First glances: the vision of infants. the Friedenwald lecture.hist-innov.comotion.uw.edu/.../Teller-lecture-First-Glances-The-Vision-of-Infants.pdfTwo other measurement techniques—visual

First Glances: The Vision of InfantsThe Friedenwald Lecture

Davida Y. Teller

L wenty-five years ago, when my children were small,scientists knew almost nothing about the developmentof vision in human infants. William James1 had opinedthat the infant's perceptual world was a blooming,buzzing confusion. Some ophthalmologists were in-clined to suggest that infants could see almost noth-ing. Yet parents had known for millennia that infantsstare at faces and boldly patterned objects. Becauseconsistent staring implies seeing, infants must be ableto see. But what do they see, and how well? This ques-tion eventually proved irresistible to a person who wasat once a parent and a vision scientist. The beginningof science is wonder.

FORCED-CHOICE PREFERENTIALLOOKING

A few years earlier, the psychologist Robert Fantz2'3

had formalized measures of the infant's spontaneouslooking behavior into a quantitative technique that hecalled preferential looking (PL). In Fantz's PL para-digm, an infant is confronted with a series of pairs ofboldly patterned stimuli. An adult observer watchesthe infant through a peephole and scores various as-pects of the infant's looking behavior—the directionof the infant's first look, the amount of time spentlooking at each object, and the number of looks to-ward each object. These values are averaged in a groupof infants of a given age and a group looking-prefer-ence score for each pair of objects is obtained.

For a psychophysicist looking through the peep-hole, it was a natural insight to transform the observ-er's task into a two-alternative, forced-choice judg-ment. That is, the infant can be presented with a singlestimulus—a coarse black and white grating, embed-ded in a gray surround of matched space-averageluminance, for example—the left-right position ofwhich can be varied randomly from trial to trial.Rather than scoring the various characteristics of the

From the Departments of Psychology and Physiology-Biophysics, University ofWashington, Seattle.Reprint requests: Davida Y. Teller, Department of Psychology, University ofWashington, Guthrie Hall, Box 351525, Seattle, WA 98195-1525.

looking behavior, the observer's task is to use the in-fant's looking behavior as a basis for judging the loca-tion of the grating on each trial.

As shown in Figure 1, for boldly patterned stimuli,the observer's task is an easy one. If the observer cando better than chance at judging the location of thegrating over repeated trials, then barring artifact, itfollows that the infant must be able to resolve thegrating.4 Although the technique was briefly chris-tened "Peep and Tell,"5 it was soon renamed forced-choice PL, or FPL. The logic and limitations of theFPL technique have been discussed in detail else-where.6

To estimate the acuity of an infant by FPL, theinfant is tested with each of a series of spatial frequen-cies of the grating, for, say, 20 trials each, in a randomseries. The result is a data set closely analogous to aclassic forced-choice psychometric function. The in-fant's FPL acuity can be defined as the spatial fre-quency required for 75% correct judgments on diepart of the observer. Data from our first longitudinallytested infant subject, Peter, are shown in Figure 2.Because of our inexperience at the time, full psycho-metric functions were not obtained at the earliest ages.We were nonetheless astonished to see that the psy-chometric functions marched regularly leftward to-ward higher spatial frequencies, in a perfect develop-mental sequence, for all the world as though some-thing real and growing were being measured.

In our hands, the effectiveness of the FPL tech-nique begins to diminish at approximately 5 monthsafter birth. Infants will still stare at gratings for a fewtrials but not for the 80 or more trials needed to definethe psychometric function. Operant reinforcershelp.7'8 Our version of an operant technique, whichcame to be called operant PL, or OPL, employs ananimated toy as a reinforcer. Such techniques allowdata to be collected from most youngsters at eachage from infancy through toddlerhood to preschool,although 18-month-olds provide their usual challenge.

GRATING ACUITYEarly data showing growth curves for grating acuity,estimated with FPL and OPL on groups of infants, are

Investigative Ophthalmology & Visual Science, October 1997, Vol. 38, No. 11Copyright © Association for Research in Vision and Ophthalmology 2183

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2184 Investigative Ophthalmology & Visual Science, October 1997, Vol. 38, No. 11

FIGURE 1. The author as an infant, staring at something. Theforced-choice preferential looking procedure uses the infant'sspontaneous staring behavior as the basis for quantifying theinfant's visual capacities. A stimulus is presented to the infantin a left or a right location. An adult observer watches theinfant's staring behavior and uses it to judge the left-rightlocation of the stimulus in each trial of the experiment. Above-chance performance by the observer implies that the infantcan see the stimulus. Photo enhanced by Tony Young (copy-right 1997 © Tony Young; used with permission).

shown in the left side of Figure 3, with postnatal ageplotted in months on a logarithmic scale.9 Measuredwith these techniques, grating acuity increases regu-larly with age, and variability within age is small. Thus,the technique shows a great deal of face validity as ameasure of spatial resolution and its development. Asa reminder that the spatial resolutions measured maybe specific to the measurement technique used, theacuity values obtained can be labeled more specifi-cally, as FPL and OPL acuities.

Two other measurement techniques—visualevoked potentials (VEP) and optokinetic nystagmus(OKN)—were also used in early studies to estimategrating acuity in infants.10 Classic VEP acuity data fromNorcia and Tyler11 are shown in Figure 4. Interest-ingly, VEP acuities tend to be higher than FPL andoperant acuities throughout much of infancy. Severalexperimental factors, all favoring the finding of higherVEP than FPL acuity values, probably combine to con-

tribute to this difference. They include the use offlickering stimuli, signal averaging, generous scoringcriteria, and summation of signals across the wholevisual field. Moreover, VEPs are probably controlledlargely by early cortical processes, whereas behavioraldata rely on the whole infant, including later stagesof visual processing as well as central and motor pro-cessing. Optokinetic nystagmus acuities tend to fallcloser to PL than to VEP acuities.10'12"13

Monkey Model

For me,14"16 one of the major attractions of visual sci-ence is the promise it holds for empirical attacks onthe mind-body problem—that is, for working outmeaningful ways to explain psychophysically definedvisual functions on the basis of properties of the neuralsubstrate. A critical locus or critical computation for aparticular perceptual function can be defined as as ananatomic or computational stage at which informationconcerning that function is lost or importantly reorga-nized; or more poetically, as a stage or computationthat leaves its mark on that perceptual capacity.

