Imaging fast neural traffic at fascicular level with electrical impedance tomography: proof of principle in rat sciatic nerve

OBJECTIVE Understanding the coding of neural activity in nerve fascicles is a high priority in computational neuroscience, electroceutical autonomic nerve stimulation and functional electrical stimulation for treatment of paraplegia. Unfortunately, it has been little studied as no technique has yet been available to permit imaging of neuronal depolarization within fascicles in peripheral nerve. APPROACH We report a novel method for achieving this, using a flexible cylindrical multi-electrode cuff placed around nerve and the new medical imaging technique of fast neural electrical impedance tomography (EIT). In the rat sciatic nerve, it was possible to distinguish separate fascicles activated in response to direct electrical stimulation of the posterior tibial and common peroneal nerves. MAIN RESULTS Reconstructed EIT images of fascicular activation corresponded with high spatial accuracy to the appropriate fascicles apparent in histology, as well as the inverse source analysis (ISA) of compound action potentials (CAP). With this method, a temporal resolution of 0.3 ms and spatial resolution of less than 100 µm was achieved. SIGNIFICANCE The method presented here is a potential solution for imaging activity within peripheral nerves with high spatial accuracy. It also provides a basis for imaging and selective neuromodulation to be incorporated in a single implantable non-penetrating peri-neural device.

[1]  M. Bendszus,et al.  Somatotopic fascicular organization of the human sciatic nerve demonstrated by MR neurography , 2015, Neurology.

[2]  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.

[3]  Reid R. Harrison,et al.  Recording sensory and motor information from peripheral nerves with Utah Slanted Electrode Arrays , 2011, 2011 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[4]  David S. Holder,et al.  Feasibility of imaging epileptic seizure onset with EIT and depth electrodes , 2018, NeuroImage.

[5]  J. T. Taylor,et al.  First demonstration of velocity selective recording from the pig vagus using a nerve cuff shows respiration afferents , 2018, Biomedical engineering letters.

[6]  Nikolaos K. Uzunoglu,et al.  Tikhonov Regularization Techniques in Simulated Brain Electrical Tomography , 2000 .

[7]  Floris G. Wouterlood,et al.  A half century of experimental neuroanatomical tracing , 2011, Journal of Chemical Neuroanatomy.

[8]  D.M. Durand,et al.  Localization and Recovery of Peripheral Neural Sources With Beamforming Algorithms , 2009, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[9]  Kayode Williams,et al.  Review of Recent Advances in Peripheral Nerve Stimulation (PNS) , 2016, Current Pain and Headache Reports.

[10]  Théodore Papadopoulo,et al.  The adjoint method for general EEG and MEG sensor-based lead field equations , 2009, Physics in medicine and biology.

[11]  Richard H. Bayford,et al.  A cable theory based biophysical model of resistance change in crab peripheral nerve and human cerebral cortex during neuronal depolarisation: implications for electrical impedance tomography of fast neural activity in the brain , 2012, Medical & Biological Engineering & Computing.

[12]  Bart Vanrumste,et al.  Journal of Neuroengineering and Rehabilitation Open Access Review on Solving the Inverse Problem in Eeg Source Analysis , 2022 .

[13]  Jerald D. Kralik,et al.  Chronic, multisite, multielectrode recordings in macaque monkeys , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[14]  Xavier Navarro,et al.  Topographical distribution of motor fascicles in the sciatic‐tibial nerve of the rat , 2010, Muscle & nerve.

[15]  Dominique M Durand,et al.  Model-based Bayesian signal extraction algorithm for peripheral nerves , 2017, Journal of neural engineering.

[16]  David S. Holder,et al.  Imaging fast electrical activity in the brain with electrical impedance tomography , 2016, NeuroImage.

[17]  H. Curtis,et al.  ELECTRIC IMPEDANCE OF THE SQUID GIANT AXON DURING ACTIVITY , 1939, The Journal of general physiology.

[18]  R. Normann,et al.  Assessment of rat sciatic nerve function following acute implantation of high density utah slanted electrode array (25 electrodes/mm2) based on neural recordings and evoked muscle activity , 2014, Muscle & nerve.

