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Infant visual acuity and its meridional variation
INFANT
VISUAL
ACUITY
AND ITS MERIDIONAL
VARIATION
JAM GWIAZDA. SARAH BRILL,INDRA MOHINDRAand RICHARDHELD’ Department of Psychology, ElGl39. Massachusetts Institute of Technology. 79 Amherst Street. Cambridge, MA 02139, U.S.A. (Received 19 September 1977; in recisedform
7 March 1978)
Abstract-One hundred and four infants were tested using a preferential looking procedure. Results for subsets of these infants tested in three experiments were as follows: Median preference at the 75% level for vertical gratings over a homogeneous field increased monotonically from 3.0c/deg at 17 weeks of age to 8.0 c/deg at 45 weeks of age; at the 58% level it increased from 3.7 c/deg to 11.8 c/deg. In the second experiment main axes gratings were directly paired with oblique gratings of the same spatial frequency. Results showed that the median spatial frequency at which main axes gratings were preferred over obliques (oblique effect) increased with age at a rate similar to the preference for vertical gratings. In the third experiment, vertical gratings were paired with the homogeneous field, and in separate sessionson the same infants, oblique gratings were paired with the homogeneous field. Preference thresholds for vertical gratings were similar to those for oblique gratings in very young infants, but the preference threshold for vertical gratings increased more rapidly with age, becoming almost I octave greater by I I months. Key Words-infant oblique effect.
visual development; acuity: preferential looking; meridional variations in acuity;
INTRODUCTION Although studies of the acuity of infants have a long history. few investigators have dealt with either its meridional variation (Teller, Morse, Borton and Regal. 1974; Leehey, Moskowitz-Cook, Brill and Held, 1975). or its development past the first 6 months of life. Several recent findings now stress the importance of just such analyses. They have their origins in reports claiming that animals reared during an early period of development in environments containing only selectively oriented edges show a corresponding bias in the incidence of single cells in visual cortex responsive to oriented edges (Hirsch and Spine& 1971; Blakemore and Cooper, 1970). The subsequent claim that environment shapes orientational sensitivity has become controversial as a result of new results (Stryker and Sherk. 1975: Stryker, Sherk, Leventhal and Hirsch, 1978). Nevertheless, out of the enthusiasm following the original reports came two analogous interpretations of aspects of human vision. First, it was concluded that the oblique effect-the lessened acuity for oblique contours as compared to horizontals and verticals defined with respect to retinal coordinates (Emsley, 1925; Leibowitz, 1953; Timney and Muir, 1976)-found in the vision of adults results from living in the carpentered urban world with its alleged excess of vertical and horizontal over oblique edges (Annis and Frost, 1973). Second, it was reported that adult astigmats suffer optically uncorrectable losses of acuity ranging up to 50% for contours along the habitually blurred orientations on their retinas. This meridional amblyopia ’ Please address reprint requests to: Professor Richard Held, Department of Psychology. ElGl39, Massachusetts Institute of Technology. 79 Amherst Street, Cambridge, MA 02139, U.S.A.
was said to result from chronic exposure to the blurring (Mitchell, Freeman, Millodot and Haegerstrom, 1973). Evaluation of both of these inferred consequences for human vision requires more precise knowledge of the early state of infant vision. We need to know what, if any, non-optical meridional biases exist in the neonate and how visual development normally proceeds in infants free of astigmatism. Knowledge of the visual acuity of infants and its measurement has been growing over the past decade or two, as witnessed by an ever increasing number of publications related to the subject (Dayton, Jones, Aiu, Rawson, Steele and Rose, 1964; Atkinson, Braddick and Braddick, 1974; Teller et al., 1974; Banks and Salapatek, 1976; Marg, Freeman. Peltzman and Goldstein, 1976; Atkinson. Braddick and Moar, 1977a, b; Dobson and Teller, in press). A number of different responses-including preferential looking, optokinetic nystagmus, and the visually-evoked potential-have been used to measure acuity. Dobson and Teller (in press) have summarized results obtained using the three methods and have concluded that the optokinetic nystagmus and preferential looking techniques tend to produce similar acuity estimates, while the visually-evoked potential studies tend to show better acuity by l-2 octaves. The latter conclusion is inconsistent with data reported by Harris, Atkinson and Braddick (1976) who found similar contrast sensitivity functions and, hence, the same acuity thresholds obtained by preferential looking and evoked potential measurements taken on a single infant. Dobson and Teller attribute the different acuity values to differences in the scoring criteria used. They found good agreement among the studies with regard to the time-course of improvement in acuity, with most studies showing a monotonic improvement of 2-3 octaves over the first 6 months of life.
Central to an interpretation of the growth of acuity are chronological studies made during the first few years after birth. The meridional variation in acuity. Its chronology. and its c3uxs have been 3 primary concern of this laboratory (Leehey or a/., 1975: Gwiazda. Brill and Held. 1976; Held. Mohindra. Gwiazda and Brill. 1977: Gwiazda. Brill and Held. 1975). In the following experiments we will define an infant’s acuity threshold 3s the highest spatial frequency at which the preference for gratings over a homogeneous field was not less than a criterion percentage. 75”: and 58“; were chosen 3s the preference criteria. We tested a large number of infants and combined sessions across infants in order to provide normative acuity data against which to measure an individual infant’s performance during the first year of life. Three experiments were performed on infants with insignificant astigmatism (less than I diopter of cylindrical refractive error): Exprri~~ent 1: Measurements of visual preference obtained by presenting each infant with a set of
paired stimuli consisting of a vertical grating paired with 3 homogeneous field of equal space-averaged luminance. The gratings varied in spatial frequency. Two levels of contrast were used (95:; and 357;).
E.uprri,trrrrr 2: Measurements of visual preference obtained by presenting each infant with one main axis grating (either vertical or horizontal) simultaneously paired with one oblique grating (either 45’ or 135”) of equal luminance, contrast, and spatial frequency. This experiment of a previously 1975).
constitutes a larger scale replication reported experiment (Leehey et al..
Experimenr 3 : Measurements of visual preference for both vertical and oblique gratings taken on the same infants using the procedure of Experiment I.
