Fascicular nerve stimulation and recording using a novel double-aisle regenerative electrode

OBJECTIVE As artificial prostheses become more refined, they are most often used as a therapeutic option for hand amputation. By contrast to extra- or intraneural interfaces, regenerative nerve electrodes are designed to enable electrical interfaces with regrowing axonal bundles of injured nerves, aiming to achieve high selectivity for recording and stimulation. However, most of the developed designs pose an obstacle to the regrowth mechanisms due to low transparency and cause impairment to the nerve regeneration. APPROACH Here we present the double-aisle electrode, a new type of highly transparent, non-obstructive regenerative electrode. Using a double-side thin-film polyimide planar multi-contact electrode, two nerve fascicles can regenerate without physical impairment through two electrically isolated aisles. MAIN RESULTS We show that this electrode can be used to selectively record and stimulate fascicles, acutely as well as chronically, and allow regeneration in nerve gaps of several millimeters without impairment. SIGNIFICANCE This multi-aisle regenerative electrode may be suitable for neuroprosthetic applications, such as prostheses, for the restoration of hand function after amputation or severe nerve injuries.

[1]  S. J. Kim,et al.  Functional Regeneration of a Severed Peripheral Nerve With a 7‐mm Gap in Rats Through the Use of An Implantable Electrical Stimulator and a Conduit Electrode With Collagen Coating , 2010, Neuromodulation : journal of the International Neuromodulation Society.

[2]  Nitish V. Thakor,et al.  Classification of phases of hand grasp task by the extraction of miniature compound nerve action potentials (mCNAPs) , 2015, 2015 7th International IEEE/EMBS Conference on Neural Engineering (NER).

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

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

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

[6]  G. Lundborg,et al.  In Vivo Regeneration of Cut Nerves Encased in Silicone Tubes: Growth across a Six‐millimeter Gap , 1982, Journal of neuropathology and experimental neurology.

[7]  Silvestro Micera,et al.  Chronic multichannel neural recordings from soft regenerative microchannel electrodes during gait , 2015, Scientific Reports.

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

[9]  S. Micera,et al.  Preferential Enhancement of Sensory and Motor Axon Regeneration by Combining Extracellular Matrix Components with Neurotrophic Factors , 2016, International journal of molecular sciences.

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

[11]  Nitish V. Thakor,et al.  Neural prosthesis for motor function restoration in upper limb extremity , 2014, 2014 IEEE Biomedical Circuits and Systems Conference (BioCAS) Proceedings.

[12]  Shih-Cheng Yen,et al.  A Bionic Neural Link for peripheral nerve repair , 2012, 2012 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[13]  X Navarro,et al.  Histologic assessment of sciatic nerve regeneration following resection and graft or tube repair in the mouse. , 1996, Restorative neurology and neuroscience.

[14]  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.

[15]  T. Kuiken,et al.  Neural Interfaces for Control of Upper Limb Prostheses: The State of the Art and Future Possibilities , 2011, PM & R : the journal of injury, function, and rehabilitation.

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

[17]  T. Brushart,et al.  Joseph H. Boyes Award. Dispersion of regenerating axons across enclosed neural gaps. , 1995, The Journal of hand surgery.

[18]  A. Valero-Cabré,et al.  Superior muscle reinnervation after autologous nerve graft or poly‐L‐lactide‐ϵ‐caprolactone (PLC) tube implantation in comparison to silicone tube repair , 2001, Journal of neuroscience research.

[19]  Keith P. Myers,et al.  Ethical considerations in elective amputation after traumatic peripheral nerve injuries , 2014, Neurology. Clinical practice.

[20]  Silvestro Micera,et al.  On the identification of sensory information from mixed nerves by using single-channel cuff electrodes , 2009, Journal of NeuroEngineering and Rehabilitation.

[21]  C. Azevedo-Coste,et al.  Comparative analysis of transverse intrafascicular multichannel, longitudinal intrafascicular and multipolar cuff electrodes for the selective stimulation of nerve fascicles , 2011, Journal of neural engineering.

[22]  S. Micera,et al.  A three-dimensional self-opening intraneural peripheral interface (SELINE) , 2015, Journal of neural engineering.

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

[24]  Luca Citi,et al.  On the use of wavelet denoising and spike sorting techniques to process electroneurographic signals recorded using intraneural electrodes , 2008, Journal of Neuroscience Methods.

[25]  Dario Farina,et al.  Elective amputation and bionic substitution restore functional hand use after critical soft tissue injuries , 2016, Scientific Reports.

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

[27]  Loredana Zollo,et al.  Literature Review on Needs of Upper Limb Prosthesis Users , 2016, Front. Neurosci..

