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Infant color vision: A search for short-wavelength-sensitive mechanisms by means of chromatic adaptation
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INFANT COLOR VISION: A SEARCH FOR SHORT-WAVELENGTH-SENSITIVE MECHANISMS BY MEANS OF CHROMATIC ADAPTATION ELIZABEW PULOS, DAVIDA Y. TELLER and STEVEN L. BUCK
Departments of Psychology and Physiology/Biophysics. Child Development and Mental Retardation Center and Regional Primate Research Center. University of Washington. Seattle, WA 98195. U.S.A. (Received 11 October 1979)
Abstract--Incremental thresholds for short- and middle-wavelength test spots. projected upon blue and yellow backgrounds. were determined for 2 mth old infants. Three out of four infants tested showed a change in relative sensitivity to 460 and 560 nm test spots with a change in the wavelength composition of the backgrounds, indicating the existence of at least two separately adaptable chromatic mechanisms. When infant spectral sensitivity under yellow adaptation was examined in more detail. however. it did not agree with that of adults tested under comparable conditions. In adults. the yellow background revealed a short-wavelength mechanism (&,,,z = 44Onm) in isolation. but did not do so in most 2 and 3 mth old infants. The infants who were least sensitive to short wavelengths on an absolute scale also deviated most from adult-like spectral sensitivity. We tentatively interpret this difference between adults and infants as an immaturity of the infant’s short-wavelength-sensitive mechanism.
INTRODUCTION
The color vision of young infants has been at issue for almost a century (see Bornstein. 1978: Werner and Wooten, 1979; Salapatek and Banks. 1979, for recent reviews). The abiding difficulty in studying the color vision of human infants has been the experimental separation of chromatic (hue and saturation) from achromatic (brightness) cues. If an infant is able to discriminate one chromatic stimulus from another, it remains to be demonstrated that the discrimination is made on the basis of wavelength composition, and not intensity. Recent well-controlled work has shown that young infants are, indeed, able to perform certain wavelength discriminations, even when brightness artifacts are eliminated. 2 mth old infants have been shown to discriminate broad-band blue, blue-green. orange, red. reddish-purple and bluish-purple from white (Peeples and Teller, 1975; Teller er al., 1978): and 11-12 week old infants discriminate red from green (Schaller, 1975). Unlike adult protanopes and deuteranopes (Pitt. 1935) most 2 and 3 mth old infants are able to make wavelength discriminations along the green-red spectral locus (Bomstein, 1976; Teller et al., 1979). Thus. there is no reason to suspect that color-normal infants lack either the long-wavelength-sensitive (LWS) or middle-wavelength-sensitive (MWS) color mechanisms typical of trichromatic adults. There is no good evidence, however, that young infants are normal trichromats, and there is weak evidence that they may not be. Teller et al. (1978) found that 2 mth olds failed to discriminate yellow-green 485
(dominant wavelengths: 538 nm and 561 nm) and mid-purple stimuli from white within a narrow intensity band close to the adult heterochromatic brightness match. Although the infants’ pattern of discrimination failures does not exemplify any of the standard dichromacies, it suggests a possible tritan-like defect indicative of an absence or anomaly of the shortwavelength-sensitive (SWS) mechanism, and invites study of the infant’s SWS mechanism. The shape of the photopic spectral sensitivity curve of trichromatic adults can be altered, and individual chromatic mechanisms studied in relative isolation, by means of chromatic adaptation (Stiles, 1949. 1959). These shifts of relative sensitivity can be dramatic; for example, the relative sensitivity to 460 nm and 560 nm lights can be shifted readily by two or more log units (e.g. Wald. 1964). Such shifts in photopic spectral sensitivity are taken to indicate the presence of at least two color mechanisms operating in the wavelength range tested. In the extreme, the sensitivity of all but one of the color mechanisms can be so depressed that the subject’s spectral sensitivity is determined by the single remaining mechanism over a broad spectral region. Chromatic backgrounds of moderate intensity (approximately 3.5 log td) can be sufficient to isolate the SWS mechanism over a considerable wavelength range (Sperling and Harwerth, 1971: Wooten er al., 1975). The present experiments were undertaken to investigate the malleability of infant spectral sensitivity under conditions of chromatic adaptation, and by this means to explore SWS mechanisms in human infants.
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Infants were held by an adult in front of a rearprojection screen. The screen was front-illuminated by yellow or blue adapting lights. An IS’ diameter test field of variable wavelength and intensity could be rear-projected with its center 31’ to the left or right of a centrally located peephole. The forced-choice preferential looking (FPL) method (Teller er al.. 1974: Teller. 1979) was used for data collection. In FPL testing, an adult observer watches the infant from behind the peephole. On the basis of the infant’s eye movements and visual fixation. the observer is required to judge the location of the stimulus on each trial. The test spot intensity needed for the observer to be 759, correct is taken as an estimate of the infant’s threshold.
The optical system used to produce the test spots is shown in Fig. I. The source was a 1000 Watt xenon arc (Schoeffel No. L-160) driven by a regulated power supply (Sorenson No. SRL 40-50). The test beam passed through two heat-reflecting mirrors H, and Hz.A simple optical projection system consisting of lenses L, and L2 brought the image of an aperture rl into focus on the rear-projection screen 5. A flicker vane V could be used to flicker the test stimulus at 0.5 Hz. A pivoting mirror M, and fixed mirrors Mz. .M, and M, directed the test beam to either the right or left hand side of the screen. Narrow-band interference filters (Bausch and Lomb and Corion, 8-13 nm bandwidth at 50”; transmission) and neutral filters (Kodak and Oriel) at F regulated the chromaticity and intensity of the test beam. The observer viewed the infant through the peephole P. The aperture A was a circular hole divided by two opaque vertical strips into three apertures. The opaque strips and lighted apertures were of approximately equal width. Thus. the test spot was a circular striped field of about 18’ overall diameter at the infant’s viewing distance of 30cm + 5 cm. It was projected with its center 31’ to either the right or the left of the peephole, which was located in the center of the screen (see inset. Fig. 1). The rear-projection screen (Stewart Filmscreens Lumiglas l/8 A 90) measured 90 x 122cm (72 x 76’) and was homogeneous except for the 6mm peephole in its center. The screen was mounted in a wooden frame. and was surrounded by white draperies. The draperies reduced the visual distractions available to the infant. and helped to diffuse the screen illumination and to maintain the infant’s state of visual adaptation between trials. The screen and drapes were diffusely frontilluminated by the following sources. either alone or in combination: (1) a low-pressure sodium lamp (QL Luminaire No. LPS 200-155). emitting only the sodium line at 589.6 nm: (2) broad-band “gold” fluor-
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escent lamps (Westinghouse No. F40GO; nominal peak energy at 595 nm; nominal CIE coordinates x = 0.510. ,r = 0.469: (3) broadband “blue” fluorescent lamps (Westinghouse No. F4OB: nominal peak energy at 435 nm: nominal CIE coordinates x = 0.205. J = 0.183). Yellow backgrounds were produced with various combinations of low-pressure sodium and gold fluorescent sources. and covered the intensity range from 1.4 to 1.8 logcd;m2 (2.2 to 2.6 log td assuming a 2.7 mm pupil). The blue background, produced by the blue fluorescent lamps. was I.5 log cd/m’ (2.3 log td). Calibrarions
Integrated background luminance was measured with a SE1 exposure meter. The spectral transmittance of the interference filters used to produce the test stimuli was measured with a Carey 14 recording spectrophotometer. The density of neutral filters placed in the test beam was calibrated in sirrc for the test wavelengths used by means of an International Light IL510 photomultiplier photometer. The equipment available to us was not sufficient to describe accurately either the spectral characteristics or the integrated radiances of the projected narrowband test stimuli. The integrated radiance of the narrow-band test stimuli was estimated psychophysitally, as follows. Absolute scotopic thresholds were determined for each test stimulus for each of two
Infant chromatic adaptation
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Complete data sets were collected from a total of 14 infants. By mothers’ report, all infants were born within 2 weeks of their due dates. Of these, 7 were tested at 2 mth. 4 were tested at 3 mth, and 3 were tested at both 2 and 3mth of age, for a total of 17 data sets. 6 additional infants came into the lab but did not complete testing: 2 due to illness, 1 due to sleepiness, and 3 due to fussiness. Only female infants were tested to minimize the chance of including an infant with nonstandard color vision in the study. Data sets took from 6 to 11 visits to complete. The 2mth olds were tested between the 46th and 71st postnatal day, and the mean age at the midpoint of testing was 58.4 days. 3 mth olds were tested between the 78th and 97th postnatal day, at a mean age of 87.7 days. Adult subjects were 2 color-normal females in their mid-twenties.
