Minimally invasive endovascular stent-electrode array for high-fidelity, chronic recordings of cortical neural activity

High-fidelity intracranial electrode arrays for recording and stimulating brain activity have facilitated major advances in the treatment of neurological conditions over the past decade. Traditional arrays require direct implantation into the brain via open craniotomy, which can lead to inflammatory tissue responses, necessitating development of minimally invasive approaches that avoid brain trauma. Here we demonstrate the feasibility of chronically recording brain activity from within a vein using a passive stent-electrode recording array (stentrode). We achieved implantation into a superficial cortical vein overlying the motor cortex via catheter angiography and demonstrate neural recordings in freely moving sheep for up to 190 d. Spectral content and bandwidth of vascular electrocorticography were comparable to those of recordings from epidural surface arrays. Venous internal lumen patency was maintained for the duration of implantation. Stentrodes may have wide ranging applications as a neural interface for treatment of a range of neurological conditions.

[1]  S. Simpson,et al.  LOCALISATION OF THE MOTOR AREA IN THE SHEEP , 1911 .

[2]  C. Bagley CORTICAL MOTOR MECHANISM OF THE SHEEP BRAIN , 1922 .

[3]  S. Furman,et al.  An Intracardiac Pacemaker for Stokes–Adams Seizures , 2006, The New England journal of medicine.

[4]  N. G. Ghoshal,et al.  Innervation of the Forearm and Foot in the Ox (Bos taurus), Sheep (Ovis aries) and Goat (Capra hircus) , 1967 .

[5]  S. Hilal,et al.  Development and use of the POD catheter in the cerebral vascular system. , 1969, Medical research engineering.

[6]  S K Hilal,et al.  Intravascular intracranial EEG recording. Technical note. , 1973, Journal of neurosurgery.

[7]  E. Eger,et al.  Pregnancy decreases the requirement for inhaled anesthetic agents. , 1974, Anesthesiology.

[8]  E. Rubel,et al.  Mechanosensory projections to cerebral cortex of sheep , 1974, The Journal of comparative neurology.

[9]  C. S. Thomas,et al.  The incidence of venous thrombosis following long-term transvenous pacing. , 1976, The Annals of thoracic surgery.

[10]  B. Kaye,et al.  Termination of malignant ventricular arrhythmias with an implanted automatic defibrillator in human beings , 1981 .

[11]  D. Thomson,et al.  Spectrum estimation and harmonic analysis , 1982, Proceedings of the IEEE.

[12]  C. C. Wood,et al.  Human cortical potentials evoked by stimulation of the median nerve. I. Cytoarchitectonic areas generating short-latency activity. , 1989, Journal of neurophysiology.

[13]  P. Serruys,et al.  Coronary Stenting With a New, Radiopaque, Balloon‐Expandable Endoprosthesis in Pigs , 1991, Circulation.

[14]  William M. Rabinowitz,et al.  Better speech recognition with cochlear implants , 1991, Nature.

[15]  The divergent actions of volatile anaesthetics on background neuronal activity and reactive capability in the central nervous system in cats , 1993 .

[16]  J. Schramm,et al.  Somatosensory evoked potential phase reversal and direct motor cortex stimulation during surgery in and around the central region. , 1996, Neurosurgery.

[17]  S. Boniface,et al.  Endovascular electroencephalography: the technique and its application during carotid amytal assessment. , 1997, Journal of neurology, neurosurgery, and psychiatry.

[18]  Allan H. Ropper,et al.  Evoked potentials in clinical medicine (second of two parts). , 1982 .

[19]  J. Isner,et al.  Stent endothelialization. Time course, impact of local catheter delivery, feasibility of recombinant protein administration, and response to cytokine expedition. , 1997, Circulation.

[20]  H Shibasaki,et al.  “Cavernous Sinus EEG”: A New Method for the Preoperative Evaluation of Temporal Lobe Epilepsy , 1997, Epilepsia.

[21]  I. Rampil A Primer for EEG Signal Processing in Anesthesia , 1998, Anesthesiology.

[22]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[23]  W. Grovum,et al.  Electrical stimulation of the medial frontal lobe elicits a pattern of body movements in sheep , 1999, Brain Research.

[24]  A. Dale,et al.  Cortical Surface-Based Analysis II: Inflation, Flattening, and a Surface-Based Coordinate System , 1999, NeuroImage.

[25]  Christian Casanova,et al.  On the use of isoflurane versus halothane in the study of visual response properties of single cells in the primary visual cortex , 2003, Journal of Neuroscience Methods.

[26]  C. Hamm,et al.  Pulmonary Vein Diameter Reduction After Radiofrequency Catheter Ablation for Paroxysmal Atrial Fibrillation Evaluated by Contrast-Enhanced Three-Dimensional Magnetic Resonance Imaging , 2003, Circulation.

[27]  Filippo Cademartiri,et al.  Noninvasive Angiographic Evaluation of Coronary Stents with Multi-Slice Spiral Computed Tomography , 2003, Herz.

[28]  John K Triedman,et al.  Patient, procedural, and hardware factors associated with pacemaker lead failures in pediatrics and congenital heart disease. , 2004, Heart rhythm.

[29]  Andreas Hierlemann,et al.  Impedance characterization and modeling of electrodes for biomedical applications , 2005, IEEE Transactions on Biomedical Engineering.

