Annals of Biomedical Engineering, VoL20, pp. 439-449, 1992 Printed in the USA.All rights reserved.
0090-6964/92 $5.00 + .00 Copyright 9 1992PergamonPress Ltd.
Simulation of a Phosphene-Based Visual Field: Visual Acuity in a Pixelized Vision System Kichul Cha, Kenneth H o r c h , and Richard A. N o r m a n n Department of Bioengineering University of Utah Salt Lake City, UT (Received 1/4/91; Revised 6/27/91) A visual prosthesis f o r the blind using electrical stimulation o f the visual cortex will require the development o f an array o f electrodes. Passage o f current through these electrodes is expected to create a visual image made up o f a matrix o f discrete phosphenes. The quality o f the visual sense thus provided will be a function o f many parameters, particularly the number o f electrodes and their spacing. We are conducting a series o f psychophysical experiments with a portable "phosphene" simulator to obtain estimates o f suitable values f o r electrode number and spacing. The simulator consists o f a small video camera and monitor worn by a normally sighted human subject. To simulate a discrete phosphene field, the monitor is masked by an opaque perforated film. The visual angle subtended by images f r o m the masked monitor is 1.7 ~ or less, depending on the mask, and falls within the fovea o f the subject. In the study presented here, we measured visual acuity as a function o f the number o f pixels and their spacing in the mask. Visual acuity was inversely proportional to pixel density, and trained subjects could achieve about 20/26 visual acuity with a 1024 pixel image. We conclude that 625 electrodes implanted in a I cm by I cm area near the foveal representation o f the visual cortex should produce a phosphene image with a visual acuity o f approximately 20/30. Such an acuity could provide useful restoration o f functional vision f o r the profoundly blind. K e y w o r d s - P h o s p h e n e simulation, Visual prosthesis, Visual acuity.
INTRODUCTION Punctate electrical stimulation of the visual cortex evokes the sensation of a spot of light (phosphene) in the visual field. This suggests that a limited but functional visual sense might be created by electrical stimulation of the visual cortex with an array of electrodes. Feasibility studies of this concept have been performed by Brindley and Lewis (6) and Dobelle and coworkers (11,13). They stimulated the surface of the human visual cortex with an array o f electrodes and found that the resulting phosphenes could produce useful visual patterns and provide a higher rate of information transfer than that obtained by tactile transmission. For example, a blind volunteer was able to read "braille" transmitted by cortical electrical stimulation much faster than Acknowledgments--This project was supported by the W.M. Keck Foundation. Address correspondence to Dr. Ken Horch, Department of Bioengineering, 2480 MEB, University of Utah, Salt Lake City, UT 84112. 439
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K. Cha, K. Horch, and R.A. Normann
he could read tactile braille (13), a significant observation because slow transmission rates have been a serious problem in visual aid devices which act via other sensory modalities. However the electrodes used in these studies were positioned on the surface of the cortex and failed to produce images that were useful for functional restoration of vision because of the limited number of phosphenes and their irregular, noncontiguous distribution. Electrode spacing limits the total number of electrodes which can be implanted in a given area of cortex. The number and spacing of the electrodes determine the acuity and the scope of the resulting visual sense. Based on these considerations, a functionally useful visual prosthesis would require an array of numerous, closely spaced electrodes. Stimulation of the visual cortex with penetrating electrodes can evoke phosphenes with less current than is required with surface stimulation (1,3,10), producing more focal excitation of neurons and allowing electrodes to be placed closer together. We have been able to produce an array of closely spaced electrodes which penetrate the visual cortex as a multichannel, silicon-based microstructure (7,23,29). In order to develop a visual prosthesis based on penetrating cortical electrodes, it is essential to know how many electrodes are needed and how closely spaced they should be in order to achieve a given quality of visual sensation. We are addressing this issue by conducting psychophysical experiments with a phosphene simulator which optically creates visual sensations similar to those expected to be produced by intracortical stimulation of the foveal projection in the brain. This paper describes the apparatus and presents data from the first of our studies: determining spatial resolution (visual acuity) as a function of pixel number and spacing. The results indicate that an array of 625 electrodes spaced approximately 400/~m apart could provide good acuity when implanted in foveal cortex. METHODS Phosphene Simulator
The device was designed to optically simulate the visual sensation of a field of punctate phosphenes similar to that produced by electrical stimulation of the visual cortex with an array of penetrating electrodes. Figure 1 is a diagram of the optics used
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FIGURE 1. Simulator optics. The subject views a small video monitor which projects an image encoded by a miniature video camera, A perforated mask placed over the monitor fragments the image into discrete pixels, which are sized below the limit of visual resolution for the subjects. Lenses adjust the size of the projected image so that it subtends an angle of 1.7 ~ with the largest mask. The acceptance angle of the camera can be adjusted by external lenses.
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in the simulator. A small monochrome video monitor projects images encoded by a camera to the subject's right eye. Optical lenses are placed between the monitor and the subject's eye to reduce the image size and to correct for the subject's ametropia. The monitor is masked with a perforated film to create a field of punctate phosphenes. The mask was made by photographically projecting an array of small holes onto a thin Cr film with a pattern generator, developing the image and etching it chemically. Because the monitor screen is viewed only through the holes, the image consists of a discrete number o f dots (pixels). Each perforation on the mask is a 63.5 • 63.5 #m square. The visual acuity of the human eye is such that subjects cannot resolve changes in intensity within a pixel, but can recognize differences in image brightness between different perforations. Thus, each pixel appears to the subject as a point source o f light which is uniform in intensity. Simulation Parameters
Three parameters are important in determining the quality o f a pixelized image: the number of pixels, their density, and their range of intensities. In an implanted electrode array, the brightness of individual phosphenes can be modulated by the amplitude of current injected through a given electrode (6,11). We have paid little attention to brightness modulation in the work reported here because this experiment uses high contrast stimuli: white targets presented on a black background. Two sets of masks were prepared (Fig. 2). Each set contained four masks: 1024 (32 • 32), 625 (25 • 25), 256 (16 x 16), or 100 (10 x 10) pixels. The 32 x 32 mask was the same for both sets and had a center-to-center spacing between neighboring pix-
FIGURE 2. Masks used in the present study. The basic mask provided a 3 2 • 32 array of pixels, with a pixel spacing of twice the size of an individual pixel. Fixed-field (FF) masks covered the same visual
angle as the basic mask, but spaced the pixels uniformly within this area. Fixed-spacing (FS) masks maintained the same spacing as the basic mask, but restricted the field size. The clear mask limited the visual field to the same visual angle as the FF masks.