An observer seated behind the screen peered through the peephole and tried to guess the test spot position (left or right) from the infant’s looking behavior. The observer was free at all times to instruct the holder how to position the infant. Blinders on either side of the observer’s head prevented him or her from seeing the test spot. Trials had no fixed duration: a trial continued for as long as necessary for the observer to make a judgment. A third adult, the experimenter. set the wavelength. intensity and position of the test spot at the beginning of each trial, and gave the observer immediate feedback on the accuracy of his or her judgments. The method of constant stimuli was used to generate psychometric functions. In general, a l-1.5 log unit intensity range was sufficient to span the function from near chance to near 1000~,correct. With the first 6 infants tested, this range was covered in 0.5 log unit steps. Later infants were tested in 0.3 log unit steps. Three stimulus levels per function, chosen on the basis of previously collected data. were selected initially for the infant to view. These were presented randomly five times each within a 15-trial block. When a block of trials was completed for one test wavelength. the test wavelength was changed. and testing continued. If, after several days of testing, the stimulus intensities selected did not appear to span the psychometric function, new intensity levels were added at the top or bottom of the range. When two different backgrounds were used, background color alternated from one day to the next. A psychometric function was collected for each combination of test wavelength and background color. Two or more psychometric functions were generated for each infant in the 2 week period allotted for testing. For each infant, trials were evenly distributed among all the conditions tested. Infants varied somewhat in their enthusiasm for the task, and different psychometric functions represent from 12 to 30 trials per point. A cumulative normal ogive was fit to the empirical functions by the method of least squares. The upper and lower asymptotes were constrained at lOOO/;and SO%, respectively. Each percent-correct value was weighted by the reciproca! of its standard error before further computation. Thresholds were estimated to be the stimulus intensity yielding 754, correct on the best fitting cumulative normal curve.
Procedure
Adult su6ject.s
The experimental room, rear-projection screen, and white curtains were bathed in either blue or yellow light. A narrow-band test spot was rear-projected to either the left or right side of the screen. superimposed upon the chromatic background. The infant was held in front of the screen by the holder, who slowly turned the infant from side to side, giving her an opportunity to view both possible test spot positions. The holder wore a visor that kept him or her blind to the location of the test spot.
Adults were tested with direct viewing under three conditions of adaptation: yellow-, blue-, and darkadaptation. All viewing was binocular, and no artificial pupils were used. The dark-adapted measurements are described above (see Calibrations). For the yellow- and blue-adapted measurements, thresholds were estimated with two different psychophysical methods. First, thresholds were measured with steady fixation by the descending method of limits. The test spot, flickering at 0.5 Hz. appeared only on the left
adult observers, fixating 31’ to the right of the test spot. The test spot was flickered at 0.50 Hz (SO?; duty cycle). Threshold was measured by a descending method of limits. The results of 10 trials at each wavelength were averaged to obtain an estimate of threshold. These measured thresholds were then compared to the CIE scotopic luminosity function. Vi (Wyszecki and Stiles. 1967, p. 379). If the radiance of the screen was the same when transilluminated by light passing through each interference filter. then the additional density needed to reduce each test stimulus to absolute threshold should follow the V; function. We interpret the deviations of the data from the Vi function to reflect the deviations of our test stimuli from radiometric equality. A set of correction factors was generated by averaging the adult data and determining the deviation of this average from the V; function at each wavelength used. These correction factors have been applied to all the data shown in the remainder of the paper. A limitation of this method is that the average spectral sensitivity of our two adult observers may not match exactly that specified by the V>, function because of normal variation in prereceptoral absorption at shorter wavelengths. This would distort the absolute shapes of all of the spectral sensitivity curves reported here, but would not affect the differences between these curves. dark-adapted
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Fig. 2. Spectral sensitivity functions for adult observers EL (0) and EP (At under yellow (top) and blue (bottom) adaptation. The continuous curves were fit by eye to the data. The change of shape of the spectral sensitivity functions indicates that at least two independently adaptable chromatic mechanisms subserve detection of test spots for adult observers under the conditions in which infants were tested.
Spectral sensitivity curves for two adult observers, obtained by means of the method of limits. are shown in Fig. 2. Thresholds were roughly 0.5 log unit lower when determined by the method of constant stimuli. but the shapes of the spectral sensitivity functions were similar for the two methods. .Against the yellow background (1.4 log cd, m’). spectral sensitivity rose to a peak at about 440nm. and then dropped off at longer wavelengths. Spectaf sensitiv-iry functions of similar shape have been reported b>- Wald (19641, Wooten and Wald (1973). and Wooten, Fuld and Spillman (1975) for broadband yellow or yellowishwhite adapting backgrounds. The shape of the curve suggests that the yellow background so desensitized the MWS and LWS mechanisms that the curve traces the spectral sensitivity of the SWS mechanism in isolation from 400 to 500 nm. A yellow background of I .7 log cd,‘m’ produced a curve of similar shape. The mechanisms revealed against the blue background (1.5 log cd:‘m’f are less clear cut. Sensitivity rises sharply between 400 and 420 nm. dips at 460 nm, then rises again at longer wavelengths. Sperling and Harwerth (1971) reported curves of similar shape under blue adaptation. They attributed the detection
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side of the screen. The subject fixated the center of the
test spot. On each trial, an experimenter decreased the intensity of the test spot in 0.1 log unit steps until the subject could no longer see it. The lowest intensity at which the test spot remained visible was recorded. The results of 10 trials at each wavelength were averaged to obtain an estimate of threshold. Second, thresholds were determined with a standard spatial forced-choice technique. Fixation points were provided on both sides of the screen, in the centers of the two test spot positions. In order to mimic the free fixation conditions used with the infants, the aduh subjects alternated fixation every few seconds between the two fixation points. The test spot was projected to either the right or the left side of the screen, and was cycled on and off at about 0.5 Hz. Psychometric functions were determined for each waveiength, and threshold was defined as the stimulus intensity that permitted the subject to judge the position of the test spot correctly 75% of the time. In sum, there are three main differences between infant and adult data collection-psychophysical method, fixation control, and the temporal characteristics of the stimulus. For reasons detailed in the Discussion section, we believe that these differences do not jeopardize the results or conclusions of this study.
Fig. 3. Psychometric functions of two infants, each tested at two test wavelengths against two adapting backgrounds. Test spots: O+460 nm: 0. 560 nm. Backgrounds: continuous curves, yellow: broken curves. blue. Threshold for detecting the test stimuli against each background was taken to be the 7.5’; correct level of the best fitting cumulative normal ogive (not shown). Changes of background reversed the infants’ relative sensitivity to the two test wavelengths. This demonstrates that at least two chromatic mechanisms subserve these i&ants’ color vision over the range of 460-560 nm.
infant chromatic adaptation
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shown here, sensitivity to 460 nm relative to 560 nm test lights clearly shifts with the shift of chromatic background.
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Fig. 4. Relative sensitivity of same two adults shown in Fig. 2 (a), same 2 infants shown in Fig. 3 (0) and two additional infants (0) to 460 and 560 nm test spots projected against blue (broken curve) and yellow (continuous curve) backerounds. Three of four infants displayed differences’in spectral sensitivity, measured on the iwo backgrounds. similar to that shown by adults. One infant showed no reliable change in spectral sensitivity.
of short wavelengths (~460 nm) to the SWS mechanism. detection of middle wavelengths to the MWS mechanism, and detection of wavelengths greater than 490nm to the LWS mechanism. Overall, the change of chromatic background produced a clear change of spectral sensitivity, signalling the participation of at least two chromatic mechanisms, presumably SWS and MWS, in the determination of these data sets. Infant psvchomerricfunftions Figure 3 shows psychometric functions, generated with 460 and 560 nm test spots against the same two backgrounds (1.5 log cd/m’ blue and 1.4 log cd/m’ yellow), for two 2 mth old infants. All data sets drop from a high percent correct to near chance with a l-2 log unit change in test intensity. For both infants * As usual, it must be emphasized that these data provide only a lower bound estimate of the infant’s visual capacities: there is obviously no evidence that the infant cannot see berror than the levels estimated by any given technique. Further, psychophysical data alone do not reveal the Iocation of information loss within the organism. These problems, of course. are not confined to the FPL technique, nor indeed to the field of infant psychophysics (cf. Teller. f979).
