A regenerative microchannel neural interface for recording from and stimulating peripheral axons in vivo

Neural interfaces are implanted devices that couple the nervous system to electronic circuitry. They are intended for long term use to control assistive technologies such as muscle stimulators or prosthetics that compensate for loss of function due to injury. Here we present a novel design of interface for peripheral nerves. Recording from axons is complicated by the small size of extracellular potentials and the concentration of current flow at nodes of Ranvier. Confining axons to microchannels of ~100 µm diameter produces amplified potentials that are independent of node position. After implantation of microchannel arrays into rat sciatic nerve, axons regenerated through the channels forming 'mini-fascicles', each typically containing ~100 myelinated fibres and one or more blood vessels. Regenerated motor axons reconnected to distal muscles, as demonstrated by the recovery of an electromyogram and partial prevention of muscle atrophy. Efferent motor potentials and afferent signals evoked by muscle stretch or cutaneous stimulation were easily recorded from the mini-fascicles and were in the range of 35-170 µV. Individual motor units in distal musculature were activated from channels using stimulus currents in the microampere range. Microchannel interfaces are a potential solution for applications such as prosthetic limb control or enhancing recovery after nerve injury.

[1]  J. Hursh CONDUCTION VELOCITY AND DIAMETER OF NERVE FIBERS , 1939 .

[2]  R. Stein,et al.  Principles Underlying New Methods for Chronic Neural Recording , 1975, Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques.

[3]  R. S. Pickard,et al.  A review of printed circuit microelectrodes and their production , 1979, Journal of Neuroscience Methods.

[4]  David J. Edell,et al.  A Peripheral Nerve Information Transducer for Amputees: Long-Term Multichannel Recordings from Rabbit Peripheral Nerves , 1986, IEEE Transactions on Biomedical Engineering.

[5]  H. Schmalbruch,et al.  Fiber composition of the rat sciatic nerve , 1986, The Anatomical record.

[6]  J M Anderson,et al.  Inflammatory response to implants. , 1988, ASAIO transactions.

[7]  W.L.C. Rutten,et al.  Sensitivity and selectivity of intraneural stimulation using a silicon electrode array , 1991, IEEE Transactions on Biomedical Engineering.

[8]  G. Kovacs,et al.  Regeneration microelectrode array for peripheral nerve recording and stimulation , 1992, IEEE Transactions on Biomedical Engineering.

[9]  K. Najafi,et al.  Functional regeneration of glossopharyngeal nerve through micromachined sieve electrode arrays , 1992, Brain Research.

[10]  W. Grill,et al.  Selective control of muscle activation with a multipolar nerve cuff electrode , 1993, IEEE Transactions on Biomedical Engineering.

[11]  E. Lewis,et al.  Silicon-substrate microelectrode arrays for parallel recording of neural activity in peripheral and cranial nerves , 1994, IEEE Transactions on Biomedical Engineering.

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

[13]  T. A. Frieswijk,et al.  3D neuro-electronic interface devices for neuromuscular control: design studies and realisation steps. , 1995, Biosensors & bioelectronics.

[14]  M. Sahin,et al.  Selective recording with a multi-contact nerve cuff electrode , 1996, Proceedings of 18th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[15]  Ronald Raymond Riso,et al.  Performance of alternative amplifier configurations for tripolar nerve cuff recorded ENG , 1996, Proceedings of 18th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[16]  J.J. Struijk,et al.  Fascicle selective recording with a nerve cuff electrode , 1996, Proceedings of 18th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[17]  W. Grill,et al.  Quantification of recruitment properties of multiple contact cuff electrodes. , 1996, IEEE transactions on rehabilitation engineering : a publication of the IEEE Engineering in Medicine and Biology Society.

[18]  G. Lundborg,et al.  Rat sciatic nerve regeneration through a micromachined silicon chip. , 1997, Biomaterials.

[19]  K. Najafi,et al.  Long term chronic recordings from peripheral sensory fibers using a sieve electrode array , 1997, Journal of Neuroscience Methods.

[20]  J S Walter,et al.  Multielectrode nerve cuff stimulation of the median nerve produces selective movements in a raccoon animal model. , 1997, The journal of spinal cord medicine.

[21]  E. Valderrama,et al.  Stimulation and recording from regenerated peripheral nerves through polyimide sieve electrodes. , 1998, Journal of the peripheral nervous system : JPNS.

[22]  W.L.C. Rutten,et al.  Extracellular potentials from active myelinated fibers inside insulated and noninsulated peripheral nerve , 1998, IEEE Transactions on Biomedical Engineering.

[23]  H B Boom,et al.  Endoneural selective stimulating using wire-microelectrode arrays. , 1999, IEEE transactions on rehabilitation engineering : a publication of the IEEE Engineering in Medicine and Biology Society.

