An ovine model of cerebral catheter venography for implantation of an endovascular neural interface

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Neural interface technology may enable the development of novel therapies to treat neurological conditions, including motor prostheses for spinal cord injury. Intracranial neural interfaces currently require a craniotomy to achieve implantation and may result in chronic tissue inflammation. Novel approaches are required that achieve less invasive implantation methods while maintaining high spatial resolution. An endovascular stent electrode array avoids direct brain trauma and is able to record electrocorticography in local cortical tissue from within the venous vasculature. The motor area in sheep runs in a parasagittal plane immediately adjacent to the superior sagittal sinus (SSS). The authors aimed to develop a sheep model of cerebral venography that would enable validation of an endovascular neural interface.


Cerebral catheter venography was performed in 39 consecutive sheep. Contrast-enhanced MRI of the brain was performed on 13 animals. Multiple telescoping coaxial catheter systems were assessed to determine the largest wide-bore delivery catheter that could be delivered into the anterior SSS. Measurements of SSS diameter and distance from the motor area were taken. The location of the motor area was determined in relation to lateral and superior projections of digital subtraction venography images and confirmed on MRI.


The venous pathway from the common jugular vein (7.4 mm) to the anterior SSS (1.2 mm) was technically challenging to selectively catheterize. The SSS coursed immediately adjacent to the motor cortex (< 1 mm) for a length of 40 mm, or the anterior half of the SSS. Attempted access with 5-Fr and 6-Fr delivery catheters was associated with longer procedure times and higher complication rates. A 4-Fr catheter (internal lumen diameter 1.1 mm) was successful in accessing the SSS in 100% of cases with no associated complications. Complications included procedure-related venous dissection in two major areas: the torcular herophili, and the anterior formation of the SSS. The bifurcation of the cruciate sulcal veins with the SSS was a reliable predictor of the commencement of the motor area.


The ovine model for cerebral catheter venography has generalizability to the human cerebral venous system in relation to motor cortex location. This novel model may facilitate the development of the novel field of endovascular neural interfaces that may include preclinical investigations for cortical recording applications such as paralysis and epilepsy, as well as other potential applications in neuromodulation.

ABBREVIATIONS CJV = common jugular vein; CSV = cruciate sulcal vein; ECoG = electrocorticography; ID = inner diameter; IJV = internal jugular vein; IQR = interquartile range; SSS = superior sagittal sinus.

Article Information

Correspondence Thomas J. Oxley, Vascular Bionics Laboratory, Melbourne Brain Centre, Departments of Medicine and Neurology, Royal Melbourne Hospital, The University of Melbourne, Parkville, Victoria 3050, Australia. email:

INCLUDE WHEN CITING Published online April 28, 2017; DOI: 10.3171/2016.11.JNS161754.

Disclosures Dr. Oxley has received support of non–study-related clinical or research effort from Synchron. Dr. Mitchell has received support of non–study-related clinical or research effort from Codman Johnson & Johnson, Stryker, and Medtronic. Dr. Davis has received modest travel support from Boehringer Ingelheim, BMS, Pfizer, and Medtronic; and has received modest honoraria from Boehringer Ingelheim and Medtronic for serving on an advisory board. Drs. Oxley and Opie hold shares in SmartStent Pty, Ltd., and Synchron, Inc.

© AANS, except where prohibited by US copyright law.



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    Ovine cerebral venography. A telescoping coaxial catheter system comprising a sheath and up to 3 catheters was fed over a microwire (B) to navigate the tortuous venous pathway from CJV to SSS. The CJV was exposed via cut-down at the proximal third of the neck (A). Standardized lateral (D) and superior (E) digital subtraction venogram projections were recorded in each animal to record vessel diameters and conduct surgical planning. A native radiograph (C) demonstrates the telescoping catheter system in situ with “J” curve on the leading microwire to reduce trauma. Figure is available in color online only.

  • View in gallery

    Sheep cerebral venography in relation to motor cortex. A sagittal plane MRI slice in the midline (A) demonstrates allocated fiducial points (green dots) along the course of the SSS, commencing at the torcular herophili and separated by 5-mm increments. Box and whisker plots (C) demonstrate the SSS diameters (upper) and distance from motor cortical surface (lower) at each incremental fiducial point along the SSS. Three-dimensional reconstructions of the SSS in a lateral (B) and superior (E) projection of 1 animal are shown, with the corresponding superior projection from digital subtraction venography (D). Graphical representation of the motor cortex from cortical stimulation mapping literature2 demonstrates somatotopic representation of motor function geographically across the superior frontal gyrus (F; red = hind limb, yellow = forelimb, green = head and eyes, purple = face, mouth, and tongue). Reconstruction using MRI images of the cortical surface of an individual sheep brain with superimposed SSS reconstruction demonstrates motor areas in relation to CSVs (F). Figure is available in color online only.