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Figure 4 summarizes sensitivity for 460 nm and 560 nm test spots against the blue and yellow backgrounds, for the two adults and two infants described above, and for two additional infants. All six subjects are plotted on the same relative sensitivity scale. Both adults are more sensitive to 460 nm than to 560 nm under yellow-adaptation, but more sensitive to 560 nm than to 460nm under blue-adaptation. Like the adults, three of the infants were more sensitive to 560nm than to 460nm when the background was blue. while the fourth infant (Rachel) was about equally sensitive to both wavelengths. When the background was yellow, two of the infants (Dana and Elizabeth) were more sensitive to 460nm than to 56Onm. and the other two infants (Shannon and Rachel) were about equally sensitive to both wavelengths. Although the latter two infants did not show the same yellow-adapted spectral sensitivity found with adults, one of them (Shannon) did show a change in spectral sensitivity in the expected direction with changes in chromatic adaptation. The other (Rachel) showed no convincing change. On the whole, the infants demonstrated absolute sensitivity lower by 1 to 2 log units than the adults for both test wavelengths and both conditions of adaptation.’ But, like the adults, spectral sensitivities for three of the four infants changed in a predictable fashion with changes in the spectral com~sition of the back~ound. We conclude that at least some 2mth olds have at least two separately adaptable visual mechanisms operating over the short-wavelength half of the spectrum. In the following experiments we attempt to identify these mechanisms. More extensive short-wavelength spectral sensitivity curves, obtained from two additional 2 mth old infants, are shown in Fig. 5. Thresholds were obtained at each of several wavelengths between 420 and 540nm, against a yellow background of 1.75 logcd/m2. The figure also shows the adult yeilow-adapted spectral sensitivity curve, redrawn from Fig. 2. The data sets from the infants have been shifted vertically (by 3.1 and 3.3 log units) to coincide with the adult curve at 460 nm. The data from the two infants are in rough agreement, and indicate that sensitivity increases as the wavelength increases from 440 to 5OOnm. The infants differ substantially from the adults tested, and from published estimates of spectral sensitivity of the classical adult SWS mechanism. Thus, these two infants have failed to reveal a classical SWS mechanism under conditions that reveal the mechanism in adult subjects. Finally, four additional 2 mth old infants were tested at 460 and 500 nm against a 1.75 log cd/m2 yellow background. Of these, three were retested at 3 mth. Four additional 3 mth olds were also tested.
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TestWaveleqth ( n m ) Fig. 5. Spectral sensitivity of 2 mth old infants under yellow-adaptation. The continuous curve is the spectral sensitivity of adults tested under similar conditions of yellow-adaptation, repeated from Fig. 2. The yellow background failed to reveal a chromatic mechanism in infants that resembled the SWS mechanism of adults when tested under similar conditions, All data sets are shifted vertically to match at 460 nm.
The data sets from these infants and from the 2 mth olds shown in Fig. 5 are plotted in Fig. 6. Several trends are apparent in Fig. 6. Although data from the two groups overlap, the 3 mth olds. on the average. demonstrated higher absolute sensitivities than the 2 mth olds at both wavelengths. The relative log sensitivities for 2 and 3 mth old infants, respectively, were I.5 + 0.6 and 2.3 k 0.4 at 460 nm and 1.5 + 0.3 and 2.0 2 0.2 at 500 nm. The 3 mth olds on the average show 0.3 log unit higher sensitivity to 460 than to 500 nm, while for the 2 mth olds this difference is zero. Both within and across age groups, there was greater variability among infants in sensitivity to 460 than to 500 nm light. Three of the infants in Fig. 6 were tested at both 2 and 3 mths of age. Kathleen (squares) was very sensitive to both wavelengths at 2 mth, and remained so at 3 mth. At both ages, she was about 0.6 log unit more sensitive to 460 than to 500nm. For this subject, maturation produced a change in overall sensitivity, but not a change in spectral sensitivity. A second infant, Diana (upside-down triangles), showed a change with age in both overall sensitivity and spectral sensitivity. At 2 mth she was relatively more sensitive to 560 nm than to 460 nm, while by 3 mth she was about 0.3 log unit more sensitive to 460 nm. A third infant, Jeanie (triangles), also improved in overall sensitivity as she became older. Her spectral sensitivity, however, remained flat from 2 to 3 mths of age. Thus, maturation over this time period seems to elevate demonstrated sensitivity in individual infants, but does not always bring a change in spectral sensitivity. There is also a strong correlation (r = 0.92) across groups between an infant’s absolute sensitivity to 460 nm and her relative sensitivity to 460 vs 500 nm light. This trend is readily visible in the fan-like arrangement of the slopes of the lines in Fig. 6. The two infants who were least sensitive to 460 nm light on an absolute scale were also less sensitive to 460 nm than
to 500 nm light. Infants who were intermediate in sensitivity to the 460 nm test spot showed approximately equal sensitivity to 460 and 5GQnm. The six infants who were more sensitive to 460 nm also showed higher relative sensitivity to 460 than to 5OOnm light-a pattern closely resembling that shown by adults. Under yellow-adaptation. adults were about 0.6 log unit more sensitive to 460 than to 500 nm: the infants with the steepest slopes come very close to this value, although they remain 1.5-2.5 log units less sensitive than adults in absolute terms. DISCL’SSIOS These experiments have shown that (1) some 2 mth olds have at least two separately adaptable visual mechanisms in the short-to-middle-wavelength region of the spectrum; (2) adaptation sufficient to reveal a SWS mechanism with a peak at 440 nm in adults does not do so consistently in infants: (3) young infants differ greatly from one another in their relative sensitivity to short wavelengths under yellow-adaptation: and (4) under yellow adaptation there is a strong correlation between an infant’s absolute sensitivity to short-wavelength light (460 nm, in this case) and the
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Fig. 6. Relative sensitivity to 460 and 5OOnm for 2 adults (top) and IO infants (bottom) under yellow-adaptation. The solid symbols are from 3 mth olds. and the open symbols from 2 mth olds. Three of the infants, shown by squares, triangles, and upside-down triangles. were tested at both 2 and 3 mth of age. The sensitivity to 460 nm relative to 500 nm under yellow-adaptation varies considerably among infants. About 8Y, of this variance can be accounted for by differences among infants’ absolute sensitivity to the 460 nm test spot. That is. infants most sensitive to short-wavelength light also displayed the most adult-like spectral sensitivity.
Infant chromatic adaptation shape of the infant’s short-wavelength spectrai sensitivity function (relative sensitivity to 46Onm vs 500 nm or 560 nm lights), such that infants most sensitive to short-wavelength light also display the most adult-like spectral sensitivity. For several reasons. we believe that the procedural differences between adult and infant data collection are unlikely to jeopardize the conclusions of this study. We particularly point out that two different techniques were used to test adults, with highly similar results; that the free fixation of infants was mimicked by a condition of alternating fixation in adults: that free fixation tends to enhance blue sensitivity, not diminish it (Yager, 1970); that most of the conclusions drawn depend upon comparisons within or between infants. rather than to any adult standard (or physical calibration): and finally, that the infants with highest absolute sensitivity appear to approach most closely the adult standard, thus providing additional internal consistency within the experiment itself.