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els o f 127 t~m, twice the width of a perforation. All masks had the same size pixels, but the spacings between pixels and the size of the fields were varied as follows. Fixed-field masks incorporated a square array of pixels uniformly spaced over a 1.7 ~ visual field. In these masks, the larger the number of pixels, the closer the pixel spacing. The spacing between centers o f the neighboring pixels for each mask in this set can be calculated by dividing 1.7 ~ by the number of pixels in a column or a row. Fixed-spacing masks had the same pixel spacing as the 32 • 32 mask, but the number of pixels was varied. The larger the number of pixels in these masks, the larger the subtended field. In addition to pixel masks, a clear mask was prepared. This allowed the subjects to view the monitor directly, but with optics and a visual field size, 1.7 ~ which matched those present with the pixelized masks. Acuity Tests
A common and internationally accepted method of measuring visual acuity was employed in these tests (16,30,32). The letter " E " was presented on a computer monitor as a white target on a black background. The contrast o f the E on the monitor was maintained above 80% and the size of each branch of the E was 20% o f the height o f the E. The orientation o f the E was randomly varied by the computer among four o r t h o g o n a l directions, and the size o f the E was varied at each presentation. The subject sat 1 m from the computer monitor, viewed the screen through the simulator, and indicated the orientation of the E using a keypad. The target was presented for 1.5 s, a time sufficient to judge the direction of the E (2). The subjects were encouraged to use head movements during inspection of the target. A staircase procedure was used to determine threshold size for detecting target orientation. If the subject correctly identified the orientation of the E, the letter was made smaller on the subsequent presentation. Otherwise, it was made larger. Threshold was defined as the letter size where the subject changed from correct to incorrect identification of orientation, or vice versa. A trial took 2 to 3 min, during which the threshold was checked 5 times, starting with a size E that was well above threshold. The highest and lowest threshold values were discarded from the data set. Between trials, the subject removed the simulator and rested for 3 to 5 min. Six subjects were recruited from the undergraduate student population at the University of Utah. All subjects had an uncorrected visual acuity o f 20/30 or better. Each subject participated in a 1 h session, consisting o f 6-7 trials, per day over a 3 month period. RESULTS Simulator
Figure 3 is a photograph of the simulator. The device consists of a Sony HVM-302 monochrome video camera with the automatic gain control disabled, a JVC VF-P1U CRT monitor, and optical lenses, all o f which are mounted on a pair o f ski goggles. The lens o f the goggles has been replaced with a piece of opaque plastic. The simulator is portable and can be powered by a battery pack. The subject has complete mobility and can scan objects with voluntary head movements.
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FIGURE 3. The visual phosphene simulator. The optical system is mounted on a pair of ski goggles which are occluded except where the screen of the video monitor (M) is placed. A lens placed in front of the video camera (C), which is mounted just above the monitor, controls the field magnification ratio. Lenses placed between the monitor and the subject's eye adjust the size of the visual field presented to the subject. The monitor is masked by an array of pinholes, so the image is composed of discrete spots of light. The device is portable and the subject can scan objects with head movements. The only visual input available to the subject is the image on the masked monitor. A battery belt (B) is worn around the waist so that the subject can move around freely.
Pixelized Images
Figure 4 shows images photographed from the masked monitor, and should be viewed from a distance such that each image appears about the size of your thumb nail viewed at arms' length. The three images are presented in order to give the reader
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FIGURE 4. An image viewed with different masks. The object was photographed directly from the simulator through a "clear" mask (A), a 3 2 • 3 2 mask (B), and a 16 • 16 fixed-field mask (C). The image size seen by the subjects is equivalent to the size of your thumb nail viewed at arm's length.
a feel for the relationship between image quality and pixel density. The left photograph was taken through a "clear" mask. The clear mask exposed the same portion of the monitor as the fixed-field masks but was not divided into pixels, so that the resulting image was continuous. The other two photographs were taken through fixed-field masks containing different numbers of pixels. Images viewed with different fixed-spacing masks would be portions o f the image viewed with a 32 x 32 mask image. From this figure, it is clear that as pixel spacing increases, acuity decreases. Each pixel produced by the simulator corresponds to a separate punctate phosphene, similar to what is expected to be produced by a single cortical electrode. The number of phosphenes and their spacing is simulated by using masks with different numbers of perforations and different perforation spacings. Visual A cuity
The size of an object's image on the simulator's monitor depends not only on the actual size of the object, but also on the acceptance angle of the camera, which can be varied by external lenses. For the acuity tests, this was held constant at 13 ~. The image was condensed and projected onto the 1.7 ~ field seen by the subject looking at the monitor. To provide a standardized reference, the acuity data presented here are estimated from the angular size of the letter E as presented to the subject's eye. The actual size of a target can be calculated by multiplying this value by the field magnification ratio, 7.6. For the first two weeks, the six subjects were trained with a 32 • 32 mask and a clear mask to familiarize themselves with the device. The average acuity for all subjects using a 32 x 32 mask improved by more than a factor of two over this time. After this period, subject performance stabilized, and each subject was given 10 sets of trials for each mask in the two sets. In addition, trials with the clear mask were conducted to determine if subject performance might somehow be limited by the optics o f the simulator. Figure 5 shows average visual acuity during the final 10 sets of trials as a function of the center-to-center angular spacing between neighboring pixels. Solid symbols show results with fixed-field masks, and open symbols show results with fixed-spacing masks.
