A Neural Interface for a Cortical Vision Prosthesis

View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Vision Research 39 (1999) 2577–2587 A neural interface for a cortical vision prosthesis Richard A. Normann *, Edwin M. Maynard, Patrick J. Rousche, David J. Warren Department of Bioengineering, Uni6ersity of Utah, 2840 Merrill Engineering Building, Salt Lake City, UT 84112, USA Received 11 August 1998; received in revised form 7 December 1998 Abstract The development of a cortically based vision prosthesis has been hampered by a lack of basic experiments on phosphene psychophysics. This basic research has been hampered by the lack of a means to safely stimulate large numbers of cortical neurons. Recently, a number of laboratories have developed arrays of silicon microelectrodes that could enable such basic studies on phosphene psychophysics. This paper describes one such array, the Utah electrode array, and summarizes neurosurgical, physiological and histological experiments that suggest that such an array could be implanted safely in visual cortex. We also summarize a series of chronic behavioral experiments that show that modest levels of electrical currents passed into cortex via this array can evoke sensory percepts. Pending the successful outcome of biocompatibility studies using such arrays, high count arrays of penetrating microelectrodes similar to this design could provide a useful tool for studies of the psychophysics of phosphene perception in human volunteers. Such studies could provide a proof-of-concept for cortically based artificial vision. © 1999 Published by Elsevier Science Ltd. All rights reserved. Keywords: Neuroprosthetics; Artificial vision; Electrode arrays; Multielectrode recordings; Biocompatibility 1. Introduction with an array of electrodes implanted subdurally over its surface. These studies showed that currents in the The concept of cortically based artificial vision had milliampere range were required to evoke individual its origins in studies of the functional architecture of phosphenes, and that currents passed through groups the cerebral cortex. Wilder Penfield observed the behav- of electrodes that were spaced too close to neighboring ioral consequences of electrically stimulating various electrodes produced highly non-linear interactions be- regions of cerebral cortex and noted that there was a tween the evoked phosphenes. It became clear from rational map of visual space onto the primary visual these experiments that stimulating visual cortex via an cortex (Penfield & Rasmussen, 1950). He observed that array of surface electrodes would not be an effective electrical stimulation of the surface of the visual cortex means to produce a useful visual sense in individuals generally evoked the perception of points of light with total blindness. (called phosphenes) at specific regions in space. These Recent experiments by Schmidt et al. (1996) have observations have led a number of investigators to caused renewed interest in cortically based visual pros- propose that electrical stimulation of visual cortex via thetics. They stimulated visual cortex of a profoundly arrays of electrodes might provide the profoundly blind blind human volunteer with groups of microelectrodes with a limited form of functional vision. Subsequent that were designed to penetrate the cortex to the level experiments in the late sixties and early seventies by of its normal thalamic input. Neural stimulation via Brindley (Brindley & Lewin, 1968), Dobelle (Dobelle & Mladejovsky, 1974), Pollen (Pollen, 1975), and their penetrating electrodes has been long known to occur co-workers demonstrated that a field of individual pho- with electrical currents that are much smaller than sphenes could be evoked by stimulating visual cortex those used to excite neurons via surface stimulation. Schmidt and his coworkers demonstrated that phosphenes could be evoked with currents that were orders * Corresponding author. Tel.: +1-801-5817645; fax: +1-801- 58189661. of magnitude lower than those used with surface stimu- E-mail address: [email protected] (R.A. Normann) lation, and that simple patterned perceptions could be 0042-6989/99/$ - see front matter © 1999 Published by Elsevier Science Ltd. All rights reserved. PII: S0042-6989(99)00040-1 2578 R.A. Normann et al. / Vision Research 39 (1999) 2577–2587 evoked by current stimulation via small groups of these 2. A high electrode count, penetrating electrode array: microelectrodes. Unfortunately, the electrode arrays design considerations used by Schmidt et al. were too sparse to allow them to answer the key question upon which a cortical ap- The cornerstone of a visual neuroprosthetic is the proach to artificial vision must be based: does patterned interface between the functioning neurons in the