Ž .Brain Research 813 1998 181–186

Short communication

Visual sensations produced by optic nerve stimulation using an implantedself-sizing spiral cuff electrode

Claude Veraart a,), Christian Raftopoulos b, J. Thomas Mortimer c, Jean Delbeke a, Delphine Pins a,Geraldine Michaux a, Annick Vanlierde a, Simone Parrini a, Marie-Chantal Wanet-Defalque a´

a Neural Rehabilitation Engineering Laboratory, UniÕersite Catholique de LouÕain, AÕenue Hippocrate, 54, UCL-54.46 B-1200 Brussels, Belgium´b Neurosurgery Department, St. Luc UniÕersity Hospital, B-1200 Brussels, Belgium

c Applied Neural Control Laboratory, Department of Biomedical Engineering, Case Western ReserÕe UniÕersity, CleÕeland 44106-4912, USA

Accepted 8 September 1998

Abstract

A blind volunteer with retinitis pigmentosa was chronically implanted with a self-sizing spiral cuff electrode around an optic nerve.Electrical stimuli applied to the nerve produced localized visual sensations that were broadly distributed throughout the visual field andcould be varied by changing the stimulating conditions. These results demonstrate the potential for constructing a visual prosthesis, basedon electrical stimulation of the optic nerve, for blind subjects who have intact retinal ganglion cells. q 1998 Elsevier Science B.V. Allrights reserved.

Keywords: Visual prosthesis; Retinitis pigmentosa; Optic nerve stimulation; Self-sizing spiral cuff electrode

Following upon Brindley’s groundbreaking investiga-w xtion on occipital cortex stimulation 2 , several similar

attempts to electrically evoke a visual sensation in blindw xindividuals have been undertaken 6,13 . Recently, electri-

cal stimulation of the peripheral visual system has alsobeen suggested. In retinitis pigmentosa photoreceptor cellsdisappear, while ganglion cells and their axonal processes

w xare spared 11,14 . Direct electrical activation of these cellsw xusing retinal implants is now investigated 7,12 . The work

we report here consists in an alternative to retinal implantfor vision rehabilitation in totally blind retinitis pigmentosapatients. Optic nerve electrical stimulation, with a multi-contact electrode and utilizing selective activation tech-

w xniques 4,16 , provides an opportunity to create phosphenesover a wide portion of the visual field with only a fewcontacts and a few stimulators.

Selected among six totally blind candidates with retini-w xtis pigmentosa 3 , a 59-year old female volunteer, who

gave her informed consent, has been chronically implantedw xwith a self sizing spiral cuff electrode 10,16 around her

) Corresponding author. Fax: q 32-2-764-9422; E-mail:veraart@gren.ucl.ac.be; URL: http:rrwww.md.ucl.ac.berentitesrfsiorgrenrintro.htm

right optic nerve. This subject was affected by a dominantautosomal form of retinitis pigmentosa whose first symp-toms appeared when she was 28. She was left with a merelight perception from the age of 40, and was diagnosedtotally blind at 57. This project fully complies with theDeclaration of Helsinki, and was approved by the localEthics committee. The four-contact self-sizing spiral cuffelectrode was designed by the authors, in collaboration

Ž .with NeuroTech Louvain-la-Neuve, Belgium , and fabri-Ž .cated by Axon Engineering Willoughby, OH 44094, USA .

The electrode was intracranially implanted through a pteri-onal transsylvian approach and installed around the opticnerve after careful dissection of the arachnoidal strands.Electrode leads were brought outside the skull, and through

Žthe skin where they ended in an external connector Fig..1 .

Stimulation started on day 2 post-surgery. Then thevolunteer progressively worked up to a level of two 3-h-stimulation sessions a week. Charge balanced single pulsesand trains were used. Stimulation was either monopolar,using a surface indifferent anode, or bipolar between twocontacts within the cuff. Charge density was always kept

Ž 2 . wbelow 150 mCr cm phase up to 50 Hz below 50Ž 2 . xmCr cm phase up to 333 Hz , corresponding to a charge

Ž .per phase of 300 nCrphase respectively 100 nCrphase

0006-8993r98r$ - see front matter q 1998 Elsevier Science B.V. All rights reserved.Ž .PII: S0006-8993 98 00977-9

( )C. Veraart et al.rBrain Research 813 1998 181–186182

Fig. 1. Sketch of the implanted material. The self-sizing spiral cuff electrode was implanted intracranially and the first part of its cable lay on the duramater up to the inferior part of the skull opening. After crossing the dura on the lateral aspect of the skull the lead passes through the skull. The second partof the cable courses below the skin and along the outer surface of the skull. A subcutaneous connector is embedded in the skull, over the ear. A second