METHOD Suhjvcrs One hundred and four full term infants ranging from 7 to 50 weeks of age and with insignificant astigmatism were tested. Of these infants. ninety-nine were white, five were black. Their spherical component of refraction ranged from -1.75D to +3.75D. with most values between zero and +Z.OOD. demonstrating the hyperopia typical of infants. No optical correction was applied since our stimuli were presented at 50 cm distance (- Z.OOD)making nearsightedness of negligible consequence and farsightedness correctable by accommodation. Most infants were solicited through letters sent to parents whose names were obtained from central files of birth certificates in Cambridge and Boston. Massachusetts. Responses to the letters averaged I so/,. Each infant was refracted every 4-6 weeks by near retinoscopy (Mohindra. 1977). We have observed that many infants in this age range show transient astigmatism (Held er al., 1977). Data from infants who showed less than I diopter of astigmatism within 3 weeks of the testing session were included in the analysis. Preliminary data on the incidence of astigmatic refractive error and its infhtence on acuity have been reported elsewhere (Held er a/.. 1977: Mohindra. Held. Gwiazda and Brill. 1978: Held. in press). .Appamrus The apparatus consisted of a wooden partition containing two circular translucent screens, one to the right and
ox to the lsi’t oi a red firc;ltlon lizhI. tended II of visual ~tngle lwlth crntex
E;ish ,crx:: rus xparat~? 5, ?i
of visual angle. The scieeni ‘here rnl2< from Ch,rr:e:t:~ Charprint 916 h ICV, rag zhnical rrzelng :.ellum Tx~ Kodak Carousel projectors (auto-focus 850 HJ. each equipped with a Kodak zoom lens (Ektanar-C\. uere used for projection. .A Kodak Wratten 1.0 nectral densit;, filter covered each lens. fn Experiment I. vertical black and white square-wabe gratings were paired with homogeneous test fields of equal space-averaged luminance ill cd,‘m’l and were projected simultaneously onto the rear of their respective screens. They were made up of one of live spatial frequencies: 0.75. 1.5. 3.0. 6.0. and 12.0 cycles per degree ic degl of visual angle. In Experiment 2. either vertical or horizontal gratings were paired with either left or right oblique gratings of the same spatial frequency (ranging from 0.3s to 12.0c!degl. In Experiment 3. either vertical (90’1 or right oblique (45’) gratings were paired with homogeneous test fields of equal space-averaged luminance. Spatial frequencies of the gratings ranged from 0.75 to lZ.Oc.deg. The slides were produced photographically using black and white high contrast film from two originals consisting of strips of black Chartpak pressure-sensitive .graphic taoe mounted on white plexiglas. The resulting projected gratings had a 50-50 dutv. c\rcle within -+1”,. . The luminance of the black and white gratmgs was measured at all spatial frequencies using a Gamma Scientific DR-I Digital Radiometer with a Model ZOZC-IC Photomultiplier Detecter coupled to a hl~tiel 20X-31 High Efficiency Photometric Telescope with 3 I aperture. The contrast of the gratings was 95’?,,for the lowest three spa. tial frequencies (0.38. 0.75 and 1.5 c’degt. 9-V, for 3.0 c,deg. for 12.0~ dsg [con9l”,, for 6.0~ dep. and 90”, trast = (L, - L2) (L, + L.;J. where L, is the luminance of the light area and LJ is the luminance of the dark area]. In some sessions. contrast was reduced to 3Y; with mean luminance remaining at 34cd:m’. This was accomplished by placing a Kodak Wratten O.-t neutral density filter over each Kodak lens while projecting sufficient additional light onto the two screens uith a Regent slide projector. Aside from the slide projectors and red fixation light. no other light source was present during the session. Slides containing brightly colored circles on a dark background were presented during the intervals between presentation of the gratings to help maintain the attention of the infant to the screens. Procedure
Initially the infant and parent entered a lighted room. The infant was situated in front of and facing the screens onto which the colored circles were projected. The experimenter aligned the infant’s head and eyes with a mark on an adjacent wall which was 5Ocm from the stimuli. The parent was instructed to keep the infant in that position throughout the session. When the infant and parent were comfortable the room was darkened. During most experimental sessions. the infant sat on the parent’s lap. In a few sessions the younger infants were held over the parent’s shoulder. with the head uptight and centered between the stimuli. Some of the older infants were allowed to stand on the chair while being held by- the parent. The infants’ eyes were level with the stimuli Sucking on a bottle or pacifier seemed, in some cases, to maintain the infants’ calmness and attention. Fewer than 5:; of the infants were eliminated due to fussiness or sleepiness. Before each trial. the red fixation light was flashed to msure that the infant was looking str&ht ahead. Occasionally the experimenter tapped on the center of the partition or made soft clucking or animal-like noises to gain the infant’s attention while flashing the red light. If this was unsuccessful. the experimenter occasionall> waved
Infant visual acuity and both hands back and forth over the two screens to attract the infant‘s attention. When the infant’s gaze was directed at the fixation light. the stimuli were presented. Side of presentation was counterbalanced for both spatial frequency and orientation. and the order of presentation of, stimulus pairs was pseudo-randomized in a manner described below. During each trial the experimenter looked at the infant’s head and eye movements through a peephole directly beneath the fixation light. and made a forced-choice judgment as to which side the infant preferentially fixated. Light from the stimuli was sufficient to illuminate the infant’s face. Comeal reflections of the gratings were too small to be resolved by the experimenter. The experimenter made a judgment based on one or more cues given by the infant. such as first fixation. duration of fixation, and facial expression. The experimenter wore goggles with one eye occluded to insure that location of the gratings was unknown. The order of presentation of the stimuli was also unknown. The length of each trial was variable. depending on the length of time required by the experimenter to make a judgment. Trials for the younger infants (under :! months) whose head and eye movements were less well developed were usually IOsec in length. while those for the older infants were approximately 5 set in length. The 5-10s~~ trials gave the infant ample time to observe both stimuli. As soon as a judgment was made. the trial stimuli were removed and the colored circles were presented while the observation was recorded and the procedure for gaining the infant’s attention was repeated. Sixty trials were usually run in a session which was completed in a maximum of IO min if no breaks were taken. If necessitated by restlessness of the infant. a break was taken during the session but this was usually required only for infants under 3 months of age. The slides were arranged so that every spatial frequency could be tested four times in twenty trials. This set was then cycled through three times to constitute sixty trials. In this way. if an infant became fussy. the experiment could be terminated after either two or three cycles. A minimum of two cycles was neccessary for inclusion in the results. We have found that this combination of apparatus and procedure allows us to test infants from soon after birth up to an average of I year of age. Among the novel features of our procedure, working in darkness may be the most important: it assures minimal loss of attention to the stimuli.
its
1559
meridional variation
in three age groups. Ail infants were tested binocularly on five spatial frequencies (0.75. 1.5. 3.0, 6.0 and 12.0 c/deg). To obtain measures of visual preference for vertical gratings over the homogeneous field raw scores of the infant’s looking behavior at each spatial frequency were converted into percentages of preference for the grating. An infant’s acuity threshold was defined as the highest spatial frequency, of the five tested, at which the infant’s preference for vertical gratings over the homogeneous field was not less than a criterion percentage. In this experiment we chose 75% and 58% as the preference criteria. Results. Within each age group a tally was made of the number of infants whose threshold fell at each spatial frequency. These data are presented as frequency histograms for each age group in Fig. I. Sessions in which preference performance fell below 75% for one spatial frequency and then increased to
EXPERLVENTS Experiment 1: Measurement of Gsual preference for certical gratings Many investigators have used the procedure of pairing a grating with a homogeneous field in order
to measure visual acuity. although none ha+ tested infants of more than 7 months of age. The data we have obtained on younger infants serve as a check on our procedures relative to those of others. Fifty-five infants from 14 to 50 weeks of age were tested in 75 sessions of either forty or sixty trials per session. Fewer than 10% of the sessions contained forty trials. For consistency of data presentation and for purposes of comparison between experiments. the data from all the experiments were arbitrarily divided into IO-week age groups from 0 to 50 weeks. In this experiment the youngest infant tested was I4 weeks old; therefore the youngest age group is from 14-20 weeks. No infant was tested more than once within a given age group. Thirty-nine infants had a session in only one age group, twelve infants had a session in two age groups, and four infants had a session
60
t
n=20
Spatial frequency,
I I
c /deg’
Fig. I. Percentage of infants in each of four age groups from I4 to 50 weeks of age meeting 75% criterion of preferring vertical gratings to a homogeneous field. The “other” category refers to those infants whose preference performance fell below 750/i for one spatial frequency and then increased to 750,bor greater for a higher spatial frequency.
E.yprrimenr 2: Mrasurrmenr of ~1suu1 prrjbtincc. hc;racior when rerrical or horkontai yrarinys art’ puir?d wtr/! ohliqur gratings
A---. l -e
m----m
Age,
58% mterion 75% criterion Oblique effect
weeks
Fig. 2. Circles and triangles show median spatial frequencies for four age groups at which infants preferred a vertical grating over a homogeneous field at the 750/gand 58% criteria. respectively. Squares show median spatial frequencies for each of five age groups within which infants preferred either a vertical or a horizontal grating over an oblique !rating at one spatial frequency at least 67”; of the time. Mean ages ranged from I I to J5 weeks.