There are two main factors that may explain the individual differences among infants in absolute and relative sensitivity. These are differences in prerecep toral absorption and differences in the relative sensitivity of a SWS mechanism. Short wavelengths are especially susceptible to prereceptoral absorption losses within the eye, especially in the lens and macular pigment. In addition, the densities of both lens and macular pigments are reported to vary substantially among adults, leading to individual differences in adult photopic and scotopit visual spectral sensitivity functions and in metamerit color matches involving short wavelengths (for a review, see Ruddock, 1972). Despite these qualitative characteristics, we think it is unlikely on quantitative grounds that either of these prereceptoral pigments contribute to any major degree to the differences seen among infants in the present experiment. The extinction spectrum of the lens peaks in the ultraviolet. It is relatively low and flat for wavelengths of 450nm and above, and changes by only about 0.1 log unit between 460 and 500 nm. Thus, individual differences in density in this wavelength range must have small effects at best. In addition there is some evidence (Werner, 1979) and much sp~u~ation that infants have, on the average, less dense lens pigmentation than do adults (but cf. Cooper and Robson. 19691,a factor that would render such differential effects even smaller for infants than for adults. The macular pigment absorbs most strongly between 410 and 510nm, with a peak at about 460nm (Wyszecki and Stiles. 1967, p. 128). and thus has appropriate spectral characteristics to explain the individual differences found in the present experiment. However, to account for the more than 2 log unit
491
variation in sensitivity among infants at 46Onm and the more than 1 log unit variation at 500 nm shown in Fig. 6, one would have to assume the presence of very high densities of macular pigment in the least sensitive infants. Contrary to this assumption. it is widely believed that the macular pigment is less dense in infants than in adults (cf. Werner, 1979). although no modern data have been published on this topic. It would also be necessary to assume that. despite being shielded from the incoming light by high densities of macular pigment, the region of retina detecting the test. stimulus is nonetheless located behind the assumed pigment. For a large test fieid the combined likelihood of these factors is low; and we conclude that explanations for the present individual differences are more likely to be found at neural than at prereceptoral levels. The remaining major possibility is that individual infants differ markedly in the relative sensitivity of a SWS mechanism. In adults. the relative sensitivity of the SWS cone mechanism has been reported to vary across individuals (Wald, 1964). across retinal regions (Wald, 1964; Wooten and Wald. 1973). and with other factors such as time during d~k-adaptation (Wooten er ai., 1975). Thus, variations across infants during development seem plausible. Large individual differences among infants in relative sensitivity to 450nm light may also be seen in the VEP data of Dobson (1976). Thus, the idea that individual infants differ markedly in the relative sensitivity of their SWS mechanism seems to us the most likely explanation of the individual differences seen in the present experiment. The
co~rribut~on of rods
The yellow-adapted spectra1 sensitivity of the two most extensively tested 2 mth olds, shown in Fig. 5, resembles the adult scotopic curve. It is reasonable that the rods might detect short wavelengths under the conditions used if the SWS cone mechanism were absent or comparatively insensitive. The longwavelength background and large, short-wavelength test stimuli would be well-suited for rod isolation. Aguilar and Stiles (1954) found that long-wavelength backgrounds of about 3.2 log Scot td are necessary to saturate the rod system. Thus, even the brightest yellow backgrounds used here, which correspond to about 2.4 log Scot td, were below adult rod saturation level. Yet it would be unduly speculative to conclude that rods determine the thresholds shown in Fig. 5. Indeed, these data could reflect a combination of infant SWS, MWS, and/or rod mechanisms, any of which may differ from those of the adult. It is interesting to note that Abramov and Gordon. (1977) report a curve of similar shape for adult photopic spectral sensitivity measured 45’ in the peripheral retina, without being able to attribute it with any certainty to any particular receptor mechanism.
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infants to adrtlrs
Previous studies of infant photopic spectral sensitivity have yielded some superficial inconsistencies in the question of the average relative sensitivity of 2-3 mth old infants vs adults in the short-wavelength region of the spectrum. On the basis of VEP data, Dobson (1976) and Moskowitz-Cook (1979) have concluded that on the average infant spectral sensitivity is relatively high in the short-wavelength region; while on the basis of behavioral data Peeples and Teller (1978) have concluded that infants and adults have similar relative sensitivities throughout the spectrum. The present study suggests that the majority of infants are relatively less sensitive than adults in the shortwavelength region, under both yellow- and biueadaptation conditions. Thus, published studies have covered the range of possible outcomes, although the reported differences in previous studies have been small. There are many differences in technique, stimulus conditions, adaptation conditions, etc., among the various studies. We have not been able to choose with conviction among the many possible reasons for the differences among studies, nor indeed to decide whether the differences should be considered real or attributed to different random samples from highly variable populations. It is worth noting that both directions of difference between infants and adults could legitimately be found. If, for example. the infant has a poorly developed SWS system but a lower density of macular pigment than the adult, these factors could interplay to give either kind of result. Under conditions in which the SWS cones never determine the threshold for either age group, infants could be relatively more sensitive than adults in the short-wavelength region, owing to their advantage in prereceptoral absorption factors. But under conditions in which adults use their SWS cones for detection of short wavelengths, infants could be relatively less sensitive than adults at short wavelengths. The question of the shapes of photopic spectral sensitivity curves, especially in the blue region of the spectrum, is one of the most complex topics in visual psychophysics and electrophysiology, and there is no reason to expect it to be less complex in developing systems. It seems likely that small -inconsistenci& across studies in the relative sensitivity of infants and adults to short-wavelength light will be the rule, rather than the exception, until larger samples and more systematic variations of experimental conditions are carried out. In summary, under the present conditions. three out of four 2 mth old infants showed changes of spectral sensitivity with chromatic adaptation within the short- to middle-wavelength range, thus revealing the presence of at least two chromatic mechanisms. However, yellow-adaptation conditions that were sufficient to reveal the SWS mechanism in adults did not consistently do so in 2 and 3 mth old infants.
To unite these results. we offer the interpretation that the SW’S mechanism lags behind the others in early postnatal development. We further suggest that the development of short-wavelength sensitivity follows a different time course in different infants. and that as a group the 2 and 3 mth old infants tested were in the midst of such a developmental process.
.-lckno~~edg~tnents-This research was supported in part bv NIH Postdoctoral Fellowshio EY 041567 from the National Eve Institute to Steven E&k; NICHD Grant HD 02274. Research in Mental Retardation and Child Development; and NSF grant BNS 76-01503 to Davida Teller. We thank Jean Kellv. Clifton Lee. Elvse Litvack. and Greg Stewart for laboratory assistance: karjorie Zachow for secretarial assistance; and Drs Israel Abramov. Marc Bornstein. Walter Makous, Anne Moskowitz-Cook and Bill Wooten for comments on the manuscript, REFERENCES
Abramov 1. and Gordon J. (1977) Color vision in the peripheral retina. 1. Spectral sensitivity. J. opr. Sac. Am. 67, 195-202. Aguilar hl. and Stiles W. S. (1954) Saturation of the rod mechanism of the retina at high levels of stimulation. Oprica
.Acra 1, 59-65.
Bornstein \l. H. (1976) Infants are trichromats. J. exp. Child Psvchol. 21. 425-445. Bornstein iI. H. (1978) Chromatic vision in infancy. In Advances in Child Dewlopmenr and Behavior (Edited by Reese H. W. and Liositt L. P.). Vol. 12. Academic Press. New York. ’ Cooper G. F. and Robson 1. G. (1969) The yellow colour of the lens of man and other primates. J. Ph?siol. 203, 411317. Dobson V. (1976) Spectral sensitivity of the 2-month infant as measured by the visually evoked potential. C’isionRes. 16, 367-374. Moskowitz-Cook A. (1979) The development of photopic spectral sensitivity in human infants. Vision Res. 19, 1133-1142. Peeples D. R. and Teller D. Y. (19i5) Color vision and brightness discrimination in two-month-old human infants. Science 189, 1102-l 103. Peeples D. R. and Teller D. Y. (1978) White-adapted photopic spectral sensitivity in human infants. Vision Rex 18, 49-53. Pitt F. H. G. (1935) Characteristics of dichromatic vision, with an appendix on anomalous trichromatic vision. Great Britain Medical Research Council. Special Report Series, No. 200.