Ž .lead, with an open helix, passes down the neck to exit the skin below the clavicle see the small lozenge , and is terminated with an external connector. Thepurpose of the implanted connector is to allow removal of the easily accessible implanted material if needed, or to provide a means of self-sizing cuffelectrode to be subsequently connected to an implanted stimulator.

with a contact area of 0.2 mm2. Determination of currentintensity thresholds for generation of a phosphene was

w xdone using the two-staircase limit method 5 .To assess phosphene location, a pointing hemisphere

with a radius of 0.45 m was used. The volunteer’s headwas stabilized in front of the hemispheric surface using aframe to support her forehead, chin and parietal skull. Herright eye was positioned at hemisphere center. The rightEOG was recorded, and eye movements were monitoredwith a TV camera. When ready for a stimulus, the volun-teer places her head in fixed position, constrained by theframe, and reaches into the hemisphere to place her left

Žindex finger on the fixation point a polymer disk at thew x .intersection of the visual axis 1 with the hemisphere . She

was then instructed to ‘look at’ the fixation point with asteady gaze throughout the stimulation test run. The testrun was delimited by two beep sounds. With her leftforefinger still in contact with the fixation point, as aproprioceptive reference, the subject then indicated theevoked phosphene, with the right hand fingers, as a shapeon the hemisphere. Phosphene characteristics were

recorded, which included position, dimensions and organi-zation, subjective brightness, dots diameter, foregroundand background colors, motion, etc. Occasionally, some

Žsham stimulations no stimulation pulse between two beep.sounds were delivered. They systematically resulted in a

lack of perception by the subject.At day 118 post-surgery, some 1465 phosphenes had

been documented. Transverse thresholds reached generallytwice or more the corresponding monopolar thresholds.This did indirectly confirm the proper electrode position.We have not observed a threshold increase over the timesince implantation. Electrical stimuli applied to the con-tacts in the self-sizing spiral cuff electrode have neverevoked sensations other than visual. Most phospheneswere reported to consist of a set of dots either in a clusterof 2 to 5, or arranged in rows, arrays, or lumps of 6 to 30.

ŽDot diameter ranged from 8 to 42 min of arc 1 to 5.5 mm.at the distance of 0.45 m . Sometimes, a kind of surround

of lesser brightness was described around each dot in aphosphene. Solid lines, bars, or triangles devoid of dotstructure were occasionally reported, usually near percep-

( )C. Veraart et al.rBrain Research 813 1998 181–186 183

Žtion threshold. Phosphene area or envelope area for dot.phosphenes generally ranged from about 1 to 50 square

degrees. Brightness was graded on a scale of 1 to 9 with‘very, very weak’ graded as 1 and ‘very, very bright’graded as 9.

Phosphenes were often reported as colored. In the firstdays after surgery, they generally appeared to our subjectas gold-yellow against a black visual field. Thereafter blue,white, or plain yellow colors were described. With dotphosphenes, the otherwise black visual field sometimesappeared colored in blue, red, or yellow, in between the

Ž .dots. Occasionally, a solid colored surface red, or yellowwas described adjacent to the envelope of a dot phosphene.

Among 156 phosphenes collected at the hospital up today 8 post-surgery, 37% were described as moving; most

often, they consisted of lines, instead of dots. Afterwards,1308 of the next 1309 phosphenes appeared consistentlyimmobile and steady.

Current intensity thresholds for phosphene perceptionŽwere determined using five pulse duration 25, 50, 100,

.200, and 400 ms . This study included single pulses, aswell as trains of 5, 9, and 17 pulses, respectively, gener-ated at 40, 80, and 160 Hz. As in the classical strength–

w xduration curve 8 current intensity thresholds diminishedwith increasing pulse duration. Furthermore, as illustratedin Fig. 2 threshold clearly diminished when train frequencyincreased, and might even be as low as 30 mA for pulsesof 400 ms in duration.

An additional observation resulting from this strength–duration–frequency representation was that, for a given

Fig. 2. Strength–duration–frequency surface. For given values of pulse duration and train frequency, each datum point represents the mean currentthreshold, of the four contacts, for perception. By extension, single pulses are referred to as zero frequency. The representation of the classical

Ž .strength–duration curve, illustrated here in the zero frequency frontal plane, has also been drawn in frontal planes 40, 80, and 160 Hz for trains of 100 msŽ .duration. As a result, along the five transverse planes corresponding to the different pulse duration 25, 50, 100, 200, and 400 ms , a clear drop in

perceptual threshold appears when the stimulus frequency increases.