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FIGURE 5. Average visual acuity, expressed as Snellen acuity, versus spacing between mask pixels (perforations), expressed in terms of subtended visual angle. The solid symbols show average values • standard deviations from the experiments in which the pixel spacing varied with pixel number (fixed-field masks). The open symbols show the results from experiments in which the pixel spacing was held constant while the number of pixels was varied (fixed-spacing masks). Fixed-field mask sizes were: clear (plotted as equivalent to a mask made up of fused pixels), 32 x 32, 25 • 25, 16 • 16 and 10 x 10. The line shows expected acuity if the subject required a 2.1 x 2.1 pixel grid to recognize the orientation of the target letter.
The left-most solid symbol is data from the clear mask condition. The spacing was calculated by assuming that the mask was completely filled with pixels. Subjects exhibited an average acuity of about 20/20 under this condition: individual values depended on the subject's own acuity. Acuities with other masks depended on the type of mask used. Acuity fell to 20/26 with a 32 • 32 mask and to 20/100 with a 10 • 10 fixed-field mask. Between the 25 • 25 and 10 • 10 masks, inclusive, acuity was inversely proportional to pixel spacing with fixed-field masks. With fixed-spacing masks, which had different numbers of pixels but the same spacing as the 32 x 32 mask, subjects manifested the same acuity as with the 32 x 32 mask. From this, we conclude that pixel density, rather than pixel number, is the key component in determining acuity with this system. The number of pixels required to determine the orientation of the E can be calculated from the acuity tests. For each mask, a threshold size E covered a grid of about 2.1 x 2.1 pixels (Fig. 5). Less formal tests with a Landolt C as the target gave similar results, suggesting that a sampling frequency of about 2 cycles/character is required to identify the orientation of that letter. DISCUSSION Simulator
The portable phosphene array simulation system described here successfully provides a pixelized visual field to subjects, while allowing them freedom to scan their
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environment with head movements. This creates a visual sense similar to what we expect would be produced by an array of electrodes implanted into the visual cortex. One potentially significant difference between our device and a cortical implant is that the simulator allows subjects to scan the phosphene field with eye movements. In subjects implanted with an array of cortical electrodes, eye movements would produce an apparent shift in the perceived location o f the field, but no change in the image with respect to its apparent location on the retina. However, recent experiments using a stabilized image system indicate that this is not an important effect for acuity (Cha, et al., unpublished paper). Subjects became adept at using the device relatively rapidly: their performance stabilized at near normal acuity with high density masks after less than 10 hours of practice over a 2-week period. More complicated visual tasks, such as spatial orientation, are expected to take more practice, but informal tests have indicated that even in these cases subjects can readily learn to use the visual information provided by the simulator. We believe, therefore, that this system provides a valid and useful tool for quantifying basic design parameters for visual prosthetic cortical implants. Pixel Density
The subjects' visual acuity with the simulator depended primarily on pixel spacing, much as the spatial resolution of the eye depends on receptor density in the retina (18). The essentially linear relationship between visual acuity and pixel density indicates that the sampling density required to determine the orientation of a letter was constant. Calculation showed that this density was somewhat over 4 pixels per letter, a value comparable to the 5 pixels per letter suggested by Brindley as sufficient to read ideally designed letters (5). Similarly, a reading test with text sampled by a dot matrix array showed that subjects could read text in which each letter consisted of a 2.8 x 2.8 array of dots (25). Head M o v e m e n t s
Neither eye movements (24) nor smooth movements of a target (34) enhance or impair visual acuity. However, we observed that voluntary head movements did help our subjects with the low pixel density masks. For example, our subjects showed a sudden improvement in performance right after they were encouraged to use head movements. This effect was not apparent with high density masks. Acuity improvement with voluntary head movements may be due to temporal integration during inspection o f a target object, or it may be a result of the subjects using head movements to find the best viewing position to identify the orientation of the target letter. For patients using a visual prosthesis in which the camera is attached to a pair o f eyeglass frames, voluntary head movements may be useful in improving spatial resolution, in detecting obstacles and in spatial orientation. Applications
This study tested a visual sense composed of a number of simulated punctate phosphenes distributed evenly within the foveal visual field. To apply our results to the design of an array of electrodes, we need consider the relationship between the array and the anatomical structure o f the human visual cortex.