[24]  L. Wallman,et al.  Perforated silicon nerve chips with doped registration electrodes: in vitro performance and in vivo operation , 1999, IEEE Transactions on Biomedical Engineering.

[25]  Ken Yoshida,et al.  Intrafascicular electrodes for stimulation and recording from mudpuppy spinal roots , 2000, Journal of Neuroscience Methods.

[26]  Jeff Winter,et al.  An improved configuration for the reduction of EMG in electrode cuff recordings: a theoretical approach , 2000, IEEE Transactions on Biomedical Engineering.

[27]  A. Branner,et al.  A multielectrode array for intrafascicular recording and stimulation in sciatic nerve of cats , 2000, Brain Research Bulletin.

[28]  M. A. Johnson,et al.  Chronic recording of regenerating VIIIth nerve axons with a sieve electrode. , 2000, Journal of neurophysiology.

[29]  J Rozman,et al.  Selective recording of electroneurograms from the sciatic nerve of a dog with multi-electrode spiral cuffs. , 2000, The Japanese journal of physiology.

[30]  T Stieglitz,et al.  Selective fascicular stimulation of the rat sciatic nerve with multipolar polyimide cuff electrodes. , 2001, Restorative neurology and neuroscience.

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

[32]  Xavier Navarro,et al.  Functional impact of axonal misdirection after peripheral nerve injuries followed by graft or tube repair. , 2002, Journal of neurotrauma.

[33]  X. Navarro,et al.  Changes in crossed spinal reflexes after peripheral nerve injury and repair. , 2002, Journal of neurophysiology.

[34]  D. Durand,et al.  Functionally selective peripheral nerve stimulation with a flat interface nerve electrode , 2002, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[35]  Christian Hofer,et al.  A stimulator for functional activation of denervated muscles. , 2002, Artificial organs.

[36]  W. Rutten Selective electrical interfaces with the nervous system. , 2002, Annual review of biomedical engineering.

[37]  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.

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

[39]  Iasonas F. Triantis,et al.  On cuff imbalance and tripolar ENG amplifier configurations , 2005, IEEE Transactions on Biomedical Engineering.

[40]  Silvestro Micera,et al.  A critical review of interfaces with the peripheral nervous system for the control of neuroprostheses and hybrid bionic systems , 2005, Journal of the peripheral nervous system : JPNS.

[41]  Christian Hofer,et al.  Electrical stimulation of denervated muscles: first results of a clinical study. , 2005, Artificial organs.

[42]  P. Wehling,et al.  The influence of bacterial collagenase on regeneration of severed rat sciatic nerves , 2005, Acta Neurochirurgica.

[43]  G. E. Loeb,et al.  Analysis and microelectronic design of tubular electrode arrays intended for chronic, multiple singleunit recording from captured nerve fibres , 1977, Medical and Biological Engineering and Computing.

[44]  N. Lago,et al.  Design, in vitro and in vivo assessment of a multi-channel sieve electrode with integrated multiplexer , 2006, Journal of neural engineering.

[45]  K. Horch,et al.  An intrafascicular electrode for recording of action potentials in peripheral nerves , 2006, Annals of Biomedical Engineering.

[46]  Ken Yoshida,et al.  Assessment of Biocompatibility of Chronically Implanted Polyimide and Platinum Intrafascicular Electrodes , 2007, IEEE Transactions on Biomedical Engineering.

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

[48]  James W. Fawcett,et al.  Recording with microchannel electrodes in a noisy environment , 2008, 2008 30th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[49]  Jian Zhang,et al.  Recording and stimulating properties of chronically implanted longitudinal intrafascicular electrodes in peripheral fascicles in an animal model , 2008, Microsurgery.

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

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

[52]  James M. Anderson,et al.  Foreign body reaction to biomaterials. , 2008, Seminars in immunology.

[53]  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.

[54]  Bruce C Wheeler,et al.  Novel MEA platform with PDMS microtunnels enables the detection of action potential propagation from isolated axons in culture. , 2009, Lab on a chip.

[55]  Stéphanie P. Lacour,et al.  Microchannel Electrodes for Recording and Stimulation: In Vitro Evaluation , 2009, IEEE Transactions on Biomedical Engineering.

[56]  R. E. Cameron,et al.  Novel use of X-ray micro computed tomography to image rat sciatic nerve and integration into scaffold , 2010, Journal of Neuroscience Methods.

[57]  Wim L. C. Rutten,et al.  In vitro Verification of a 3-D Regenerative Neural Interface Design: Examination of Neurite Growth and Electrical Properties Within a Bifurcating Microchannel Structure , 2010, Proceedings of the IEEE.

[58]  T Stieglitz,et al.  Use of an Experimentally Derived Leadfield in the Peripheral Nerve Pathway Discrimination Problem , 2011, IEEE Transactions on Neural Systems and Rehabilitation Engineering.