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Contrast effects of the three primary colors on human visual evoked potentials
Electroencephalograph)' and clinical Neurophvsiologv. 1983, 5 5 : 5 5 7 - 5 6 6 Elsevier Scientific Publishers Ireland, Ltd.
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C O N T R A S T E F F E C T S OF T H E T H R E E PRIMARY C O L O R S O N H U M A N VISUAL EVOKED P O T E N T I A L S t.z W.R. K L E M M 3, R.A. G O O D S O N and R.G. A L L E N Laser EjJet'ts Branch, USA F School of A erospace Medicine, Brooks Air Force Base, Tex. 78235 (U. S, A.) (Accepted for publication: January 13, 1983)
A principal and commonly studied property of human vision is the ability to discern different degrees of luminance or contrast. Contrast response can be derived psychophysiologically or in a more objective way from the electroencephalographic visual evoked potential (VEP) which is caused by a black-and-white stimulus containing a known contrast (for an introduction to this literature, see Kelly 1973 and DeValois and DeValois 1980). The white-light stimulus in such studies is of course a mixture of the primary colors, blue, red and green. The contribution that each makes to the overall contrast response is not known. Although it seems reasonable to expect that a person's contrast response to white light is in some way related to his sensitivity to the component colors, there is no evidence of the nature of this relationship. Single-cell responsiveness in the visual cortex of monkeys indicates that color contrast may be processed by cells other than the well-known 'simple, complex and hyper-complex' cells that are sensitive to achromatic contrast. Chromatic stimuli are sequentially processed by 4 classes of cortical
i Tile voluntary informed consent of the subjects used in this report was obtained in accordance with A F R 169-3. z The research reported in this paper was conducted by personnel of the Laser Effects Branch, Radiation Sciences Division, U S A F School of Aerospace Medicine, Aerospace Medical Division, AFSC, United States Air Force, Brooks Air Force Base, Tex., U.S.A. 3 To whom reprint requests should be sent: Departments of Veterinary A n a t o m y and Veterinary Small Animal Medicine and Surgery, Texas A and M, University College Station, Tex. 77843, U.S.A.
neurons (located in layer IV) that are a distinctly separate population from the achromatic-sensitive cells (Michael 1978a). These cells have a dual-opponent color organization, with fields consisting of a central rectangular strip of one color (red or green) and two antagonistic flanks with the reverse opponent arrangement. Thus, these color-specific cells could well influence the VEP response to colored counterphased stimuli and make the responses to color much different than to white-light stimuli. In short, one may not be able to predict the response to color on the basis of the response to white light. Indeed, early literature on color effects on transient VEPs suggests that the responses are color specific, although interpretations of such results are controversial (Regan 1972; Spekreijse et al. 1977). Contrast response for color vision has not to our knowledge been studied under conditions where the objective was to discriminate between different contrast levels of the same patternedstimulus color, with accompanying comparison of the sensitivities for different colors. Indeed, for technical reasons, few laboratories are appropriately equipped to perform this kind of study with the more modern technique of counterphased pattern stimulation. Of the few color vision studies that have been reported, a common approach has been to evaluate vision by counterphasing (alternatively reversing) various spatio-temporal patterns of two different colors or of one color and black (Regan 1973, 1974). Studies employing two luminance levels of the same color have been reported, but they involved unstructured stimuli (Regan 1968). Subsequent evoked response studies showed that the human visual system probably
0013-4649/83/0000-0000/$03.00 © 1983 Elsevier Scientific Publishers Ireland, Ltd.
558 processes color information differently when the colored stimulus is spatially structured (Regan 1973, 1977). A black-and-white checkerboard counterphased-pattern stimulus is popular for various reasons, not the least of which is the relatively large VEP that it produces (Regan 1972; Spekreijse 1980). Of particular interest to lhis present research is the question of whether contrast effects with colored checks vary in the same way as with black-and-white. We therefore wished to test for contrast effects, given a constant mean luminance level, for each of the 3 primary colors that contribute to the white-light effects that have been tested by others.
Methods
Subjects The subjects were 10 healthy adult males, of whom 7 had been subjects in previous studies involving counterphased black-and-white-patterned stimuli. All subjects had normal visual acuity (or were corrected by eyeglasses which were worn during the study). All subjects had normal color vision, as indicated by the FarnsworthMunsell 100-hue test.
Visual stimulation The stimulus was a checkerboard pattern, viewed binocularly, involving two luminance levels of the same color (either blue, red, or green). This patterned stimulus was presented on an Aydin 8026 high-resolution color monitor. The 1/2-amplitude bandwidth for the phosphors was 420-480, 500-550 and 600-680 nm for blue, green and red, respectively. The average luminance of the screen was the same for all presentations, 1.35 f i e The subject was situated, with chin resting comfortably on a head rest and support, 1 m from the screen. The contrast between counterphased checks was varied in steps of 0.1, from 0.1 to 0.5. The luminance settings required to achieve the desired degree of contrast while holding average luminance the same was determined from the formula B p / B a , where Bp = the peak deviation ( + or - ) from the average overall luminance, and Ba = the average
W.R. KLEMM ET AL. overall luminance (1.35 ftL). Direct photometric monitoring confirmed that the average luminance remained constant during all patterned stimulus or ' b l a n k screen' trials. The target size was 3.4 ° in diameter, and the element size of each check was 4.37 c/degree (6.8 rain of arc/check). This small check size was selected to maximize the contribution of the cones to the response to each color. A counterphase reversal rate of 6 Hz was used. This frequency had been proved to be effective in evoking VEPs in our previous studies. Lower reversal rates were avoided because our previous studies revealed that there could be a problem with 'contamination' of the spectral analysis with spontaneous delta frequencies; occasionally, for example, inspection of the averaged wave form disclosed components that were at the stimulus frequency but clearly not synchronously driven by the stimulus.
Electroencephalographic recording Silver cup electrodes were used to record the electroencephalogram (EEG) from 3 sites. One electrode was placed on the midline 2.5 cm above the inion and the other electrodes were placed on the right and left hemispheres, 2 cm lateral to the midline electrode; a reference electrode was placed on one ear and a ground on the other. Signals were processed on a Grass 78D multichannel recorder, with half-amplitude filtration settings at 0.3-300 Hz. Signals were displayed by pen (90 Hz cutoff) and simultaneously tape recorded on a multiplechannel, frequency-modulated, Ampex recorder (model 2200) at 17 i m p / s e c speed. Also recorded was a series of synchronizing pulses which triggered the successive 1 sec averaging epochs for the VEP. Subjects were seated in a darkened room with the chin resting comfortably in a head support; they were instructed to focus at all times on a small dot in the center of the visual field. White noise was delivered binaurally through earphones.
Data analysis Using a PDP 11/34 computer, the EEG was digitized and averaged for 90 successive 1 sec epochs. The averaged VEP was then further
E V O K E D RESPONSES TO P A T T E R N E D , C O L O R E D STIMULI
559
analyzed by spectral analysis, using the Fast Fourier Transform (FFT) with a rectangular window and no digital filtering. The power spectrum (PSD) was calculated with 1 Hz resolution, but in a typical VEP the vast majority of the total power was contained precisely at the fundamental counterphase frequency (6 Hz) and at the corresponding 2nd and 3rd harmonics. Values reported are the sum of the powers at these 3 frequencies. Prior to each experimental session a 20 ~V square wave was fed into the amplifiers, processed through the entire system, and analyzed to compare the power at the fundamental and harmonic frequencies to assure equalization of gain and spectral wave form in each recording channel. Commonly the power for a given 90 sec epoch was smaller than that for shorter epochs (30 sec). When the averages and corresponding complete spectra were plotted for the 3 subepochs and the 90 sec epoch, it was clear that the larger power values for the subepochs included a substantial amount of noise (i.e., some of the power at 6 Hz was 'accidental' and not a phase-locked response to the stimulus). Since the longer averaging period reduces noise, we regarded the 90 sec PSDs as our most reliable data, and only those values are reported. To permit correlation analysis between the power of the VEP and the simultaneously occurring amount of alpha activity, we also computed power over the band of 8-12 Hz. Average power was calculated at each individual frequency (1 Hz resolution) and for the total of all integer frequencies within the alpha band. The alpha power was computed during the maximum-contrast trials during the last 2 replication trials. The power was computed during each successive second, and these values averaged over the 90 sec of each trial.
were tested again in the same sequence, using 2 trials at the maximum contrast of 0.5, as a test of replicability.