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Input to primary visual cortex is basically a two-dimensional retinotopic map (14,22). However, because the cortex is folded in a convoluted pattern, phosphenes produced by two adjacent electrodes can appear far apart in the visual field if the electrodes fall on separate gyri (14). An array of electrodes designed to penetrate into the cortex and implanted in a single gyrus would avoid this problem of spatial discontinuity. However, this requires that the electrode array be sufficiently small to fit on a single gyrus. The cortical magnification factor, defined as the linear distance in the cortex corresponding to an angular distance of 1 ~ in the visual field, is about 6 m m / ~ at the foveal projection (8,9,17,21). Accordingly, two phosphenes, produced by electrodes 315 #m apart, should appear separated by about 3' of arc in the visual field. A 32 x 32 electrode array, with center-to-center spacing of 315 #m between electrodes, should occupy about 1 cm 2. When implanted near the foveal projection, such an array should produce a total visual field of about 1.7 ~ . However it is not always possible to know what part of the foveal projection is represented on a particular location of a given gyrus in humans due to cortical variations between individuals (33). If an implanted array deviates from the center of the foveal projection, neighboring phosphenes will appear further apart because the cortical magnification ratio decreases. As a result, the apparent size of the visual field will increase. How closely neighboring electrodes can be placed before corresponding phosphenes fuse with each other is an important question because it sets an upper limit on electrode density. The limit of two point discrimination in the fovea, l' of arc, corresponds to about 100/~m in layer IVc of visual cortex (21). Cortical penetrating electrodes should be designed to target this layer because it has small receptive fields (10). If intracortical electrodes were spaced such that they evoked contiguous but discrete phosphenes, an array of 625-1024 electrodes could be packed in a square matrix with an area of 1 cm 2. Future Study
The goal of our cortical prostheses work is to provide the blind with a functional visual sense which can be used to facilitate the activities of daily life. The data presented here show that we can achieve high visual acuity in a restricted visual field with a limited number of pixels, provided that they are closely spaced. Such "tunnel vision" would be adequate for pattern recognition tasks such as reading (26, Cha, et al., unpublished paper), but the restricted visual field would be a serious problem in orientation and mobility (15,27). To solve the latter problem it may be possible to use an optical field expander which expands the field of view at the expense of making objects look smaller. Field expanders decrease visual acuity in proportion to the field magnification ratio, but have been found to enhance orientation and mobility if patients have a central visual acuity of at least 20/50 (19,20). CONCLUSION A visual sense composed of about 625 discrete phosphenes within a visual field of 1.7 ~ provides 20/30 visual acuity. Such a visual sense could be useful for pattern recognition tasks, and could be produced, in principle, with a 25 x 25 array of intracortical electrodes implanted within a 1 cm 2 area on a single gyrus of the primary visual
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cortex near the foveal projection. We believe that such a visual prosthesis could be developed using current microfabrication technologies (4,7,23,28,29,31).
REFERENCES 1. Bak, M.; Girvin, J.P.; Hambrecht, F.T.; Kufta, C.V.; Loeb, G.E.; Schmidt, E.M. Visual sensations produced by intracortical microstimulation of the human occipital cortex. Med. Biol. Eng. Comput. 28:257-259; 1990. 2. Baron, W.S.; Westheimer, G. Visual acuity as a function of exposure duration. J. Opt. Soc. Am. 63:212-219; 1973. 3. Bartlett, J.R.; Doty, R.W. An exploration of the ability of macaques to detect microstimulation of striate cortex. Acta Neurobiol. Exp. 40:713-728; 1980. 4. BeMent, S.L.; Wise, K.D.; Anderson, D.J.; Najafi, K.; Drake, K.L. Solid-state electrodes for multichannel multiplexed intracortical neuronal recording. IEEE Trans. Biomed. Eng. BME-33:230-241; 1986. 5. Brindley, G.S. The number of information channels needed for efficient reading. J. Physiol. 177:44; 1965. 6. Brindley, G.S.; Lewin, W.S. The sensations produced by electrical stimulation of the visual cortex. J. Physiol. 196:479-493; 1968. 7. Campbell, P.K.; Jones, K.E.; Huber, R.J.; Horch, K.W.; Normann, R.A. A silicon-based, three dimensional-neural interface: Manufacturing processes for an intracortical electrode array. IEEE Trans. Biomed. Eng. 38:758-768; 1991. 8. Cowey, A.; Rolls, E.T. Human cortical magnification factor and its relation to visual acuity. Exp. Brain Res. 21:447-454; 1974. 9. Daniel, P.M.; Whitteridge, D. The representation of the visual field on the calcarine cortex in baboons and monkeys. J. Physiol. 148:33-34; 1959. 10. DeYoe, E.A.; Lewine, J.; Doty, R.W. Optimal stimuli for detection of intracortical currents applied to striate cortex of awake macaque monkeys. Proc. Ann. Intl. Conf. IEEE Eng. Med. Biol. Soc. 11:934-936; 1986. 11. Dobelle, W.H.; Mladejovsky, M.G. Phosphenes produced by electrical stimulation of human occipital cortex, and their application to the development of a prosthesis for the blind. J. Physiol. 243:553576; 1974. 12. Dobelle, W.H.; Mladejovsky, M.G.; Evans, J.R.; Roberts, T.S.; Girvin, J.P. 'Braille' reading by a blind volunteer by visual cortex stimulation. Nature 259:111-112; 1976. 13. Dobelle, W.H.; Mladejovsky, M.G.; Girvin, J.P. Artificial vision for the blind: Electrical stimulation of visual cortex offers hope for a functional prosthesis. Science 183:440-444; 1974. 14. Dobelle, W.H.; Turkel, J.; Henderson, D.C.; Evans, J.R. Mapping the representation of the visual field by electrical stimulation of human visual cortex. Am. J. Ophthal. 88:727-735; 1979. 15. Faye, E.E. Clinical low vision. Boston: Little, Brown and Company; 1984: pp. 192-193. 16. Fern, K.D.; Manny, R.E. Visual acuity of the preschool child: A review. Am. J. Optom. Physiol. Opt. 63:319-345; 1986. 17. Fox, P.T.; Miezin, F.M.; Allman, J.M.; van Essen, D.C.; Raichle, M.E. Retinotopic organization of human visual cortex mapped with positron-emission tomography. J. Neurosci. 7:913-922; 1987. 18. Hirsch, J.; Curcio, C.A. The spatial resolution capacity of human foveal retina. Vision Res. 29:10951101; 1989. 19. Hoeft, W.W.; Feinbloom, W.; Brilliant, R.; Gordon, R.; Hollander, C.; Newman, J.; Novak, E.; Rosenthal, B.; Voss, E. Amorphic lenses: A mobility aid for patients with retinitis pigmentosa. Am. J. Optom. Physiol. Opt. 62:142-148; 1985. 20. Holm, O.C. A simple method for widening restricted visual fields. Arch. Ophthal. 84:611-612; 1970. 21. Hubel, D.H. Eye, brain and vision. New York: Scientific American Library; 1988: pp. 127-135. 22. Hubel, D.H.; Wiesel, T.N. Receptive fields and functional architecture of monkey striate cortex. J. Physiol. 195:215-243; 1968. 23. Jones, K.E.; Campbell, P.K.; Normann, R.A. A glass/silicon composite intracortical electrode array. Ann. Biomed. Eng. 20:423-437; 1992. 24. Keesey, U.T. Effects of involuntary eye movements on visual acuity. J. Opt. Soc. Am. 50:769-774; 1960.