75”,, or greater for a higher spatial frequency were not used to estimate resolution performance. but rather were placed in a category called “other”. The percentages of sessions falling into the “other” category are 50,,, O”,,. 10%; and 1.5?,, for the four age groups: thus. most of the data are orderly. The modal spat ial frequency increases from 3.0 c/deg in the l&20 Heck group to 6.0c;deg by the age of 41-50 weeks. The median threshold spatial frequency was determined for each age group. These medians are plotted as a function of mean age and shown by the circles in Fig. 2. This figure shows that. using our procedure. the logarithm of visual acuity for vertical gratings increases linearly with chronological age from I4 to 50 Lveeks. At the 7.5”,; preference level it ranges from 3,0c,‘deg in 14-20 week-old infants to 8.0c/deg in the 41-50 week group. In Snellen notation, the range of acuity is from 20/200 to 20180. The triangles in Fig. 2 represent median threshold spatial frequencies taken on the same data using 58”, preference as the criterion instead of 75qW These points also increase linearly with age. from 3.7c/deg (20 150) in 14-20 week-old infants to 11.8 c,‘deg (20 50) in the 41-50 week group. Using this lower criterion increases the acuity threshold by slightly more than 4 octave. on the average. Lowering the contrast of the gratings from 9j00 to 35”” reduces the infants’ median acuity threshold bk 2 octaves. on the average, for twenty-four infants from I I to 50 weeks of age who were tested at both contrast levels. The medians are shown in Table 1. Table
I. Median spatial frequency at 75”, preference criterion for two levels of contrast
Age (weeks) 1420 21-30 3140 41-50
Number of 35%; contrast infants (cideg) 4 9 6 5
I .07 I .07 I .07 2.14
95”; contrast (c/W
3.00 3.63 7.24 8.50
In an earlier study we established the presence of an oblique effect as early as 6 weeks of age (Leehe) er al., 1975) by directly pairing oblique with slther horizontal or vertical gratings in a two-choice preference procedure. Results showed that the spatial frequency at which the infants maximally prefer main axes over oblique gratings increases monotonically with age over the range of spatial frequencies we tested. In the present experiment. replicating and extsnding the earlier study, ninety-seven infants were shown either a vertical or horizontal grating paired with an oblique one for a total of one hundred and forty four sessions. The infants in the youngest age group. i- I3
14-20
30
t
/ I
wks
nz36
Spatial frequency ,
c/&g
Fig. 3. Percentage of infants in each of five age groups from 7 to 50 weeks of age meeting 67% criterion for preferring a horizontal or vertical grating over an obtique grating at one of the five spatial frequcricies tested. “No maximum” refers to those infants whose preference for either vertical or horizontal gratings did not reach 675; at an) spatial frequency. Infants who showed two. or more . equal .. maxima of at least 67”& are cleslgnated as “Other
1561
Infant visual acuity and its meridional variation weeks of age. were shown gratings ranging from 0.38
to 6.0c/deg. while those in the older four age groups were shown gratings ranging from 0.75 to lZ.Oc/deg. The older four age groups are the same as those in Experiment 1. No infant was tested more than once within a given age group. Sixty-three infants had a session in only one age group, twenty-four infants had a session in two age groups, seven infants in three age groups and three infants in four age groups. Resulrs. The great majority of infants show a clearly defined preference maximum for main axes gratings over obliques of 670,6 or greater at one of the five spatial frequencies tested. This will be the definition of an oblique effect. Figure 3 shows the percentage of infants within an age group who had such maxima at each of the spatial frequencies tested. Infants who showed two or more equal maxima of at least 67% are designated as “other”. Those whose preference for either vertical or horizontal gratings over oblique did not reach 67% at any spatial frequency are categor-
Experiment 3: Measurement of Gsual preference for certical and oblique gratings
Noting the good agreement between the preference
ized as “no maximum”.
Vertical
Spatial
The modal spatial frequency increased from 0.75 c/deg in the 7-13 week group to 6.0c/deg in the 41-50 week group. The percentage of infants not having any maxima decreases with increasing age, while the percentage having two or more maxima increases slightly with age. The median spatial frequency at which a preference maximum occurred was determined for each age group. These medians are plotted in Fig 2 as a function of age for each group of infants and are represented by squares. These points show the same trend as does acuity for vertical gratings, with the exception of the youngest age group, for which no acuity data were obtained. The oblique effect points are lower than the corresponding acuity points by $ octave. on the average, using the 75% preference level, and $ octave. on the average, using the 58% IeveL
frequency,
I
c/ded
Spotidl frequency,
c /deg
Fig. 4. Percentage of infants in each of four age groups from 14 to 50 weeks of age meeting 75:;, criterion for preferring vertical (left side of figure) or oblique (right side of figure) gratings over a homogeneous field. The “other” category refers to those infants whose preference performance fell below 759; for one spatial frequency and then increased to 75:” or greater for a higher spatial frequency.
threshold for vertical _aatings as measured in- Expcriment I. and the spatial frequency of the maximum preference for vertical or horizontal gratings over obliques as measured in Experiment 2. we wondered why previous investigators claim to have found no evidence for lowered acuity for oblique gratings using the fixation preference paradigm (Teller er al.. 1974). fn this experiment. we used the method described in Experiment I and obtained comparable measures of visual preference for oblique and vertical gratings. Twenty-nine infants ranting in age from I4 to 50 weeks were tested in a total of forty-three sets of two sessions each. One session in each set paired vertical gratings with a homogeneous field, and the other session paired right oblique gratings with the homogeneous field. The sessions were spaced no more than 3 weeks apart. In twenty-nine sets of sessions the vertical gratings were presented first. No infant had more than one set of sessions within an age group. Seventeen infants had a set of sessions in only one age group. Ten infants had a set of sessions in two age groups and two had a set of sessions in three age groups. All but one of the sessions pairing vertical gratings with a homogeneous field were also included in Experiment 1. Rrsulrs. Preference for vertical and oblique gratings is shown in Fig. 4 for each of four age groups. The percentage preferences were determined as in Experiment 1. The modal preference for vertical gratings using the 7.5’, level increases from 3.0c’deg in the 14-20 week-old infants to lZ.Ocideg in the 41-50 week-olds. similar to Experiment 1. At the same time. preference for oblique gratings remains at 3.0 cycles from I4 to 40 weeks of age, only reaching 6.0c:deg by 41-50 weeks. Median spatial frequencies were determined as in the first two experiments and are shown by the solid lines in Fig. 5. Using either the 7504 or 5846 preference criterion the median spatial frequency for vertical gratings increases approximately I+ octaves from 1-I to 50 weeks of age, while that for oblique gratings increases only about ;’ octave during the same period of development. By using the lower criterion of $8:;. the acuity threshold for both vertical and oblique gratings increases by slightly more than f octave. on the average.
c46
I
I
30
20 Age,
I 40
weeks
Fig, 5. Median spatial frequency at 75% and 58% criteria for preferring either a vertical or an oblique grating to a homogeneous field. Mean ages ranged from 17 to 4-t
weeks of age.
