Robust penetrating microelectrodes for neural interfaces realized by titanium micromachining

Neural prosthetic interfaces based upon penetrating microelectrode devices have broadened our understanding of the brain and have shown promise for restoring neurological functions lost to disease, stroke, or injury. However, the eventual viability of such devices for use in the treatment of neurological dysfunction may be ultimately constrained by the intrinsic brittleness of silicon, the material most commonly used for manufacture of penetrating microelectrodes. This brittleness creates predisposition for catastrophic fracture, which may adversely affect the reliability and safety of such devices, due to potential for fragmentation within the brain. Herein, we report the development of titanium-based penetrating microelectrodes that seek to address this potential future limitation. Titanium provides advantage relative to silicon due to its superior fracture toughness, which affords potential for creation of robust devices that are resistant to catastrophic failure. Realization of these devices is enabled by recently developed techniques which provide opportunity for fabrication of high-aspect-ratio micromechanical structures in bulk titanium substrates. Details are presented regarding the design, fabrication, mechanical testing, in vitro functional characterization, and preliminary in vivo testing of devices intended for acute recording in rat auditory cortex and thalamus, both independently and simultaneously.

[1]  D. Hubel,et al.  Laminar and columnar distribution of geniculo‐cortical fibers in the macaque monkey , 1972, The Journal of comparative neurology.

[2]  William D. Callister,et al.  Materials Science and Engineering: An Introduction , 1985 .

[3]  J. Winer,et al.  Patterns of reciprocity in auditory thalamocortical and corticothalamic connections: Study with horseradish peroxidase and autoradiographic methods in the rat medial geniculate body , 1987, The Journal of comparative neurology.

[4]  Khalil Najafi,et al.  Flexible miniature ribbon cables for long-term connection to implantable sensors , 1990 .

[5]  K. Najafi,et al.  Scaling limitations of silicon multichannel recording probes , 1990, IEEE Transactions on Biomedical Engineering.

[6]  W. Reichert,et al.  Polyimides as biomaterials: preliminary biocompatibility testing. , 1993, Biomaterials.

[7]  M. Nicolelis,et al.  Sensorimotor encoding by synchronous neural ensemble activity at multiple levels of the somatosensory system. , 1995, Science.

[8]  Erika E. Fanselow,et al.  Behavioral Modulation of Tactile Responses in the Rat Somatosensory System , 1999, The Journal of Neuroscience.

[9]  D. Kipke,et al.  Long-term neural recording characteristics of wire microelectrode arrays implanted in cerebral cortex. , 1999, Brain research. Brain research protocols.

[10]  T Stieglitz,et al.  Implantable microsystems. Polyimide-based neuroprostheses for interfacing nerves. , 1999, Medical device technology.

[11]  S. Senturia Microsystem Design , 2000 .

[12]  T. Stieglitz,et al.  Micromachined, Polyimide-Based Devices for Flexible Neural Interfaces , 2000 .

[13]  S. Campbell The Science and Engineering of Microelectronic Fabrication , 2001 .

[14]  M A Nicolelis,et al.  Thalamocortical and corticocortical interactions in the somatosensory system. , 2001, Progress in brain research.

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

[16]  T. Stieglitz,et al.  Flexible BIOMEMS with Electrode Arrangements on Front and Back Side as Key Component in Neural Prostheses and Biohybrid Systems , 2002 .

[17]  R W Guillery,et al.  The role of the thalamus in the flow of information to the cortex. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[18]  K. Mabuchi,et al.  A 3D flexible parylene probe array for multichannel neural recording , 2003, First International IEEE EMBS Conference on Neural Engineering, 2003. Conference Proceedings..

[19]  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.

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

[21]  S. Retterer,et al.  Controlling cellular reactive responses around neural prosthetic devices using peripheral and local intervention strategies , 2003, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[22]  Abu Samah Zuruzi,et al.  High-aspect-ratio bulk micromachining of titanium , 2004, Nature materials.

[23]  K. Mabuchi,et al.  3D flexible multichannel neural probe array , 2004 .

[24]  John K. Chapin,et al.  Ceramic-based multisite electrode arrays for chronic single-neuron recording , 2004, IEEE Transactions on Biomedical Engineering.

[25]  N. C. MacDonald,et al.  Inductively Coupled Plasma Etching of Bulk Titanium for MEMS Applications , 2005 .

[26]  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.

[27]  Karen A. Moxon,et al.  Nanostructured surface modification of ceramic-based microelectrodes to enhance biocompatibility for a direct brain-machine interface , 2004, IEEE Transactions on Biomedical Engineering.

[28]  Jiping He,et al.  Biocompatible benzocyclobutene (BCB)-based neural implants with micro-fluidic channel. , 2004, Biosensors & bioelectronics.