Ruddock K. H. (1972) Light transmission through the ocular media and macular pigment and its significance for psychophysical investigation. Handbook of Sensor! Physiology. Vol. VII, 4. Springer, Berlin. Salapatek P. and Banks M. S. (1978) infant sensory assessment: vision. In Communicorice and Cognirice Abilities: E:arly Behavioral Assessment (Edited by Minifie F. D. and Lloyd L. X.). University Park Press. Baltimore. Schaller ht. J. (1975) Chromatic vision in human infants: conditioned operant fixation to “hues” of varying intensity. Bull. psychon. Sot. 6, 39-42. Sperlmg H. and Harwerth R. S. (1971). Red-green cone interactions in the increment-threshold spectral sensitivity of primates. Science 172. 180-184. Stiles W. S. (1949) The determination of the spectral sensitivities of the retinal mechanisms by sensory methods. .Ved. Tijdschr. Natuurk. 15, 125-146. Stiles W. S. (1959) Color vision: the approach through increment-threshold sensitivity. Proc. natn. acad. Sci. 45, 100-I 14.
Infant chromatic adaptation Teller D. Y. (;979) The forced-choice preferential looking procedure: a psychophysical technique for use with human infants. rnfnnr Befiav. Derek 2, 135-158. Teller D. Y., Morse R.. Borton R. and Regal D. (1974) Visual acuity for vertical and diagonal gratings in human infants. Vision Res. 14, 1433-1439. Teller D. Y.. Peeples D. R. and Sekel M. (1978) Discrimination of chromatic from white light by two-month old human infants. Vision Res. 18, 4138. Teller D. Y., Morris D. and Alexander K. (1979) Rayfeigh disseminations in young human infants: a progress report. Spring Meet. ARYO, Sarasota, Florida. 30 April-4 May, 1979. Wald G. (1964) Receptors of human color vision. Science 145, 1007-1016.
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Werner J. S. (1979) Developmental change in scotopic sensitivity and the absorption spectrum of the human ocular media Ph.D. dissertation, Brown University. Werner J. S. and Wooten B. R. Human infant color vision and color perception. In preparation. Wooten B. R. and Wald G. (1973) Color vision mechanisms in the peripheral retinas of normal and dichromatic observers. J. gen. Physio[. 61. 125-145. Wooten 8. R.. Fuld K. and Spillmann L. (1975) Photopic spectral sensitivity of the peripheral retina. 1. opt. See. Am 65.334-342. Wyszecki G. and Stiles W. S. (1967) Color Science. Wilev. ~--, , kew York. Yager D. (1970) Spectral sensitivity with the freely moving eye. Vision Res. 10, 521-523.
YO 0401-0185502.00.0
INFANT COLOR VISION: A SEARCH FOR SHORT-WAVELENGTH-SENSITIVE MECHANISMS BY MEANS OF CHROMATIC ADAPTATION ELIZABEW PULOS, DAVIDA Y. TELLER and STEVEN L. BUCK
Departments of Psychology and Physiology/Biophysics. Child Development and Mental Retardation Center and Regional Primate Research Center. University of Washington. Seattle, WA 98195. U.S.A. (Received 11 October 1979)
Abstract--Incremental thresholds for short- and middle-wavelength test spots. projected upon blue and yellow backgrounds. were determined for 2 mth old infants. Three out of four infants tested showed a change in relative sensitivity to 460 and 560 nm test spots with a change in the wavelength composition of the backgrounds, indicating the existence of at least two separately adaptable chromatic mechanisms. When infant spectral sensitivity under yellow adaptation was examined in more detail. however. it did not agree with that of adults tested under comparable conditions. In adults. the yellow background revealed a short-wavelength mechanism (&,,,z = 44Onm) in isolation. but did not do so in most 2 and 3 mth old infants. The infants who were least sensitive to short wavelengths on an absolute scale also deviated most from adult-like spectral sensitivity. We tentatively interpret this difference between adults and infants as an immaturity of the infant’s short-wavelength-sensitive mechanism.
INTRODUCTION
The color vision of young infants has been at issue for almost a century (see Bornstein. 1978: Werner and Wooten, 1979; Salapatek and Banks. 1979, for recent reviews). The abiding difficulty in studying the color vision of human infants has been the experimental separation of chromatic (hue and saturation) from achromatic (brightness) cues. If an infant is able to discriminate one chromatic stimulus from another, it remains to be demonstrated that the discrimination is made on the basis of wavelength composition, and not intensity. Recent well-controlled work has shown that young infants are, indeed, able to perform certain wavelength discriminations, even when brightness artifacts are eliminated. 2 mth old infants have been shown to discriminate broad-band blue, blue-green. orange, red. reddish-purple and bluish-purple from white (Peeples and Teller, 1975; Teller er al., 1978): and 11-12 week old infants discriminate red from green (Schaller, 1975). Unlike adult protanopes and deuteranopes (Pitt. 1935) most 2 and 3 mth old infants are able to make wavelength discriminations along the green-red spectral locus (Bomstein, 1976; Teller et al., 1979). Thus. there is no reason to suspect that color-normal infants lack either the long-wavelength-sensitive (LWS) or middle-wavelength-sensitive (MWS) color mechanisms typical of trichromatic adults. There is no good evidence, however, that young infants are normal trichromats, and there is weak evidence that they may not be. Teller et al. (1978) found that 2 mth olds failed to discriminate yellow-green 485
(dominant wavelengths: 538 nm and 561 nm) and mid-purple stimuli from white within a narrow intensity band close to the adult heterochromatic brightness match. Although the infants’ pattern of discrimination failures does not exemplify any of the standard dichromacies, it suggests a possible tritan-like defect indicative of an absence or anomaly of the shortwavelength-sensitive (SWS) mechanism, and invites study of the infant’s SWS mechanism. The shape of the photopic spectral sensitivity curve of trichromatic adults can be altered, and individual chromatic mechanisms studied in relative isolation, by means of chromatic adaptation (Stiles, 1949. 1959). These shifts of relative sensitivity can be dramatic; for example, the relative sensitivity to 460 nm and 560 nm lights can be shifted readily by two or more log units (e.g. Wald. 1964). Such shifts in photopic spectral sensitivity are taken to indicate the presence of at least two color mechanisms operating in the wavelength range tested. In the extreme, the sensitivity of all but one of the color mechanisms can be so depressed that the subject’s spectral sensitivity is determined by the single remaining mechanism over a broad spectral region. Chromatic backgrounds of moderate intensity (approximately 3.5 log td) can be sufficient to isolate the SWS mechanism over a considerable wavelength range (Sperling and Harwerth, 1971: Wooten er al., 1975). The present experiments were undertaken to investigate the malleability of infant spectral sensitivity under conditions of chromatic adaptation, and by this means to explore SWS mechanisms in human infants.
186
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Infants were held by an adult in front of a rearprojection screen. The screen was front-illuminated by yellow or blue adapting lights. An IS’ diameter test field of variable wavelength and intensity could be rear-projected with its center 31’ to the left or right of a centrally located peephole. The forced-choice preferential looking (FPL) method (Teller er al.. 1974: Teller. 1979) was used for data collection. In FPL testing, an adult observer watches the infant from behind the peephole. On the basis of the infant’s eye movements and visual fixation. the observer is required to judge the location of the stimulus on each trial. The test spot intensity needed for the observer to be 759, correct is taken as an estimate of the infant’s threshold.