Protocol
R.G.
Each subject was stimulated with 90 sec trials, each separated by a 15 sec 'blank screen' which had the same color and overall luminance as the immediately following stimuli trial. The first trials were presented at 6 Hz in descending sequence from 0.5 to 0.1 contrast, followed by a repeat of the 0.5 contrast trial. Colors were tested in the order of blue, red and green. Then these colors
Results
Replicability For each color, the 6 Hz stimulus at a contrast of 0.5 was repeated in each subject 4 times, twice in the contrast tests and twice during replication testing. No consistent trends suggestive of either habituation or of a practice effect were noted for repeating a stimulus condition. Variation among the 4 replicate trials depended on the subject and the color. The variation ranged from standard errors of 10% of the mean power to 54% of the mean. Analysis of the variation in each subject (Table I) revealed that some subjects were distinctly more consistent than others (compare R.H. and W.K. to C.J. and F.R.). Some differences in variance within a subject seemed to depend on color. The amount of variance tended to be inversely related to the magnitude of the
TABLE I Variation of evoked responses - - log of standard deviation. Subject
W.K. R.H. G.C. J.B.
W.G. C.J. F.R.
Mean, all colors
Color Blue
Red
Green
0.10 (2.62) * 0.21 (2.75) 0.28 (2.20) 0.13 (2.52) 0.20 (2.51) 0.31 (1.38) 0.12 (1.68) 0.47 (2.40)
0.19 (2.42) 0.13 (2.74) 0.12 (2.30) 0.22 (2.23) 0.21 (2.62) 0.13 (1.73) 0.23 (1.87) 0.29 (2.40)
0.13 (2.52) 0.12 (2.69) 0.08 (2.30) 0.19 (2.33) 0.17 (2.51) 0.22 (1.54) 0.35 (1.79) 0.41 (1.63)
0.14 (2.52) 0.15 (2.73) 0.16 (2.27) 0.18 (2.36) 0.19 (2.55) 0.22 (1.55) 0.23 (1.78) 0.39 (2.14)
Stimulus of 6 Hz, 0.5 contrast, n = 4 for each condition. * Mean power, log scale.
560
W.R. K L E M M ET AL.
evoked response, although F.R. was unusual in having large responses and large variances.
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Relationship to alpha activity For each color (at 0.5 contrast) we tested the possibility that overall alpha activity and the VEP might interfere with each other. Including all subjects, no statistically significant correlations could be demonstrated (the largest, - 0 . 4 4 , was to blue). Similar results were obtained when computations did not include data from the t~o subjects with consistently small VEPs.
Relationship between VEP and subjective impressions Most subjects had definite subjective color 'preferences,' believing that they responded poorly or well to one or more colors. When these impressions were compared with the actual magnitude of the VEP, it was obvious that subjects were often wrong. For example, G.C. thought he responded especially well to red, yet the power at 6 Hz was essentially the same for all colors. R.H. thought that red was his best color, but his power did not vary much with color and blue produced the largest power. J.B. believed that he responded the same to all colors, but his average power with blue was twice that of his response to red. C J . thought that red was 'irritating' and he even had mental lapses where he did not remember seeing the screen, yet his largest power values were with red.
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Contrast effects The shapes of the VEP contrast-response curves are shown in Figs. 1-3. For each color, the response magnitude was generally very low at the lowest contrast and generally appeared to reach a maximum in the region of 0.3-0.5. The 3 highercontrast stimuli producing the greatest response varied by color and by subject. The shape of the curves exhibited saturation at the higher contrasts for some subjects. Some caveats must be kept in mind when deciding upon the true shape of these contrast-response curves. Each data point has associated with it an unknown amount of variability, and within-subject variability problems in VEP studies are common
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0.70 0.61 1.00 0.79 0.39 1.00 0.62 0.68
0.74 0.46 0.65 1.00 0.40 0.81 0.90 0.83
0.70 0.07 0.45 0.06 0.13 .0.67 0.29 0.48
0.74 0.05 0.29 0.07 0.14 0.54 0.42 0.59
0.49 0.02 0.27 0.04 0.14 0.40 0.39 0.64
0.49 0.13 0.60 0.57 0.42 0.60 0.85 0.89
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0.56 0.03 0.24 0.01 0.07 0.15 0.10 0.29
0.56 0.23 0.54 0.18 0.22 0.22 0.21 0.40
0.2
0.28 0.03 0.25 0.01 0.03 0.09 0.01 0.02
0.28 0.23 0.54 0.16 0.10 0.13 0.01 0.03
0.1
0.54 0.04 0.27 0.01 0.26 0.50 0.46 0.44
0.54 0.35 0.59 0.17 0.77 0.74 1.00 0.61
0.5
0.50 0.08 0.18 0.05 0.28 0.30 0.23 0.30
0.50 0.72 0.39 0.69 0.84 0.45 0.51 0.42
0.5
_ Red
0.70 0.04 0.16 0.07 0.24 0.11 0.12 0.36
0.70 0.34 0.36 0.89 0.70 0.17 0.25 0.50
0.4
* Each subject's greatest power value was set to 1.00. ** The largest power value in the entire group of data points was set to 1.00.
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Color effects. Relative VEP power.
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0.43 0.04 0.21 0.05 0.22 0.11 0.07 0.20
0.43 0.37 0.47 0.61 0.66 0.17 0.16 0.29
0.3
0.40 0.03 0.14 0.04 0.17 0.16 0.03 0.07
0.40 0.23 0.31 0.52 0.50 0.24 0.07 0.09
0.2
0.19 0.02 0.23 0.03 0.06 0.03 0.01 0.15
0.19 0.15 0.51 0.41 0.18 0.04 0.02 0.21
0.1
0.81 0.07 0.08 0.06 0.15 0.08 0.26 0.71
0.81 0.64 0.18 0.83 0.44 0.12 0.57 1.00
0.5
0.53 0.12 0.11 0.02 0.26 0.16 0.28 0.25
0.53 1.00 0.25 0.22 0.76 0.23 0.60 0.35
0.5
Green
0.55 0.04 0.19 0.03 0.34 0.05 0.26 0.18
0.55 0.37 0.42 0.36 1.00 0.07 0.57 0.26
0.4
1.00 0.05 0.26 0.02 0.25 0.05 0.16 0.21
1.00 0.47 0.59 0.31 0.73 0.08 0.35 0.30
0.3
0.55 0.03 0.19 0.01 0.16 0.06 0.13 0.09
0.55 0.28 0.42 0.11 0.48 0.10 0.27 0.13
0.2
0.08 0.01 0.22 0.01 0.003 0.03 0.01 0.02
0.08 0.07 0.48 0.07 0.01 0.05 0.03 0.02
0.1
0.42 0.04 0.22 0.05 0.19 0.04 0.31 0.23
0.42 0.31 0.49 0.64 0.55 0.06 0.68 0.32
0.5
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W.R. K LEMM ET AL.