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25. Legge, G.E.; Pelli, D.G.; Rubin, G.S.; Schleske, M.M. Psychophysics of reading-I. Normal vision. Vision Res. 25:239-252; 1985. 26. Legge, G.E.; Rubin, G.S.; PeUi, D.G.; Schleske, M.M. Psychophysics of reading-II. Low vision. Vision Res. 25:253-266; 1985. 27. Marron, J.A.; Bailey, I.L. Visual factors and orientation-mobility performance. Am. J. Optom. Physiol. Opt. 59:413-426; 1982. 28. Najafi, K.; Wise, K.D. An implantable multielectrode array with on-chip signal processing. IEEE J. Solid-State Circuits SC-21:1035-1044; 1986. 29. Normann, R.A.; Campbell, P.K.; Jones, K.E. A silicon based electrode array for intracortical stimulation: Structure and electrical properties. Proc. Ann. Intl. Conf. IEEE Eng. Med. Biol. Soc. 11:939940; 1989. 30. Pan American Health Organization. Primary eye care manual. Washington, DC: World Health Organization; 1985. 31. Prohaska, O.J.; Olcaytug, F.; Pfunder, P.; Dragaun, H. Thin-film multiple electrode probes: Possibilities and limitations. IEEE Trans. Biomed. Eng. BME-33:223-229; 1986. 32. Simons, K. Visual acuity and the functional definition of blindness. In: Tasman, W., ed. Clinical ophthalmology, Vol. 5, Chapter 51. New York: J.B. Lippincott Co.; 1990. 33. Stensaas, S.S.; Eddington, D.K.; Dobelle, W.H. The topography and variability of the primary visual cortex in man. J. Neurosurg. 40:747-755; 1974. 34. Westheimer, G.; McKee, S.P. Visual acuity in the presence of retinal-image motion. J. Opt. Soc. Am. 65:847-850; 1975.
0090-6964/92 $5.00 + .00 Copyright 9 1992PergamonPress Ltd.
Simulation of a Phosphene-Based Visual Field: Visual Acuity in a Pixelized Vision System Kichul Cha, Kenneth H o r c h , and Richard A. N o r m a n n Department of Bioengineering University of Utah Salt Lake City, UT (Received 1/4/91; Revised 6/27/91) A visual prosthesis f o r the blind using electrical stimulation o f the visual cortex will require the development o f an array o f electrodes. Passage o f current through these electrodes is expected to create a visual image made up o f a matrix o f discrete phosphenes. The quality o f the visual sense thus provided will be a function o f many parameters, particularly the number o f electrodes and their spacing. We are conducting a series o f psychophysical experiments with a portable "phosphene" simulator to obtain estimates o f suitable values f o r electrode number and spacing. The simulator consists o f a small video camera and monitor worn by a normally sighted human subject. To simulate a discrete phosphene field, the monitor is masked by an opaque perforated film. The visual angle subtended by images f r o m the masked monitor is 1.7 ~ or less, depending on the mask, and falls within the fovea o f the subject. In the study presented here, we measured visual acuity as a function o f the number o f pixels and their spacing in the mask. Visual acuity was inversely proportional to pixel density, and trained subjects could achieve about 20/26 visual acuity with a 1024 pixel image. We conclude that 625 electrodes implanted in a I cm by I cm area near the foveal representation o f the visual cortex should produce a phosphene image with a visual acuity o f approximately 20/30. Such an acuity could provide useful restoration o f functional vision f o r the profoundly blind. K e y w o r d s - P h o s p h e n e simulation, Visual prosthesis, Visual acuity.
INTRODUCTION Punctate electrical stimulation of the visual cortex evokes the sensation of a spot of light (phosphene) in the visual field. This suggests that a limited but functional visual sense might be created by electrical stimulation of the visual cortex with an array of electrodes. Feasibility studies of this concept have been performed by Brindley and Lewis (6) and Dobelle and coworkers (11,13). They stimulated the surface of the human visual cortex with an array o f electrodes and found that the resulting phosphenes could produce useful visual patterns and provide a higher rate of information transfer than that obtained by tactile transmission. For example, a blind volunteer was able to read "braille" transmitted by cortical electrical stimulation much faster than Acknowledgments--This project was supported by the W.M. Keck Foundation. Address correspondence to Dr. Ken Horch, Department of Bioengineering, 2480 MEB, University of Utah, Salt Lake City, UT 84112. 439
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he could read tactile braille (13), a significant observation because slow transmission rates have been a serious problem in visual aid devices which act via other sensory modalities. However the electrodes used in these studies were positioned on the surface of the cortex and failed to produce images that were useful for functional restoration of vision because of the limited number of phosphenes and their irregular, noncontiguous distribution. Electrode spacing limits the total number of electrodes which can be implanted in a given area of cortex. The number and spacing of the electrodes determine the acuity and the scope of the resulting visual sense. Based on these considerations, a functionally useful visual prosthesis would require an array of numerous, closely spaced electrodes. Stimulation of the visual cortex with penetrating electrodes can evoke phosphenes with less current than is required with surface stimulation (1,3,10), producing more focal excitation of neurons and allowing electrodes to be placed closer together. We have been able to produce an array of closely spaced electrodes which penetrate the visual cortex as a multichannel, silicon-based microstructure (7,23,29). In order to develop a visual prosthesis based on penetrating cortical electrodes, it is essential to know how many electrodes are needed and how closely spaced they should be in order to achieve a given quality of visual sensation. We are addressing this issue by conducting psychophysical experiments with a phosphene simulator which optically creates visual sensations similar to those expected to be produced by intracortical stimulation of the foveal projection in the brain. This paper describes the apparatus and presents data from the first of our studies: determining spatial resolution (visual acuity) as a function of pixel number and spacing. The results indicate that an array of 625 electrodes spaced approximately 400/~m apart could provide good acuity when implanted in foveal cortex. METHODS Phosphene Simulator
The device was designed to optically simulate the visual sensation of a field of punctate phosphenes similar to that produced by electrical stimulation of the visual cortex with an array of penetrating electrodes. Figure 1 is a diagram of the optics used
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FIGURE 1. Simulator optics. The subject views a small video monitor which projects an image encoded by a miniature video camera, A perforated mask placed over the monitor fragments the image into discrete pixels, which are sized below the limit of visual resolution for the subjects. Lenses adjust the size of the projected image so that it subtends an angle of 1.7 ~ with the largest mask. The acceptance angle of the camera can be adjusted by external lenses.