The optical system used to produce the test spots is shown in Fig. I. The source was a 1000 Watt xenon arc (Schoeffel No. L-160) driven by a regulated power supply (Sorenson No. SRL 40-50). The test beam passed through two heat-reflecting mirrors H, and Hz.A simple optical projection system consisting of lenses L, and L2 brought the image of an aperture rl into focus on the rear-projection screen 5. A flicker vane V could be used to flicker the test stimulus at 0.5 Hz. A pivoting mirror M, and fixed mirrors Mz. .M, and M, directed the test beam to either the right or left hand side of the screen. Narrow-band interference filters (Bausch and Lomb and Corion, 8-13 nm bandwidth at 50”; transmission) and neutral filters (Kodak and Oriel) at F regulated the chromaticity and intensity of the test beam. The observer viewed the infant through the peephole P. The aperture A was a circular hole divided by two opaque vertical strips into three apertures. The opaque strips and lighted apertures were of approximately equal width. Thus. the test spot was a circular striped field of about 18’ overall diameter at the infant’s viewing distance of 30cm + 5 cm. It was projected with its center 31’ to either the right or the left of the peephole, which was located in the center of the screen (see inset. Fig. 1). The rear-projection screen (Stewart Filmscreens Lumiglas l/8 A 90) measured 90 x 122cm (72 x 76’) and was homogeneous except for the 6mm peephole in its center. The screen was mounted in a wooden frame. and was surrounded by white draperies. The draperies reduced the visual distractions available to the infant. and helped to diffuse the screen illumination and to maintain the infant’s state of visual adaptation between trials. The screen and drapes were diffusely frontilluminated by the following sources. either alone or in combination: (1) a low-pressure sodium lamp (QL Luminaire No. LPS 200-155). emitting only the sodium line at 589.6 nm: (2) broad-band “gold” fluor-
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escent lamps (Westinghouse No. F40GO; nominal peak energy at 595 nm; nominal CIE coordinates x = 0.510. ,r = 0.469: (3) broadband “blue” fluorescent lamps (Westinghouse No. F4OB: nominal peak energy at 435 nm: nominal CIE coordinates x = 0.205. J = 0.183). Yellow backgrounds were produced with various combinations of low-pressure sodium and gold fluorescent sources. and covered the intensity range from 1.4 to 1.8 logcd;m2 (2.2 to 2.6 log td assuming a 2.7 mm pupil). The blue background, produced by the blue fluorescent lamps. was I.5 log cd/m’ (2.3 log td). Calibrarions
Integrated background luminance was measured with a SE1 exposure meter. The spectral transmittance of the interference filters used to produce the test stimuli was measured with a Carey 14 recording spectrophotometer. The density of neutral filters placed in the test beam was calibrated in sirrc for the test wavelengths used by means of an International Light IL510 photomultiplier photometer. The equipment available to us was not sufficient to describe accurately either the spectral characteristics or the integrated radiances of the projected narrowband test stimuli. The integrated radiance of the narrow-band test stimuli was estimated psychophysitally, as follows. Absolute scotopic thresholds were determined for each test stimulus for each of two
Infant chromatic adaptation
187
Complete data sets were collected from a total of 14 infants. By mothers’ report, all infants were born within 2 weeks of their due dates. Of these, 7 were tested at 2 mth. 4 were tested at 3 mth, and 3 were tested at both 2 and 3mth of age, for a total of 17 data sets. 6 additional infants came into the lab but did not complete testing: 2 due to illness, 1 due to sleepiness, and 3 due to fussiness. Only female infants were tested to minimize the chance of including an infant with nonstandard color vision in the study. Data sets took from 6 to 11 visits to complete. The 2mth olds were tested between the 46th and 71st postnatal day, and the mean age at the midpoint of testing was 58.4 days. 3 mth olds were tested between the 78th and 97th postnatal day, at a mean age of 87.7 days. Adult subjects were 2 color-normal females in their mid-twenties.
An observer seated behind the screen peered through the peephole and tried to guess the test spot position (left or right) from the infant’s looking behavior. The observer was free at all times to instruct the holder how to position the infant. Blinders on either side of the observer’s head prevented him or her from seeing the test spot. Trials had no fixed duration: a trial continued for as long as necessary for the observer to make a judgment. A third adult, the experimenter. set the wavelength. intensity and position of the test spot at the beginning of each trial, and gave the observer immediate feedback on the accuracy of his or her judgments. The method of constant stimuli was used to generate psychometric functions. In general, a l-1.5 log unit intensity range was sufficient to span the function from near chance to near 1000~,correct. With the first 6 infants tested, this range was covered in 0.5 log unit steps. Later infants were tested in 0.3 log unit steps. Three stimulus levels per function, chosen on the basis of previously collected data. were selected initially for the infant to view. These were presented randomly five times each within a 15-trial block. When a block of trials was completed for one test wavelength. the test wavelength was changed. and testing continued. If, after several days of testing, the stimulus intensities selected did not appear to span the psychometric function, new intensity levels were added at the top or bottom of the range. When two different backgrounds were used, background color alternated from one day to the next. A psychometric function was collected for each combination of test wavelength and background color. Two or more psychometric functions were generated for each infant in the 2 week period allotted for testing. For each infant, trials were evenly distributed among all the conditions tested. Infants varied somewhat in their enthusiasm for the task, and different psychometric functions represent from 12 to 30 trials per point. A cumulative normal ogive was fit to the empirical functions by the method of least squares. The upper and lower asymptotes were constrained at lOOO/;and SO%, respectively. Each percent-correct value was weighted by the reciproca! of its standard error before further computation. Thresholds were estimated to be the stimulus intensity yielding 754, correct on the best fitting cumulative normal curve.
Procedure
Adult su6ject.s
The experimental room, rear-projection screen, and white curtains were bathed in either blue or yellow light. A narrow-band test spot was rear-projected to either the left or right side of the screen. superimposed upon the chromatic background. The infant was held in front of the screen by the holder, who slowly turned the infant from side to side, giving her an opportunity to view both possible test spot positions. The holder wore a visor that kept him or her blind to the location of the test spot.
Adults were tested with direct viewing under three conditions of adaptation: yellow-, blue-, and darkadaptation. All viewing was binocular, and no artificial pupils were used. The dark-adapted measurements are described above (see Calibrations). For the yellow- and blue-adapted measurements, thresholds were estimated with two different psychophysical methods. First, thresholds were measured with steady fixation by the descending method of limits. The test spot, flickering at 0.5 Hz. appeared only on the left
adult observers, fixating 31’ to the right of the test spot. The test spot was flickered at 0.50 Hz (SO?; duty cycle). Threshold was measured by a descending method of limits. The results of 10 trials at each wavelength were averaged to obtain an estimate of threshold. These measured thresholds were then compared to the CIE scotopic luminosity function. Vi (Wyszecki and Stiles. 1967, p. 379). If the radiance of the screen was the same when transilluminated by light passing through each interference filter. then the additional density needed to reduce each test stimulus to absolute threshold should follow the V; function. We interpret the deviations of the data from the Vi function to reflect the deviations of our test stimuli from radiometric equality. A set of correction factors was generated by averaging the adult data and determining the deviation of this average from the V; function at each wavelength used. These correction factors have been applied to all the data shown in the remainder of the paper. A limitation of this method is that the average spectral sensitivity of our two adult observers may not match exactly that specified by the V>, function because of normal variation in prereceptoral absorption at shorter wavelengths. This would distort the absolute shapes of all of the spectral sensitivity curves reported here, but would not affect the differences between these curves. dark-adapted
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Fig. 2. Spectral sensitivity functions for adult observers EL (0) and EP (At under yellow (top) and blue (bottom) adaptation. The continuous curves were fit by eye to the data. The change of shape of the spectral sensitivity functions indicates that at least two independently adaptable chromatic mechanisms subserve detection of test spots for adult observers under the conditions in which infants were tested.
Spectral sensitivity curves for two adult observers, obtained by means of the method of limits. are shown in Fig. 2. Thresholds were roughly 0.5 log unit lower when determined by the method of constant stimuli. but the shapes of the spectral sensitivity functions were similar for the two methods. .Against the yellow background (1.4 log cd, m’). spectral sensitivity rose to a peak at about 440nm. and then dropped off at longer wavelengths. Spectaf sensitiv-iry functions of similar shape have been reported b>- Wald (19641, Wooten and Wald (1973). and Wooten, Fuld and Spillman (1975) for broadband yellow or yellowishwhite adapting backgrounds. The shape of the curve suggests that the yellow background so desensitized the MWS and LWS mechanisms that the curve traces the spectral sensitivity of the SWS mechanism in isolation from 400 to 500 nm. A yellow background of I .7 log cd,‘m’ produced a curve of similar shape. The mechanisms revealed against the blue background (1.5 log cd:‘m’f are less clear cut. Sensitivity rises sharply between 400 and 420 nm. dips at 460 nm, then rises again at longer wavelengths. Sperling and Harwerth (1971) reported curves of similar shape under blue adaptation. They attributed the detection
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test spot. On each trial, an experimenter decreased the intensity of the test spot in 0.1 log unit steps until the subject could no longer see it. The lowest intensity at which the test spot remained visible was recorded. The results of 10 trials at each wavelength were averaged to obtain an estimate of threshold. Second, thresholds were determined with a standard spatial forced-choice technique. Fixation points were provided on both sides of the screen, in the centers of the two test spot positions. In order to mimic the free fixation conditions used with the infants, the aduh subjects alternated fixation every few seconds between the two fixation points. The test spot was projected to either the right or the left side of the screen, and was cycled on and off at about 0.5 Hz. Psychometric functions were determined for each waveiength, and threshold was defined as the stimulus intensity that permitted the subject to judge the position of the test spot correctly 75% of the time. In sum, there are three main differences between infant and adult data collection-psychophysical method, fixation control, and the temporal characteristics of the stimulus. For reasons detailed in the Discussion section, we believe that these differences do not jeopardize the results or conclusions of this study.