[19]  Dominique M Durand,et al.  Fabrication of High Contact-Density, Flat-Interface Nerve Electrodes for Recording and Stimulation Applications. , 2016, Journal of visualized experiments : JoVE.

[20]  H. S. Gasser,et al.  The classification of nerve fibers. , 1941 .

[21]  S SUNDERLAND,et al.  The intraneural topography of the sciatic nerve and its popliteal divisions in man. , 1948, Brain : a journal of neurology.

[22]  Andreas Dedner,et al.  A Fast Parallel Solver for the Forward Problem in Electrical Impedance Tomography , 2015, IEEE Transactions on Biomedical Engineering.

[23]  J. Newell,et al.  Distinguishability of inhomogeneities using planar electrode arrays and different patterns of applied excitation. , 2003, Physiological measurement.

[24]  D.B. McCreery,et al.  Bidirectional Telemetry Controller for Neuroprosthetic Devices , 2010, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[25]  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.

[26]  Dominique M. Durand,et al.  Stable Detection of Movement Intent From Peripheral Nerves: Chronic Study in Dogs , 2017, Proceedings of the IEEE.

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

[28]  Andrew W. McEvoy,et al.  Design for a three-dimensional printed laryngoscope blade for the intubation of rats , 2014, Lab Animal.

[29]  José Zariffa A review of source separation and source localization approaches in peripheral nerves , 2014, 2014 48th Asilomar Conference on Signals, Systems and Computers.

[30]  Sliman J. Bensmaia,et al.  Biological and bionic hands: natural neural coding and artificial perception , 2015, Brain Stimulation.

[31]  Anna N. Vongerichten,et al.  Characterisation and imaging of cortical impedance changes during interictal and ictal activity in the anaesthetised rat , 2016, NeuroImage.

[32]  Kirill Y Aristovich,et al.  A method for reconstructing tomographic images of evoked neural activity with electrical impedance tomography using intracranial planar arrays , 2014, Physiological measurement.

[33]  Zhongwei Chen,et al.  Three‐dimensional reconstruction and visualization of the median nerve from serial tissue sections , 2009, Microsurgery.

[34]  H A C Wark,et al.  Behavioral and cellular consequences of high-electrode count Utah Arrays chronically implanted in rat sciatic nerve , 2014, Journal of neural engineering.

[35]  D. Isaacson Distinguishability of Conductivities by Electric Current Computed Tomography , 1986, IEEE Transactions on Medical Imaging.

[36]  E. Somersalo,et al.  Existence and uniqueness for electrode models for electric current computed tomography , 1992 .

[37]  S SUNDERLAND,et al.  The intraneural topography of the radial, median and ulnar nerves. , 1945, Brain : a journal of neurology.

[38]  Martin Schuettler,et al.  A novel method for recording neuronal depolarization with recording at 125–825 Hz: implications for imaging fast neural activity in the brain with electrical impedance tomography , 2011, Medical & Biological Engineering & Computing.

[39]  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.

[40]  Kirill Y Aristovich,et al.  Investigation of potential artefactual changes in measurements of impedance changes during evoked activity: implications to electrical impedance tomography of brain function , 2015, Physiological measurement.

[41]  D. S. Holder,et al.  Impedance changes during the compound nerve action potential: Implications for impedance imaging of neuronal depolarisation in the brain , 1992, Medical and Biological Engineering and Computing.

[42]  D. Hutchinson,et al.  A histological analysis of human median and ulnar nerves following implantation of Utah slanted electrode arrays. , 2016, Biomaterials.

[43]  C. Koch,et al.  The origin of extracellular fields and currents — EEG, ECoG, LFP and spikes , 2012, Nature Reviews Neuroscience.

[44]  Feng Zhang,et al.  Longitudinal intrafascicular electrodes in collection and analysis of sensory signals of the peripheral nerve in a feline model , 2005, Microsurgery.

[45]  B Wodlinger,et al.  Selective recovery of fascicular activity in peripheral nerves , 2011, Journal of neural engineering.

[46]  Dustin J Tyler,et al.  Neural interfaces for somatosensory feedback: bringing life to a prosthesis. , 2015, Current opinion in neurology.

[47]  James Avery,et al.  A Versatile and Reproducible Multi-Frequency Electrical Impedance Tomography System , 2017, Sensors.