Part of the appeal of visual development is its po-tential for extending this promise. Visual functionsmature because the visual substrate matures, and thecauses of functional maturation undoubtedly lie inneural maturation. But the length of the big toe ma-

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FIGURE 2. Data from the first infant tested widi the forced-choice preferential looking technique in the author's labo-ratory. The abscissa shows the width of each of the stripesin an acuity grating (that is, one half of the period of thegrating). High spatial frequencies {fine stripes) are at the left,and low spatial frequencies {coarse stripes) are at the righton the abscissa. The ordinate shows the observer's percent-age of correct judgments of the left-right location of thegrating, based on the infant's looking behavior. The dashedline shows chance performance. The parameter is age inmonths. At 1.5 and 2 months, incomplete psychometricfunctions were obtained, because of the experimenters' in-experience and the absence of coarser grating stimuli. At 3,4, 5, and 6 months, infant Peter showed increasingly highgrating acuities (modified from Teller et al4).


The Friedenwald Lecture 2185

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FIGURE 3. Increases in forced-choice preferential looking (•) and operant acuity (A) as a func-tion of age, in human infants (left) and macaque monkey infants {right). Human age is plottedin months, and monkey age is plotted in weeks. Both species show similar acuity values nearbirth. Acuity increases steadily with age in both species but faster by approximately a factor offour in monkeys than in human infants. These early data helped to establish the infant macaqueas a good animal model for human visual development. The dotted line represents a mnemonic:Acuity in cycles per degree is roughly numerically equivalent to age, in mondis for humaninfants and in weeks for macaque infants (from Teller9).

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tures too, and we do not see it as causal in relation tothe development of grating acuity. The puzzle is,which of the many immaturities of the visual substrateprovide the critical immaturities17 that limit a particularvisual capacity at a particular age?

If analyzing the neural causes of visual immaturi-ties is part of the goal, then the enterprise requiresan animal model because it requires invasive experi-ments. To establish the animal model, behavioral datamust be collected on both species. The more exactlyparallel the behavioral paradigms across species, thebetter one can establish an age conversion and theresults of invasive work on the monkey infant to thehuman infant with maximum confidence and mini-mum risk.

Early work in the Infant Primate Laboratory at theUniversity of Washington showed that FPL techniqueswork well with infant macaque monkeys,18 and specializedoperant techniques could also be used.19 The right sideof Figure 3 shows the growth of FPL and operant acuityin infant pigtail macaques, with age plotted in weeks. Thegrowth curves for human and monkey infants are similarwhen plotted in months and weeks, respectively. Thegrowth of grating acuity thus conforms at least roughlyto the 4:1 rule often seen in measures of sensory andcognitive development: Human and macaque infants aresimilar at birth and have similar growth curves, but a weekin the life of an infant monkey is like a month in die lifeof a human infant. With the accumulation of more dataon more visual functions, it will be important to refinethis rule.



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FIGURE 5. The author's grandson is introduced to an acuitycard. Note the look of rapturous attention—possibly a famil-ial trait. To test an infant's acuity, a clinically trained ob-server selects cards with finer and finer gratings and notesthe spatial frequency at which the infant's staring behaviordrops out. That spatial frequency provides an estimate ofthe infant's acuity (copyright 1997 © Tony Young; used withpermission).

Of course, to fulfill its promise, the enterprise alsorequires that anatomic and (especially) physiologicalwork be carried out in infant monkeys. Interestingly,single-unit recording in infant monkeys has been slowin coming of age, and we have had a curious repetitionof historical order: As was true until the last two de-cades in adult vision science, in infant vision the psy-chophysics still leads the physiology. In consequence,as will be seen below, the findings and puzzles thatarise from behavioral studies of infant visual develop-ment provide many hints for functionally interestingphysiological experiments.

Acuity Cards

Since the time that PL techniques were first devel-oped, they have been used to characterize the visionof infants with known or suspected neural and visualproblems,20 and several of the earliest infancy labora-tories took on clinical problems. But the time-consum-ing nature of FPL testing in individual infants madeit unsuitable for wide-scale clinical use.

At the same time, the remarkable intensity andconsistency of the infant's staring behavior suggestedthat in the hands of a practiced clinician, a less strin-gent variation of PL testing might still provide validand reliable acuity estimates. The result of this line ofthinking was a set of acuity cards, each with a gratingof a different spatial frequency, displaced to one sideof a central peephole. A practiced clinical observercan present a coarse grating for one of two trials, flip-ping the card to vary the left-right location of thegrating, and judge directly whether or not the infantcan resolve the grating. If so, the observer moves to

finer and finer gratings until the infant's staring be-havior falls apart. The spatial frequency of the card,which ellicits marginal staring behavior, provides anestimate of the infant's acuity.21 An infant's informalintroduction to an acuity card is shown in Figure 5.

Results of a series of validation studies with the acuitycards showed that acuities could be estimated in lessthan 5 minutes per eye, diat testability rates and intra-and interobserver reliabilities were high, and that theaverage acuity values obtained at each age agreed wellwith those obtained with more formal PL techniques.22

Acuity cards are now used in many pediatric clinicalsettings. Most recendy, formal age norms have been de-veloped,23 as is shown in Figure 6.

Two major limitations of the acuity cards mustbe stated. First, the test-retest reliability of estimatedacuities is on the order of an octave (a factor of two),although the actual value varies with age.22 Second,the cards are obviously a measure of grating (resolu-tion) acuity, whereas the Snellen chart measures letter(recognition) acuity. For both of these reasons, theacuity cards are not an optimal instrument for measur-ing small differences in acuity, including some clini-cally important interocular differences that would beclassified as mild to moderate amblyopia. It is hopedthat a more sensitive instrument for the early detec-tion of amblyopia will eventually be developed,normed, and validated. In the meantime, the acuitycards provide a more quantitative guide than did theophthalmologist's "fix and follow," to whether or notan infant's or young child's vision is developing on anormal time course.