visual electrical stimulation via a high electrode count elec- pathways, and implanted devices that can excite these trode array evoke discriminable patterned percepts, or neurons. This system must individually stimulate a very nondiscriminable blobs of light? If this psychophysical large number of neurons that have retained function experiment can be performed, and the former result even though more distal neurons have been irreparably maintains, cortically based artificial vision could be- damaged by the etiology of the blindness. This interface come a reality. bypasses the malfunctioning distal components in the In order to answer this critical question (and many visual pathway and directly excites neural pathways others associated with phosphene psychophysics), re- that are proximal to the implant site. Recent work at searchers need a new class of tools: arrays of microelec- the University of Utah (Jones et al., 1992), at the trodes that can be safely implanted into the visual University of Michigan by Wise et al. (Hoogerwerf & pathways, and that will allow periodic injections of Wise, 1994), and Stanford University (Kewley et al., electrical currents at many closely spaced sites. Such 1997) has focused on the use of silicon as an electrode arrays could eventually also form the cornerstone of material from which high electrode count arrays can be visual neuroprosthetic systems. It therefore is clear that fabricated. Silicon is highly biocompatible (Stensaas & progress in cortically based artificial vision systems is Stensaas, 1978; Yuen et al., 1987; Schmidt et al., 1993), directly linked to progress in the development of high can be micromachined using standard microfabrication electrode count microelectrode arrays. technologies, and can incorporate integrated electron- Over the past few years, the research efforts of an ics. The Michigan and Stanford electrode arrays have increasing number of laboratories around the world been built to take advantage of the planar photolitho- have been committed to the development of such ar- graphic manufacturing techniques used in the semicon- rays. Work has been focused mainly on arrays that will ductor industry, while the Utah arrays were designed interface to neurons of the retina (Humayun et al., from the ground up to meet the needs of a neural 1995; Wyatt & Rizzo, 1996; Chow & Chow, 1997; interface. As such, new manufacturing techniques had Eckmiller 1997; Zrenner et al., 1997) or to neurons of to be developed in order to build this device. These the visual cortex (Wise & Najafi, 1991; Jones et al., techniques have been described elsewhere (Jones et al., 1992; Schmidt et al., 1996), although a recent study has 1992). described phosphene generation via optic nerve stimula- The Utah electrode array (UEA), shown in Fig. 1, tion (Veraart et al., 1998a,b). Because of the impor- provides a multichannel interface to the visual cortex. It tance of the neural interface in a visual prosthesis, has a large number of 1.5 mm long electrodes (typically much of this paper will focus on one example of such a 100 in a 10×10 square grid) that project out from a penetrating cortical electrode array: the Utah electrode very thin (0.2 mm) substrate and that are separated array. We will discuss considerations that were used in from each other by 0.4 mm. The tips of the electrodes its design, how the array can be implanted in the visual are metalized with platinum to facilitate electronic to cortex, and its biocompatibility as revealed by histolog- ionic transduction. As the array’s substrate must rest ical and electrophysiological experiments. The immedi- on the cortical surface, minimizing its thickness was an ate motivation behind much of what we have developed important design consideration: if it was too thin, it at the University of Utah has not been to create vision might break upon insertion, if it was too thick, the dura neuroprosthetic systems (not enough is known about and the skull would produce a constant downward the human visual pathways to optimally design such a force on the array, tending to push it into the cortex. system today). Rather, we have been trying to create The large number of penetrating electrodes in the experimental systems that will allow researchers to bet- UEA presents a very large surface area to the cortex ter understand the vertebrate visual system though elec- and the implanted array tends to self anchor to the trophysiological and behavioral experiments. When the cortical tissues. Such an array has the strong advantage long term biocompatibility of these experimental im- that it floats in the cortical tissues. As the cortex moves plant systems has been demonstrated, these systems due to respiration and blood pumping,

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