(Spekreijse 1980). Our experience indicates that there is enough variation to require a conservative evaluation of curve shape (Table II). These data were also plotted in terms of amplitude (i.e., the square root of the power) as a log function of contrast, inasmuch as linear relationships on such scales have been reported between amplitude and contrast for black-and-white stimuli (Campbell and Maffei 1970). For the 6 subjects showing the largest VEP magnitudes and the larges! signal-to-noise ratios, only one (F.R.) produced results that seemed to indicate a possible linear relationship for all 3 colors, and his replication trials were not consistent (Table II). Four of the other subjects had results clearly indicating a saturation effect for at least 2 of the 3 colors. Colors which apparently caused saturation effects varied by subject and did not correlate with the subjectively preferred colors. A given subject commonly had a physiologically 'preferred' color in that VEP amplitudes at that color were conspicuously larger than at other colors (see normalized data, Table II); this color was not always the one which the subject preferred psychophysically. No one color stood out as preferred across subjects (Figs. 1-3 and Table II). However, in 5 subjects, blue caused generally larger power values than did other colors in these subjects (see data for J.B., R.G., and F.R. for examples). Of the remaining 5 subjects, one (R.H.) had his largest response to green, and the others responded about equally to each color.
Subjects differed greatly in the magnitude of VEP responses (Table II). Note for example in Fig. 3 that the response at a contrast of 0.3 in subject R.H. was about 4 times larger than that of any other subject at that contrast (he also responded conspicuously better at 3 other contrast levels). Two subjects had such small VEPs that their data were omitted from the illustrations and the tables. Not only did subjects differ several-fold in VEP magnitude, but at a given color the shape of the contrast-response curves apparently differed. Many subjects seemed to have notable differences in the curve shape at certain colors. Note for example the curve of R.H. to green, compared to the curve of other subjects at green or even to his own responses at the other colors. As another example, subject F.R. had an almost linearly increasing response to blue, as did W.K. to red and green (but not blue).
Hemispheric differences For a given subject, the VEPs to the physiologically preferred color were largest over the midline electrode. The degree of hemispheric lateralization was generally mild, except for subject W.K. (Fig. 4). Such results also show that the previously described large effects of contrast and of color also applied to recordings taken over both hemispheres. In all subjects with conspicuous responses, the 800 E
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EVOKED RESPONSESTO PATTERNED, COLORED STIMULI shapes of the contrast-response curves derived from laterally placed electrodes were similar to those seen for midline-derived data. One subject had unusual responses at high contrast, wherein the responses to red and green did not increase with increasing contrast; these changes were evident not only at the midline (Table II, J.B.) but also at both lateral electrodes (Fig. 5).
Discussion
563 jects. This suggests that the neural mechanisms for processing spatial visual input are likewise color dependent, a conclusion which is supported by several other aspects of the present results. The between-subject variability is quite evident. Pertinent to this observation is a recent psychophysical study with sinusoidal red and green gratings which showed that subjects could not detect contrast if the image were stabilized on the retina (Kelly 1981). Thus, any inter-subject variability in eye movement during fixation on the target might well have accounted for differences in VEP.
Contrast effects
Color-specific effects
The contrast data for most subjects and most conditions appear to be non-linear. These response patterns do not show the same relationship between VEP amplitude and log contrast, as shown with black and white stimulation as originally described by Campbell and Maffei (1970) and by Tyler et al. (1978). It is noted that Ginsburg et al. (1980) in psychophysical testing with suprathreshold black-and-white stimuli found a linear relationship between a subject's estimate of contrast and the actual contrast. If our demonstration of apparent non-linearity should be confirmed, then two conclusions emerge: (1) The reported linear responses to black-andwhite gratings may be more apparent than real, reflecting a kind of averaging of the non-linearities in the responses at various wave lengths. Our small check sizes, chosen because we were trying to differentiate color responses in the dense cone area, do not seem to account for our curve shapes because linear curves are still reported even with very small black and white checks (Campbell and Maffei 1970; Tyler et al., 1978). This explanation seems more parsimonious with the widely held belief that neuronal function in general tends to be non-linear. (2) If non-linearities exist in color processing, they would serve to restrict the kind of mathematical modeling (Ginsburg et al. 1980) which may prove to be appropriate for analysis of the visual cues that are required for the perception of the color of complex objects. The differences in shapes of contrast-response curves were also color dependent in certain sub-
The common inability of subjects to identify those colors to which they respond most effectively suggests that this aspect of visual processing in the primary visual cortex may occur at a subconscious level. These results with color also confirm similar results in our previous experiments with blackand-white vertical gratings (Klemm et al. 1980). Of more fundamental importance is the fact that there were clear differences in the PSDs with certain colors in certain subjects. At a given and equal level of intensity, contrast and check size, the VEP amplitude varied markedly among and within subjects, depending on the color being tested. The psychological and behavioral implications of these differences in color responsiveness are not known, but they can be presumed to exist on the basis of other reports as well as our own (see references in Siegfried 1978). The most straightforward way to test for colorspecific VEP effects might seem to be the use of a counterphase stimulus where red, green or blue checks alternate with black. However, this approach is said to be ineffective for revealing color specificities (White et al. 1977). Color-specific effects have been observed for specific components of transient VEP responses to unstructured red, green or blue flash stimuli superimposed on various adapting colored backgrounds (White et al. 1977). This adaptation or isolation technique is based on the selective modulation of one color system while driving the other into saturation. Regan (1956) had previously reported that VEP amplitudes were larger for isolated red and blue
564 than for yellow sinusoidally modulated stimuli. All 3 colors evoked responses over the range of about 8 - 2 0 Hz, with a peak near 10 Hz; response to yellow was much smaller than to red or blue even for a stimulus that was 10 times brighter. In a later study Regan (1974) reported interesting interference effects from superimposing a colored spot over a counterphasing checkerboard pattern of red or green alternating with black. The color of the spot which was most effective in reducing the response to the red checks was not, as might be expected, when the spot's color was the same (676 nm) as the red checks. Using a similar chromatic adaptation technique and unstructured stimuli, White and Hintze (1978) concluded from transient VEPs that the two eyes differed and that this was reflected in the VEP response to the different stimulus colors. Spekreijse et al. (1977) reported that the transient evoked response to each of the isolated colors tested (red, green, yellow and blue) showed similar wave forms and were also similar to white-light responses. All colors evoked contrast-related responses, and the amplitude of the VEP appeared to be linear when plotted against the log of contrast for red and green, but not for yellow. Responses to yellow seemed to saturate at about 8% contrast, whereas no saturation was seen for red or green up to 50% contrast. In a psychophysical study of contrast threshold at different spatial frequencies, Kelly (1973) found that when using intense adapting colors that isolated red, green or blue responses, the responses differed from each other and from the white-light grating. The green mechanism seemed to be the most sensitive and the blue much less sensitive. Isolated blue mechanisms seem to be particularly anomalous, and one human VEP study has shown that flash-evoked responses to blue light were less complex and more delayed than were red-green responses. It also took a larger check size to produce maximal responses with blue light (Klingaman and Moscowitz-Cook 1979). However, this study only involved 3 subjects, and the 'inferiority' of blue may not be universal. Our results of relatively larger responses to blue in 5 subjects certainly indicate that blue can be a relatively effective stimulus under steady-state conditions.
