Visual Evoked Potentials Determine Chronic Signal Quality in a Stent- OPEN ACCESS Electrode Endovascular Neural Interface
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Biomed. Phys. Eng. Express 4 (2018) 055018 https://doi.org/10.1088/2057-1976/aad714 PAPER Visual evoked potentials determine chronic signal quality in a stent- OPEN ACCESS electrode endovascular neural interface RECEIVED 22 June 2018 G Gerboni1,2,3,7, S E John1,2,3,4, G S Rind2,3,4, S M Ronayne2,3, C N May2,3, T J Oxley2,3,4, D B Grayden1,2, REVISED N L Opie2,3,4,8 and Y T Wong5,6,8 12 July 2018 1 NeuroEngineering Laboratory, Department of Biomedical Engineering, The University of Melbourne, VIC 3010, Australia ACCEPTED FOR PUBLICATION 2 31 July 2018 Vascular Bionics Laboratory, Department of Medicine, Royal Melbourne Hospital, The University of Melbourne, VIC 3010, Australia 3 Florey Institute of Neuroscience and Mental Health, 30 Royal Parade, Parkville, VIC 3052, Melbourne, Australia PUBLISHED 4 Synchron, Inc. Palo Alto, CA, 94301, United States of America 20 August 2018 5 Department of Physiology, Monash University, Clayton, VIC 3800, Melbourne, Australia 6 Department of Electrical and Computer Systems Engineering, Monash University, Clayton, VIC 3800, Melbourne, Australia Original content from this 7 Authors to whom any correspondence should be addressed. work may be used under 8 Joint senior authors. the terms of the Creative Commons Attribution 3.0 E-mail: [email protected] licence. Any further distribution of Keywords: brain-machine interface, neural signals, endovascular electrodes, visual evoked potentials, neural interfaces this work must maintain attribution to the Supplementary material for this article is available online author(s) and the title of the work, journal citation and DOI. Abstract Brain-machine interfaces directly communicate between the brain and external devices. An effective trade-off between signal quality and safety required for successful clinical translation has yet to be achieved, and represents a great challenge for engineers, neuroscientists, and clinicians. The StentrodeTM, an endovascular neural interface that allows neural signals to be recorded from within a cortical vessel, has demonstrated feasibility with safety for up to six months in a large animal model. Easily-obtained electrophysiological signals to evaluate the effect of implant duration on recording performance are essential for ongoing evaluation of the device. In this work, we demonstrate that a non-invasive and quick visual stimulation technique can be used to assess chronic signal quality of an endovascular neural interface in awake freely moving animals. Visual stimulation requires little or no training to elicit a large, consistent, and well-characterized response. We report the stability of recording quality with the Stentrode over 30 days using voltage measures of signal-to-noise ratio (18.78±1.92 dB, mean±std) and peak-to-peak voltages (56.07±9.56 μV) computed on visual evoked responses. Signal amplitude and electrochemical impedance spectroscopy suggest that stabilization of the electrode-tissue interface occurred over the first 20 days. However, during this stabilization period, recording quality was minimally impacted. 1. Introduction of time with high spatial and temporal resolution (Lebedev & Nicolelis 2006, Slutzky & Flint 2017). Enabling long-term, bi-directional communication Surface electrodes placed above (epidural) and below between the brain and external devices has potential (subdural) the dura mater provide access to electro- applications ranging from brain-machine interfaces corticography (ECoG) signals, with promising perfor- (BMIs) and disease monitoring to treatment of mance in motor BMIs (Chao et al 2010, Yanagisawa traumatic, genetic, and degenerative conditions, and et al 2012, Wang et al 2013) and stability for years also provides a powerful tool to study nervous system after implantation (Ryapolova-Webb et al 2014, organization and function (Chen et al 2017). The Nurse et al 2017). Penetrating microelectrodes design of an effective and clinically viable neural have achieved the highest spatial resolution to date, interface relies on a trade-off between invasiveness and allowing chronic access to the activity of localized signal quality; i.e. the ability to implant electrode populations of neurons (Nicolelis et al 2003, Chestek arrays with minimal damage and disruption while et al 2011,Schwarzet al 2014) and enabling the providing an informative signal over a long period control of dexterous robotic arm movement in humans © 2018 IOP Publishing Ltd Biomed. Phys. Eng. Express 4 (2018) 055018 G Gerboni et al (Collinger et al 2012, Hochberg et al 2012,Bouton with the Stentrode and adjacent subdural and epidural et al 2016, Flesher et al 2016,Ajiboyeet al 2017). grids 4 weeks after implantation. Importantly, results However, these approaches require open-skull surgery showed similarities across devices in signal quality to access the brain for electrode implantation, enhan- measures that are relevant for BMI applications, e.g. cing the risks of subdural hematoma and compromis- bandwidth, signal-to-noise ratio (SNR), decoding acc- ing the stability of the blood-brain barrier if placed in or uracy, and spatial resolution. MicroCT and histology ( below the subdural space Hamer et al 2002,Van reported endothelialization of endovascular electrode ) Gompel et al 2008, Normann & Fernandez 2016 . 