A Comparison of Color and Luminance Discrimination in Amblyopia

Arthur Bradley,* Charles Dahlman, Eugene Swirkes,t and Karen De Valois

Using isochromatic luminance gratings and isoluminant red-green color gratings, examined luminance and color discrimination in amblyopia were examined. Complete color and luminance contrast sensitivity functions were measured monocularly from each eye of six normal and six amblyopic observers. Similar spatial frequency-specific color and luminance discrimination deficits were found in five of the amblyopes. One amblyope with a slight luminance deficit showed no color deficit. It appears that color and luminance discrimination are similarly affected in most amblyopes when spatial factors are effectively controlled. Invest Ophthalmol Vis Sci 27:1404-1409, 1986

Amblyopia is defined clinically as a reduction in vi- more severe amblyopia. Therefore, although the data sual acuity with no apparent refractive or pathological are not plentiful, these tests suggest that color discrim- cause.1 Recently, psychophysical studies have found a ination may be normal in amblyopia. wide variety of visual anomalies associated with am- While color discrimination may appear to be normal blyopia. Most amblyopes exhibit spatial frequency- in amblyopia when measured with standard tests, it is specific reductions in contrast sensitivity.2"5 Amblyopic important to realize that, in amblyopia, luminance sensitivity is reduced maximally at high spatial fre- discrimination also appears approximately normal quencies, but can be normal, or nearly so, at low spatial when tested with large targets.1516 Thus, although the frequencies. A spatial frequency-dependent deficit is published descriptions of color discrimination in am- observed on a wide variety of monocular visual tasks blyopia may indeed reflect an inherently different effect in amblyopia. For example, phase discrimination,6 of amblyopia on chromatic and luminance discrimi- motion detection,7 flicker detection,8 spatial frequency nation (normal color vision but impaired luminance discrimination,9 and orientation discrimination10 all discrimination), these results are also consistent with show larger deficits at higher spatial frequencies than a spatial frequency specific deficit for both color and at low frequencies. luminance discrimination that does not show up when All of the studies described above involved lumi- amblyopes are tested with large (low spatial frequency) nance varying patterns. Little is known about color targets. Because of the interesting neurophysiological discrimination in amblyopia. Published reports on this implications of these possibilities, we have compared subject are scarce,""14 and do not report systematic luminance and color discrimination as a function of variations of the spatial parameters of their stimuli. spatial frequency in six amblyopes. Five of the six am- Three studies""13 used clinically available color dis- blyopes exhibit a similar spatial frequency-specific def- crimination tests (HRR plates, D-15, 28-Hue), and icit for both color and luminance discrimination. one14 examined wavelength discrimination with 1° targets. These studies found either normal color dis- Materials and Methods crimination in fixating amblyopes, or reduced discrimination consistent with the eccentric fixation in Subjects Six normal and six amblyopic subjects participated From the School of Optometry and the Department of Psychology, in these experiments. All volunteered after receiving a University of California, Berkeley, California, and the tDepartments complete description of the experimental protocol. of Chemistry and Psychobiology, University of California, Santa Cruz, Clinical data from all six amblyopes are shown in California. Table 1. * Present address: Department of Visual Sciences, Indiana Uni- versity. Supported by Grants PHS EY-00014 and NSF BNS 82-02275 (to Apparatus ES and KDeV). Submitted for publication: June 17, 1985. Horizontal luminance and color sinusoidal gratings Reprint requests: Arthur Bradley, School of Optometry, Indiana (mean luminance 8 ft. L.) were generated on a Mit- University, Bloomington, IN 47405. subishi (Torrance, CA) 30 Hz interlaced RGB monitor.

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Table 1. Clinical data from the six amblyopic subjects used in this study Fixation of Patient Subject Age Refractive error Visual acuity Strabismus amblyopic eye history

CD 38 +3.00 20/15 6AEXO Unsteady P +7.50-1.25X85 20/200 1AI S(36) ss 15 +0.25 20/15 NONE Unsteady noP -8.50 -3.25 X 09 20/100 centric noS ML 28 +7.50 20/20 6AEXO, 8AHypo Steady U +7.50 20/200 0.5AN noS DR 34 piano-0.25 X 115 20/20 NONE Unsteady noP + 1.25-0.75X65 20/50 centric noS DM 30 + 1.50 20/15 8AESO, 2AHYPO Steady noP +2.5 20/70 1-2 AN S(22) BS 39 -1.75 -1.00 X 180 20/15 small angle Steady P -1.00-1.50 X 15 20/200 esotrope centric noS

NA = non-amblyopic eye, A = amblyopic eye, I = inferior, N = nasal, ESO S = surgery (the number in brackets indicates the age of surgery). U = patching esotropia, EXO = exotropia, HYPO = hypotropia, P = childhood patching, history unknown.