DISCL SIO\
Experiment I demonstrates that acuity for vertical gratings. as measured by our procedure. increaxs with age-from 3.0c:deg at 4 months to approximately 8.0 c.‘deg by 11 months. These results are similar to those obtained by others using the fixation preference and optokinetic nystagmus techniques (Dobson and Teller. in press) for infants up to 6 months of age. Our procedure has enabled us to extend testing sessions to I year. thereby revealing the continuing increase in acuity after 6 months. The acuity data graphed in Figs 1 and 2 for the oldest age group indicate that we should have included gratings of higher spatial frequency in our testing procedure. In fact. when we used the W, criterion to determine the acuity threshold nineteen out of twenty infants in the 41-50 week age group had thresholds at 12.0cideg. The clearcut changes shown after 6 months of age have an important implication for the duration over which acuity improves during infancy. Several investigators. using pattern evoked potential procedures. hare claimed that adult levels of acuity are reached by 6 months of age (Marg et al., 1976: Sokoi. 1978). It has been suggested that the differences between these results and the slower growth of acuity shown by behavioral methods is attributable to different criteria used for determining thresholds (Dobson and Teller, in press: Sokol. 19751. However. a mere change in threshold criterion will not eliminate the continuous increase in acuity occurring after 6 months, as a glance at Fig. 1 shous. Lowering the contrast of the gratings from 95”; to 3Y0 reduces the median acuity threshold by 1 octaves. on the average. These results at the two contrast levels are in agreement with those reported by Banks and Salapatek (1976) on five Z-month-old infants. More recently. Atkinson rt al. (f977a) have reported a difference of 1 octave, on the average. in I-. 2-. and 3-month-old infants. Experiment 3 shows the presence of an oblique effect (a preference maximum for main axes gratings over obliques at one spatial frequency) as early as we have tested (7-13 weeks of age). The results show the same increase in the spatial frequency of maximum preference for main axes gratings wtth age as that reported earher by this laboratory (Leehey er al.. 1975). Figure 1 shows good agreement between the median spatial frequencies of maximum preference for vertical or horizontal gratings (Experiment 7) and those of the preference for vertical gratings over the homogeneous field (Experiment 1) as age increases. This result is consistent with our earlier conclusion (Leehey et al.. 1975) that the maximum preference for horizontal or vertical gratings over obliques occurs at or near the acuity threshold. It is cisar from Fig. 2 that increasing the criterion used to determine the acuity threshold to greater than 75”,,, could bring these points into line. Experiment 3 shows that acuity for vertical gratings increases more rapidly with age than that for oblique gratings. At the 759; preference Ievei acuity for vertical gratings increases from j.Oc;deg in the 1l-30 week group to 9,Oc’deg in infants 41-50 weeks old. while acuity for oblique gratings increases from 3.0
Infant vtsual acuity and its meridional variation
to 5.3 c,deg during the same period. At the 580;, preference level acuity for vertical gratings increases from 3.6 to 11.2 c/deg. while acuity for oblique gratings increases from 4.3 to 6.9 cjdeg. Using their technique on a small sample of infants of less than 6 months of age (with a mean age of approximately 15 weeks). Teller rf al. (1974) did not find a statistically significant difference in acuity for vertical, as compared to oblique gratings-a result consistent with ours at that age level. The magnitude of the difference between acuities for vertical and oblique gratings in the older age groups is surprisingly large, particularly in the oldest group in which it amounts to almost an octave. In Caucasian adults. this difference averages 2OY<(Timney and Muir. 1976). a fraction of an octave. The comparison suggests that the oblique effect increases in magnitude during the first year but must decrease during a later period. These results are reminiscent of the findings of Leventhal and Hirsch (1977) and Imbert (personal communication) on the development of the orientation-sensitive single units of the kitten cortex. The development of units sensitive to horizontal and vertical edges appears to differ in time and susceptibility to deprivation from that of obliquesensitive units. Taken together. the results of Experiments 2 and 3 are paradoxical. On the one hand, results from Experiment 2 support the conclusion that the oblique effect is present at the earliest age we have tested. On the other hand, Experiment 3 fails to demonstrate an acuity difference between vertical and oblique gratings for the youngest infants. Our experiments do not provide an answer to this paradox, but we can suggest the following possibilities. One possibility might be that when we measure
occur at several levels of the visual system ranging from retina to cortex. Discovery of an oblique effect in early infancy at spatial frequencies considerably below those at which it has been found in adults has an interesting implication for this change. It suggests that the anisotropy in the visual system. evidenced by the oblique effect. antedates in time the changes that result in increasing acuity during the first year of life. The differential sensitivity to orientation suggests that the anisotropy is of cortical origin. If the increase in acuity with age results from subcortical changes, then we can conceive of the accompanying increases in contrast sensitivity, in the frequency of maximum contrast sensitivity, and in the cutoff frequency (acuity) as the result of increasing resolution at the subcortical levels that feed into the anisotropic cortex. Alternatively, the increasing resolution may itself result from changes in cortex occurring in close proximity to the locus of the anisotropy. This account of the development of the visual acuity in infants serves as essential baseline data for assessing both the optical and neural effects on vision of habitual blurring such as typically occur in astigmats. Acknowledgements-This research was funded by research grants from: The National Eye Institute (NIH No. 5-ROIEYOl191-OS), the National Institute for Neurological and Communicative Diseases and Stroke (NIH No. 5-POI-NS-123363-03X and The Spencer Foundation (No. LTR-DTD-71373). The first author was supported by a Liza Minnelli Award, Fight For Sight, Inc., New York City (No. F-303). The authors would like to thank Joseph Bauer, D. Alfred Owens, and Joseph Thomas for their helpful comments. and George Timberlake for assistance in measuring the.luminance of the stimuli.
vertical and oblique acuity in Experiment 3 we have only tested infants whose results fall into the “no maximum” category for the oblique effect in Experiment
2. In the 14-20 week age group the “no maximum” percentage reaches 220/d of all the sessions in that group. “No maximum” results in Experiment 2 would be consistent with the lack of an acuity difference between vertical and oblique gratings in Experiment
3. A close look at individual infants, however, reveals that of the seven infants from 14-20 weeks of age tested on both experiments, none had data which fell into the “no maximum” category for the oblique effect Another possible conclusion is that there are small differences in the apparent contrast of the gratings such that a main axis grating, when directly paired with an oblique grating, would look clearer at or near threshold. The small difference in apparent contrast may not be detected, however, when each grating is independently paired with a homogeneous field. With the older infants (21-50 weeks) there is a clear acuity difference between vertical and oblique which can be detected by both methods. Very recently, Mayer (1977) reported data showing that the magnitude of the oblique effect increases from 5 years of age to adulthood. While this increase may occur. we cannot accept her conclusion that the “anisotropy develops fairly late in childhood’*. We do not know &y acuity increases from birth through the first year of life. Developmental changes
1563
REFERENCES
Annis R. C. and Frost B. (1973) Human visual ecology and orientation anisotropies in acuity. Science 182. 729-73 I. Atkinson J., Braddick 0. and Braddick F. (1974) Acuity and contrast sensitivity of infant vision. Xature 247. 403-404. Atkinson J., Braddick 0. and Moar K. (1977a) Development of contrast sensitivity over the first three months of life in the human infant. Vision Res. 17. 1037-1044. Atkinson J., Braddick 0. and Moar K. (1977b) Contrast sensitivity of the human infant for moving and static gratings. Vision Res. 17, 1045-1047. Banks M. S. and Salaoatek P. (1976) Contrast sensitivitv function of the infant visual‘ system. Vision Res. 18. 867-869. Blakemore C. and Cooper G. F. (1970) Development of the brain depends on the visual environment. Nature 228, 477-478. Dayton G. O., Jones M. H.. Aiu P.. Rawson R. A.. Steele B. and Rose M. (1964) Developmental study of coordinated eye movements in the human infant. Archs Ophrhal. 71. 865-870.
Dobson V. and Teller D. Y. (in press) Assessment of visual acuity in human infants. In Visual Psychophysics: its Physiological Basis (edited by Armington J.. Krauskopf J. and Wooten 8.). Academic Press, New York. Emsley H. H. (1925) Irregular astigmatism of the eye: eRect of correcting lenses. Trans. opt. Sot. Land. 27, 28-42. Gwiazda J., Brill S. and Held R. (1976) Meridional acuity’ in infant astigmats. Abstract of presentation given at
meeting of Association for Research in Vision and Ophthalmology. Inc. (A.R.V.O.). Sarasota. Florida. April X-30. Gwiazda J.. Brill S. and Held R. (1978) Fast measurement of visual acuity in infants from two weeks to one year of age. Abstract of presentation given at meeting of Association for Research in Vision and Ophthalmology. Inc. (A.R.V.O.). Sarasota. Florida. April 3O-May 5. Harris L.. Atkinson J. and Braddick 0. (1976) Visual contrast sensitivity of a six-month old infant measured by the evoked potential. Xarure 264, 570-571. Held R. (in press) Development of visual acuity in normal and astigmatic infants. In Fronriers in Visud Science (edited by Cool S. and Smith E. L.). Springer-Verlag. New York. Held R.. Mohindra I.. Gwiazda J. and Brill S. (1977)Visual acuity of astigmatic infants and its meridional variation. Abstract of presentation given at meeting of Association for Research in Vision and Ophthalmology. Inc. (A.R.V.O.), Sarasota, Florida. April 25-29. Hirsch H. V. B. and Spinelli D. N. (1971) Modification of the distribution of receptive field orientation in cats by selective visual exposure during development. Expl Brain Res. 12. 509-527. Leehey S. C.. Moskowitz-Cook A.. Brill S. and Held R. (1975) Orientational anisotropy in infant vision. Science 190 (4217). 900-902. Leibowitz H. (1953) Some observations and theory on the variation of visual acuity with the orientation of the test object. J. opr. Sot. Am. 43. 902-905. Leventhal A. G. and Hirsch H. V. B. 11977) Effects of earlv. experience upon orientation sensitivity and binocularity of neurons in visual cortex OF cats. Proc. Nar. Ad. Sci.. U.S.A. 74. 1272-1276.