Fig. 3. Psychometric functions of two infants, each tested at two test wavelengths against two adapting backgrounds. Test spots: O+460 nm: 0. 560 nm. Backgrounds: continuous curves, yellow: broken curves. blue. Threshold for detecting the test stimuli against each background was taken to be the 7.5’; correct level of the best fitting cumulative normal ogive (not shown). Changes of background reversed the infants’ relative sensitivity to the two test wavelengths. This demonstrates that at least two chromatic mechanisms subserve these i&ants’ color vision over the range of 460-560 nm.
infant chromatic adaptation
489
shown here, sensitivity to 460 nm relative to 560 nm test lights clearly shifts with the shift of chromatic background.
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Fig. 4. Relative sensitivity of same two adults shown in Fig. 2 (a), same 2 infants shown in Fig. 3 (0) and two additional infants (0) to 460 and 560 nm test spots projected against blue (broken curve) and yellow (continuous curve) backerounds. Three of four infants displayed differences’in spectral sensitivity, measured on the iwo backgrounds. similar to that shown by adults. One infant showed no reliable change in spectral sensitivity.
of short wavelengths (~460 nm) to the SWS mechanism. detection of middle wavelengths to the MWS mechanism, and detection of wavelengths greater than 490nm to the LWS mechanism. Overall, the change of chromatic background produced a clear change of spectral sensitivity, signalling the participation of at least two chromatic mechanisms, presumably SWS and MWS, in the determination of these data sets. Infant psvchomerricfunftions Figure 3 shows psychometric functions, generated with 460 and 560 nm test spots against the same two backgrounds (1.5 log cd/m’ blue and 1.4 log cd/m’ yellow), for two 2 mth old infants. All data sets drop from a high percent correct to near chance with a l-2 log unit change in test intensity. For both infants * As usual, it must be emphasized that these data provide only a lower bound estimate of the infant’s visual capacities: there is obviously no evidence that the infant cannot see berror than the levels estimated by any given technique. Further, psychophysical data alone do not reveal the Iocation of information loss within the organism. These problems, of course. are not confined to the FPL technique, nor indeed to the field of infant psychophysics (cf. Teller. f979).
sonsiticit)
Figure 4 summarizes sensitivity for 460 nm and 560 nm test spots against the blue and yellow backgrounds, for the two adults and two infants described above, and for two additional infants. All six subjects are plotted on the same relative sensitivity scale. Both adults are more sensitive to 460 nm than to 560 nm under yellow-adaptation, but more sensitive to 560 nm than to 460nm under blue-adaptation. Like the adults, three of the infants were more sensitive to 560nm than to 460nm when the background was blue. while the fourth infant (Rachel) was about equally sensitive to both wavelengths. When the background was yellow, two of the infants (Dana and Elizabeth) were more sensitive to 460nm than to 56Onm. and the other two infants (Shannon and Rachel) were about equally sensitive to both wavelengths. Although the latter two infants did not show the same yellow-adapted spectral sensitivity found with adults, one of them (Shannon) did show a change in spectral sensitivity in the expected direction with changes in chromatic adaptation. The other (Rachel) showed no convincing change. On the whole, the infants demonstrated absolute sensitivity lower by 1 to 2 log units than the adults for both test wavelengths and both conditions of adaptation.’ But, like the adults, spectral sensitivities for three of the four infants changed in a predictable fashion with changes in the spectral com~sition of the back~ound. We conclude that at least some 2mth olds have at least two separately adaptable visual mechanisms operating over the short-wavelength half of the spectrum. In the following experiments we attempt to identify these mechanisms. More extensive short-wavelength spectral sensitivity curves, obtained from two additional 2 mth old infants, are shown in Fig. 5. Thresholds were obtained at each of several wavelengths between 420 and 540nm, against a yellow background of 1.75 logcd/m2. The figure also shows the adult yeilow-adapted spectral sensitivity curve, redrawn from Fig. 2. The data sets from the infants have been shifted vertically (by 3.1 and 3.3 log units) to coincide with the adult curve at 460 nm. The data from the two infants are in rough agreement, and indicate that sensitivity increases as the wavelength increases from 440 to 5OOnm. The infants differ substantially from the adults tested, and from published estimates of spectral sensitivity of the classical adult SWS mechanism. Thus, these two infants have failed to reveal a classical SWS mechanism under conditions that reveal the mechanism in adult subjects. Finally, four additional 2 mth old infants were tested at 460 and 500 nm against a 1.75 log cd/m2 yellow background. Of these, three were retested at 3 mth. Four additional 3 mth olds were also tested.
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The data sets from these infants and from the 2 mth olds shown in Fig. 5 are plotted in Fig. 6. Several trends are apparent in Fig. 6. Although data from the two groups overlap, the 3 mth olds. on the average. demonstrated higher absolute sensitivities than the 2 mth olds at both wavelengths. The relative log sensitivities for 2 and 3 mth old infants, respectively, were I.5 + 0.6 and 2.3 k 0.4 at 460 nm and 1.5 + 0.3 and 2.0 2 0.2 at 500 nm. The 3 mth olds on the average show 0.3 log unit higher sensitivity to 460 than to 500 nm, while for the 2 mth olds this difference is zero. Both within and across age groups, there was greater variability among infants in sensitivity to 460 than to 500 nm light. Three of the infants in Fig. 6 were tested at both 2 and 3 mths of age. Kathleen (squares) was very sensitive to both wavelengths at 2 mth, and remained so at 3 mth. At both ages, she was about 0.6 log unit more sensitive to 460 than to 500nm. For this subject, maturation produced a change in overall sensitivity, but not a change in spectral sensitivity. A second infant, Diana (upside-down triangles), showed a change with age in both overall sensitivity and spectral sensitivity. At 2 mth she was relatively more sensitive to 560 nm than to 460 nm, while by 3 mth she was about 0.3 log unit more sensitive to 460 nm. A third infant, Jeanie (triangles), also improved in overall sensitivity as she became older. Her spectral sensitivity, however, remained flat from 2 to 3 mths of age. Thus, maturation over this time period seems to elevate demonstrated sensitivity in individual infants, but does not always bring a change in spectral sensitivity. There is also a strong correlation (r = 0.92) across groups between an infant’s absolute sensitivity to 460 nm and her relative sensitivity to 460 vs 500 nm light. This trend is readily visible in the fan-like arrangement of the slopes of the lines in Fig. 6. The two infants who were least sensitive to 460 nm light on an absolute scale were also less sensitive to 460 nm than
to 500 nm light. Infants who were intermediate in sensitivity to the 460 nm test spot showed approximately equal sensitivity to 460 and 5GQnm. The six infants who were more sensitive to 460 nm also showed higher relative sensitivity to 460 than to 5OOnm light-a pattern closely resembling that shown by adults. Under yellow-adaptation. adults were about 0.6 log unit more sensitive to 460 than to 500 nm: the infants with the steepest slopes come very close to this value, although they remain 1.5-2.5 log units less sensitive than adults in absolute terms. DISCL’SSIOS These experiments have shown that (1) some 2 mth olds have at least two separately adaptable visual mechanisms in the short-to-middle-wavelength region of the spectrum; (2) adaptation sufficient to reveal a SWS mechanism with a peak at 440 nm in adults does not do so consistently in infants: (3) young infants differ greatly from one another in their relative sensitivity to short wavelengths under yellow-adaptation: and (4) under yellow adaptation there is a strong correlation between an infant’s absolute sensitivity to short-wavelength light (460 nm, in this case) and the
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Fig. 6. Relative sensitivity to 460 and 5OOnm for 2 adults (top) and IO infants (bottom) under yellow-adaptation. The solid symbols are from 3 mth olds. and the open symbols from 2 mth olds. Three of the infants, shown by squares, triangles, and upside-down triangles. were tested at both 2 and 3 mth of age. The sensitivity to 460 nm relative to 500 nm under yellow-adaptation varies considerably among infants. About 8Y, of this variance can be accounted for by differences among infants’ absolute sensitivity to the 460 nm test spot. That is. infants most sensitive to short-wavelength light also displayed the most adult-like spectral sensitivity.