Zero contrast luminance and color gratings were iden- computer control. Threshold settings were recorded by tical: a homogeneous 8 ft. L. yellow field comprising computer and subsequently averaged (geometric a 4 ft. L. contribution from each of the red and green means) and printed out. This method produced average color guns. From this zero contrast condition, two types standard errors of less than 0.07 log units. of patterns are generated. In both cases, the R and G Prior to each experiment, subjects were shown su- signals were modulated equally in luminance, produc- prathreshold stimuli. They were then encouraged to ing sinusoidal red and green luminance gratings of the practice setting color and luminance gratings to same luminance contrast. A yellow luminance-mod- threshold contrasts. For patterns defined by luminance ulated grating was obtained by presenting the red and contrast, a criterion of "just seeing stripes" on the green luminance gratings with the same spatial phase. screen was used. For color contrast, subjects were in- Conversely, isoluminant color-modulated red-green structed to set thresholds when they could "just see gratings were produced by presenting the red and green colored stripes." Subjects were encouraged to adopt a luminance gratings 180 degrees out of phase. All grat- low criterion for both tests, and maintain the same ings were sinusoidally counter-phase modulated at 1 criterion when tested with their amblyopic and non- Hz. amblyopic eyes. In addition to the contrast sensitivity measurements, Procedure all amblyopes were tested monocularly with both HRR Photometric (Spectra-Pritchard; Photo Research, pseudo-isochromatic plates and with the D-15 color Burbank, CA) luminance calibrations for each gun were vision tests. adjusted slightly for each eye of all amblyopic observers using individual flicker photometric settings made prior Results to each experiment. No significant differences between the flicker matches for the amblyopic and non-am- In addition to recording color and luminance con- blyopic eyes were observed for any of the six amblyopes. trast sensitivity functions from both eyes of amblyopes, Gratings were viewed from 172 cm, at which dis- we conducted similar tests on a sample of six previously tance the circular aperture subtended 9°. All subjects untested, naive, visually normal observers. Each of were instructed to fixate the center of the screen. This these observers had corrected visual acuity of 20/20 in large field ensured that even the eccentrically fixating each eye, less than 0.25 diopter difference in refractive amblyopes in our sample (Table 1) were stimulated error between the eyes, and no strabismus. foveally. Complete contrast sensitivity data from one normal All subjects were tested monocularly with each eye. observer are shown in Figure 1 A. Luminance contrast Contrast sensitivities at seven spatial frequencies (0.25, sensitivity (circles) shows a pattern typical for gratings 0.7, 1.4,2.8,4.0, 5.6, 8.0 c/deg.) were measured. Three modulated sinusoidally at 1 Hz. With this temporal threshold settings were made at each spatial frequency modulation, the pronounced low spatial frequency fall- using a method of adjustment procedure. The complete off in sensitivity observed with stationary gratings is series of 21 stimuli were randomly interleaved under attenuated.17 Sensitivity peaks near 2 c/deg and declines