W.R. KLEMM ET AL. Feature detection Contemporary vision theorists put great emphasis on the edge-detection properties of visual systems. Historically, these properties have been studied in terms of edge boundaries between white and black, but even with color, the psychophysical importance of edge effects has been known for some time (McCree 1960). Kelly (1974) has shown with alternating 2-color stimulation that edge detection makes a major contribution to the VEP. Response magnitude was least when the flickering stimulus was patternless and greatest when there were large numbers of edges in a checkerboard pattern. Thus, the visual cortex seems to be organized in such a way as to permit edge detection at specific wave lengths. The existence of wave length-specific edge detectors has recently been confirmed by the discovery of cells that selectively respond to colored edges, both stationary (Michael 1978a) and moving (Michael 1978b). Therefore, VEPs in response to white-light stimuli are presumably integrated or 'averaged' over the individual responses at the various wave length components of white light. If so, our results would suggest that the edge-detection properties of the visual cortex vary with color (in addition to contrast). By inference, the white-light responses would not necessarily reflect the response characteristics at given wave lengths, nor do they necessarily reflect the large differences among or within subjects in the ability to respond to certain wave lengths.
Summa~ In this study we evaluated in humans the question of whether contrast effects with patterned color stimuli varied in the same way as is known to occur with black-and-white stimuli. Using a counterphasing checkerboard pattern, we evaluated the steady-state visual evoked potential (VEP) in 10 subjects for the response to different contrast levels in each of the 3 primary colors. Overall mean luminance of each color was photometrically equated and kept constant during all trials. The VEP was computer-averaged for 90 consecutive I sec epochs of stimulation, and the power at the
EVOKED RESPONSES TO PATTERNEI). COLORED STIMULI
appropriate frequency was calculated. For each color, the contrast-response curves revealed small power values at low contrast (0.1) and larger power at the 3 high-contrast settings (0.3--0.5). Power varied markedly by color and by subject. The shape of the curves, depending on color and subject, often indicated a saturation of response. A given subject commonly had a physiologically 'preferred' color in that the power with that color was consistently larger. Most subjects had definite subjective color 'preferences,' believing that they perceived the contrast better for one or two colors. However, these impressions were often not validated by the VEP responses to the various colors. These results indicate that white-light VEP responses may not necessarily reflect the response characteristics of specific colors, nor do they necessarily reflect the large inter- and intra-subject differences in color responses noted in this study.
565
couleur et selon le sujet. La forme des courbes, d6pendante de la couleur et du sujet, a souvent indiqu6 une saturation de la r6ponse. Un sujet donn6 avait commun6ment une couleur 'pr6f6r6e' physiologiquement, c'est-~-dire que la puissance pour cette couleur 6tait plus grande. La plupart des sujets avaient d'indiscutables 'pr6f6rences' subjectives de couleurs, croyant qu'ils percevaient mieux le contraste pour une ou deux couleurs. Toutefois ces impressions ne furent pas souvent confirm6es par les r6ponses PEV aux diff6rentes couleurs. Ces r6sultats indiquent que les r6ponses PEV la lumi6re blanche ne refl6tent pas n6cessairement les caract6ristiques des r6ponses ~ des couleurs donn6es, et ne traduisent pas non plus obligatoirement la grande diff6rence inter- et intra-individuelle dans les r6ponses aux couleurs, telles que nous les rapportons dans cette 6tude.
References R6sum6
Effets de contraste avec les trois couleurs primaires sur les potentiels 6voqu6s humains Dans cette 6tude nous avons recherch6 chez l'homme si les effets de contraste avec des stimulus color6s varient de la m~me fagon (qui est bien connue) qu'avec des stimulus en noir et blanc. En utilisant un 6chiquier h renversement, nous avons 6valu~ le potentiel ~voqu~ visuel (PEV) en r~gime stable chez 10 sujets, en r6ponse h diff6rents niveaux de contraste, et ceci pour chacune des 3 couleurs primaires. La luminance moyenne totale dans chaque primaire 6tait 6galisbe photom6triquement et maintenue constante au cours de tousles essais. Le PEV 6tait moyenn6 sur ordinateur pour 90 p+riodes cons~cutives de stimulation de 1 sec et la puissance 6tait calculb.e pour la fr6quence appropri6e. Pour chaque couleur, les courbes de r6ponse au contraste ont accus6 des valeurs de puissance basse faible contraste (0,1) et plus importante pour les 3 niveaux 61ev6s de contraste test6s (0,3-0,5). La puissance h vari6 de faqon importante selon la
Campbell, F.W. and Maffei, L. Electrophysiological evidence for the existence of orientation and size detectors in the human visual system. J. Physiol. (Lond.), 1970, 207: 635-652. DeValois, R.L. and DeValois, K.K. Spatial vision. Ann. Rev. Psychol., 1980, 31: 309-341. Ginsburg, A.P., Cannon, M.W. and Nelson, M.A. Suprathreshold processing of complex visual stimuli: evidence for linearity in contrast perception. Science, 1980, 208: 619-621. Kelly. D.H. Lateral inhibition in human colour mechanisms. J. Physiol. (Lond.), 1973, 228: 55-72. Kelly, D.H. Spatio-temporal frequency characteristics of color-vision mechanisms. J. Opt. Soc. Amer., 1974, 64: 983--990. Kelly, D.H. Disappearance of stabilized chromatic gratings. Science, 1981, 214: 1257-1258. Klemm, W.R., Gibbons, W.D., Allen, R.G. and Richey, E.O. Ocular dominance and brain lateralization effects on the visual evoked response. Physiol. Psychol., 1980, 8: 409-416. Klingaman, R.L. and Moscowitz-Cook, A. Assessment of the visual acuity of human color mechanisms with the visually evoked cortical potential. Invest. Ophthal., 1079, 18: 1273 -1277. McCree, K.J. Color confusion produced by voluntary fixation. Optica Acta, 1960, 7: 281-290. Michael, C.R. Color vision mechanisms in monkey striate cortex: simple cells with dual opponent-color receptive fields. J. Neurophysiol., 1978a, 41: 1233-1249. Michael, CR. Color-sensitive complex cells in monkey striate cortex. J. Neurophysiol., 1978b, 41: 1250-1266.
566 Regan, D. An effect of stimulus colour on average steady-state potentials evoked in man. Nature (Lond), 1966, 210: 1056-1057. Regan, D. Chromatic adaptation and steady-state evoked potentials. Vision Res., 1968, 8: 149-158. Regan, D. Evoked Potentials in Psychology, Sensory Physiology, and Clinical Medicine. Chapman and Hall, London, 1972. Regan, D. Evoked potentials specific to spatial patterns of luminance and colour. Vision Res., 1973, 13: 2381-2402. Regan, D. Electrophysiological evidence for colour channels in human pattern vision. Nature (Lond.), 1974, 250: 437-439. Regan, D. Evoked potential indicators of the processing of pattern, color, and depth information. In: J.E. Desmedt (Ed.), Visual Evoked Potentials in Man: New Developments. Clarendon Press, Oxford, 1977: 234-285. Siegfried, J.B. VECP: its spectral sensitivity. In: J.C. Armington, J. Krauskopf and B.R. Wooten (Eds.), Visual Psychophysics and Physiology. Academic Press, New York, 1978: 257-266.
W.R. KLEMM ET AL. Spekreijse, H. Pattern evoked potentials: principles, methodology, and phenomenology. In: C. Barber (Ed.), Evoked Potentials. MTP Press, Lancaster, 1980: 55-74. Spekreijse, H., Estevez, O. and Reits, D. Visual evoked potentials and the physiological analysis of visual processes in man. In: J.E. Desmedt (Ed.), Visual Evoked Potentials in Man: New Developments. Clarendon Press, Oxford, 1977: 16-89. Tyler, C.W., Apkarian, P. and Nakayama, K. Multiple spatialfrequency tuning of electrical responses from human visual cortex. Exp. Brain Res., 1978, 33: 535-550. White, C.T. and Hintze, R.W. Color evoked potentials: cortical and subcortical elements. In: D. Lehmann and E. Callaway (Eds.), Human Evoked Potentials. Plenum Press. New York, 1978: 431-442. White, C.T., Kataoka, R.W. and Martin, J.I. Colour-evoked potentials: development of a methodology for the analysis of the processes involved in colour vision. In: J.E. Desmedt (Ed.), Visual Evoked Potentials in Man: New Developments. Clarendon Press, Oxford, 1977: 250-272.