Infant chromatic adaptation shape of the infant’s short-wavelength spectrai sensitivity function (relative sensitivity to 46Onm vs 500 nm or 560 nm lights), such that infants most sensitive to short-wavelength light also display the most adult-like spectral sensitivity. For several reasons. we believe that the procedural differences between adult and infant data collection are unlikely to jeopardize the conclusions of this study. We particularly point out that two different techniques were used to test adults, with highly similar results; that the free fixation of infants was mimicked by a condition of alternating fixation in adults: that free fixation tends to enhance blue sensitivity, not diminish it (Yager, 1970); that most of the conclusions drawn depend upon comparisons within or between infants. rather than to any adult standard (or physical calibration): and finally, that the infants with highest absolute sensitivity appear to approach most closely the adult standard, thus providing additional internal consistency within the experiment itself.
There are two main factors that may explain the individual differences among infants in absolute and relative sensitivity. These are differences in prerecep toral absorption and differences in the relative sensitivity of a SWS mechanism. Short wavelengths are especially susceptible to prereceptoral absorption losses within the eye, especially in the lens and macular pigment. In addition, the densities of both lens and macular pigments are reported to vary substantially among adults, leading to individual differences in adult photopic and scotopit visual spectral sensitivity functions and in metamerit color matches involving short wavelengths (for a review, see Ruddock, 1972). Despite these qualitative characteristics, we think it is unlikely on quantitative grounds that either of these prereceptoral pigments contribute to any major degree to the differences seen among infants in the present experiment. The extinction spectrum of the lens peaks in the ultraviolet. It is relatively low and flat for wavelengths of 450nm and above, and changes by only about 0.1 log unit between 460 and 500 nm. Thus, individual differences in density in this wavelength range must have small effects at best. In addition there is some evidence (Werner, 1979) and much sp~u~ation that infants have, on the average, less dense lens pigmentation than do adults (but cf. Cooper and Robson. 19691,a factor that would render such differential effects even smaller for infants than for adults. The macular pigment absorbs most strongly between 410 and 510nm, with a peak at about 460nm (Wyszecki and Stiles. 1967, p. 128). and thus has appropriate spectral characteristics to explain the individual differences found in the present experiment. However, to account for the more than 2 log unit
491
variation in sensitivity among infants at 46Onm and the more than 1 log unit variation at 500 nm shown in Fig. 6, one would have to assume the presence of very high densities of macular pigment in the least sensitive infants. Contrary to this assumption. it is widely believed that the macular pigment is less dense in infants than in adults (cf. Werner, 1979). although no modern data have been published on this topic. It would also be necessary to assume that. despite being shielded from the incoming light by high densities of macular pigment, the region of retina detecting the test. stimulus is nonetheless located behind the assumed pigment. For a large test fieid the combined likelihood of these factors is low; and we conclude that explanations for the present individual differences are more likely to be found at neural than at prereceptoral levels. The remaining major possibility is that individual infants differ markedly in the relative sensitivity of a SWS mechanism. In adults. the relative sensitivity of the SWS cone mechanism has been reported to vary across individuals (Wald, 1964). across retinal regions (Wald, 1964; Wooten and Wald. 1973). and with other factors such as time during d~k-adaptation (Wooten er ai., 1975). Thus, variations across infants during development seem plausible. Large individual differences among infants in relative sensitivity to 450nm light may also be seen in the VEP data of Dobson (1976). Thus, the idea that individual infants differ markedly in the relative sensitivity of their SWS mechanism seems to us the most likely explanation of the individual differences seen in the present experiment. The
co~rribut~on of rods
The yellow-adapted spectra1 sensitivity of the two most extensively tested 2 mth olds, shown in Fig. 5, resembles the adult scotopic curve. It is reasonable that the rods might detect short wavelengths under the conditions used if the SWS cone mechanism were absent or comparatively insensitive. The longwavelength background and large, short-wavelength test stimuli would be well-suited for rod isolation. Aguilar and Stiles (1954) found that long-wavelength backgrounds of about 3.2 log Scot td are necessary to saturate the rod system. Thus, even the brightest yellow backgrounds used here, which correspond to about 2.4 log Scot td, were below adult rod saturation level. Yet it would be unduly speculative to conclude that rods determine the thresholds shown in Fig. 5. Indeed, these data could reflect a combination of infant SWS, MWS, and/or rod mechanisms, any of which may differ from those of the adult. It is interesting to note that Abramov and Gordon. (1977) report a curve of similar shape for adult photopic spectral sensitivity measured 45’ in the peripheral retina, without being able to attribute it with any certainty to any particular receptor mechanism.
E. PULOSrr d[.
432 Comparison.
of‘
infants to adrtlrs
Previous studies of infant photopic spectral sensitivity have yielded some superficial inconsistencies in the question of the average relative sensitivity of 2-3 mth old infants vs adults in the short-wavelength region of the spectrum. On the basis of VEP data, Dobson (1976) and Moskowitz-Cook (1979) have concluded that on the average infant spectral sensitivity is relatively high in the short-wavelength region; while on the basis of behavioral data Peeples and Teller (1978) have concluded that infants and adults have similar relative sensitivities throughout the spectrum. The present study suggests that the majority of infants are relatively less sensitive than adults in the shortwavelength region, under both yellow- and biueadaptation conditions. Thus, published studies have covered the range of possible outcomes, although the reported differences in previous studies have been small. There are many differences in technique, stimulus conditions, adaptation conditions, etc., among the various studies. We have not been able to choose with conviction among the many possible reasons for the differences among studies, nor indeed to decide whether the differences should be considered real or attributed to different random samples from highly variable populations. It is worth noting that both directions of difference between infants and adults could legitimately be found. If, for example. the infant has a poorly developed SWS system but a lower density of macular pigment than the adult, these factors could interplay to give either kind of result. Under conditions in which the SWS cones never determine the threshold for either age group, infants could be relatively more sensitive than adults in the short-wavelength region, owing to their advantage in prereceptoral absorption factors. But under conditions in which adults use their SWS cones for detection of short wavelengths, infants could be relatively less sensitive than adults at short wavelengths. The question of the shapes of photopic spectral sensitivity curves, especially in the blue region of the spectrum, is one of the most complex topics in visual psychophysics and electrophysiology, and there is no reason to expect it to be less complex in developing systems. It seems likely that small -inconsistenci& across studies in the relative sensitivity of infants and adults to short-wavelength light will be the rule, rather than the exception, until larger samples and more systematic variations of experimental conditions are carried out. In summary, under the present conditions. three out of four 2 mth old infants showed changes of spectral sensitivity with chromatic adaptation within the short- to middle-wavelength range, thus revealing the presence of at least two chromatic mechanisms. However, yellow-adaptation conditions that were sufficient to reveal the SWS mechanism in adults did not consistently do so in 2 and 3 mth old infants.
To unite these results. we offer the interpretation that the SW’S mechanism lags behind the others in early postnatal development. We further suggest that the development of short-wavelength sensitivity follows a different time course in different infants. and that as a group the 2 and 3 mth old infants tested were in the midst of such a developmental process.
.-lckno~~edg~tnents-This research was supported in part bv NIH Postdoctoral Fellowshio EY 041567 from the National Eve Institute to Steven E&k; NICHD Grant HD 02274. Research in Mental Retardation and Child Development; and NSF grant BNS 76-01503 to Davida Teller. We thank Jean Kellv. Clifton Lee. Elvse Litvack. and Greg Stewart for laboratory assistance: karjorie Zachow for secretarial assistance; and Drs Israel Abramov. Marc Bornstein. Walter Makous, Anne Moskowitz-Cook and Bill Wooten for comments on the manuscript, REFERENCES
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