BEYOND GRATING ACUITY: OTHERVISUAL FUNCTIONS

Thanks to the efforts of many people and many labora-tories, our understanding of infant vision has come a

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The Friedenwald Lecture

INFANT VISUAL PERCEPTION

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long way in the past 25 years. This section of the articlecontains a brief summary of our knowledge about thedevelopment of a variety of basic visual functions: spa-tial contrast sensitivity, color vision and scotopic vi-sion, temporal vision and motion, stereopsis and fu-sion, and vernier acuity and orientation discrimina-tion. The figures were selected to capture the essenceof knowledge about each function, and at the sametime, to represent work from as many laboratories andindividuals as possible. Excellent in-depth reviews onthese and other aspects of visual development may befound in several edited volumes.24"26

Spatial Contrast Sensitivity

In the broader context of visual psychophysics, gratingacuity is identified closely with the high-frequency cut-off of the spatial contrast sensitivity function (CSF).From the beginning,27 FPL and related techniqueswere applied to the measurement of CSFs. To date,behavioral CSFs have been measured in human in-fants only during the first 8 postnatal months28"31 andduring the 3- to 5-year age range32 and in infant mon-keys during the intervening age range.33 The mostextensive VEP data have been reported by Norcia etal.34

Representative data from human and monkey in-fants are shown in Figures 7 and 8, respectively. Theimmediately most interesting aspects of the data arethat the CSFs appear to shift vertically and horizontallyduring development. It has been argued that whentest conditions are held constant, data sets at all agescan be fit with the same shape-invariant function,

2187

shifted only vertically in sensitivity, and horizontally inspatial scale.35

The CSF has long been modeled as the upperenvelope of a set of more or less independent, spatial-frequency-tuned channels.36'37 In this context, twoclasses of developmental models can be proposed. Ihad thought that the different spatial channels wouldgrow in sensitivity independendy, like teeth, each oneincreasing in sensitivity by the amount required tomodel the CSF at each age. An alternative3839 is thatall of the spatial channels shift together both in sensi-tivity and in spatial scale during development. Thelatter suggestion has recendy been confirmed on thebasis of covariance structure analyses of individual dif-ferences.30'31'40 Estimates of the developmental shiftsof sensitivity and scale, for the two lowest frequencychannels from Wilson's model, are shown in Figure9. Recent data extend these analyses to the red-greencolor domain.41"44

At the anatomic level, the known immaturities ofthe primate fovea45'46 provide a likely critical locus forlimiting infant acuity and contrast sensitivity. At birth,infant foveal cones are coarsely packed; in combina-tion with changes in eye size, the change in packingdensity affords a predicted change in spatial scale ofapproximately 1:4 between birth and adulthood, ingood correspondence with the spatial scale shift seenin CSFs.

Infants' foveal cones also have very short outer

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Spatial Frequency (c/deg)FIGURE 9. Estimates of the development of the two lowestspatial frequency channels proposed by Wilson et al.37 Theestimates are based on a covariance structure analysis ofindividual differences in data taken from 4-, 6-, and 8-month-old infants and from adults (from Peterzell and Teller40).

segments, and probably inferior wave-guide proper-ties. These immaturities, together with the reducedretinal coverage resulting from the coarse spacing,doubtless result in a drastic reduction of quantumcatch. Quantitative models of the information pro-cessing capabilities of the infant fovea have been devel-oped.38'39'47"'19 Moreover, single-unit recordings frommonkey lateral geniculate nucleus (LGN) show thatthe LGN neurons with the highest acuities have acuit-ies only approximately a factor of two higher than thebehaviorally measured acuities of young infant mon-keys.50'51 Thus, much but not all of the limit on infantacuity, and the reductions in sensitivity and spatialscale seen in infants' CSFs, are probably attributableto critical immaturities that take place before the levelof the LGN. Remarkably, the infant seems to be agood and faithful psychophysical subject and comesclose to being able to report on the activity of her bestLGN neurons.

Thus, in the case of acuity and contrast sensitivity,surprisingly little of the developmental deficit is left tobe accounted for by later sensory, cognitive, motiva-tional, or motor immaturities. Moreover, these losses ofsensitivity and scale will doubtless play through impor-tantly, to influence the development of many other vi-

sual functions. Foveal immaturity is clearly a critical ele-ment for modeling many of the losses of function seen invisual development. Quantitative modeling of sensitivitylosses in extrafoveal retina has also been undertaken.52

Color Vision and Scotopic Vision

For me, there is nothing more fascinating than sittingin my Cartesian theater and watching the world inTechnicolor. Moreover, color psychophysics is scien-tifically attractive because, here more than in anyother branch of psychophysics, behavioral data oftenreveal the "signatures" of underlying physiologicalmechanisms.53 Color was thus a tantalizing topic toinvestigate at the very beginning of the study of infantvision.

At the scientific level, color vision can be definedas the capacity to discriminate among lights of differ-ent wavelength composition, on the basis of the differ-ence in wavelength composition.54 Differential re-sponding to lights or objects of different wavelengthcomposition, in itself, is not a sufficient demonstrationof color vision, because of the problem that the infantmight be responding to luminance (or brightness)differences rather than to differences in wavelengthcomposition. Twenty-five years ago, the infant's phot-opic spectral luminosity function was as unknown asthe infant's wavelength discrimination capacities, andflicker photometry was not readily performed on in-fant subjects. The problem was, where to begin?

An FPL-based paradigm for demonstrating colorvision in infants, without knowing the infant's spectralefficiency function, was developed in our early work.5

In this paradigm, an infant could be presented witha white or a red stimulus, of any of many differentluminance levels, embedded to the left or the rightof center in a white surround. First, the infant waspresented with a series of white stimuli of differentluminances, and we measured the infant's Weber frac-tion— the threshold luminance difference betweenstimulus and surround required for the infant to stareat the white stimulus.