557
C O N T R A S T E F F E C T S OF T H E T H R E E PRIMARY C O L O R S O N H U M A N VISUAL EVOKED P O T E N T I A L S t.z W.R. K L E M M 3, R.A. G O O D S O N and R.G. A L L E N Laser EjJet'ts Branch, USA F School of A erospace Medicine, Brooks Air Force Base, Tex. 78235 (U. S, A.) (Accepted for publication: January 13, 1983)
A principal and commonly studied property of human vision is the ability to discern different degrees of luminance or contrast. Contrast response can be derived psychophysiologically or in a more objective way from the electroencephalographic visual evoked potential (VEP) which is caused by a black-and-white stimulus containing a known contrast (for an introduction to this literature, see Kelly 1973 and DeValois and DeValois 1980). The white-light stimulus in such studies is of course a mixture of the primary colors, blue, red and green. The contribution that each makes to the overall contrast response is not known. Although it seems reasonable to expect that a person's contrast response to white light is in some way related to his sensitivity to the component colors, there is no evidence of the nature of this relationship. Single-cell responsiveness in the visual cortex of monkeys indicates that color contrast may be processed by cells other than the well-known 'simple, complex and hyper-complex' cells that are sensitive to achromatic contrast. Chromatic stimuli are sequentially processed by 4 classes of cortical
i Tile voluntary informed consent of the subjects used in this report was obtained in accordance with A F R 169-3. z The research reported in this paper was conducted by personnel of the Laser Effects Branch, Radiation Sciences Division, U S A F School of Aerospace Medicine, Aerospace Medical Division, AFSC, United States Air Force, Brooks Air Force Base, Tex., U.S.A. 3 To whom reprint requests should be sent: Departments of Veterinary A n a t o m y and Veterinary Small Animal Medicine and Surgery, Texas A and M, University College Station, Tex. 77843, U.S.A.
neurons (located in layer IV) that are a distinctly separate population from the achromatic-sensitive cells (Michael 1978a). These cells have a dual-opponent color organization, with fields consisting of a central rectangular strip of one color (red or green) and two antagonistic flanks with the reverse opponent arrangement. Thus, these color-specific cells could well influence the VEP response to colored counterphased stimuli and make the responses to color much different than to white-light stimuli. In short, one may not be able to predict the response to color on the basis of the response to white light. Indeed, early literature on color effects on transient VEPs suggests that the responses are color specific, although interpretations of such results are controversial (Regan 1972; Spekreijse et al. 1977). Contrast response for color vision has not to our knowledge been studied under conditions where the objective was to discriminate between different contrast levels of the same patternedstimulus color, with accompanying comparison of the sensitivities for different colors. Indeed, for technical reasons, few laboratories are appropriately equipped to perform this kind of study with the more modern technique of counterphased pattern stimulation. Of the few color vision studies that have been reported, a common approach has been to evaluate vision by counterphasing (alternatively reversing) various spatio-temporal patterns of two different colors or of one color and black (Regan 1973, 1974). Studies employing two luminance levels of the same color have been reported, but they involved unstructured stimuli (Regan 1968). Subsequent evoked response studies showed that the human visual system probably
0013-4649/83/0000-0000/$03.00 © 1983 Elsevier Scientific Publishers Ireland, Ltd.
558 processes color information differently when the colored stimulus is spatially structured (Regan 1973, 1977). A black-and-white checkerboard counterphased-pattern stimulus is popular for various reasons, not the least of which is the relatively large VEP that it produces (Regan 1972; Spekreijse 1980). Of particular interest to lhis present research is the question of whether contrast effects with colored checks vary in the same way as with black-and-white. We therefore wished to test for contrast effects, given a constant mean luminance level, for each of the 3 primary colors that contribute to the white-light effects that have been tested by others.
Methods
Subjects The subjects were 10 healthy adult males, of whom 7 had been subjects in previous studies involving counterphased black-and-white-patterned stimuli. All subjects had normal visual acuity (or were corrected by eyeglasses which were worn during the study). All subjects had normal color vision, as indicated by the FarnsworthMunsell 100-hue test.
Visual stimulation The stimulus was a checkerboard pattern, viewed binocularly, involving two luminance levels of the same color (either blue, red, or green). This patterned stimulus was presented on an Aydin 8026 high-resolution color monitor. The 1/2-amplitude bandwidth for the phosphors was 420-480, 500-550 and 600-680 nm for blue, green and red, respectively. The average luminance of the screen was the same for all presentations, 1.35 f i e The subject was situated, with chin resting comfortably on a head rest and support, 1 m from the screen. The contrast between counterphased checks was varied in steps of 0.1, from 0.1 to 0.5. The luminance settings required to achieve the desired degree of contrast while holding average luminance the same was determined from the formula B p / B a , where Bp = the peak deviation ( + or - ) from the average overall luminance, and Ba = the average
W.R. KLEMM ET AL. overall luminance (1.35 ftL). Direct photometric monitoring confirmed that the average luminance remained constant during all patterned stimulus or ' b l a n k screen' trials. The target size was 3.4 ° in diameter, and the element size of each check was 4.37 c/degree (6.8 rain of arc/check). This small check size was selected to maximize the contribution of the cones to the response to each color. A counterphase reversal rate of 6 Hz was used. This frequency had been proved to be effective in evoking VEPs in our previous studies. Lower reversal rates were avoided because our previous studies revealed that there could be a problem with 'contamination' of the spectral analysis with spontaneous delta frequencies; occasionally, for example, inspection of the averaged wave form disclosed components that were at the stimulus frequency but clearly not synchronously driven by the stimulus.
Electroencephalographic recording Silver cup electrodes were used to record the electroencephalogram (EEG) from 3 sites. One electrode was placed on the midline 2.5 cm above the inion and the other electrodes were placed on the right and left hemispheres, 2 cm lateral to the midline electrode; a reference electrode was placed on one ear and a ground on the other. Signals were processed on a Grass 78D multichannel recorder, with half-amplitude filtration settings at 0.3-300 Hz. Signals were displayed by pen (90 Hz cutoff) and simultaneously tape recorded on a multiplechannel, frequency-modulated, Ampex recorder (model 2200) at 17 i m p / s e c speed. Also recorded was a series of synchronizing pulses which triggered the successive 1 sec averaging epochs for the VEP. Subjects were seated in a darkened room with the chin resting comfortably in a head support; they were instructed to focus at all times on a small dot in the center of the visual field. White noise was delivered binaurally through earphones.
