microchannel electrode array for peripheral nerve interfacing , 2011, 2011 5th International IEEE/EMBS Conference on Neural Engineering.

[45]  O. B. Ozdoganlar,et al.  Chronic tissue response to carboxymethyl cellulose based dissolvable insertion needle for ultra-small neural probes. , 2014, Biomaterials.

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

[47]  K. M. Chan,et al.  Improving peripheral nerve regeneration: From molecular mechanisms to potential therapeutic targets , 2014, Experimental Neurology.

[48]  J. Fawcett,et al.  Long Micro-Channel Electrode Arrays: A Novel Type of Regenerative Peripheral Nerve Interface , 2009, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[49]  M. C. Rodrigues,et al.  Peripheral Nerve Repair with Cultured Schwann Cells: Getting Closer to the Clinics , 2012, TheScientificWorldJournal.

[50]  P. Kennedy.  The cone electrode: a long-term electrode that records from neurites grown onto its recording surface , 1989, Journal of Neuroscience Methods.

[51]  Daniel C Millard,et al.  Microchannel-based regenerative scaffold for chronic peripheral nerve interfacing in amputees. , 2015, Biomaterials.

[52]  David J. Anderson,et al.  Novel multi-sided, microelectrode arrays for implantable neural applications , 2011, Biomedical microdevices.

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

[54]  G. Wallace,et al.  Conducting polymers for neural interfaces: challenges in developing an effective long-term implant. , 2008, Biomaterials.

[55]  Douglas J. Bakkum,et al.  Revealing neuronal function through microelectrode array recordings , 2015, Front. Neurosci..

[56]  A. Michael,et al.  Brain Tissue Responses to Neural Implants Impact Signal Sensitivity and Intervention Strategies , 2014, ACS chemical neuroscience.

[57]  Michelle K. Leach,et al.  Combining topographical and genetic cues to promote neuronal fate specification in stem cells. , 2012, Biomacromolecules.

[58]  Florian Solzbacher,et al.  A comparison of the tissue response to chronically implanted Parylene-C-coated and uncoated planar silicon microelectrode arrays in rat cortex. , 2010, Biomaterials.

[59]  William R. Stauffer,et al.  Surface immobilization of neural adhesion molecule L1 for improving the biocompatibility of chronic neural probes: In vitro characterization. , 2008, Acta biomaterialia.

[60]  K. Najafi,et al.  A micromachined silicon sieve electrode for nerve regeneration applications , 1994, IEEE Transactions on Biomedical Engineering.

[61]  Yuliang Cao,et al.  Electrodeposited polypyrrole/carbon nanotubes composite films electrodes for neural interfaces. , 2010, Biomaterials.

[62]  Wei He,et al.  Nanoscale neuro-integrative coatings for neural implants. , 2005, Biomaterials.

[63]  C. Avendaño,et al.  Fiber composition of the rat sciatic nerve and its modification during regeneration through a sieve electrode , 2008, Brain Research.

[64]  R. Bellamkonda,et al.  Stabilizing electrode-host interfaces: a tissue engineering approach. , 2001, Journal of rehabilitation research and development.

[65]  G. Lundborg,et al.  Vascular Endothelial Growth Factor Has Neurotrophic Activity and Stimulates Axonal Outgrowth, Enhancing Cell Survival and Schwann Cell Proliferation in the Peripheral Nervous System , 1999, The Journal of Neuroscience.

[66]  P. Rossini,et al.  Double nerve intraneural interface implant on a human amputee for robotic hand control , 2010, Clinical Neurophysiology.

[67]  E K Purcell,et al.  In vivo evaluation of a neural stem cell-seeded prosthesis , 2009, Journal of neural engineering.

[68]  Nigel H Lovell,et al.  Cell attachment functionality of bioactive conducting polymers for neural interfaces. , 2009, Biomaterials.

[69]  M. Brenner,et al.  Update in facial nerve paralysis: tissue engineering and new technologies , 2014, Current opinion in otolaryngology & head and neck surgery.

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

[71]  Jae Young Lee,et al.  Polypyrrole-coated electrospun PLGA nanofibers for neural tissue applications. , 2009, Biomaterials.

[72]  Kasey Catt,et al.  Evaluation of poly(3,4-ethylenedioxythiophene)/carbon nanotube neural electrode coatings for stimulation in the dorsal root ganglion , 2015, Journal of neural engineering.

[73]  Vikash Gilja,et al.  Long-term Stability of Neural Prosthetic Control Signals from Silicon Cortical Arrays in Rhesus Macaque Motor Cortex , 2010 .

[74]  P. Tresco,et al.  A strategy to passively reduce neuroinflammation surrounding devices implanted chronically in brain tissue by manipulating device surface permeability. , 2015, Biomaterials.

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

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

[77]  Darren M. Whiten,et al.  Histopathology of human cochlear implants: Correlation of psychophysical and anatomical measures , 2005, Hearing Research.

[78]  Fan-Gang Zeng,et al.  Cochlear Implants: System Design, Integration, and Evaluation , 2008, IEEE Reviews in Biomedical Engineering.

[79]  J. Fawcett,et al.  Polyimide micro-channel arrays for peripheral nerve regenerative implants , 2008 .

[80]  Mario I. Romero-Ortega,et al.  Modality-Specific Axonal Regeneration: Toward Selective Regenerative Neural Interfaces , 2011, Front. Neuroeng..

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

[82]  Stefanie Dimmeler,et al.  Translational strategies and challenges in regenerative medicine , 2014, Nature Medicine.

[83]  M. Keith,et al.  A neural interface provides long-term stable natural touch perception , 2014, Science Translational Medicine.

[84]  L. Carin,et al.  Relationship between intracortical electrode design and chronic recording function. , 2013, Biomaterials.

[85]  Christine E. Schmidt,et al.  Conducting polymers in biomedical engineering , 2007 .

[86]  Barbara Canlon,et al.  Protection of auditory neurons from aminoglycoside toxicity by neurotrophin-3 , 1996, Nature Medicine.

[87]  Wei He,et al.  Nanoscale laminin coating modulates cortical scarring response around implanted silicon microelectrode arrays , 2006, Journal of neural engineering.

[88]  P. Kennedy,et al.  The cone electrode: Ultrastructural studies following long-term recording in rat and monkey cortex , 1992, Neuroscience Letters.

[89]  Joshua H. Jennings,et al.  Tools for Resolving Functional Activity and Connectivity within Intact Neural Circuits , 2014, Current Biology.

[90]  Christine E Schmidt,et al.  Nerve growth factor-immobilized polypyrrole: bioactive electrically conducting polymer for enhanced neurite extension. , 2007, Journal of biomedical materials research. Part A.