[28]  Nicholas B Langhals,et al.  Regenerative Electrode Interfaces for Neural Prostheses. , 2016, Tissue engineering. Part B, Reviews.

[29]  A. Chong,et al.  Early Clinical Experience With Collagen Nerve Tubes in Digital Nerve Repair , 2009 .

[30]  T Laurell,et al.  The geometric design of micromachined silicon sieve electrodes influences functional nerve regeneration. , 2001, Biomaterials.

[31]  Xavier Navarro,et al.  Fascicular Topography of the Human Median Nerve for Neuroprosthetic Surgery , 2016, Front. Neurosci..

[32]  Nitish V. Thakor,et al.  Implantable neurotechnologies: a review of micro- and nanoelectrodes for neural recording , 2016, Medical & Biological Engineering & Computing.

[33]  J. Forsberg,et al.  Traumatic and trauma-related amputations: Part II: Upper extremity and future directions. , 2010, The Journal of bone and joint surgery. American volume.

[34]  C. Novak,et al.  Evidence and techniques in rehabilitation following nerve injuries. , 2013, Hand clinics.

[35]  M. Lanzettà,et al.  Human hand allograft: report on first 6 months , 1999, The Lancet.

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

[37]  Dario Farina,et al.  The Extraction of Neural Information from the Surface EMG for the Control of Upper-Limb Prostheses: Emerging Avenues and Challenges , 2014, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[38]  A. Levey,et al.  Very early activation of m-calpain in peripheral nerve during Wallerian degeneration , 2002, Journal of the Neurological Sciences.

[39]  M. Ninkovic,et al.  Technical and Surgical Details of Hand Transplantation , 2007 .

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

[41]  Chao Song,et al.  A regenerative microchannel device for recording multiple single‐unit action potentials in awake, ambulatory animals , 2016, The European journal of neuroscience.

[42]  S. Micera,et al.  Focal release of neurotrophic factors by biodegradable microspheres enhance motor and sensory axonal regeneration in vitro and in vivo , 2016, Brain Research.

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

[44]  N. Lago,et al.  Effects of motor and sensory nerve transplants on amount and specificity of sciatic nerve regeneration , 2007, Journal of neuroscience research.

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

[46]  Ravi V. Bellamkonda,et al.  Regenerative Scaffold Electrodes for Peripheral Nerve Interfacing , 2013, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[47]  Eugenio Guglielmelli,et al.  Invasive neural interfaces: the perspective of the surgeon. , 2014, The Journal of surgical research.

[48]  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.

[49]  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.

[50]  Michael J Yaszemski,et al.  Controlling dispersion of axonal regeneration using a multichannel collagen nerve conduit. , 2010, Biomaterials.

[51]  E. Biddiss,et al.  Upper limb prosthesis use and abandonment: A survey of the last 25 years , 2007, Prosthetics and orthotics international.

[52]  Geoffroy C. Sisk,et al.  Rehabilitation following hand transplantation , 2014, Hand.

[53]  W. Lee,et al.  Technical Aspects of the Recipient Operation in Hand Transplantation , 2011, Journal of Reconstructive Microsurgery.

[54]  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.

[55]  Daniel W. Moran,et al.  Regenerated Sciatic Nerve Axons Stimulated through a Chronically Implanted Macro-Sieve Electrode , 2016, Front. Neurosci..

[56]  M. J. Moore,et al.  ACCURACY OF MOTOR AXON REGENERATION ACROSS AUTOGRAFT, SINGLE‐LUMEN, AND MULTICHANNEL POLY(LACTIC‐CO‐GLYCOLIC ACID) NERVE TUBES , 2008, Neurosurgery.

[57]  Xavier Navarro,et al.  Correlation between target reinnervation and distribution of motor axons in the injured rat sciatic nerve. , 2006, Journal of neurotrauma.

[58]  J. Fawcett,et al.  A regenerative microchannel neural interface for recording from and stimulating peripheral axons in vivo , 2012, Journal of neural engineering.

[59]  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.

[60]  X. Navarro,et al.  Neural plasticity after peripheral nerve injury and regeneration , 2007, Progress in Neurobiology.

[61]  E. Valderrama,et al.  Peripheral nerve regeneration through microelectrode arrays based on silicon technology. , 1996, Restorative neurology and neuroscience.

[62]  Nitish V. Thakor,et al.  Erratum to: Implantable neurotechnologies: bidirectional neural interfaces—applications and VLSI circuit implementations , 2016, Medical & Biological Engineering & Computing.

[63]  Mario I. Romero,et al.  Early Interfaced Neural Activity from Chronic Amputated Nerves , 2009, Front. Neuroeng..