Data analysis Using a PDP 11/34 computer, the EEG was digitized and averaged for 90 successive 1 sec epochs. The averaged VEP was then further
E V O K E D RESPONSES TO P A T T E R N E D , C O L O R E D STIMULI
559
analyzed by spectral analysis, using the Fast Fourier Transform (FFT) with a rectangular window and no digital filtering. The power spectrum (PSD) was calculated with 1 Hz resolution, but in a typical VEP the vast majority of the total power was contained precisely at the fundamental counterphase frequency (6 Hz) and at the corresponding 2nd and 3rd harmonics. Values reported are the sum of the powers at these 3 frequencies. Prior to each experimental session a 20 ~V square wave was fed into the amplifiers, processed through the entire system, and analyzed to compare the power at the fundamental and harmonic frequencies to assure equalization of gain and spectral wave form in each recording channel. Commonly the power for a given 90 sec epoch was smaller than that for shorter epochs (30 sec). When the averages and corresponding complete spectra were plotted for the 3 subepochs and the 90 sec epoch, it was clear that the larger power values for the subepochs included a substantial amount of noise (i.e., some of the power at 6 Hz was 'accidental' and not a phase-locked response to the stimulus). Since the longer averaging period reduces noise, we regarded the 90 sec PSDs as our most reliable data, and only those values are reported. To permit correlation analysis between the power of the VEP and the simultaneously occurring amount of alpha activity, we also computed power over the band of 8-12 Hz. Average power was calculated at each individual frequency (1 Hz resolution) and for the total of all integer frequencies within the alpha band. The alpha power was computed during the maximum-contrast trials during the last 2 replication trials. The power was computed during each successive second, and these values averaged over the 90 sec of each trial.
were tested again in the same sequence, using 2 trials at the maximum contrast of 0.5, as a test of replicability.
Protocol
R.G.
Each subject was stimulated with 90 sec trials, each separated by a 15 sec 'blank screen' which had the same color and overall luminance as the immediately following stimuli trial. The first trials were presented at 6 Hz in descending sequence from 0.5 to 0.1 contrast, followed by a repeat of the 0.5 contrast trial. Colors were tested in the order of blue, red and green. Then these colors
Results
Replicability For each color, the 6 Hz stimulus at a contrast of 0.5 was repeated in each subject 4 times, twice in the contrast tests and twice during replication testing. No consistent trends suggestive of either habituation or of a practice effect were noted for repeating a stimulus condition. Variation among the 4 replicate trials depended on the subject and the color. The variation ranged from standard errors of 10% of the mean power to 54% of the mean. Analysis of the variation in each subject (Table I) revealed that some subjects were distinctly more consistent than others (compare R.H. and W.K. to C.J. and F.R.). Some differences in variance within a subject seemed to depend on color. The amount of variance tended to be inversely related to the magnitude of the
TABLE I Variation of evoked responses - - log of standard deviation. Subject
W.K. R.H. G.C. J.B.
W.G. C.J. F.R.
Mean, all colors
Color Blue
Red
Green
0.10 (2.62) * 0.21 (2.75) 0.28 (2.20) 0.13 (2.52) 0.20 (2.51) 0.31 (1.38) 0.12 (1.68) 0.47 (2.40)
0.19 (2.42) 0.13 (2.74) 0.12 (2.30) 0.22 (2.23) 0.21 (2.62) 0.13 (1.73) 0.23 (1.87) 0.29 (2.40)
0.13 (2.52) 0.12 (2.69) 0.08 (2.30) 0.19 (2.33) 0.17 (2.51) 0.22 (1.54) 0.35 (1.79) 0.41 (1.63)
0.14 (2.52) 0.15 (2.73) 0.16 (2.27) 0.18 (2.36) 0.19 (2.55) 0.22 (1.55) 0.23 (1.78) 0.39 (2.14)
Stimulus of 6 Hz, 0.5 contrast, n = 4 for each condition. * Mean power, log scale.
560
W.R. K L E M M ET AL.
evoked response, although F.R. was unusual in having large responses and large variances.
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Relationship to alpha activity For each color (at 0.5 contrast) we tested the possibility that overall alpha activity and the VEP might interfere with each other. Including all subjects, no statistically significant correlations could be demonstrated (the largest, - 0 . 4 4 , was to blue). Similar results were obtained when computations did not include data from the t~o subjects with consistently small VEPs.
Relationship between VEP and subjective impressions Most subjects had definite subjective color 'preferences,' believing that they responded poorly or well to one or more colors. When these impressions were compared with the actual magnitude of the VEP, it was obvious that subjects were often wrong. For example, G.C. thought he responded especially well to red, yet the power at 6 Hz was essentially the same for all colors. R.H. thought that red was his best color, but his power did not vary much with color and blue produced the largest power. J.B. believed that he responded the same to all colors, but his average power with blue was twice that of his response to red. C J . thought that red was 'irritating' and he even had mental lapses where he did not remember seeing the screen, yet his largest power values were with red.
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Contrast effects The shapes of the VEP contrast-response curves are shown in Figs. 1-3. For each color, the response magnitude was generally very low at the lowest contrast and generally appeared to reach a maximum in the region of 0.3-0.5. The 3 highercontrast stimuli producing the greatest response varied by color and by subject. The shape of the curves exhibited saturation at the higher contrasts for some subjects. Some caveats must be kept in mind when deciding upon the true shape of these contrast-response curves. Each data point has associated with it an unknown amount of variability, and within-subject variability problems in VEP studies are common
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0.70 0.61 1.00 0.79 0.39 1.00 0.62 0.68
0.74 0.46 0.65 1.00 0.40 0.81 0.90 0.83
0.70 0.07 0.45 0.06 0.13 .0.67 0.29 0.48
0.74 0.05 0.29 0.07 0.14 0.54 0.42 0.59
0.49 0.02 0.27 0.04 0.14 0.40 0.39 0.64
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0.56 0.03 0.24 0.01 0.07 0.15 0.10 0.29
0.56 0.23 0.54 0.18 0.22 0.22 0.21 0.40
0.2
0.28 0.03 0.25 0.01 0.03 0.09 0.01 0.02
0.28 0.23 0.54 0.16 0.10 0.13 0.01 0.03
0.1
0.54 0.04 0.27 0.01 0.26 0.50 0.46 0.44
0.54 0.35 0.59 0.17 0.77 0.74 1.00 0.61
0.5
0.50 0.08 0.18 0.05 0.28 0.30 0.23 0.30
0.50 0.72 0.39 0.69 0.84 0.45 0.51 0.42
0.5
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0.70 0.04 0.16 0.07 0.24 0.11 0.12 0.36
0.70 0.34 0.36 0.89 0.70 0.17 0.25 0.50
0.4
* Each subject's greatest power value was set to 1.00. ** The largest power value in the entire group of data points was set to 1.00.
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0.43 0.04 0.21 0.05 0.22 0.11 0.07 0.20
0.43 0.37 0.47 0.61 0.66 0.17 0.16 0.29
0.3
0.40 0.03 0.14 0.04 0.17 0.16 0.03 0.07
0.40 0.23 0.31 0.52 0.50 0.24 0.07 0.09
0.2
0.19 0.02 0.23 0.03 0.06 0.03 0.01 0.15
0.19 0.15 0.51 0.41 0.18 0.04 0.02 0.21
0.1
0.81 0.07 0.08 0.06 0.15 0.08 0.26 0.71
0.81 0.64 0.18 0.83 0.44 0.12 0.57 1.00
0.5
0.53 0.12 0.11 0.02 0.26 0.16 0.28 0.25
0.53 1.00 0.25 0.22 0.76 0.23 0.60 0.35
0.5
Green
0.55 0.04 0.19 0.03 0.34 0.05 0.26 0.18
0.55 0.37 0.42 0.36 1.00 0.07 0.57 0.26
0.4
1.00 0.05 0.26 0.02 0.25 0.05 0.16 0.21
1.00 0.47 0.59 0.31 0.73 0.08 0.35 0.30
0.3
0.55 0.03 0.19 0.01 0.16 0.06 0.13 0.09
0.55 0.28 0.42 0.11 0.48 0.10 0.27 0.13
0.2
0.08 0.01 0.22 0.01 0.003 0.03 0.01 0.02
0.08 0.07 0.48 0.07 0.01 0.05 0.03 0.02
0.1
0.42 0.04 0.22 0.05 0.19 0.04 0.31 0.23
0.42 0.31 0.49 0.64 0.55 0.06 0.68 0.32
0.5
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(Spekreijse 1980). Our experience indicates that there is enough variation to require a conservative evaluation of curve shape (Table II). These data were also plotted in terms of amplitude (i.e., the square root of the power) as a log function of contrast, inasmuch as linear relationships on such scales have been reported between amplitude and contrast for black-and-white stimuli (Campbell and Maffei 1970). For the 6 subjects showing the largest VEP magnitudes and the larges! signal-to-noise ratios, only one (F.R.) produced results that seemed to indicate a possible linear relationship for all 3 colors, and his replication trials were not consistent (Table II). Four of the other subjects had results clearly indicating a saturation effect for at least 2 of the 3 colors. Colors which apparently caused saturation effects varied by subject and did not correlate with the subjectively preferred colors. A given subject commonly had a physiologically 'preferred' color in that VEP amplitudes at that color were conspicuously larger than at other colors (see normalized data, Table II); this color was not always the one which the subject preferred psychophysically. No one color stood out as preferred across subjects (Figs. 1-3 and Table II). However, in 5 subjects, blue caused generally larger power values than did other colors in these subjects (see data for J.B., R.G., and F.R. for examples). Of the remaining 5 subjects, one (R.H.) had his largest response to green, and the others responded about equally to each color.