Second, the infant was presented with the redstimulus embedded in the white surround. The lumi-nance of the red stimulus was varied in steps smallerthan the infant's Weber fraction, so that for the infant,at least one of the red stimuli (whichever one fellclosest to the infant's luminance match) would beindistinguishable from the surround on the basis ofluminance differences alone. As is shown in Figure10, 2-month-old infants stared reliably at the red fieldat all of the different luminance levels, including byinference, the stimulus that represents the infant'sred-white luminance match. This result is strong evi-dence that the infant can make the red-white discrim-ination on the basis of the difference in wavelengthcomposition. We therefore concluded that the infant



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FIGURE 10. An early demonstration of color vision in 2-month-old infants. The abscissa shows the log-relative lumi-nance of a red or white bar presented in a white screen.The arrow in each panel marks the adult luminance matchof the red or white bar to the screen. The lower panel showsthe infant's brightness discrimination capacity—that is, dis-crimination of the white bar from the white screen. Theupper panel shows that the infant can discriminate the redbar from the white screen at all relative luminances, includ-ing, by inference, the infant's red-white brightness match.The infant therefore must have some form of color vision(from Peeples and Teller5).

has at least two functional photoreceptor types, andthe necessary neural machinery to compare their out-puts and to use them as the basis of a behavioral re-sponse. Several other demonstrations of color visionin infants occurred at about the same time.55

In a series of subsequent studies we made use ofthis paradigm to test other chromatic discriminations.We were able to show that 2-month-old infants candiscriminate broad-band reds, oranges, greens, blue-greens, blues, bluish purples and reddish purples fromwhite, but fail in zones centered in the yellow-greensand midpurples.56 The results of this early study areshown in Figure 11.

Most 2 month olds also make both Rayleigh discrim-inations57 and tritan discriminations,58 suggesting thatthe red-green and tritan channels of early chromaticprocessing59 are functional at that age. Fewer 1 montholds respond to these color differences, suggesting thatconsistent responsiveness to large color differencesemerges during the second postnatal month. We alsoshowed that test field size is an important variable, withthe onset of the infant's responses to chromatic differ-ences coming later the smaller the size of the chromaticfield.60 Even the use of eight degree fields, however, inour hands, reveals only minimal chromatic discrimina-tion in very young infants,61 although other investigatorsfind earlier onsets.62

Results of more recent studies have helped to

resolve the problem of the infant's photopic lumi-nosity function. In particular, motion-nulling tech-niques63"65 show that infant photopic spectral sensi-tivity closely resembles that of adults tested undersimilar conditions. And as shown in Figure 12, whenconditions approximating those traditional inflicker photometry are used, the VEP-based spectralluminosity function of infants closely resembles V*.throughout much of the spectrum.66 Hence, therecan be little doubt that a neural pathway that carriesa weighted sum of L (long-wavelength-sensitive, or"red") cone and M (midwavelength-sensitive, or"green") cone inputs is present and functional inyoung infants.

Several other paradigms have also been used tostudy the mechanisms of infant color vision. Underbright yellow adaptation, VEP techniques reveal a spec-tral maximum at ~440 nm—the signature of functionalS (short-wavelength-sensitive, or "blue") cones.67 Witha high-intensity, 580-nm background, FPL techniquesreveal a Sloan notch—the signature of L and M conesand a red-green opponent process.68 More recent VEPdata using receptor-isolating stimuli confirm the pres-ence of L cones, M cones, and rods.69

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FIGURE ll. CIE chromaticity diagram showing chromaticitiesof stimuli used to test 2-month-old infants in an early colorvision study. Closed circles show the stimuli that infants dis-criminated from the white screen; open circles show thestimuli that infants failed to discriminate; and half-open cir-cles show chromaticities on which some infants succeeded,whereas others failed. The infants discriminated red (R),orange (O), most greens (Gl, G2), blue-green (GB), blue(B), bluish purples (PB) and reddish purples (PR) from thewhite screen, but failed with some yellows (Y), yellow-greens(GY, YG), and midpurples (PI and P2; from Teller et alr>f>).



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FIGURE 12. Photopic spectral luminosity functions, based ona visually evoked potential variant of flicker photometry, foradults (•) and infants (O). The solid line shows the 10° CIEVx function, and the dotted line shows Vos's modified 2° Vxfunction (from Bieber et al66).

Scotopic Vision. By 1 month after birth, infantsshow a dark-adapted spectral sensitivity curve that iswell fit by the adult standard scotopic curve, V \ ,throughout most of the spectrum.7071 It follows thatinfants' rod photoreceptors, and postreceptoral pro-cessing sufficient for a behavioral response to rod-initiated signals, must be functional by this age (andpresumably at birth). A summary of the change inabsolute sensitivity of rod vision with age is shown inFigure 13. Further analyses of scotopic vision havebeen presented elsewhere.5272

Current Status of Infant Color Vision. More recentwork in infant color vision has moved toward the useof isoluminant red-green gratings, and toward thestudy of chromatic spatial and temporal contrast sensi-tivity functions and motion processing. This work isdiscussed in the sections on spatial and temporal pro-cessing. Suffice it to say here that there is broad (butnot universal)6273 agreement across laboratories andtechniques that for most infants, red-green discrimi-nation emerges in the second postnatal month.

The emergence of tritan discriminations is lesswell studied, and the few available reports seem con-tradictory. In results in our original study,56 the failurezone of 2 month olds falls suggestively near a tritanaxis. More recently, 2-month-old infants have beenshown to make tritan discriminations between mono-chromatic lights.58'61 But most recently, 2 and 4 montholds have failed to produced directionally appropriateeye movements in response to moving tritan grat-ings74; and we (Dobkins and Teller 1995, unpublisheddata) have had trouble getting infants to respond con-sistently to the largest tritan modulations through

white that can be produced on conventional videosystems. The most likely explanation for these incon-sistencies is that most infants' chromatic contrastthresholds for tritan gratings fall outside the limits ofthe video gamut for modulations through white, butinside the spectrum locus. A four-channel, spectrallytunable, high-intensity video projection system is cur-rently under construction in our laboratory, and wehope to clarify the extent and nature of infants' tritandiscriminations within the next few years.