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in the simulator. A small monochrome video monitor projects images encoded by a camera to the subject's right eye. Optical lenses are placed between the monitor and the subject's eye to reduce the image size and to correct for the subject's ametropia. The monitor is masked with a perforated film to create a field of punctate phosphenes. The mask was made by photographically projecting an array of small holes onto a thin Cr film with a pattern generator, developing the image and etching it chemically. Because the monitor screen is viewed only through the holes, the image consists of a discrete number o f dots (pixels). Each perforation on the mask is a 63.5 • 63.5 #m square. The visual acuity of the human eye is such that subjects cannot resolve changes in intensity within a pixel, but can recognize differences in image brightness between different perforations. Thus, each pixel appears to the subject as a point source o f light which is uniform in intensity. Simulation Parameters
Three parameters are important in determining the quality o f a pixelized image: the number of pixels, their density, and their range of intensities. In an implanted electrode array, the brightness of individual phosphenes can be modulated by the amplitude of current injected through a given electrode (6,11). We have paid little attention to brightness modulation in the work reported here because this experiment uses high contrast stimuli: white targets presented on a black background. Two sets of masks were prepared (Fig. 2). Each set contained four masks: 1024 (32 • 32), 625 (25 • 25), 256 (16 x 16), or 100 (10 x 10) pixels. The 32 x 32 mask was the same for both sets and had a center-to-center spacing between neighboring pix-
FIGURE 2. Masks used in the present study. The basic mask provided a 3 2 • 32 array of pixels, with a pixel spacing of twice the size of an individual pixel. Fixed-field (FF) masks covered the same visual
angle as the basic mask, but spaced the pixels uniformly within this area. Fixed-spacing (FS) masks maintained the same spacing as the basic mask, but restricted the field size. The clear mask limited the visual field to the same visual angle as the FF masks.
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els o f 127 t~m, twice the width of a perforation. All masks had the same size pixels, but the spacings between pixels and the size of the fields were varied as follows. Fixed-field masks incorporated a square array of pixels uniformly spaced over a 1.7 ~ visual field. In these masks, the larger the number of pixels, the closer the pixel spacing. The spacing between centers o f the neighboring pixels for each mask in this set can be calculated by dividing 1.7 ~ by the number of pixels in a column or a row. Fixed-spacing masks had the same pixel spacing as the 32 • 32 mask, but the number of pixels was varied. The larger the number of pixels in these masks, the larger the subtended field. In addition to pixel masks, a clear mask was prepared. This allowed the subjects to view the monitor directly, but with optics and a visual field size, 1.7 ~ which matched those present with the pixelized masks. Acuity Tests
A common and internationally accepted method of measuring visual acuity was employed in these tests (16,30,32). The letter " E " was presented on a computer monitor as a white target on a black background. The contrast o f the E on the monitor was maintained above 80% and the size of each branch of the E was 20% o f the height o f the E. The orientation o f the E was randomly varied by the computer among four o r t h o g o n a l directions, and the size o f the E was varied at each presentation. The subject sat 1 m from the computer monitor, viewed the screen through the simulator, and indicated the orientation of the E using a keypad. The target was presented for 1.5 s, a time sufficient to judge the direction of the E (2). The subjects were encouraged to use head movements during inspection of the target. A staircase procedure was used to determine threshold size for detecting target orientation. If the subject correctly identified the orientation of the E, the letter was made smaller on the subsequent presentation. Otherwise, it was made larger. Threshold was defined as the letter size where the subject changed from correct to incorrect identification of orientation, or vice versa. A trial took 2 to 3 min, during which the threshold was checked 5 times, starting with a size E that was well above threshold. The highest and lowest threshold values were discarded from the data set. Between trials, the subject removed the simulator and rested for 3 to 5 min. Six subjects were recruited from the undergraduate student population at the University of Utah. All subjects had an uncorrected visual acuity o f 20/30 or better. Each subject participated in a 1 h session, consisting o f 6-7 trials, per day over a 3 month period. RESULTS Simulator
Figure 3 is a photograph of the simulator. The device consists of a Sony HVM-302 monochrome video camera with the automatic gain control disabled, a JVC VF-P1U CRT monitor, and optical lenses, all o f which are mounted on a pair o f ski goggles. The lens o f the goggles has been replaced with a piece of opaque plastic. The simulator is portable and can be powered by a battery pack. The subject has complete mobility and can scan objects with voluntary head movements.
