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Visual pattern detection in preterm neonates
INFANT
BEHAVIOR
AND
DEVELOPMENT
8,
47-63
(1985)
Visual Pattern Detection in Preterm Neonates* PATRICIA ANN SHEPHERD, JOSEPH F. FAGAN, III, AND KATHLEEN
A. KLEINER
Case Western Reserve University The purpose of the present study was to test the ability of preterm neonates to resolve square-wave gratings varying in spatial frequency, contrast, and orientation. The sample included 184 infants born prematurely at an average of 34 weeks, 6 days who were tested at a mean postconceptional age of 37 weeks, 4 days. The preferential looking procedure was employed for testing the neonates’ resolution of the gratings. Spatial frequencies included .06, .ll, .23, .46, .92, 1.85. 3.69, and 7.30 cycles/degree. Controsts were 66%. 38%. 22%. 17%. and 13%. The major results were that detection of the gratings varied as a function of contrast and spotial frequency. Higher spatial frequencies required more contrast to be resolved and, on an absolute basis, the infants were able to detect spatial frequencies OS high as .92 to 1.02 c/deg and contrast as low as 13%. Horizontal and vertical gratings did not differ in detectability. In general, the present results indicate much more refined pattern-detection capacities in the preterm neonate than has previously been demonstrated. visual
acuity
contrast
sensitivity
preterm
neonates
pattern
detection
Whether the visual system of the healthy human newborn is functional has ceased to be a subject for debate since research in recent years has conclusively demonstrated that some visual perception is present even in preterm neonates (Miranda, 1970; Morante, Dubowitz, Levene, & Dubowitz, 1982). Instead, debate now focuses on how well the human newborn can see. For the most part, work has been conducted with full-term newborns (e.g., Adams, 1982). There has been very little study of visual perception in prematurely born neonates, i.e., infants born prior to a term gestation of 38-40 weeks postconception. In the present study, therefore, we examined three aspects of the premature neonates’ visual perception: their sensitivity to contrast differences in stimuli, their ability to see fine patterns at high contrast, i.e., their visual acuity, and their ability to resolve patterns presented in either a horizontal or a vertical orientation. Visual acuity and contrast sensitivity were chosen for study because they provide a widely accepted description of visual functioning across all ages of subjects. Orientation was included as a variable simply because it was easy to obtain and would add to our information about how premature neonates perceive form. * We wish to thank Drs. Velma Dobson and Ronald Boothe for their help with data analyses in preparation of this manuscript. We are indebted to our reviewers who gave such thoughtful and extensive comments on earlier drafts of this manuscript. Requests for reprints should be made to the first author at The Child Development and Mental Retardation Center, University of Washington, WJ-10, Seattle, WA 98195. 47
48
SHEPHERD,
FAGAN.
AND
KLEINER
In an early study of infant visual perception, Fantz, Ordy, and Udelf (1962) paired high-contrast, square-wave gratings (i.e., patterns with uniform, sharply contrasting black-and-white stripes) with plain gray targets of equal luminance.’ Since infants typically prefer to look longer at patterned than at plain targets, the assumption made was that the gratings would be preferred to the unpatterned gray targets, so long as the stripes in the gratings were resolvable by the infants. The finest grating (i.e., that grating with the highest spatial frequency or number of stripes) preferred to gray was then taken to indicate the infants’ estimated level of minimum separable acuity. Since 1962, numerous studies have explored the development of minimum separable acuity in infants (e.g., Dobson & Teller, 1978; Gwiazda, Brill, Mohindra, & Held, 1978, 1980). At present, infant visual acuity is believed to improve from approximately 1 .O cycle/degree (c/deg) or a Snellen acuity of about 201600 at birth to 5.0 c/deg or a Snellen of about 20/120 at 6 months in normal, full-term infants, although some disagreement exists regarding the acuity estimates given for newborns and l-month-old infants (Banks & Salapatek, 1983; Dobson & Teller, 1978). The only data on minimum visual separable acuity that exist for newborn premature infants are two published reports (Miranda, 1970; Morante et al., 1982) and studies briefly mentioned in a chapter on neonatal visual perception (Miranda & Hack, 1979). Miranda (1970) reported that the visual acuity of infants averaging 35 weeks from conception at the time of testing was roughly the same acuity as full-term