Finally, three laboratories have carried the studyof chromatic discrimination beyond early infancy. Asis shown in Figure 14, CSFs for red-green stimulicontinue to increase in sensitivity and in spatial scaleduring at least the first 6 postnatal months.41"43 Simi-larly, the VEP onset waveform has been traced longitu-dinally in detail in several infants; the adult waveformis not reached until more than 1 year after birth.75

Finally, continuing improvements in chromatic con-trast sensitivities occur throughout adolescence.76

In terms of mechanisms, Banks and Bennett48 andBanks and Shannon77 have used an ideal observermodel to argue that infants' detection of red-greendifferences is predictable from their luminance modu-lation thresholds in combination with the physicallyavailable gamut for red-green stimuli. Hence, Bankset al argue that no differential loss of chromatic withrespect to luminance sensitivity occurs, and that nofurther modeling is needed to predict the time ofonset of red-green chromatic discriminations. Theflip side of this argument is that the growth of sensitiv-ity in central red-green and luminance channels mustbe at least approximately matched during develop-ment, to avoid introducing a differential loss into ei-ther channel.

In the case of tritan stimuli, in contrast, Banks etal argue that a differential loss of sensitivity is requiredto explain infants' apparent insensitivity. The differen-tial loss of S-cone-based sensitivity remains puzzling;but then, psychophysicists have been worrying aboutthe peculiar properties of S-cone signal processing formany years. If sensitivities to red-green and tritandifferences prove separable in the developmental con-text, developmental data would provide anothersource of support for the separation of red-green andtritan signals in early visual processing.

Temporal Vision and Motion

In another early study from our laboratory, we ex-plored the infant's critical flicker frequency (CFF) —a measure of temporal resolution.78 Infants were con-fronted with a field of 100% contrast square-waveflicker, embedded in a surround matched in time-average luminance. Because spatial resolution is ini-tially very poor, and approaches adult levels only aftera long, slow time course, our a priori expectation was



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that temporal resolution would also develop slowly.Surprisingly, we found that even very young infantswould stare at rapidly flickering stimuli. One-month-olds' temporal resolution was already ~40 Hz, and 2month olds, 3 month olds, and adults showed CFFs of~50, 52, and 55 Hz, respectively. These data wereimportant, because they allowed us to reject the hy-pothesis put forward by many early critics that infants'thresholds on all stimulus dimensions would be uni-formly limited by a general failure of motivation orattention.6

Temporal contrast sensitivity functions (tCSFs)

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provide a more inclusive description of temporal vi-sion. Infant tCSFs have been studied by several investi-gators.79"83 In the most recent study,82'83 the detectionof low spatial frequency counterphase and movinggratings was tested in 3-month-old infants. The resultsare shown in the left panel of Figure 15. Infant tCSFsshowed a downward shift of sensitivity of ~1.5 logunits compared with that of adults. In infants and inadults, tCSFs peaked near 6 Hz and were nearly identi-cal in shape. Both groups were slightly more sensitiveto moving than to counterphasing gratings. Moreover,extrapolation of the infant curve to the cutoff fre-quency yields an estimate of CFF that is roughly consis-tent with that found by Regal,78 given that Regal usedsquare-wave flicker.

Thus, as discussed, although infant spatial visionmanifests shifts in spatial scale, no analogous shift intemporal scale seems to occur. This difference helpsto explain the relative maturity of infants' CFFs com-pared with the relative immaturity of their grating acu-ity. That is, a horizontal shift of either CSF wouldproduce a quantitatively corresponding shift of thecutoff frequency (a factor of four in the case of spatialvision, but apparently zero in the case of temporalvision). But to the extent that the high frequencylimbs of spatial and temporal CSFs fall sharply withfrequency, vertical shifts produce relatively smallerchanges in both domains.

Direction-of-Motion Coding. Infants exhibit direc-tionally appropriate OKN from birth onward.12 Thus,the pathways that control these eye movements mustbe capable of analyzing the direction of motion of

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2192 Investigative Ophthalmology 8c Visual Science, October 1997, Vol. 38, No. 11

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visual stimuli in earliest infancy. However, more recentstudies using other response systems, including VEPand FPL techniques, have so far failed to provide evi-dence of direction-of-motion coding before approxi-mately 2 postnatal months.84 Data from Wattam-Bell(personal communication) are shown in Figure 16.Broader reviews of the development of motion pro-cessing have also been published.85'86

The critical immaturities that limit infants' tempo-ral- and motion-processing capabilities remain ob-scure, and data are extremely scarce. The only avail-able temporal response functions of single neurons inearly infancy, obtained in neonatal vervet monkeyLGN, peak at low temporal frequencies,51 and theseinvestigators conclude that the temporal resolution ofsingle LGN cells increases considerably after birth.These data, although scanty, would predict a leftwardshift in temporal scale, which is not seen in the humanbehavioral data of Figure 15. Single cortical units havebeen shown to be sensitive to the direction of motionof low spatial frequency gratings in neonatal mon-keys,87 but to improve in selectivity with age. The devel-opmental physiology of subcortical pathways, whichprobably contribute to the control of eye movementresponses to moving stimuli, also remains to be ex-plored.

Chromatic Flicker and Chromatic Motion Processing.In recent studies of red-green chromatic processing,moving or counterphase red-green isoluminant grat-ings have most typically been employed. Counterphasingred-green gratings evoke measurable VEPs in 2 montholds,41"43;73 and possibly in younger infants.73 Two-month-old infants make OKN-like eye movements inresponse to moving red-green gratings. "

Recently, we have reported that FPL-based tCSFs formoving and counterphase red-green gratings are bandpass in 3 month olds.84 This result is surprising, becausetCSFs for red-green gratings are low pass in adults. Thesedata are shown in the right panel of Figure 15.

At the physiological level, findings in modern ana-tomic and physiological studies suggest the presenceof two distinct subpathways from the retina to thecortex.91 These are the M or magnocellular pathway,and the P or parvocellular pathway. In adults, M-initi-ated signals are thought to dominate the processingof motion, whereas P-initiated signals are thought todominate the processing of color. On the basis of ourobservation of band-pass tCSFs for red-green chro-matic modulation in infants, we have speculated thatin the immature visual system, temporally modulatedred-green chromatic gratings might be detected byM- rather than P-initiated signals.84



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However, we have also shown more recently thateye movement responses persist when quadrature-shifted gratings are used,92 thus militating against non-linearities generated at red-green edges in the Mpathway as the basis for motion discrimination. In anycase, the change in shape of the chromatic tCSFs be-tween infancy and adulthood clearly invites study atthe physiological level.