Marg E.. Freeman J. (1976) Visual evoked potential
D. N., Peltzman F. and Goldst
150-153. Mayer IM. (1977) Development of anisotropy III !ate -_htldhood. Vision Res. 17. 703-710. Mitchell D. E.. Freeman R. D.. Millodot IM. and HaegerStrom G. (19733 Meridional amblyopia: evidence for modification of the human visual system by early visual experience. C’ision Res. 13. 535-558. Mohindra 1. (1977) A non-cycloplegic refraction technique for infants and young children. J. Im. Opr. -tss. 48. 5 18-523. Mohindra I.. Held R.. Gwiazda J. and Briil S. (19751 Asttgmatism in children during the first five years of life. Abstract of presentation given at meeting of Assoctation for Research in Vision and Opthalmology. Inc. (A.R.V.O.). Sarasota. Florida. April ?O-May 5. Sokol S. (1978) Measurement of infant visual acuity from pattern reversal evoked potentials. Vision Res. 18. 33-39. Stryker M. P. and Sherk H. (1975) Modification of cortical orientation-selectivity in the cat by restricted visual experience: a re-examination. Science 190 (4217). 904-905. Stryker M. P.. Sherk H.. Leventhal A. G. and Hirsch H. (1978) Physiological consequences for the cat’s vtsual cortex of effectively restricting early vtsual experience with oriented contours. J. Nerrroph~sioi. -Il. 896-909. Teller D. Y.. Morse Visual acuity for
R.. Borton R. and Regal D. (1971) vertical and diagonal gratings in
human infan&. Vision Res. 14. 1433-1339. Timney B. N. and Muir D. W. (1976) Orientational anisotropy: incidence and magnitude in Caucasian and Chinese subjects. Science 193. 699-700
VISUAL
ACUITY
AND ITS MERIDIONAL
VARIATION
JAM GWIAZDA. SARAH BRILL,INDRA MOHINDRAand RICHARDHELD’ Department of Psychology, ElGl39. Massachusetts Institute of Technology. 79 Amherst Street. Cambridge, MA 02139, U.S.A. (Received 19 September 1977; in recisedform
7 March 1978)
Abstract-One hundred and four infants were tested using a preferential looking procedure. Results for subsets of these infants tested in three experiments were as follows: Median preference at the 75% level for vertical gratings over a homogeneous field increased monotonically from 3.0c/deg at 17 weeks of age to 8.0 c/deg at 45 weeks of age; at the 58% level it increased from 3.7 c/deg to 11.8 c/deg. In the second experiment main axes gratings were directly paired with oblique gratings of the same spatial frequency. Results showed that the median spatial frequency at which main axes gratings were preferred over obliques (oblique effect) increased with age at a rate similar to the preference for vertical gratings. In the third experiment, vertical gratings were paired with the homogeneous field, and in separate sessionson the same infants, oblique gratings were paired with the homogeneous field. Preference thresholds for vertical gratings were similar to those for oblique gratings in very young infants, but the preference threshold for vertical gratings increased more rapidly with age, becoming almost I octave greater by I I months. Key Words-infant oblique effect.
visual development; acuity: preferential looking; meridional variations in acuity;
INTRODUCTION Although studies of the acuity of infants have a long history. few investigators have dealt with either its meridional variation (Teller, Morse, Borton and Regal. 1974; Leehey, Moskowitz-Cook, Brill and Held, 1975). or its development past the first 6 months of life. Several recent findings now stress the importance of just such analyses. They have their origins in reports claiming that animals reared during an early period of development in environments containing only selectively oriented edges show a corresponding bias in the incidence of single cells in visual cortex responsive to oriented edges (Hirsch and Spine& 1971; Blakemore and Cooper, 1970). The subsequent claim that environment shapes orientational sensitivity has become controversial as a result of new results (Stryker and Sherk. 1975: Stryker, Sherk, Leventhal and Hirsch, 1978). Nevertheless, out of the enthusiasm following the original reports came two analogous interpretations of aspects of human vision. First, it was concluded that the oblique effect-the lessened acuity for oblique contours as compared to horizontals and verticals defined with respect to retinal coordinates (Emsley, 1925; Leibowitz, 1953; Timney and Muir, 1976)-found in the vision of adults results from living in the carpentered urban world with its alleged excess of vertical and horizontal over oblique edges (Annis and Frost, 1973). Second, it was reported that adult astigmats suffer optically uncorrectable losses of acuity ranging up to 50% for contours along the habitually blurred orientations on their retinas. This meridional amblyopia ’ Please address reprint requests to: Professor Richard Held, Department of Psychology. ElGl39, Massachusetts Institute of Technology. 79 Amherst Street, Cambridge, MA 02139, U.S.A.
was said to result from chronic exposure to the blurring (Mitchell, Freeman, Millodot and Haegerstrom, 1973). Evaluation of both of these inferred consequences for human vision requires more precise knowledge of the early state of infant vision. We need to know what, if any, non-optical meridional biases exist in the neonate and how visual development normally proceeds in infants free of astigmatism. Knowledge of the visual acuity of infants and its measurement has been growing over the past decade or two, as witnessed by an ever increasing number of publications related to the subject (Dayton, Jones, Aiu, Rawson, Steele and Rose, 1964; Atkinson, Braddick and Braddick, 1974; Teller et al., 1974; Banks and Salapatek, 1976; Marg, Freeman. Peltzman and Goldstein, 1976; Atkinson. Braddick and Moar, 1977a, b; Dobson and Teller, in press). A number of different responses-including preferential looking, optokinetic nystagmus, and the visually-evoked potential-have been used to measure acuity. Dobson and Teller (in press) have summarized results obtained using the three methods and have concluded that the optokinetic nystagmus and preferential looking techniques tend to produce similar acuity estimates, while the visually-evoked potential studies tend to show better acuity by l-2 octaves. The latter conclusion is inconsistent with data reported by Harris, Atkinson and Braddick (1976) who found similar contrast sensitivity functions and, hence, the same acuity thresholds obtained by preferential looking and evoked potential measurements taken on a single infant. Dobson and Teller attribute the different acuity values to differences in the scoring criteria used. They found good agreement among the studies with regard to the time-course of improvement in acuity, with most studies showing a monotonic improvement of 2-3 octaves over the first 6 months of life.
Central to an interpretation of the growth of acuity are chronological studies made during the first few years after birth. The meridional variation in acuity. Its chronology. and its c3uxs have been 3 primary concern of this laboratory (Leehey or a/., 1975: Gwiazda. Brill and Held. 1976; Held. Mohindra. Gwiazda and Brill. 1977: Gwiazda. Brill and Held. 1975). In the following experiments we will define an infant’s acuity threshold 3s the highest spatial frequency at which the preference for gratings over a homogeneous field was not less than a criterion percentage. 75”: and 58“; were chosen 3s the preference criteria. We tested a large number of infants and combined sessions across infants in order to provide normative acuity data against which to measure an individual infant’s performance during the first year of life. Three experiments were performed on infants with insignificant astigmatism (less than I diopter of cylindrical refractive error): Exprri~~ent 1: Measurements of visual preference obtained by presenting each infant with a set of
paired stimuli consisting of a vertical grating paired with 3 homogeneous field of equal space-averaged luminance. The gratings varied in spatial frequency. Two levels of contrast were used (95:; and 357;).