[30]  M. MacIver,et al.  Anesthetic-induced burst suppression EEG activity requires glutamate-mediated excitatory synaptic transmission. , 2005, Cerebral cortex.

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

[32]  G. Deuschl,et al.  A randomized trial of deep-brain stimulation for Parkinson's disease. , 2006, The New England journal of medicine.

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

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

[35]  David A. Steinman,et al.  An image-based modeling framework for patient-specific computational hemodynamics , 2008, Medical & Biological Engineering & Computing.

[36]  Qing-lin Zhang,et al.  Endoscopic and microscopic anatomy of the superior sagittal sinus and torcular herophili , 2009, Journal of Clinical Neuroscience.

[37]  Hirokazu Takahashi,et al.  Intravascular Neural Interface with Nanowire Electrode. , 2009, Electronics and communications in Japan = Denki Gakkai ronbunshi.

[38]  Shailendra Kapoor,et al.  Subthalamic nucleus stimulation in severe obsessive-compulsive disorder. , 2009, The New England journal of medicine.

[39]  B. Metscher MicroCT for comparative morphology: simple staining methods allow high-contrast 3D imaging of diverse non-mineralized animal tissues , 2009, BMC Physiology.

[40]  Toshiki Yoshimine,et al.  Neural decoding using gyral and intrasulcal electrocorticograms , 2009, NeuroImage.

[41]  Robert Oostenveld,et al.  Gain of the human dura in vivo and its effects on invasive brain signal feature detection , 2010, Journal of Neuroscience Methods.

[42]  Anton Maksimenko,et al.  First experiments on the Australian Synchrotron Imaging and Medical beamline, including investigations of the effective source size in respect of X-ray imaging. , 2010, Journal of synchrotron radiation.

[43]  Alice K. Cho,et al.  Retinal prostheses: current clinical results and future needs. , 2011, Ophthalmology.

[44]  Robert Oostenveld,et al.  FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data , 2010, Comput. Intell. Neurosci..

[45]  G. M. Halmágyi,et al.  Transverse Sinus Stenting for Idiopathic Intracranial Hypertension: A Review of 52 Patients and of Model Predictions , 2011, American Journal of Neuroradiology.

[46]  A. Schulze-Bonhage,et al.  First long term in vivo study on subdurally implanted Micro-ECoG electrodes, manufactured with a novel laser technology , 2011, Biomedical microdevices.

[47]  J. Wang,et al.  Visualization of the Internal Cerebral Veins on MR Phase-Sensitive Imaging: Comparison with 3D Gadolinium-Enhanced MR Venography and Fast-Spoiled Gradient Recalled Imaging , 2011, American Journal of Neuroradiology.

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

[49]  Francesco Migliavacca,et al.  Hemodynamics and In-stent Restenosis: Micro-CT Images, Histology, and Computer Simulations , 2011, Annals of Biomedical Engineering.

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

[51]  H. Yokoi,et al.  Electrocorticographic control of a prosthetic arm in paralyzed patients , 2012, Annals of neurology.

[52]  Naotaka Fujii,et al.  Decoding continuous three-dimensional hand trajectories from epidural electrocorticographic signals in Japanese macaques , 2012, Journal of neural engineering.

[53]  Milan Sonka,et al.  3D Slicer as an image computing platform for the Quantitative Imaging Network. , 2012, Magnetic resonance imaging.

[54]  Giuseppe Lanzino,et al.  Venous sinus stenting for idiopathic intracranial hypertension: a review of the literature , 2012, Journal of NeuroInterventional Surgery.

[55]  S. Dey Stenting versus Aggressive Medical Therapy for Intracranial Arterial Stenosis , 2012 .

[56]  Garrett B Stanley,et al.  The impact of chronic blood-brain barrier breach on intracortical electrode function. , 2013, Biomaterials.

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

[58]  David M. Himes,et al.  Prediction of seizure likelihood with a long-term, implanted seizure advisory system in patients with drug-resistant epilepsy: a first-in-man study , 2013, The Lancet Neurology.

[59]  Mark R. Bower,et al.  Intravenous recording of intracranial, broadband EEG , 2013, Journal of Neuroscience Methods.

[60]  Robin C. Ashmore,et al.  An Electrocorticographic Brain Interface in an Individual with Tetraplegia , 2013, PloS one.

[61]  Nicholas P. Szrama,et al.  Characterization of the effects of the human dura on macro- and micro-electrocorticographic recordings , 2014, Journal of neural engineering.

[62]  Allison T. Connolly,et al.  Computational modeling of an endovascular approach to deep brain stimulation , 2014, Journal of neural engineering.

[63]  Jan M. Rabaey,et al.  24.1 A miniaturized 64-channel 225μW wireless electrocorticographic neural sensor , 2014, 2014 IEEE International Solid-State Circuits Conference Digest of Technical Papers (ISSCC).

[64]  H. Schneider,et al.  The Ovine Cerebral Venous System: Comparative Anatomy, Visualization, and Implications for Translational Research , 2014, PloS one.

[65]  Yuji Tanabe,et al.  Wireless power transfer to deep-tissue microimplants , 2014, Proceedings of the National Academy of Sciences.

[66]  P. Mitchell,et al.  Endovascular therapy for ischemic stroke. , 2015, The New England journal of medicine.

[67]  Hester F. Lingsma,et al.  A randomized trial of intraarterial treatment for acute ischemic stroke. , 2015, The New England journal of medicine.