Stereopsis and FusionThe capacity for stereovision — the ability to per-ceive depth on the basis of binocular disparity—wasalso an early target of developmental studies. Earlywork93"97 was undertaken in three different labora-tories, using three very different paradigms: line ste-reograms and a PL procedure,94'95 random dots witha tracking version of FPL,96 and random dots withVEP measures.97 The results of the three studies aresummarized in Figure 17.98 Remarkably, investiga-tors in all three studies agree that the response tobinocular disparity is absent in almost all infants lessthan 3 months old, and has its onset between 3 and6 postnatal months. A similar time course of onset,in weeks rather than in months, has also been dem-onstrated recently in infant monkeys.99

The time of onset of stereopsis does not changewhen very large patterned fields are used as stimuli.100

In that large stimuli would allow fusion of right eyeand left eye patterns at many different values of eyealignment, as in the "wallpaper effect," results ob-tained in this study argue against the hypothesis thatthe emergence of the response to disparity is causedby the development of eye alignment and argue infavor of a more sensory explanation.

2193

Stereoacuity. Figure 18 shows longitudinal data onthe development of stereoacuity in individual infants,measured with line stereograms.94'101 Again, remark-ably, the onset of responsiveness to disparity occurs atdifferent ages in different infants; but once the re-sponse appears, stereoacuity develops rapidly, reach-ing 1' disparity within a few weeks of the first responseto large disparities. It is particularly striking, as shownin the figure, that large changes in stereoacuity occurduring a time span that produces only minimalchanges in grating acuity, so that it is difficult to modelboth with the same modeling elements.

The data set shown in Figure 18, with the ex-tremely rapid improvement of stereoacuity in individ-ual infants, seems to me one of the most striking in theentire field of infant vision. Although few longitudinalstudies of the development of visual function havebeen undertaken, I know of no claim of a domainother than binocularity in which development is sorapid, or in which individual development is so muchmore rapid than the development of the group aver-age.

Fusion and Rivalry. Given that very young infantsapparently do not respond to disparity differences, thequestion then arose: What is the infant's prestereopticbinocular vision like? Held102 and Shimojo et al103

showed that prestereoptic infants prefer the combina-tion of a vertical grating in one eye and a horizontalgrating in the other—a pattern that would be ri-valrous in adults—to binocularly identical gratings.Suddenly, at about the same age at which the response

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to disparity emerges, infants also shift to a strong pref-erence for binocularly identical patterns. These au-thors suggest that the infant's prestereoptic vision isa superposition of left- and right-eye views and that theswitch of preference indicates the onset and resultingavoidance of perceptual rivalry.

Regarding neural mechanisms, there is anatomicevidence that ocular dominance columns in primatesare not fully segregated at birth and continue to segre-gate during the early postnatal weeks or months.104105

Thus, there is a possible coincidence of time coursesbetween the final segregation of ocular dominancecolumns and the onset of stereopsis, at approximately3 months after birth. On this basis, Held102 hypothe-sized that in early postnatal vision, left eye and righteye inputs might converge on the same cells in layer4 of cortical area VI, increasing the number of binocu-

lar neurons. This convergence was hypothesized tocause a loss of eye-of-origin information, and a conse-quent disabling of disparity selectivity of neurons inthe upper cortical layers. According to this view, theonset of stereopsis could be caused by the sorting outof left-eye and right-eye inputs in layer 4, enablingdisparity detectors to work.

Surprisingly, it took 12 years before this elegantand attractive physiological hypothesis was tested di-rectly in infant monkeys. Very recently, it has beenshown with a binocular phase paradigm that, in con-tradiction to the hypothesis, the ocular dominanceproperties and the disparity selectivity of neurons inVI are adult-like at birth.87 It will be interesting to seewhether these findings can be incorporated success-fully into the original model.

The recent work87 also confirmed earlier find-



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FIGURE 19. Longitudinal development of vernier acuity (rightordinate: lower points and dashed line) and grating acuity (leftordinate: upper points and solid line) in the same infant mon-keys, plotted as a function of age in weeks. The two functionsimprove during a similar period, but vernier acuity startsout with a larger deficit and develops more rapidly. Thelarger symbols show data from earlier studies on humaninfants, plotted in months. The higher vernier acuity valuesseen in human infants in some studies are probably an arti-fact of stimulus differences among the studies (from Ki-orpes1, I I O \

ings106 that the sensitivity and spatial tuning propertiesof VI neurons are immature (as they are at the LGNand presumably at the retina). Chino et al87 arguethat immaturities of sensitivity and spatial scale alonemight be sufficient in principle to prevent the infant'sbehavioral response to disparity targets. It is difficultto see, however, how these properties could causeboth the long, slow development of grating acuity andthe rapid improvement of stereoacuity shown in Fig-ure 18. Another alternative would be that the matura-tion of behavioral responsiveness to binocular dispar-ity is caused by the maturation of disparity-tuned neu-rons at a later critical locus in visual processing.

Vernier Acuity and Orientation Selectivity

Finally, we return to two further aspects of form per-ception, the perception of vernier offsets and the dis-crimination of variations of orientation.

Vernier acuity is a measure of the smallest visibledisplacement between two stimuli. It has been studied(with some controversy) in human infants,107"109 andmost recently and definitively in monkey infants.110

Data on vernier acuity and on grating acuity from thesame animals are shown in Figure 19."° These data

show a typical developmental time course for gratingacuity and a larger developmental change and a con-sistently more rapid time course for vernier acuity.Both functions probably approach adult levels atabout the same age, approximately 40 to 60 weeks.Longitudinal data from within each animal showeda developmental course similar to that of the groupaverage, rather than the more abrupt developmentalcourse seen in the case of stereopsis.