E.uprri,trrrrr 2: Measurements of visual preference obtained by presenting each infant with one main axis grating (either vertical or horizontal) simultaneously paired with one oblique grating (either 45’ or 135”) of equal luminance, contrast, and spatial frequency. This experiment of a previously 1975).
constitutes a larger scale replication reported experiment (Leehey et al..
Experimenr 3 : Measurements of visual preference for both vertical and oblique gratings taken on the same infants using the procedure of Experiment I.
METHOD Suhjvcrs One hundred and four full term infants ranging from 7 to 50 weeks of age and with insignificant astigmatism were tested. Of these infants. ninety-nine were white, five were black. Their spherical component of refraction ranged from -1.75D to +3.75D. with most values between zero and +Z.OOD. demonstrating the hyperopia typical of infants. No optical correction was applied since our stimuli were presented at 50 cm distance (- Z.OOD)making nearsightedness of negligible consequence and farsightedness correctable by accommodation. Most infants were solicited through letters sent to parents whose names were obtained from central files of birth certificates in Cambridge and Boston. Massachusetts. Responses to the letters averaged I so/,. Each infant was refracted every 4-6 weeks by near retinoscopy (Mohindra. 1977). We have observed that many infants in this age range show transient astigmatism (Held er al., 1977). Data from infants who showed less than I diopter of astigmatism within 3 weeks of the testing session were included in the analysis. Preliminary data on the incidence of astigmatic refractive error and its infhtence on acuity have been reported elsewhere (Held er a/.. 1977: Mohindra. Held. Gwiazda and Brill. 1978: Held. in press). .Appamrus The apparatus consisted of a wooden partition containing two circular translucent screens, one to the right and
ox to the lsi’t oi a red firc;ltlon lizhI. tended II of visual ~tngle lwlth crntex
E;ish ,crx:: rus xparat~? 5, ?i
of visual angle. The scieeni ‘here rnl2< from Ch,rr:e:t:~ Charprint 916 h ICV, rag zhnical rrzelng :.ellum Tx~ Kodak Carousel projectors (auto-focus 850 HJ. each equipped with a Kodak zoom lens (Ektanar-C\. uere used for projection. .A Kodak Wratten 1.0 nectral densit;, filter covered each lens. fn Experiment I. vertical black and white square-wabe gratings were paired with homogeneous test fields of equal space-averaged luminance ill cd,‘m’l and were projected simultaneously onto the rear of their respective screens. They were made up of one of live spatial frequencies: 0.75. 1.5. 3.0. 6.0. and 12.0 cycles per degree ic degl of visual angle. In Experiment 2. either vertical or horizontal gratings were paired with either left or right oblique gratings of the same spatial frequency (ranging from 0.3s to 12.0c!degl. In Experiment 3. either vertical (90’1 or right oblique (45’) gratings were paired with homogeneous test fields of equal space-averaged luminance. Spatial frequencies of the gratings ranged from 0.75 to lZ.Oc.deg. The slides were produced photographically using black and white high contrast film from two originals consisting of strips of black Chartpak pressure-sensitive .graphic taoe mounted on white plexiglas. The resulting projected gratings had a 50-50 dutv. c\rcle within -+1”,. . The luminance of the black and white gratmgs was measured at all spatial frequencies using a Gamma Scientific DR-I Digital Radiometer with a Model ZOZC-IC Photomultiplier Detecter coupled to a hl~tiel 20X-31 High Efficiency Photometric Telescope with 3 I aperture. The contrast of the gratings was 95’?,,for the lowest three spa. tial frequencies (0.38. 0.75 and 1.5 c’degt. 9-V, for 3.0 c,deg. for 12.0~ dsg [con9l”,, for 6.0~ dep. and 90”, trast = (L, - L2) (L, + L.;J. where L, is the luminance of the light area and LJ is the luminance of the dark area]. In some sessions. contrast was reduced to 3Y; with mean luminance remaining at 34cd:m’. This was accomplished by placing a Kodak Wratten O.-t neutral density filter over each Kodak lens while projecting sufficient additional light onto the two screens uith a Regent slide projector. Aside from the slide projectors and red fixation light. no other light source was present during the session. Slides containing brightly colored circles on a dark background were presented during the intervals between presentation of the gratings to help maintain the attention of the infant to the screens. Procedure
Initially the infant and parent entered a lighted room. The infant was situated in front of and facing the screens onto which the colored circles were projected. The experimenter aligned the infant’s head and eyes with a mark on an adjacent wall which was 5Ocm from the stimuli. The parent was instructed to keep the infant in that position throughout the session. When the infant and parent were comfortable the room was darkened. During most experimental sessions. the infant sat on the parent’s lap. In a few sessions the younger infants were held over the parent’s shoulder. with the head uptight and centered between the stimuli. Some of the older infants were allowed to stand on the chair while being held by- the parent. The infants’ eyes were level with the stimuli Sucking on a bottle or pacifier seemed, in some cases, to maintain the infants’ calmness and attention. Fewer than 5:; of the infants were eliminated due to fussiness or sleepiness. Before each trial. the red fixation light was flashed to msure that the infant was looking str&ht ahead. Occasionally the experimenter tapped on the center of the partition or made soft clucking or animal-like noises to gain the infant’s attention while flashing the red light. If this was unsuccessful. the experimenter occasionall> waved
Infant visual acuity and both hands back and forth over the two screens to attract the infant‘s attention. When the infant’s gaze was directed at the fixation light. the stimuli were presented. Side of presentation was counterbalanced for both spatial frequency and orientation. and the order of presentation of, stimulus pairs was pseudo-randomized in a manner described below. During each trial the experimenter looked at the infant’s head and eye movements through a peephole directly beneath the fixation light. and made a forced-choice judgment as to which side the infant preferentially fixated. Light from the stimuli was sufficient to illuminate the infant’s face. Comeal reflections of the gratings were too small to be resolved by the experimenter. The experimenter made a judgment based on one or more cues given by the infant. such as first fixation. duration of fixation, and facial expression. The experimenter wore goggles with one eye occluded to insure that location of the gratings was unknown. The order of presentation of the stimuli was also unknown. The length of each trial was variable. depending on the length of time required by the experimenter to make a judgment. Trials for the younger infants (under :! months) whose head and eye movements were less well developed were usually IOsec in length. while those for the older infants were approximately 5 set in length. The 5-10s~~ trials gave the infant ample time to observe both stimuli. As soon as a judgment was made. the trial stimuli were removed and the colored circles were presented while the observation was recorded and the procedure for gaining the infant’s attention was repeated. Sixty trials were usually run in a session which was completed in a maximum of IO min if no breaks were taken. If necessitated by restlessness of the infant. a break was taken during the session but this was usually required only for infants under 3 months of age. The slides were arranged so that every spatial frequency could be tested four times in twenty trials. This set was then cycled through three times to constitute sixty trials. In this way. if an infant became fussy. the experiment could be terminated after either two or three cycles. A minimum of two cycles was neccessary for inclusion in the results. We have found that this combination of apparatus and procedure allows us to test infants from soon after birth up to an average of I year of age. Among the novel features of our procedure, working in darkness may be the most important: it assures minimal loss of attention to the stimuli.