Subjects differed greatly in the magnitude of VEP responses (Table II). Note for example in Fig. 3 that the response at a contrast of 0.3 in subject R.H. was about 4 times larger than that of any other subject at that contrast (he also responded conspicuously better at 3 other contrast levels). Two subjects had such small VEPs that their data were omitted from the illustrations and the tables. Not only did subjects differ several-fold in VEP magnitude, but at a given color the shape of the contrast-response curves apparently differed. Many subjects seemed to have notable differences in the curve shape at certain colors. Note for example the curve of R.H. to green, compared to the curve of other subjects at green or even to his own responses at the other colors. As another example, subject F.R. had an almost linearly increasing response to blue, as did W.K. to red and green (but not blue).
Hemispheric differences For a given subject, the VEPs to the physiologically preferred color were largest over the midline electrode. The degree of hemispheric lateralization was generally mild, except for subject W.K. (Fig. 4). Such results also show that the previously described large effects of contrast and of color also applied to recordings taken over both hemispheres. In all subjects with conspicuous responses, the 800 E
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Discussion
563 jects. This suggests that the neural mechanisms for processing spatial visual input are likewise color dependent, a conclusion which is supported by several other aspects of the present results. The between-subject variability is quite evident. Pertinent to this observation is a recent psychophysical study with sinusoidal red and green gratings which showed that subjects could not detect contrast if the image were stabilized on the retina (Kelly 1981). Thus, any inter-subject variability in eye movement during fixation on the target might well have accounted for differences in VEP.
Contrast effects
Color-specific effects
The contrast data for most subjects and most conditions appear to be non-linear. These response patterns do not show the same relationship between VEP amplitude and log contrast, as shown with black and white stimulation as originally described by Campbell and Maffei (1970) and by Tyler et al. (1978). It is noted that Ginsburg et al. (1980) in psychophysical testing with suprathreshold black-and-white stimuli found a linear relationship between a subject's estimate of contrast and the actual contrast. If our demonstration of apparent non-linearity should be confirmed, then two conclusions emerge: (1) The reported linear responses to black-andwhite gratings may be more apparent than real, reflecting a kind of averaging of the non-linearities in the responses at various wave lengths. Our small check sizes, chosen because we were trying to differentiate color responses in the dense cone area, do not seem to account for our curve shapes because linear curves are still reported even with very small black and white checks (Campbell and Maffei 1970; Tyler et al., 1978). This explanation seems more parsimonious with the widely held belief that neuronal function in general tends to be non-linear. (2) If non-linearities exist in color processing, they would serve to restrict the kind of mathematical modeling (Ginsburg et al. 1980) which may prove to be appropriate for analysis of the visual cues that are required for the perception of the color of complex objects. The differences in shapes of contrast-response curves were also color dependent in certain sub-
The common inability of subjects to identify those colors to which they respond most effectively suggests that this aspect of visual processing in the primary visual cortex may occur at a subconscious level. These results with color also confirm similar results in our previous experiments with blackand-white vertical gratings (Klemm et al. 1980). Of more fundamental importance is the fact that there were clear differences in the PSDs with certain colors in certain subjects. At a given and equal level of intensity, contrast and check size, the VEP amplitude varied markedly among and within subjects, depending on the color being tested. The psychological and behavioral implications of these differences in color responsiveness are not known, but they can be presumed to exist on the basis of other reports as well as our own (see references in Siegfried 1978). The most straightforward way to test for colorspecific VEP effects might seem to be the use of a counterphase stimulus where red, green or blue checks alternate with black. However, this approach is said to be ineffective for revealing color specificities (White et al. 1977). Color-specific effects have been observed for specific components of transient VEP responses to unstructured red, green or blue flash stimuli superimposed on various adapting colored backgrounds (White et al. 1977). This adaptation or isolation technique is based on the selective modulation of one color system while driving the other into saturation. Regan (1956) had previously reported that VEP amplitudes were larger for isolated red and blue
564 than for yellow sinusoidally modulated stimuli. All 3 colors evoked responses over the range of about 8 - 2 0 Hz, with a peak near 10 Hz; response to yellow was much smaller than to red or blue even for a stimulus that was 10 times brighter. In a later study Regan (1974) reported interesting interference effects from superimposing a colored spot over a counterphasing checkerboard pattern of red or green alternating with black. The color of the spot which was most effective in reducing the response to the red checks was not, as might be expected, when the spot's color was the same (676 nm) as the red checks. Using a similar chromatic adaptation technique and unstructured stimuli, White and Hintze (1978) concluded from transient VEPs that the two eyes differed and that this was reflected in the VEP response to the different stimulus colors. Spekreijse et al. (1977) reported that the transient evoked response to each of the isolated colors tested (red, green, yellow and blue) showed similar wave forms and were also similar to white-light responses. All colors evoked contrast-related responses, and the amplitude of the VEP appeared to be linear when plotted against the log of contrast for red and green, but not for yellow. Responses to yellow seemed to saturate at about 8% contrast, whereas no saturation was seen for red or green up to 50% contrast. In a psychophysical study of contrast threshold at different spatial frequencies, Kelly (1973) found that when using intense adapting colors that isolated red, green or blue responses, the responses differed from each other and from the white-light grating. The green mechanism seemed to be the most sensitive and the blue much less sensitive. Isolated blue mechanisms seem to be particularly anomalous, and one human VEP study has shown that flash-evoked responses to blue light were less complex and more delayed than were red-green responses. It also took a larger check size to produce maximal responses with blue light (Klingaman and Moscowitz-Cook 1979). However, this study only involved 3 subjects, and the 'inferiority' of blue may not be universal. Our results of relatively larger responses to blue in 5 subjects certainly indicate that blue can be a relatively effective stimulus under steady-state conditions.
W.R. KLEMM ET AL. Feature detection Contemporary vision theorists put great emphasis on the edge-detection properties of visual systems. Historically, these properties have been studied in terms of edge boundaries between white and black, but even with color, the psychophysical importance of edge effects has been known for some time (McCree 1960). Kelly (1974) has shown with alternating 2-color stimulation that edge detection makes a major contribution to the VEP. Response magnitude was least when the flickering stimulus was patternless and greatest when there were large numbers of edges in a checkerboard pattern. Thus, the visual cortex seems to be organized in such a way as to permit edge detection at specific wave lengths. The existence of wave length-specific edge detectors has recently been confirmed by the discovery of cells that selectively respond to colored edges, both stationary (Michael 1978a) and moving (Michael 1978b). Therefore, VEPs in response to white-light stimuli are presumably integrated or 'averaged' over the individual responses at the various wave length components of white light. If so, our results would suggest that the edge-detection properties of the visual cortex vary with color (in addition to contrast). By inference, the white-light responses would not necessarily reflect the response characteristics at given wave lengths, nor do they necessarily reflect the large differences among or within subjects in the ability to respond to certain wave lengths.