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FIGURE 3. The visual phosphene simulator. The optical system is mounted on a pair of ski goggles which are occluded except where the screen of the video monitor (M) is placed. A lens placed in front of the video camera (C), which is mounted just above the monitor, controls the field magnification ratio. Lenses placed between the monitor and the subject's eye adjust the size of the visual field presented to the subject. The monitor is masked by an array of pinholes, so the image is composed of discrete spots of light. The device is portable and the subject can scan objects with head movements. The only visual input available to the subject is the image on the masked monitor. A battery belt (B) is worn around the waist so that the subject can move around freely.
Pixelized Images
Figure 4 shows images photographed from the masked monitor, and should be viewed from a distance such that each image appears about the size of your thumb nail viewed at arms' length. The three images are presented in order to give the reader
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FIGURE 4. An image viewed with different masks. The object was photographed directly from the simulator through a "clear" mask (A), a 3 2 • 3 2 mask (B), and a 16 • 16 fixed-field mask (C). The image size seen by the subjects is equivalent to the size of your thumb nail viewed at arm's length.
a feel for the relationship between image quality and pixel density. The left photograph was taken through a "clear" mask. The clear mask exposed the same portion of the monitor as the fixed-field masks but was not divided into pixels, so that the resulting image was continuous. The other two photographs were taken through fixed-field masks containing different numbers of pixels. Images viewed with different fixed-spacing masks would be portions o f the image viewed with a 32 x 32 mask image. From this figure, it is clear that as pixel spacing increases, acuity decreases. Each pixel produced by the simulator corresponds to a separate punctate phosphene, similar to what is expected to be produced by a single cortical electrode. The number of phosphenes and their spacing is simulated by using masks with different numbers of perforations and different perforation spacings. Visual A cuity
The size of an object's image on the simulator's monitor depends not only on the actual size of the object, but also on the acceptance angle of the camera, which can be varied by external lenses. For the acuity tests, this was held constant at 13 ~. The image was condensed and projected onto the 1.7 ~ field seen by the subject looking at the monitor. To provide a standardized reference, the acuity data presented here are estimated from the angular size of the letter E as presented to the subject's eye. The actual size of a target can be calculated by multiplying this value by the field magnification ratio, 7.6. For the first two weeks, the six subjects were trained with a 32 • 32 mask and a clear mask to familiarize themselves with the device. The average acuity for all subjects using a 32 x 32 mask improved by more than a factor of two over this time. After this period, subject performance stabilized, and each subject was given 10 sets of trials for each mask in the two sets. In addition, trials with the clear mask were conducted to determine if subject performance might somehow be limited by the optics o f the simulator. Figure 5 shows average visual acuity during the final 10 sets of trials as a function of the center-to-center angular spacing between neighboring pixels. Solid symbols show results with fixed-field masks, and open symbols show results with fixed-spacing masks.
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FIGURE 5. Average visual acuity, expressed as Snellen acuity, versus spacing between mask pixels (perforations), expressed in terms of subtended visual angle. The solid symbols show average values • standard deviations from the experiments in which the pixel spacing varied with pixel number (fixed-field masks). The open symbols show the results from experiments in which the pixel spacing was held constant while the number of pixels was varied (fixed-spacing masks). Fixed-field mask sizes were: clear (plotted as equivalent to a mask made up of fused pixels), 32 x 32, 25 • 25, 16 • 16 and 10 x 10. The line shows expected acuity if the subject required a 2.1 x 2.1 pixel grid to recognize the orientation of the target letter.
The left-most solid symbol is data from the clear mask condition. The spacing was calculated by assuming that the mask was completely filled with pixels. Subjects exhibited an average acuity of about 20/20 under this condition: individual values depended on the subject's own acuity. Acuities with other masks depended on the type of mask used. Acuity fell to 20/26 with a 32 • 32 mask and to 20/100 with a 10 • 10 fixed-field mask. Between the 25 • 25 and 10 • 10 masks, inclusive, acuity was inversely proportional to pixel spacing with fixed-field masks. With fixed-spacing masks, which had different numbers of pixels but the same spacing as the 32 x 32 mask, subjects manifested the same acuity as with the 32 x 32 mask. From this, we conclude that pixel density, rather than pixel number, is the key component in determining acuity with this system. The number of pixels required to determine the orientation of the E can be calculated from the acuity tests. For each mask, a threshold size E covered a grid of about 2.1 x 2.1 pixels (Fig. 5). Less formal tests with a Landolt C as the target gave similar results, suggesting that a sampling frequency of about 2 cycles/character is required to identify the orientation of that letter. DISCUSSION Simulator
The portable phosphene array simulation system described here successfully provides a pixelized visual field to subjects, while allowing them freedom to scan their
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environment with head movements. This creates a visual sense similar to what we expect would be produced by an array of electrodes implanted into the visual cortex. One potentially significant difference between our device and a cortical implant is that the simulator allows subjects to scan the phosphene field with eye movements. In subjects implanted with an array of cortical electrodes, eye movements would produce an apparent shift in the perceived location o f the field, but no change in the image with respect to its apparent location on the retina. However, recent experiments using a stabilized image system indicate that this is not an important effect for acuity (Cha, et al., unpublished paper). Subjects became adept at using the device relatively rapidly: their performance stabilized at near normal acuity with high density masks after less than 10 hours of practice over a 2-week period. More complicated visual tasks, such as spatial orientation, are expected to take more practice, but informal tests have indicated that even in these cases subjects can readily learn to use the visual information provided by the simulator. We believe, therefore, that this system provides a valid and useful tool for quantifying basic design parameters for visual prosthetic cortical implants. Pixel Density
The subjects' visual acuity with the simulator depended primarily on pixel spacing, much as the spatial resolution of the eye depends on receptor density in the retina (18). The essentially linear relationship between visual acuity and pixel density indicates that the sampling density required to determine the orientation of a letter was constant. Calculation showed that this density was somewhat over 4 pixels per letter, a value comparable to the 5 pixels per letter suggested by Brindley as sufficient to read ideally designed letters (5). Similarly, a reading test with text sampled by a dot matrix array showed that subjects could read text in which each letter consisted of a 2.8 x 2.8 array of dots (25). Head M o v e m e n t s
Neither eye movements (24) nor smooth movements of a target (34) enhance or impair visual acuity. However, we observed that voluntary head movements did help our subjects with the low pixel density masks. For example, our subjects showed a sudden improvement in performance right after they were encouraged to use head movements. This effect was not apparent with high density masks. Acuity improvement with voluntary head movements may be due to temporal integration during inspection o f a target object, or it may be a result of the subjects using head movements to find the best viewing position to identify the orientation of the target letter. For patients using a visual prosthesis in which the camera is attached to a pair o f eyeglass frames, voluntary head movements may be useful in improving spatial resolution, in detecting obstacles and in spatial orientation. Applications
This study tested a visual sense composed of a number of simulated punctate phosphenes distributed evenly within the foveal visual field. To apply our results to the design of an array of electrodes, we need consider the relationship between the array and the anatomical structure o f the human visual cortex.