its
1559
meridional variation
in three age groups. Ail infants were tested binocularly on five spatial frequencies (0.75. 1.5. 3.0, 6.0 and 12.0 c/deg). To obtain measures of visual preference for vertical gratings over the homogeneous field raw scores of the infant’s looking behavior at each spatial frequency were converted into percentages of preference for the grating. An infant’s acuity threshold was defined as the highest spatial frequency, of the five tested, at which the infant’s preference for vertical gratings over the homogeneous field was not less than a criterion percentage. In this experiment we chose 75% and 58% as the preference criteria. Results. Within each age group a tally was made of the number of infants whose threshold fell at each spatial frequency. These data are presented as frequency histograms for each age group in Fig. I. Sessions in which preference performance fell below 75% for one spatial frequency and then increased to
EXPERLVENTS Experiment 1: Measurement of Gsual preference for certical gratings Many investigators have used the procedure of pairing a grating with a homogeneous field in order
to measure visual acuity. although none ha+ tested infants of more than 7 months of age. The data we have obtained on younger infants serve as a check on our procedures relative to those of others. Fifty-five infants from 14 to 50 weeks of age were tested in 75 sessions of either forty or sixty trials per session. Fewer than 10% of the sessions contained forty trials. For consistency of data presentation and for purposes of comparison between experiments. the data from all the experiments were arbitrarily divided into IO-week age groups from 0 to 50 weeks. In this experiment the youngest infant tested was I4 weeks old; therefore the youngest age group is from 14-20 weeks. No infant was tested more than once within a given age group. Thirty-nine infants had a session in only one age group, twelve infants had a session in two age groups, and four infants had a session
60
t
n=20
Spatial frequency,
I I
c /deg’
Fig. I. Percentage of infants in each of four age groups from I4 to 50 weeks of age meeting 75% criterion of preferring vertical gratings to a homogeneous field. The “other” category refers to those infants whose preference performance fell below 750/i for one spatial frequency and then increased to 750,bor greater for a higher spatial frequency.
E.yprrimenr 2: Mrasurrmenr of ~1suu1 prrjbtincc. hc;racior when rerrical or horkontai yrarinys art’ puir?d wtr/! ohliqur gratings
A---. l -e
m----m
Age,
58% mterion 75% criterion Oblique effect
weeks
Fig. 2. Circles and triangles show median spatial frequencies for four age groups at which infants preferred a vertical grating over a homogeneous field at the 750/gand 58% criteria. respectively. Squares show median spatial frequencies for each of five age groups within which infants preferred either a vertical or a horizontal grating over an oblique !rating at one spatial frequency at least 67”; of the time. Mean ages ranged from I I to J5 weeks.
75”,, or greater for a higher spatial frequency were not used to estimate resolution performance. but rather were placed in a category called “other”. The percentages of sessions falling into the “other” category are 50,,, O”,,. 10%; and 1.5?,, for the four age groups: thus. most of the data are orderly. The modal spat ial frequency increases from 3.0 c/deg in the l&20 Heck group to 6.0c;deg by the age of 41-50 weeks. The median threshold spatial frequency was determined for each age group. These medians are plotted as a function of mean age and shown by the circles in Fig. 2. This figure shows that. using our procedure. the logarithm of visual acuity for vertical gratings increases linearly with chronological age from I4 to 50 Lveeks. At the 7.5”,; preference level it ranges from 3,0c,‘deg in 14-20 week-old infants to 8.0c/deg in the 41-50 week group. In Snellen notation, the range of acuity is from 20/200 to 20180. The triangles in Fig. 2 represent median threshold spatial frequencies taken on the same data using 58”, preference as the criterion instead of 75qW These points also increase linearly with age. from 3.7c/deg (20 150) in 14-20 week-old infants to 11.8 c,‘deg (20 50) in the 41-50 week group. Using this lower criterion increases the acuity threshold by slightly more than 4 octave. on the average. Lowering the contrast of the gratings from 9j00 to 35”” reduces the infants’ median acuity threshold bk 2 octaves. on the average, for twenty-four infants from I I to 50 weeks of age who were tested at both contrast levels. The medians are shown in Table 1. Table
I. Median spatial frequency at 75”, preference criterion for two levels of contrast
Age (weeks) 1420 21-30 3140 41-50
Number of 35%; contrast infants (cideg) 4 9 6 5
I .07 I .07 I .07 2.14
95”; contrast (c/W
3.00 3.63 7.24 8.50
In an earlier study we established the presence of an oblique effect as early as 6 weeks of age (Leehe) er al., 1975) by directly pairing oblique with slther horizontal or vertical gratings in a two-choice preference procedure. Results showed that the spatial frequency at which the infants maximally prefer main axes over oblique gratings increases monotonically with age over the range of spatial frequencies we tested. In the present experiment. replicating and extsnding the earlier study, ninety-seven infants were shown either a vertical or horizontal grating paired with an oblique one for a total of one hundred and forty four sessions. The infants in the youngest age group. i- I3
14-20
30
t
/ I
wks
nz36
Spatial frequency ,
c/&g
Fig. 3. Percentage of infants in each of five age groups from 7 to 50 weeks of age meeting 67% criterion for preferring a horizontal or vertical grating over an obtique grating at one of the five spatial frequcricies tested. “No maximum” refers to those infants whose preference for either vertical or horizontal gratings did not reach 675; at an) spatial frequency. Infants who showed two. or more . equal .. maxima of at least 67”& are cleslgnated as “Other
1561
Infant visual acuity and its meridional variation weeks of age. were shown gratings ranging from 0.38
to 6.0c/deg. while those in the older four age groups were shown gratings ranging from 0.75 to lZ.Oc/deg. The older four age groups are the same as those in Experiment 1. No infant was tested more than once within a given age group. Sixty-three infants had a session in only one age group, twenty-four infants had a session in two age groups, seven infants in three age groups and three infants in four age groups. Resulrs. The great majority of infants show a clearly defined preference maximum for main axes gratings over obliques of 670,6 or greater at one of the five spatial frequencies tested. This will be the definition of an oblique effect. Figure 3 shows the percentage of infants within an age group who had such maxima at each of the spatial frequencies tested. Infants who showed two or more equal maxima of at least 67% are designated as “other”. Those whose preference for either vertical or horizontal gratings over oblique did not reach 67% at any spatial frequency are categor-
Experiment 3: Measurement of Gsual preference for certical and oblique gratings
Noting the good agreement between the preference
ized as “no maximum”.
Vertical
Spatial
The modal spatial frequency increased from 0.75 c/deg in the 7-13 week group to 6.0c/deg in the 41-50 week group. The percentage of infants not having any maxima decreases with increasing age, while the percentage having two or more maxima increases slightly with age. The median spatial frequency at which a preference maximum occurred was determined for each age group. These medians are plotted in Fig 2 as a function of age for each group of infants and are represented by squares. These points show the same trend as does acuity for vertical gratings, with the exception of the youngest age group, for which no acuity data were obtained. The oblique effect points are lower than the corresponding acuity points by $ octave. on the average, using the 75% preference level, and $ octave. on the average, using the 58% IeveL
frequency,
I
c/ded
Spotidl frequency,
c /deg
Fig. 4. Percentage of infants in each of four age groups from 14 to 50 weeks of age meeting 75:;, criterion for preferring vertical (left side of figure) or oblique (right side of figure) gratings over a homogeneous field. The “other” category refers to those infants whose preference performance fell below 759; for one spatial frequency and then increased to 75:” or greater for a higher spatial frequency.
threshold for vertical _aatings as measured in- Expcriment I. and the spatial frequency of the maximum preference for vertical or horizontal gratings over obliques as measured in Experiment 2. we wondered why previous investigators claim to have found no evidence for lowered acuity for oblique gratings using the fixation preference paradigm (Teller er al.. 1974). fn this experiment. we used the method described in Experiment I and obtained comparable measures of visual preference for oblique and vertical gratings. Twenty-nine infants ranting in age from I4 to 50 weeks were tested in a total of forty-three sets of two sessions each. One session in each set paired vertical gratings with a homogeneous field, and the other session paired right oblique gratings with the homogeneous field. The sessions were spaced no more than 3 weeks apart. In twenty-nine sets of sessions the vertical gratings were presented first. No infant had more than one set of sessions within an age group. Seventeen infants had a set of sessions in only one age group. Ten infants had a set of sessions in two age groups and two had a set of sessions in three age groups. All but one of the sessions pairing vertical gratings with a homogeneous field were also included in Experiment 1. Rrsulrs. Preference for vertical and oblique gratings is shown in Fig. 4 for each of four age groups. The percentage preferences were determined as in Experiment 1. The modal preference for vertical gratings using the 7.5’, level increases from 3.0c’deg in the 14-20 week-old infants to lZ.Ocideg in the 41-50 week-olds. similar to Experiment 1. At the same time. preference for oblique gratings remains at 3.0 cycles from I4 to 40 weeks of age, only reaching 6.0c:deg by 41-50 weeks. Median spatial frequencies were determined as in the first two experiments and are shown by the solid lines in Fig. 5. Using either the 7504 or 5846 preference criterion the median spatial frequency for vertical gratings increases approximately I+ octaves from 1-I to 50 weeks of age, while that for oblique gratings increases only about ;’ octave during the same period of development. By using the lower criterion of $8:;. the acuity threshold for both vertical and oblique gratings increases by slightly more than f octave. on the average.
c46
I
I
30
20 Age,
I 40
weeks
Fig, 5. Median spatial frequency at 75% and 58% criteria for preferring either a vertical or an oblique grating to a homogeneous field. Mean ages ranged from 17 to 4-t
weeks of age.