( )C. Veraart et al.rBrain Research 813 1998 181–186184

Žcontact in the cuff electrode, attributes brightness, color,.size, organization, position, etc. of a phosphene, perceived

at threshold for a specific pulse duration and train fre-quency, usually differed from those documented at thresh-old for another pulse duration andror train frequencies.Furthermore, phosphene attributes reported by our subjectdiffered when the same contact was stimulated at the samevalues of pulse duration and current but at different fre-quencies.

The attributes of the phosphenes were usually consistentfor trials repeated over a short period of time. As anexample when, for a first phosphene, standard deviationsof center of gravity position as a function of time are 1.18

Žhorizontal and 0.68 vertical seven measurements made on.day 84 for 93 min , for a second phosphene, they reach

Ž2.68 horizontal and 3.28 vertical nine measurements madeon day 81 for 182 min, and eight measures made on day

.84 for 101 min .

Fig. 3. Example of the retinotopic arrangement of phosphenes according to the activated contact in the self-sizing spiral cuff electrode. When a givenstimulating condition was applied to a given contact within the cuff electrode, a phosphene was reported by the volunteer provided stimulation thresholdhad been reached. By convention, phosphenes elicited by the activation of a same contact are represented in the figure as colored with the same hue.Contact position within the circular cuff is expressed in degrees. The contact–quadrant relationship which resulted from the optic nerve electrical activationis consistent with the orderly arrangement of both quadrants and contacts. This sample of 64 phosphenes collected near threshold also illustrates the broaddistribution of relatively small phosphenes within the volunteer’s visual field. All the illustrated phosphenes were perceived as motionless.

( )C. Veraart et al.rBrain Research 813 1998 181–186 185

Ž .Fig. 4. Retinotopic organization of the volunteer’s optic nerve. The probable position of the 4 contacts labeled 08, 908, 1808, and 2708 around the opticnerve is indicated on the right; on the left, the quadrant–contact relationship refers to the position in the visual field of phosphenes elicited when

Ž . w xstimulating through a given contact see also Fig. 3 . Compared to clinical data related to the retinotopy of the human optic nerve 9 , when a slant of about608 of the vertical meridian optic nerve projection, relative to the vertical axis, is reported, we observed a more limited inclination of some 208.

Phosphenes were reported to have been perceived overa large portion of the visual field, up to 358 upwards and508 downwards on the vertical meridian and 308 leftwardsand 308 rightwards on the horizontal meridian. Nearthreshold, we found a good retinotopic correspondencebetween the contact position used for a given stimulationwithin the cuff electrode, and the quadrant of the visualfield in which the volunteer drew the related phosphene.Fig. 3 illustrates this relationship for a sample of 64phosphenes with a broad distribution within the visualfield.

As illustrated in Fig. 4, the retinotopy observed here forw xthe right optic nerve is consistent with previous data 9 ,

although with a slant of the vertical meridian projectionless important than described.

As expected, phosphene location depended on gazew xdirection 15 . A steady gaze oriented sideways with re-

spect to the fixation point during the stimulus, or a saccadeending just before the stimulus, resulted in a phosphenelocation consistently referring to gaze orientation at thetime of the electrical stimulation. Similarly, any gazedisplacement, either after a while, or immediately after thestimulus, resulted in a phosphene location steadily refer-ring again to gaze orientation at the time of the stimula-tion, in this case, before the movement. Stimulation thusresulted in phosphenes coded in spatial co-ordinates, i.e.,the algebraic subtraction of actual gaze co-ordinates, fromretinal co-ordinates frozen at stimulation time. Therefore,in order to secure an accurate measurement of phospheneattributes, care was taken to explain to our subject theimportance of maintaining a fixed gaze during the pre-sentation of each test stimulation.

In summary, the axons of retinal ganglion cells in thisretinitis pigmentosa blind volunteer have thus been suc-cessfully activated by electrical stimuli applied to the opticnerve to evoke many distinct phosphenes over a large

portion of the visual field. Slight changes in the attributesof the phosphenes seem to occur over time, which suggestthat some form of learning or remodeling may occur. Theoverall picture that emerges from these preliminary studiesis one of a dormant sensory system that can be reactivatedand potentially used for functional purposes.

Acknowledgements

We thank W. Grill for contributing to a preliminaryfeasibility study; O. Glineur and B. Gerard for their assis-´tance, and C. Trullemans and M. Troosters for technicaladvice. This work was supported by the Commission of

Žthe European Union MIVIP project, ESPRIT LTR a 22. Ž .527 , and by the Belgian F.M.S.R. grant a 3.4584.98 .

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