Summa~ In this study we evaluated in humans the question of whether contrast effects with patterned color stimuli varied in the same way as is known to occur with black-and-white stimuli. Using a counterphasing checkerboard pattern, we evaluated the steady-state visual evoked potential (VEP) in 10 subjects for the response to different contrast levels in each of the 3 primary colors. Overall mean luminance of each color was photometrically equated and kept constant during all trials. The VEP was computer-averaged for 90 consecutive I sec epochs of stimulation, and the power at the
EVOKED RESPONSES TO PATTERNEI). COLORED STIMULI
appropriate frequency was calculated. For each color, the contrast-response curves revealed small power values at low contrast (0.1) and larger power at the 3 high-contrast settings (0.3--0.5). Power varied markedly by color and by subject. The shape of the curves, depending on color and subject, often indicated a saturation of response. A given subject commonly had a physiologically 'preferred' color in that the power with that color was consistently larger. Most subjects had definite subjective color 'preferences,' believing that they perceived the contrast better for one or two colors. However, these impressions were often not validated by the VEP responses to the various colors. These results indicate that white-light VEP responses may not necessarily reflect the response characteristics of specific colors, nor do they necessarily reflect the large inter- and intra-subject differences in color responses noted in this study.
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couleur et selon le sujet. La forme des courbes, d6pendante de la couleur et du sujet, a souvent indiqu6 une saturation de la r6ponse. Un sujet donn6 avait commun6ment une couleur 'pr6f6r6e' physiologiquement, c'est-~-dire que la puissance pour cette couleur 6tait plus grande. La plupart des sujets avaient d'indiscutables 'pr6f6rences' subjectives de couleurs, croyant qu'ils percevaient mieux le contraste pour une ou deux couleurs. Toutefois ces impressions ne furent pas souvent confirm6es par les r6ponses PEV aux diff6rentes couleurs. Ces r6sultats indiquent que les r6ponses PEV la lumi6re blanche ne refl6tent pas n6cessairement les caract6ristiques des r6ponses ~ des couleurs donn6es, et ne traduisent pas non plus obligatoirement la grande diff6rence inter- et intra-individuelle dans les r6ponses aux couleurs, telles que nous les rapportons dans cette 6tude.
References R6sum6
Effets de contraste avec les trois couleurs primaires sur les potentiels 6voqu6s humains Dans cette 6tude nous avons recherch6 chez l'homme si les effets de contraste avec des stimulus color6s varient de la m~me fagon (qui est bien connue) qu'avec des stimulus en noir et blanc. En utilisant un 6chiquier h renversement, nous avons 6valu~ le potentiel ~voqu~ visuel (PEV) en r~gime stable chez 10 sujets, en r6ponse h diff6rents niveaux de contraste, et ceci pour chacune des 3 couleurs primaires. La luminance moyenne totale dans chaque primaire 6tait 6galisbe photom6triquement et maintenue constante au cours de tousles essais. Le PEV 6tait moyenn6 sur ordinateur pour 90 p+riodes cons~cutives de stimulation de 1 sec et la puissance 6tait calculb.e pour la fr6quence appropri6e. Pour chaque couleur, les courbes de r6ponse au contraste ont accus6 des valeurs de puissance basse faible contraste (0,1) et plus importante pour les 3 niveaux 61ev6s de contraste test6s (0,3-0,5). La puissance h vari6 de faqon importante selon la
Campbell, F.W. and Maffei, L. Electrophysiological evidence for the existence of orientation and size detectors in the human visual system. J. Physiol. (Lond.), 1970, 207: 635-652. DeValois, R.L. and DeValois, K.K. Spatial vision. Ann. Rev. Psychol., 1980, 31: 309-341. Ginsburg, A.P., Cannon, M.W. and Nelson, M.A. Suprathreshold processing of complex visual stimuli: evidence for linearity in contrast perception. Science, 1980, 208: 619-621. Kelly. D.H. Lateral inhibition in human colour mechanisms. J. Physiol. (Lond.), 1973, 228: 55-72. Kelly, D.H. Spatio-temporal frequency characteristics of color-vision mechanisms. J. Opt. Soc. Amer., 1974, 64: 983--990. Kelly, D.H. Disappearance of stabilized chromatic gratings. Science, 1981, 214: 1257-1258. Klemm, W.R., Gibbons, W.D., Allen, R.G. and Richey, E.O. Ocular dominance and brain lateralization effects on the visual evoked response. Physiol. Psychol., 1980, 8: 409-416. Klingaman, R.L. and Moscowitz-Cook, A. Assessment of the visual acuity of human color mechanisms with the visually evoked cortical potential. Invest. Ophthal., 1079, 18: 1273 -1277. McCree, K.J. Color confusion produced by voluntary fixation. Optica Acta, 1960, 7: 281-290. Michael, C.R. Color vision mechanisms in monkey striate cortex: simple cells with dual opponent-color receptive fields. J. Neurophysiol., 1978a, 41: 1233-1249. Michael, CR. Color-sensitive complex cells in monkey striate cortex. J. Neurophysiol., 1978b, 41: 1250-1266.
566 Regan, D. An effect of stimulus colour on average steady-state potentials evoked in man. Nature (Lond), 1966, 210: 1056-1057. Regan, D. Chromatic adaptation and steady-state evoked potentials. Vision Res., 1968, 8: 149-158. Regan, D. Evoked Potentials in Psychology, Sensory Physiology, and Clinical Medicine. Chapman and Hall, London, 1972. Regan, D. Evoked potentials specific to spatial patterns of luminance and colour. Vision Res., 1973, 13: 2381-2402. Regan, D. Electrophysiological evidence for colour channels in human pattern vision. Nature (Lond.), 1974, 250: 437-439. Regan, D. Evoked potential indicators of the processing of pattern, color, and depth information. In: J.E. Desmedt (Ed.), Visual Evoked Potentials in Man: New Developments. Clarendon Press, Oxford, 1977: 234-285. Siegfried, J.B. VECP: its spectral sensitivity. In: J.C. Armington, J. Krauskopf and B.R. Wooten (Eds.), Visual Psychophysics and Physiology. Academic Press, New York, 1978: 257-266.
W.R. KLEMM ET AL. Spekreijse, H. Pattern evoked potentials: principles, methodology, and phenomenology. In: C. Barber (Ed.), Evoked Potentials. MTP Press, Lancaster, 1980: 55-74. Spekreijse, H., Estevez, O. and Reits, D. Visual evoked potentials and the physiological analysis of visual processes in man. In: J.E. Desmedt (Ed.), Visual Evoked Potentials in Man: New Developments. Clarendon Press, Oxford, 1977: 16-89. Tyler, C.W., Apkarian, P. and Nakayama, K. Multiple spatialfrequency tuning of electrical responses from human visual cortex. Exp. Brain Res., 1978, 33: 535-550. White, C.T. and Hintze, R.W. Color evoked potentials: cortical and subcortical elements. In: D. Lehmann and E. Callaway (Eds.), Human Evoked Potentials. Plenum Press. New York, 1978: 431-442. White, C.T., Kataoka, R.W. and Martin, J.I. Colour-evoked potentials: development of a methodology for the analysis of the processes involved in colour vision. In: J.E. Desmedt (Ed.), Visual Evoked Potentials in Man: New Developments. Clarendon Press, Oxford, 1977: 250-272.