  • View in gallery

    Example of a complication. Before (left) and after (right) a dissection of the origin of the CSV leading to a subdural hemorrhage (arrow) in the frontal lobe bilaterally, shown on a superior projection.



Antiga LPiccinelli MBotti LEne-Iordache BRemuzzi ASteinman DA: An image-based modeling framework for patient-specific computational hemodynamics. Med Biol Eng Comput 46:109711122008


Bagley C: Cortical motor mechanism of the sheep brain. Arch Neurol Psychiatry 7:4174531922


Barrese JCRao NParoo KTriebwasser CVargas-Irwin CFranquemont L: Failure mode analysis of silicon-based intracortical microelectrode arrays in non-human primates. J Neural Eng 10:0660142013


Carmena JMLebedev MACrist REO'Doherty JESantucci DMDimitrov DF: Learning to control a brain-machine interface for reaching and grasping by primates. PLoS Biol 1:E422003


Chapin JKMoxon KAMarkowitz RSNicolelis MAL: Real-time control of a robot arm using simultaneously recorded neurons in the motor cortex. Nat Neurosci 2:6646701999


Fedorov ABeichel RKalpathy-Cramer JFinet JFillion-Robin JCPujol S: 3D Slicer as an image computing platform for the Quantitative Imaging Network. Magn Reson Imaging 30:132313412012


Grovum WLGonzalez JS: Electrical stimulation of the medial frontal lobe elicits a pattern of body movements in sheep. Brain Res 851:2522531999


Hochberg LRBacher DJarosiewicz BMasse NYSimeral JDVogel J: Reach and grasp by people with tetraplegia using a neurally controlled robotic arm. Nature 485:3723752012


Hochberg LRSerruya MDFriehs GMMukand JASaleh MCaplan AH: Neuronal ensemble control of prosthetic devices by a human with tetraplegia. Nature 442:1641712006


Hoffmann AStoffel MHNitzsche BLobsien DSeeger JSchneider H: The ovine cerebral venous system: comparative anatomy, visualization, and implications for translational research. PLoS ONE 9:e929902014


Lemon R: The output map of the primate motor cortex. Trends Neurosci 11:5015061988


Liyanage KASteward CMoffat BAOpie NLRind GSJohn SE: Development and implementation of a Corriedale ovine brain atlas for use in atlas-based segmentation. PLoS One 11:e01559742016


McConnell GCRees HDLevey AIGutekunst CAGross REBellamkonda RV: Implanted neural electrodes cause chronic, local inflammation that is correlated with local neurodegeneration. J Neural Eng 6:0560032009


Opie NLJohn SERind GSRonayne SMGrayden DBBurkitt AN: Chronic impedance spectroscopy of an endovascular stent-electrode array. J Neural Eng 13:0460202016


Oxley TJOpie NLJohn SERind GSRonayne SMWheeler TL: Minimally invasive endovascular stent-electrode array for high-fidelity, chronic recordings of cortical neural activity. Nat Biotechnol 34:3203272016


Penfield WBoldrey E: Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain 60:3894431937


Prasad AXue QSSankar VNishida TShaw GStreit WJ: Comprehensive characterization and failure modes of tungsten microwire arrays in chronic neural implants. J Neural Eng 9:0560152012


Santhanam GRyu SIYu BMAfshar AShenoy KV: A high-performance brain-computer interface. Nature 442:1951982006


Serruya MDHatsopoulos NGPaninski LFellows MRDonoghue JP: Instant neural control of a movement signal. Nature 416:1411422002


Simpson SKing JL: Localisation of the motor area in the sheep. Exp Physiol 4:53651911


Sun JWang JJie LWang HGong X: Visualization of the internal cerebral veins on MR phase-sensitive imaging: comparison with 3D gadolinium-enhanced MR venography and fast-spoiled gradient recalled imaging. AJNR Am J Neuroradiol 32:E191E1932011


Taylor DMTillery SISchwartz AB: Direct cortical control of 3D neuroprosthetic devices. Science 296:182918322002


Tsutsumi SNakamura MTabuchi TYasumoto YIto M: Venous lacunae presenting with unusual upward protrusion: an anatomic study using high-resolution magnetic resonance imaging. Childs Nerv Syst 29:4654682013


Velliste MPerel SSpalding MCWhitford ASSchwartz AB: Cortical control of a prosthetic arm for self-feeding. Nature 453:109811012008


Wang WCollinger JLDegenhart ADTyler-Kabara ECSchwartz ABMoran DW: An electrocorticographic brain interface in an individual with tetraplegia. PLoS One 8:e553442013


Yanagisawa THirata MSaitoh YKishima HMatsushita KGoto T: Electrocorticographic control of a prosthetic arm in paralyzed patients. Ann Neurol 71:3533612012


Yushkevich PAPiven JHazlett HCSmith RGHo SGee JC: User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. Neuroimage 31:111611282006




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