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300 approximately 0.5 c/deg, such that sensitivity at 4 c/ deg is reduced by almost a factor often. We have plotted data for both the right (filled sym- 100 bols) and left (open symbols) eyes of this normal observer. The two eyes show very similar functions. The \- small fluctuations in the right and left eye functions 30 manifest themselves as small interocular sensitivity dif- f E ferences. These have been plotted in Figure IB. Circles Z 0.5 L servers (Fig. 1). The pattern observed for amblyopic eyes (open circles) is qualitatively similar. However, in .25 .5 each case, the amblyopic eye shows reduced sensitivity over all or some of the frequency range. The amblyopes SPATIAL FREQUENCY (c/deg) (BS and SS) whose data are shown in the top two panels, Fig. 1. A, Luminance (circles) and color (triangles) contrast sen- exhibited the largest difference between the two eyes. sitivity (1 /contrast threshold) data are shown for the right (filled sym- They had large interocular differences in sensitivity at bols) and left (open symbols) eyes of one normal observer. Luminance all spatial frequencies. The two amblyopes (DR and contrast is denned as (Lmax - Lmin)/(Lmax + Lmin)- Color contrast is ML), whose data are shown in the middle two panels, denned by the luminance contrast of the component red or green luminance gratings used to create it (see Materials and Methods for also exhibit reduced sensitivity at all spatial frequencies, details). Using this definition, 100% color contrast describes a color but the interocular differences are much smaller than modulation from the color of the green phosphor (X = 0.2805, Y those of BS and SS. The two data sets shown in the = 0.5994) to the color of the red phosphor (X = 0.6115, Y = 0.3524). bottom two panels (CD and DM) show interocular B, Circles and triangles represent the interocular contrast sensitivity ratios (right eye/left eye) for luminance and color, respectively. The contrast sensitivity differences over only part of the horizontal dashed line (ratio = 1.0) indicates equal sensitivity in both spatial frequency range. Subject DM manifests only a eyes. The two horizontal dotted lines represent the average (for all small contrast sensitivity deficit in his amblyopic eye, six normal observers) interocular contrast sensitivity difference (0.11 even though Snellen acuity is reduced to 20/70 (Table log units). 1). Although there are differences in the magnitude and frequency extent of the contrast sensitivity differ- slightly between 2 and 8 c/deg. Although luminance ences between the amblyopic and non-amblyopic eyes gratings up to 40-50 c/deg can be detected by normal of these six amblyopes, a similar trend exists. In all observers,18 we restricted our measurements to the 0.25 cases, the interocular difference in luminance contrast to 8 c/deg range because we wished to compare color sensitivity is greater at high than at low spatial fre- and luminance contrast sensitivity, and color contrast quencies. can only be detected over a limited range of spatial The color contrast sensitivity data are displayed in frequencies.19"22 This difference in the luminance and a similar format in Figure 3. Data from the non-am- color contrast sensitivity functions can be seen in Figure blyopic eyes (filled circles) typically lie above those from 1A. Color contrast sensitivity begins to decline above the amblyopic eyes (open circles). The non-amblyopic

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eyes exhibit contrast sensitivity functions similar to those of the normal subjects (Fig. 1). Unlike the luminance contrast sensitivity function, color contrast sensitivity functions do not show a peak, but typically show a continuous decrease above 0.25-0.5 c/deg. Al- though displaced, the amblyopic color contrast sensitivity functions also show the same pattern. Again, subjects BS and SS (top two panels) show large reductions in sensitivity at all spatial frequencies. Data from amblyopes DR and ML show smaller differences between the two eyes over the whole range of spatial frequencies. CD only shows reduced sensitivity to color contrast above 2 c/deg. Interestingly, as with his luminance data, DM showed interocular color contrast sensitivity differences within the range of normal observers. The specific goal of this study is to compare luminance and color discrimination in amblyopia. The

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30 O , 10 s \> .25 .5 I 2 4 8 .25 .5 I 2 4 8 3 SPATIAL FREQUENCY (c/deg) BS SS I Fig. 3. Monocular color contrast sensitivity functions for the non- I I amblyopic (filled circles) and amblyopic (open circles) eyes of six amblyopes (BS, SS, DR, ML, CD, DM).

color contrast sensitivity functions (Fig. 3), although very different from the luminance functions in shape (Fig. 2), seem to produce similar interocular differences between the amblyopic and non-amblyopic eyes. This apparent similarity in the color and luminance deficits is confirmed quantitatively for five of the six amblyopes. The interocular luminance (filled circles) and color (open circles) contrast sensitivity ratios (non-amblyopic/amblyopic) are shown in Figure 4. Data from each amblyope are shown in the same order as used in Figures 2 and 3. The horizontal dashed line in each panel indicates no interocular sensitivity difference (ratio = 1). The similarity between the two data sets is striking. With the exception of DM (bottom right panel), the interocular sensitivity ratio functions for both color and luminance parallel each other over the I L i i i i i i i i i i i complete range of spatial frequencies. .25 .5 I 2 4 8 .25 .5 I 2 4 8 The data in Figure 4 suggest that the color discrim- SPATIAL FREQUENCY (c/deg) ination deficit is precisely correlated with the luminance contrast sensitivity deficit. This correlation appears to Fig. 2. Monocular luminance contrast sensitivity functions for the non-amblyopic (filled circles) and amblyopic (open circles) eyes of hold across individuals (those with large luminance six amblyopes (BS, SS, DR, ML, CD, DM). deficits have large color deficits, e.g., BS), and across