[29]  Sylvain Martel,et al.  Microelectrode array fabrication by electrical discharge machining and chemical etching , 2004, IEEE Transactions on Biomedical Engineering.

[30]  Justin C. Williams,et al.  Chronic neural recording using silicon-substrate microelectrode arrays implanted in cerebral cortex , 2004, IEEE Transactions on Biomedical Engineering.

[31]  Jiping He,et al.  Polyimide-based intracortical neural implant with improved structural stiffness , 2004 .

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

[33]  D. Kipke,et al.  Cortical microstimulation in auditory cortex of rat elicits best-frequency dependent behaviors , 2005, Journal of neural engineering.

[34]  G J Suaning,et al.  Fabrication of implantable microelectrode arrays by laser cutting of silicone rubber and platinum foil , 2005, Journal of neural engineering.

[35]  D. Kipke,et al.  Microstimulation in auditory cortex provides a substrate for detailed behaviors , 2005, Hearing Research.

[36]  Jack W. Judy,et al.  Multielectrode microprobes for deep-brain stimulation fabricated with a customizable 3-D electroplating process , 2005, IEEE Transactions on Biomedical Engineering.

[37]  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.

[38]  D. Kipke,et al.  Repeated voltage biasing improves unit recordings by reducing resistive tissue impedances , 2005, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

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

[40]  Michael S. Baker,et al.  An array of microactuated microelectrodes for monitoring single-neuronal activity in rodents , 2005, IEEE Transactions on Biomedical Engineering.

[41]  David C. Martin,et al.  Sustained release of dexamethasone from hydrophilic matrices using PLGA nanoparticles for neural drug delivery. , 2006, Biomaterials.

[42]  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.

[43]  Jon A. Mukand,et al.  Neuronal ensemble control of prosthetic devices by a human with tetraplegia , 2006, Nature.

[44]  G. Loeb,et al.  Visual sensations produced by intracortical microstimulation of the human occipital cortex , 1990, Medical and Biological Engineering and Computing.

[45]  Xinyan Tracy Cui,et al.  Electrochemically controlled release of dexamethasone from conducting polymer polypyrrole coated electrode. , 2006, Journal of controlled release : official journal of the Controlled Release Society.

[46]  Daryl R. Kipke,et al.  Voltage pulses change neural interface properties and improve unit recordings with chronically implanted microelectrodes , 2006, IEEE Transactions on Biomedical Engineering.

[47]  C. Meinhart,et al.  Bulk Micromachined Titanium Microneedles , 2007, Journal of Microelectromechanical Systems.

[48]  Daryl R Kipke,et al.  Complex impedance spectroscopy for monitoring tissue responses to inserted neural implants , 2007, Journal of neural engineering.

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

[50]  Ravi V. Bellamkonda,et al.  Dexamethasone-coated neural probes elicit attenuated inflammatory response and neuronal loss compared to uncoated neural probes , 2007, Brain Research.

[51]  Richard A Normann,et al.  Technology Insight: future neuroprosthetic therapies for disorders of the nervous system , 2007, Nature Clinical Practice Neurology.

[52]  Robert V Shannon,et al.  Audiologic Outcomes With the Penetrating Electrode Auditory Brainstem Implant , 2008, Otology & neurotology : official publication of the American Otological Society, American Neurotology Society [and] European Academy of Otology and Neurotology.

[53]  I. Fried,et al.  Internally Generated Reactivation of Single Neurons in Human Hippocampus During Free Recall , 2008, Science.

[54]  Daryl R Kipke,et al.  Advanced Neurotechnologies for Chronic Neural Interfaces: New Horizons and Clinical Opportunities , 2008, The Journal of Neuroscience.

[55]  Kunal J. Paralikar,et al.  Collagenase-Aided Intracortical Microelectrode Array Insertion: Effects on Insertion Force and Recording Performance , 2008, IEEE Transactions on Biomedical Engineering.

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

[57]  Mohammad Reza Abidian,et al.  Multifunctional Nanobiomaterials for Neural Interfaces , 2009 .

[58]  Kevin J. Otto,et al.  Thin-film silica sol–gel coatings for neural microelectrodes , 2009, Journal of Neuroscience Methods.

[59]  Patrick T. McCarthy,et al.  Titanium-based multi-channel, micro-electrode array for recording neural signals , 2009, 2009 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[60]  Ho-Yin Chan,et al.  A Novel Diamond Microprobe for Neuro-Chemical and -Electrical Recording in Neural Prosthesis , 2009, Journal of Microelectromechanical Systems.

[61]  Thomas Stieglitz,et al.  In vitro evaluation of the long-term stability of polyimide as a material for neural implants. , 2010, Biomaterials.

[62]  P T McCarthy,et al.  Simultaneous recording of rat auditory cortex and thalamus via a titanium-based, microfabricated, microelectrode device , 2011, Journal of neural engineering.