Comparisons with the earlier human infant dataare also shown in Figure 19, with ages converted by the4:1 rule. Although grating acuities agree well amongspecies, vernier acuity is apparently lower at each agein infant monkeys than in human infants. However,the human studies108'109 used moving vernier offsets,whereas the monkey study110 used stationary offsets. Inall probability, a closer identity of stimulus parameterswould yield a closer identity of developmental timecourses.111 The literature on vernier acuity makes par-ticularly interesting reading in regard to the impor-tance of using appropriate units of comparison whencomparing rates of development for different visualfunctions, and in regard to the use of rates of develop-ment in inferring visual mechanisms.101

Orientation Selectivity. Studies of orientation selec-tivity explore the infant's capacity to respond to varia-tions of the orientation of a grating. Data on orienta-tion selectivity112 are shown in Figure 20. The timecourse of emergence of orientation selectivity seemsparticularly sensitive to (or perhaps just particularlywell explored with respect to) the influence of stimu-

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Age (months)FIGURE 21. Summary of maturational rates for four differentkinds of visual resolution: critical flicker frequency (fromRegal78), and grating acuity, stereoacuity, and vernier acuity(from Gwiazda et al117). The dotted line shows the measuredor estimated adult acuity value. The log acuity decrementshown by infants in relation to the adult value is plotted asa function of age (from J. Palmer and D. Peterzell, personalcommunication, 1997).

lus parameters and response measures.85 When idealhabituation techniques are used, in which test andhabituation stimuli are presented side by side duringthe test period, even newborns can demonstrate sensi-tivity to variations of orientation.113

Comparisons Across Visual Functions

With such riches of data, how can legitimate compari-son be made of the time courses of emergence ofdifferent visual functions? Figure 21 shows a selectionof data describing the emergence of four differentkinds of visual resolution—grating acuity, criticalflicker frequency, stereoacuity, and vernier acuity—during the early postnatal months. Age is plotted ona linear axis, although a log axis is equally interesting(Figs. 3, 19). The units of the four kinds of acuityhave been rendered commensurate by plotting themeasured or estimated adult value at the top of thegraph at zero on the ordinate. The acuity values ateach age are then plotted as decrements in relationto the adult value, on a logarithmically spaced scale.In such a plot, all values are plotted in log-relativeterms, so that physical units are eliminated. There aremany precedents (for example, in describing spectralsensitivity) for using such a scale to plot log decre-ments from a maximum value. In this case, such ascale has the effect of showing proportional changesin sensitivity as equal decrements from the adult value.

Adult values can be problematic and difficult toestimate in an apparatus designed for infant testing;but the problem is not fatal, because a change in theadult value assumed would result only in a vertical shift

of the affected curve. Using log-relative thresholds forcomparison among functions was originally suggestedto me by John Palmer (personal communication); andin our lab group, plots in this format have come tobe called Palmer plots.

The Palmer plot, using log-relative decrementsrelative to the adult value as the criterion of maturity,allows comparison of the relative maturational timecourses of different visual functions. In Figure 21, theinitial decrement in CFF is less than an octave (a factorof two), and CFF rapidly approaches adult levels inearly infancy. The initial decrement in grating acuityis ~7 octaves; on the linear age axis grating acuityinitially improves rapidly but then assumes the long,slow time course to which we are accustomed. Ster-eoacuity is unmeasurable until approximately 3months after birth. When first measurable, it is ~8octaves below estimated adult levels; but it rises rapidlyto within 2 octaves of adult levels by 6 months in thegroup data, and even faster for each individual infant.Finally, vernier acuity shows an initial decrement ofperhaps 7 octaves, improving at first rapidly and thenmore slowly with age, with a time course reminiscentof that for grating acuity, but delayed in time.

VIGNETTES OF VISUAL FUNCTION ATDIFFERENT AGES

Armed with these data and analyses, we can now morereadily think about the visual capacities of infants ofeach age in turn. Accordingly, summaries of our cur-rent understanding of how well infants of each agecan see are developed in this section. Because, for me,behavioral data have greater face validity than do VEPdata for telling us what infants see, behavioral dataare weighted more heavily in these vignettes.

Newborn infants most certainly see, although ac-tual data on newborns remain scarce. Their acuity andcontrast sensitivity are very poor but are measurable.Their OKN-like eye movements reveal the capacity toanalyze the direction of motion of large, high-contrastobjects, and their flicker resolution is probably quitegood. However, they should reveal no appreciation ofstereo depth, no capacity to respond to low contrastsor to fine spatial details, and probably no color vision.Their visual worlds are probably marked less by bloom-ing and buzzing than by the haziness of low-contrastsensitivity, the blurriness of spatial filtering, and theblandness of monochrome.

At 1 month, infants' behaviorally measured grat-ing acuity is —1 cyc/deg. Their behavioral contrastsensitivity is still an order of magnitude or more worsethan that of adults, and the peak of their CSF is shiftedby a factor of four or more toward lower spatial fre-quencies compared with that of adults. In contrast,their flicker resolution is ~40 Hz—approaching that



of adults. They still reveal little response to color orbinocular disparity, nor to motion by other than grosseye movement measures.

By two months, rudimentary color vision has ar-rived. Most infants can probably discriminate red,blue, and green from white and from each other, butnot yet yellows and yellow-greens. Grating acuity andcontrast sensitivity have improved slightly. Temporalresolution approaches 50 Hz, and some infants nowrespond to the subtler aspects of motion coding.

By 3 months, color vision has improved, and mostinfants now clearly code the direction of motion. Grat-ing acuity has again improved slightly, to ~3 cyc/deg,contrast sensitivity has improved a little, and CFF hasexceeded 50 Hz. But as far as we can tell, the infant'svisual world has not yet broken up into the depthplanes afforded by the use of binocular disparity as adepth cue.

By 6 months, the binocular disparity cue to depthand distance perception has come on line, and ster-eoacuity has rapidly progressed to at least 1' of arc.Grating acuity and contrast sensitivity have improvedfurther, and the peak of the CSF has probably shiftedtoward values more typical of adults. Flicker resolutionremains excellent, and presumably motion codingcontinues to improve. Few data are available beyond6 months; but for the sensory qualities reviewed here,there is no evidence to suggest any other pattern ofdevelopment than a steady rise to adult-level asymp-totes.