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20 r minance discrimination in amblyopia. Although some small differences were observed, the most striking fea- IO BS - SS ture of the data was the close similarity between the color and luminance deficits. Therefore, although all six amblyopes performed normally on both the HRR and D-15 color vision tests, we cannot conclude that their color vision is normal. Both luminance and color discrimination can appear normal or abnormal in amblyopia, depending on the choice of spatial parameters of the test stimulus. The possibility that color discrimination could re- main normal in amblyopia is interesting because of neurophysiological evidence showing that some degree of separate processing of color and luminance occurs within the primate visual system.23 The suggestion by earlier studies11"14 that color vision may have been normal in amblyopia indicated, therefore, that amblyopia might selectively affect only that subset of neurons responsible for detecting luminance differences. How- ever, our results, showing parallel deficits for color and luminance, preclude such a selective neural affect in amblyopia. In addition to our data showing impaired color discrimination in amblyopia, Harwerth and Levi24 found evidence of abnormal red-green interactions in severe amblyopia. Three possible explanations are consistent with our data. First, amblyopia affects discrimination at a point in the visual system subsequent to the segregation of color and luminance signals, but affects each system equally. Second, the effects of amblyopia on visual dis-

10 O cc _J .25 .5 I 4 8 .25 .5 I 2 4 8 ID *—* SPATIAL FREQUENCY (c/deg) O o o 1- 1 *> Fig. 4. Interocular contrast sensitivity ratios (non-amblyopic/am- 1 < 6 blyopic) for luminance (filled circles) and color (open circles). Each cr panel shows both data sets for each amblyope. Horizontal lines (ratio Ixl >- = 1) indicate equal contrast sensitivity for the two eyes. Z > spatial frequencies. The regularity of this correlation oc can be seen in Figure 5 where the magnitude of the o z interocular luminance and color deficits have been o LxJ •+ plotted against each other. Most of the data closely o CO .65 parallel the oblique dashed line (Y = X), but there is .65 10 a slight tendency for the interocular color contrast sensitivity ratio to be greater than the luminance ratio. LUMINANCE INTER- OCULAR The data from amblyope DM (+'s) cluster near the X SENSITIVITY RATIO (N/A) = 1, Y = 1 point (equal sensitivity in both eyes). Fig. 5. Interocular color contrast sensitivity ratios (N/A) have been plotted on the ordinate as a function of the magnitude of the lumi- Discussion nance interocular contrast sensitivity ratio. Each symbol-type rep- resents data from one of the six amblyopes (BS, 0; SS, O; DR, •; Controlling for the effect of spatial frequency and ML, A; CD, •; DM, +). The diagonal dashed line (Y = X) reflects eccentric fixation, we have compared color and lu- the locus of points where luminance and color deficits are identical.