2–4 weeks after device deployment (Opie et al 2017). While implanting electrodes holds great promise, Impedance spectra, recorded every two days for the factors limiting clinical translation of invasive neural first 2 weeks and weekly up to 91 days, suggested an interfacing systems include biocompatibility, safety, effect of endothelialization on impendance occurring and chronic signal stability. To achieve these outcomes, 8–14 days after implantation (Opie et al 2016). How- several groups are working to reduce the tissue response ever, neural activity was not recorded during these two by enhancing biocompatibility (Jorfi et al 2015),match- studies. Oxley et al (2016) is so far the only report on ing the stiffness of the implant with the biological long-term monitoring of signal quality accessible with medium (Lacour et al 2016,Wanget al 2017),using an endovascular neural interface. In their study, soma- drug-eluting coatings to prevent the fibrotic tissue tosensory evoked potentials and impendance spectra reaction (Boehler et al 2017, Sanchez-Rexach et al fi 2017), and exploring and refining non-invasive optical were recorded every 2 days for the rst 2 weeks and fi methods (Maharbiz et al 2017). weekly up to 28 days. No signi cant effect of time on Endovascular (within blood vessel) neural interfa- peak amplitudes was observed. However, stabilization cing systems provide an alternative approach to access and improvement in recording quality was suggested neural recordings inside the skull. Building on find- by an increase in the number of channels yielding an ings and technical refinements of diagnostic and ther- evoked response, over the first few days after implant- apeutic intracranial stenting (Fiorella et al 2011, Puffer ation. Despite some promising results suggesting a et al 2013), an endovascular approach does not require limited effect of immune response on recording qual- burr-holes or larger craniotomies, potentially redu- ity and impendace spectra, there is a paucity of data on cing complication rates and surgical durations. The chronic endovascular interfacing systems and how its first attempt to target an intracranial vessel for record- recording quality might change over time. ing epileptic activity in humans used wire electrodes Visual stimulation provides a simple, non-invasive placed in the middle cerebral artery (Penn et al 1973). tool that requires little training to elicit a neural A series of clinical and research studies further response. Short-latency flash stimulation elicits a explored the use of wire electrodes to access brain sig- widespread, transient visual evoked potential (VEP) nals (Sefcik et al 2016) in the arterial (Boniface & that is time-locked to the stimulus with a well-descri- Antoun 1997,Heet al 2016) and venous systems bed morphology and latency (J Vernon Halliday ( ) Mikuni et al 1997, Kunieda et al 2000 , comparing the et al 1972, Halliday et al 1973, Kraut et al 1985, Wright performance with scalp EEG recordings. Micro- and & Richardson 1986, Vialatte et al 2010, Odom nano-wire probes were also developed, showing feasi- et al 2016). This knowledge has been extensively ( bility for recording neural signals intracranially Ishida applied to assess functionality of visual systems in ) et al 1998 and from the spinal cord through the capil- patients (Halliday et al 1972, Halliday et al 1973, lary system (Llinás et al 2005, Watanabe et al 2009).A Tobimatsu & Celesia 2006), to diagnose conditions significant advancement was the deployment of a that impact visual functions such as Parkinson’s dis- catheter-based, multi-site recording system in the ease (Nightingale et al 1986, Onofrj et al 1986), multi- superior sagittal sinus (SSS) to record epileptic activity, ple sclerosis (Halliday et al 1973), Alzheimer’s disease showing similar performance to same-size subdural (Wright & Richardson 1986), and epilepsy (Broughton electrodes in pigs (Bower et al 2013). Recently, an & Ebe 1969) and to control BMIs (Kwak et al 2015, endovascular neural interface with platinum-disk ) electrodes mounted on a super-elastic Nitinol stent, Won et al 2016 . In our studies, we have recorded the StentrodeTM, was developed and successfully chronic cortical activation with a stent-based endovas- deployed in the SSS to record cortical signals (Oxley cular neural interface in response to visual stimuli in et al 2016). Vessel patency and safety were reported up awake, freely moving animals. We computed signal- ( ) to 190 days after implantation in a sheep model. The to-noise ratios and peak-to-peak PP voltages of the sheep did not demonstrate any neurological damage recorded neural responses for up to 30 days, showing or sign of distress throughout the experiment. How- how these measures may be used to quickly and reli- ever, to determine the range of applicability of this ably assess the chronic performance of an endovas- endovascular interfacing modality, an investigation on cular device.