BUT WHAT IS THE VISION OF INFANTSREALLY LIKE?

When scientists get hold of something, they tend torender it unrecognizable to the lay person. The origi-nal question was, what is the vision of infants like? Thescientific literature buries the answer in numbers andtechnicalities. To aid in communicating our findingsto the nonspecialist, Tony Young and I have preparedsome artists' renditions of the visual worlds of infantsof various ages. These artists' renditions are shown inFigure 22.

We made one very large assumption: that the avail-able behavioral techniques and data in fact reveal thelimits of the infant's perceptions. This assumptioncould be false in either of two directions: It is possiblethat infants' perceptual capacities are more adult-likethan our measurements would reveal. Perhaps infants'real perceptual worlds are a well-guarded secret, hid-den from vision scientists by a remarkable web of con-spiracy into which all infants are automatically born.If so, infants see better than we have yet discovered.However, it is equally possible that despite their per-formance as psychophysical subjects, infants have noconscious processes and no perceptual world at all.

Perhaps infants are zombies. But I prefer to assumethat infants are just honest subjects, and that our psy-chophysical measurements are telling us what infantssee. The color plates are constructed on die assump-tion of good faith between the adult observer and theinfant subject.

There is also another major caveat: The studiesreviewed here all concern basic sensory qualities—theinfant's detection of spatial and temporal variations,direction of motion, color differences, and binoculardisparity. The development of the more holistic as-pects of perception—image segmentation, figure-ground differentiation, object constancy, object rec-ognition, and so on—are less studied, and are, in anycase, beyond the scope of this review. We do not knowmuch about when or how the low-contrast, spatiallylow-pass filtered, monochrome patterns processed bythe infant's sensory visual system are knit together intomeaningful perceptual wholes. Reviews of the litera-ture on the more perceptual aspects of visual develop-ment may be found elsewhere.25114 Of course, theadult sees the color plates with the adult visual system,with all of the higher level perceptual capacitiesbrought to bear. To the extent that these capacitiesare missing in infants, the infant's visual world maywell be more disjointed than is the adult's perceptionof the color plates.

AND WHAT OF THE FUTURE?

Infant vision research has come a long way in 25 years.We now have a set of well-understood techniques formeasuring the visual capacities of infants, basic de-scriptions of the development of many visual func-tions, an animal model for asking causal questions,and the beginnings of clinically useful fruits to ourlabors. Moreover, quantitative anatomic and physio-logical data are beginning to become available, andwe are beginning the exchange of hints among disci-plines that has been so important to the successes ofvisual science in recent decades. And finally, quantita-tive visual theory has been imported into the disciplineand used to evaluate hypotheses about the depen-dence of visual function on visual structure in thedevelopmental context.

The discipline of visual science seems to meblessed with a consensus on a unified goal: to describeour perceptual capabilities and limitations, and to dis-cover the anatomic, physiological, and computationalproperties of the visual system that allow those capabil-ities and impose those limitations. And yet, there iswork to be done at the metatheoretical level. The en-terprise of finding the physiological causes of psycho-physically defined phenomena has always seemedphilosophically complex to me.14"16 It is no less com-plex in the developmental domain. In particular, simi-



FIGURE 22. Artist's conception of the perceptual appearance of a visual scene for infants ofdifferent ages. Plate 1 {facingpage toj)): left, newborn; right, 1 month. Plate 2 {facingpagebottom): left, 2 months; right, 3 months. Plate 3 (belotu): left, 6 months; right, adult (copyright© by Tony Young; used with permission).

larities of curve shape between psychophysical andphysiological data are the beginning, not the end, ofthe theoretical explanations; and the concept of criti-cal immaturity,17 like that of critical locus,14 will re-quire continuing scrutiny, both at the abstract leveland when imbedded implicitly or explicitly in specificarguments.

EPILOGUE

And what a privilege it's been to be there from thevery beginning of the field of infant vision, looking outthrough the peephole and directly into the infant's per-ceptual world. The days of immediate scientific discov-ery—watching our first infant Peter stare at gratings,seeing Peter's acuity data fall into a perfect develop-

mental sequence, watching infant monkeys do the same,finding out that Ron Boothe's 2-month-old daughterLyndi could discriminate red from white, hearing fromDave Regal that a 1-month-old's CFF is already 40 Hz,seeing acuity cards work for the very first time—theseare the high points of a rich and rewarding scientificlifetime. More recently, with much of the responsibilityfor the lab on John Palmer's shoulders, I still run inter-ference while infant tCSFs take form in Karen Dobkin'sand Barry Lia's hands, and spatiochromatic channels inDave Peterzell's. Most recently, I have watched MikeCrognale and John Kelly assemble a squad of in-housebabies and test them weekly for months, to provide longi-tudinal data on the emergence of VEP waveforms. Forthe privilege of continued participation I am profoundlygrateful.

FIGURE 22. {Continued)



And then there's the inadvertent contribution tothe design of infant toys. There is a mobile for infantson the market nowadays, with the choice of stimulibased loosely on the infant vision literature. One isinstructed to change the stimuli from month tomonth, to keep pace with the infant's developing vi-sual capacities. When my grandson was a month old,he got one as a gift. The next day his mom called meto say, "It's absolutely amazing how fascinated Cole iswith that mobile! He just lies there and stares andstares. . . . "

Acknowledgments

The author thanks the National Eye Institute and the Na-tional Science Foundation for their continuing support ofresearch in infant vision, most recendy by grant EY 04470.Recruitment of infant subjects is supported by the Psycho-physics module of the University of Washington Vision Re-search Core grant, EY 01730. The author also thanks allcollaborators and colleagues for their contributions, andthe infants and parents of Seatde and other cities for theircooperation in making infant vision studies possible.

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Documents

First glances: the vision of infants. the Friedenwald lecture.hist-innov.comotion.uw.edu/.../Teller-lecture-First-Glances-The-Vision-of-Infants.pdfTwo other measurement techniques—visual