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Input to primary visual cortex is basically a two-dimensional retinotopic map (14,22). However, because the cortex is folded in a convoluted pattern, phosphenes produced by two adjacent electrodes can appear far apart in the visual field if the electrodes fall on separate gyri (14). An array of electrodes designed to penetrate into the cortex and implanted in a single gyrus would avoid this problem of spatial discontinuity. However, this requires that the electrode array be sufficiently small to fit on a single gyrus. The cortical magnification factor, defined as the linear distance in the cortex corresponding to an angular distance of 1 ~ in the visual field, is about 6 m m / ~ at the foveal projection (8,9,17,21). Accordingly, two phosphenes, produced by electrodes 315 #m apart, should appear separated by about 3' of arc in the visual field. A 32 x 32 electrode array, with center-to-center spacing of 315 #m between electrodes, should occupy about 1 cm 2. When implanted near the foveal projection, such an array should produce a total visual field of about 1.7 ~ . However it is not always possible to know what part of the foveal projection is represented on a particular location of a given gyrus in humans due to cortical variations between individuals (33). If an implanted array deviates from the center of the foveal projection, neighboring phosphenes will appear further apart because the cortical magnification ratio decreases. As a result, the apparent size of the visual field will increase. How closely neighboring electrodes can be placed before corresponding phosphenes fuse with each other is an important question because it sets an upper limit on electrode density. The limit of two point discrimination in the fovea, l' of arc, corresponds to about 100/~m in layer IVc of visual cortex (21). Cortical penetrating electrodes should be designed to target this layer because it has small receptive fields (10). If intracortical electrodes were spaced such that they evoked contiguous but discrete phosphenes, an array of 625-1024 electrodes could be packed in a square matrix with an area of 1 cm 2. Future Study
The goal of our cortical prostheses work is to provide the blind with a functional visual sense which can be used to facilitate the activities of daily life. The data presented here show that we can achieve high visual acuity in a restricted visual field with a limited number of pixels, provided that they are closely spaced. Such "tunnel vision" would be adequate for pattern recognition tasks such as reading (26, Cha, et al., unpublished paper), but the restricted visual field would be a serious problem in orientation and mobility (15,27). To solve the latter problem it may be possible to use an optical field expander which expands the field of view at the expense of making objects look smaller. Field expanders decrease visual acuity in proportion to the field magnification ratio, but have been found to enhance orientation and mobility if patients have a central visual acuity of at least 20/50 (19,20). CONCLUSION A visual sense composed of about 625 discrete phosphenes within a visual field of 1.7 ~ provides 20/30 visual acuity. Such a visual sense could be useful for pattern recognition tasks, and could be produced, in principle, with a 25 x 25 array of intracortical electrodes implanted within a 1 cm 2 area on a single gyrus of the primary visual
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cortex near the foveal projection. We believe that such a visual prosthesis could be developed using current microfabrication technologies (4,7,23,28,29,31).
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25. Legge, G.E.; Pelli, D.G.; Rubin, G.S.; Schleske, M.M. Psychophysics of reading-I. Normal vision. Vision Res. 25:239-252; 1985. 26. Legge, G.E.; Rubin, G.S.; PeUi, D.G.; Schleske, M.M. Psychophysics of reading-II. Low vision. Vision Res. 25:253-266; 1985. 27. Marron, J.A.; Bailey, I.L. Visual factors and orientation-mobility performance. Am. J. Optom. Physiol. Opt. 59:413-426; 1982. 28. Najafi, K.; Wise, K.D. An implantable multielectrode array with on-chip signal processing. IEEE J. Solid-State Circuits SC-21:1035-1044; 1986. 29. Normann, R.A.; Campbell, P.K.; Jones, K.E. A silicon based electrode array for intracortical stimulation: Structure and electrical properties. Proc. Ann. Intl. Conf. IEEE Eng. Med. Biol. Soc. 11:939940; 1989. 30. Pan American Health Organization. Primary eye care manual. Washington, DC: World Health Organization; 1985. 31. Prohaska, O.J.; Olcaytug, F.; Pfunder, P.; Dragaun, H. Thin-film multiple electrode probes: Possibilities and limitations. IEEE Trans. Biomed. Eng. BME-33:223-229; 1986. 32. Simons, K. Visual acuity and the functional definition of blindness. In: Tasman, W., ed. Clinical ophthalmology, Vol. 5, Chapter 51. New York: J.B. Lippincott Co.; 1990. 33. Stensaas, S.S.; Eddington, D.K.; Dobelle, W.H. The topography and variability of the primary visual cortex in man. J. Neurosurg. 40:747-755; 1974. 34. Westheimer, G.; McKee, S.P. Visual acuity in the presence of retinal-image motion. J. Opt. Soc. Am. 65:847-850; 1975.