DISCL SIO\
Experiment I demonstrates that acuity for vertical gratings. as measured by our procedure. increaxs with age-from 3.0c:deg at 4 months to approximately 8.0 c.‘deg by 11 months. These results are similar to those obtained by others using the fixation preference and optokinetic nystagmus techniques (Dobson and Teller. in press) for infants up to 6 months of age. Our procedure has enabled us to extend testing sessions to I year. thereby revealing the continuing increase in acuity after 6 months. The acuity data graphed in Figs 1 and 2 for the oldest age group indicate that we should have included gratings of higher spatial frequency in our testing procedure. In fact. when we used the W, criterion to determine the acuity threshold nineteen out of twenty infants in the 41-50 week age group had thresholds at 12.0cideg. The clearcut changes shown after 6 months of age have an important implication for the duration over which acuity improves during infancy. Several investigators. using pattern evoked potential procedures. hare claimed that adult levels of acuity are reached by 6 months of age (Marg et al., 1976: Sokoi. 1978). It has been suggested that the differences between these results and the slower growth of acuity shown by behavioral methods is attributable to different criteria used for determining thresholds (Dobson and Teller, in press: Sokol. 19751. However. a mere change in threshold criterion will not eliminate the continuous increase in acuity occurring after 6 months, as a glance at Fig. 1 shous. Lowering the contrast of the gratings from 95”; to 3Y0 reduces the median acuity threshold by 1 octaves. on the average. These results at the two contrast levels are in agreement with those reported by Banks and Salapatek (1976) on five Z-month-old infants. More recently. Atkinson rt al. (f977a) have reported a difference of 1 octave, on the average. in I-. 2-. and 3-month-old infants. Experiment 3 shows the presence of an oblique effect (a preference maximum for main axes gratings over obliques at one spatial frequency) as early as we have tested (7-13 weeks of age). The results show the same increase in the spatial frequency of maximum preference for main axes gratings wtth age as that reported earher by this laboratory (Leehey er al.. 1975). Figure 1 shows good agreement between the median spatial frequencies of maximum preference for vertical or horizontal gratings (Experiment 7) and those of the preference for vertical gratings over the homogeneous field (Experiment 1) as age increases. This result is consistent with our earlier conclusion (Leehey et al.. 1975) that the maximum preference for horizontal or vertical gratings over obliques occurs at or near the acuity threshold. It is cisar from Fig. 2 that increasing the criterion used to determine the acuity threshold to greater than 75”,,, could bring these points into line. Experiment 3 shows that acuity for vertical gratings increases more rapidly with age than that for oblique gratings. At the 759; preference Ievei acuity for vertical gratings increases from j.Oc;deg in the 1l-30 week group to 9,Oc’deg in infants 41-50 weeks old. while acuity for oblique gratings increases from 3.0
Infant vtsual acuity and its meridional variation
to 5.3 c,deg during the same period. At the 580;, preference level acuity for vertical gratings increases from 3.6 to 11.2 c/deg. while acuity for oblique gratings increases from 4.3 to 6.9 cjdeg. Using their technique on a small sample of infants of less than 6 months of age (with a mean age of approximately 15 weeks). Teller rf al. (1974) did not find a statistically significant difference in acuity for vertical, as compared to oblique gratings-a result consistent with ours at that age level. The magnitude of the difference between acuities for vertical and oblique gratings in the older age groups is surprisingly large, particularly in the oldest group in which it amounts to almost an octave. In Caucasian adults. this difference averages 2OY<(Timney and Muir. 1976). a fraction of an octave. The comparison suggests that the oblique effect increases in magnitude during the first year but must decrease during a later period. These results are reminiscent of the findings of Leventhal and Hirsch (1977) and Imbert (personal communication) on the development of the orientation-sensitive single units of the kitten cortex. The development of units sensitive to horizontal and vertical edges appears to differ in time and susceptibility to deprivation from that of obliquesensitive units. Taken together. the results of Experiments 2 and 3 are paradoxical. On the one hand, results from Experiment 2 support the conclusion that the oblique effect is present at the earliest age we have tested. On the other hand, Experiment 3 fails to demonstrate an acuity difference between vertical and oblique gratings for the youngest infants. Our experiments do not provide an answer to this paradox, but we can suggest the following possibilities. One possibility might be that when we measure
occur at several levels of the visual system ranging from retina to cortex. Discovery of an oblique effect in early infancy at spatial frequencies considerably below those at which it has been found in adults has an interesting implication for this change. It suggests that the anisotropy in the visual system. evidenced by the oblique effect. antedates in time the changes that result in increasing acuity during the first year of life. The differential sensitivity to orientation suggests that the anisotropy is of cortical origin. If the increase in acuity with age results from subcortical changes, then we can conceive of the accompanying increases in contrast sensitivity, in the frequency of maximum contrast sensitivity, and in the cutoff frequency (acuity) as the result of increasing resolution at the subcortical levels that feed into the anisotropic cortex. Alternatively, the increasing resolution may itself result from changes in cortex occurring in close proximity to the locus of the anisotropy. This account of the development of the visual acuity in infants serves as essential baseline data for assessing both the optical and neural effects on vision of habitual blurring such as typically occur in astigmats. Acknowledgements-This research was funded by research grants from: The National Eye Institute (NIH No. 5-ROIEYOl191-OS), the National Institute for Neurological and Communicative Diseases and Stroke (NIH No. 5-POI-NS-123363-03X and The Spencer Foundation (No. LTR-DTD-71373). The first author was supported by a Liza Minnelli Award, Fight For Sight, Inc., New York City (No. F-303). The authors would like to thank Joseph Bauer, D. Alfred Owens, and Joseph Thomas for their helpful comments. and George Timberlake for assistance in measuring the.luminance of the stimuli.
vertical and oblique acuity in Experiment 3 we have only tested infants whose results fall into the “no maximum” category for the oblique effect in Experiment
2. In the 14-20 week age group the “no maximum” percentage reaches 220/d of all the sessions in that group. “No maximum” results in Experiment 2 would be consistent with the lack of an acuity difference between vertical and oblique gratings in Experiment
3. A close look at individual infants, however, reveals that of the seven infants from 14-20 weeks of age tested on both experiments, none had data which fell into the “no maximum” category for the oblique effect Another possible conclusion is that there are small differences in the apparent contrast of the gratings such that a main axis grating, when directly paired with an oblique grating, would look clearer at or near threshold. The small difference in apparent contrast may not be detected, however, when each grating is independently paired with a homogeneous field. With the older infants (21-50 weeks) there is a clear acuity difference between vertical and oblique which can be detected by both methods. Very recently, Mayer (1977) reported data showing that the magnitude of the oblique effect increases from 5 years of age to adulthood. While this increase may occur. we cannot accept her conclusion that the “anisotropy develops fairly late in childhood’*. We do not know &y acuity increases from birth through the first year of life. Developmental changes
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