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crimination occur at a point in the visual system prior isometropic and strabismic amblyopia. Invest Ophthalmol Vis to separation of luminance and color information (e.g., Sci 16:90, 1977. at the photoreceptors). Finally, it is possible that our 5. Bradley A and Freeman RD: Contrast sensitivity in anisometropic amblyopia. Invest Ophthalmol Vis Sci 21:467, 1981. data reflect some experimental artifact. Residual re- 6. Lawden MC, Hess RF, and Campbell FW: The discriminability fractive errors would impair the detection of both lu- of spatial phase relationships in amblyopia. Vision Res 22:1005, minance and chromatic gratings. Also, large luminance 1982. miscalibrations would introduce significant luminance 7. Rentschler I, Hilz R, and Brettel H: Amblyopic abnormality modulations in our nominally isoluminant gratings. If involves neural mechanisms concerned with movement processing. Invest Ophthalmol Vis Sci 20:695, 1981. these chromatic gratings were detected on the basis of 8. Bradley A and Freeman RD: Temporal sensitivity in amblyopia: the luminance artifact and not the color modulation, An explanation of conflicting reports. Vision Res 25:39, 1985. parallel deficits in both experiments would be expected. 9. Hess RF, Burr DC, and Campbell FW: A preliminary investi- Our experiments do not distinguish between the first gation of neural function and dysfunction in amblyopia-III co- two possibilities. However, recent electroretinogram operative activity of amblyopic channels. Vision Res 20:757, 25 1980. (ERG) data from amblyopes showing normal pattern 10. Skottun BC, Bradley A, and Freeman RD: Orientation discrim- ERG in the presence of large contrast sensitivity deficits ination in amblyopia. Invest Ophthalmol Vis Sci 27:532, 1986. suggest a more central site for the anomaly. Careful 11. Francois J and Verriest G: La discrimination chromatique dans repeat refractions of our subjects and previous reports l'amblyopie strabique. Doc Ophthalmol 23:318, 1967. of contrast sensitivity deficits in amblyopes when grat- 12. Roth A: Le sens chromatique dans amblyopie fonctionelle. Doc Ophthalmol 24:113, 1968. ings are produced via interference fringes2'5 make re- 13. Lumbroso BD and Proto F: Le anomalie del senso cromatico sidual refractive errors an unlikely source of our find- nei soggetti ambliopici con fissazione eccentrica. Bollettino ings. Finally, extremely large luminance mismatches d'Oculistica 42:699, 1963. (100% in some cases) would be required to attribute 14. Marre M and Marre E: Color vision in squint amblyopia. Mod our "color" contrast sensitivity data to luminance ar- Probl Ophthalmol 19:308, 1978. 15. Miller E: Investigation of the nature and cause of impaired acuity tifacts. For example, subject BS has a contrast sensi- in amblyopia. Am J Optom Physiol Optics 32:10, 1955. tivity of approximately 50 at .25 c/deg for both the 16. Fankhauser F and Rholer R: The physical stimulus, the quality "color" (red-green) gratings (Fig. 3) and luminance of the retinal image and foveal brightness discrimination in one gratings (Fig. 2). Thus, short of a 100% mismatch, BS amblyopic and two normal eyes. Doc Ophthalmol 23:149, 1967. would be unable to detect the .25 c/deg "color" grating 17. Robson JG: Spatial and temporal contrast-sensitivity functions of the human visual system. J Opt Soc Am 56:1141, 1966. solely on the basis of a luminance artifact. Therefore, 18. Campbell FW and Green DG: Optical and retinal factors affecting it is unlikely that refractive errors or luminance artifacts visual resolution. J Physiol 181:576, 1965. can account for our data. 19. van der Horst GJ and Bauman MA: Spatiotemporal chromaticity discrimination. J Opt Soc Am 59:1482, 1969. Key words: amblyopia, color vision, contrast sensitivity, spa- 20. Granger EM and Heurtley JC: Visual chromaticity-modulation tial frequency transfer function. J Opt Soc Am 63:1173, 1973. 21. Kelly DH: Spatiotemporal variation of chromatic and achromatic References contrast thresholds. J Opt Soc Am 73:742, 1983. 1. Duke-Elder WS and Wybar K: Ocular motility and strabismus. 22. Mullen KT: The contrast sensitivity of human color vision to In Systems of Ophthalmology, Duke-Elder WS, editor. London, red-green and blue-yellow chromatic gratings. J Physiol (Lond) Henry Kimpton, 1973. 359:381, 1985. 2. Gstalder RJ and Green DG: Laser interferometric acuity in am- 23. De Valois RL, Abramov I, and Jacobs GH: Analysis of response blyopia. J Pediat Ophthalmol 8:251, 1971. patterns of LGN cells. J Opt Soc Am 56:966, 1967. 3. Hess RF and Howell ER: The threshold contrast sensitivity 24. Harwerth RS and Levi DM: Increment threshold spectral sen- function in strabismic amblyopia: evidence for a two-type clas- sitivity in anisometropic amblyopia. Vision Res 17:585, 1977. sification. Vision Res 17:1049, 1977. 25. Hess RF and Baker CL: Assessment of retinal function in severely 4. Levi DM and Harwerth RS: Spatio-temporal interactions in an- amblyopic individuals. Vision Res 24:1367, 1984.

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