newborns, with both groups of infants resolving a vertically oriented .5 c/deg square-wave grating but not resolving a .9 c/deg grating. Morante et al. (1982) similarly reported that newborns born between 35 and 41 weeks who were tested for visual acuity within one week of birth were able to resolve vertical .5 c/deg square-wave gratings but not .9 c/deg gratings. Moreover, they found that infants younger than 35 weeks at test were only able to resolve a grating if it contained no more than .2 c/deg. Finally, Miranda and Hack (1979) commented that 30-week postconceptional-age infants whom they had tested were able to resolve gratings of .2 c/deg or less. Unfortunately, none of the studies report any details about the contrast at which acuity was tested, making it difficult to judge the accuracy and reliability of their estimates. Despite that, the studies demonstrate that visual acuity is a measurable attribute even of premature newborns, that newborns 35-41 weeks of postconceptional age can resolve gratings at least as fine as .5 c/deg, and that premature newborns younger than 35 weeks may have poorer acuity than older newborns. One purpose of the present study, therefore, was to replicate and extend the previous findings for premature neonates. ’ Gratings are typically describedin terms of their spatial frequencyand contrast. Spatial J-equency is defined asthe number of cyclescontainedin one degreeof visual angle, wherea cycle consistsof an adjacent light and dark stripe and visual angle is that formed by the grating at the eyeof the observer.Contrust is defined asthe maximum minus the minimum luminance of the grating divided by the sum of the two luminances. Contrast is thus a measureof the intensity differencesbetweenelementsip. the grating. Contrust sensifivity is defined as the reciprocalof contrast at the observer’sthreshold.
VISUAL
PATTERN
DETECTION
49
The measurement of vision is not limited to the study of responses to high-contrast stimuli, however. Measurement of sensitivity to contrast for a variety of spatial frequencies provides an improved description of the visual system because it addresses the question of the range of stimulation which can be detected visually. At high spatial frequencies, contrast sensitivity and acuity become similar so that visual acuity can be estimated from data regarding the least contrast necessary to detect a set of high spatial frequencies. In short, finding the minimun contrast that an infant requires to detect gratings of different frequencies adds considerably more information than that obtained by the measurement of visual acuity alone. In addition, contrast sensitivity has been evaluated in older infants (e.g., Atkinson, Braddick, & French, 1979; Atkinson, Braddick, & Moar, 1977; Banks & Salapatek, 1981), allowing comparisons with the present study. The function that relates the minimum contrast necessary to see a sample of different frequency gratings ranging from coarse to fine is termed a contrast sensifivify function. For the function, sensitivity to contrast is graphed as a function of spatial frequency. From work conducted with infants so far, it has been determined that young infants, 1 to. 3 months postnatal age at test, are sensitive to a much smaller range of contrasts and spatial frequencies than are adults (Banks & Salapatek, 1981, 1983), although after 2 months of postnatal age, the shapes of the contrast sensitivity functions for infants and adults are grossly similar. That is, the infants’ and adults’ contrast sensitivity functions demonstrate that intermediate frequencies require less contrast to be seen than do lower or higher frequencies, so that the resulting functions appear to have an inverted U-shape. Prior to 2 months postnatal age, however, the functions differ in that they do not show a low-frequency fall-off characteristic of the functions for older subjects, a phenomenon believed to be due to the immaturity of lateral inhibition processes in the young infants (e.g., Banks & Salapatek, 1983). To date, few reports have been presented with regard to sensitivity to contrast in infants less than 1 month old at the time of testing. The most recent report, and the one providing the best estimate of contrast sensitivity in newborns, was by Adams (1982), who found that newborns tested from 1 to 5 days postnatally were able to see checkerboard elements of .13 c/deg at 11% contrast. Adams, however, tested only one stimulus size. The present study there fore sought to estimate preterm neonates’ responsiveness to contrast for a variety of stimuli over a range of spatial frequencies. Finally, the data on the relative resolution of vertical and horizontal gratings is contradictory for older infants. Gwiazda et al. (1980) measured resolution of horizontal and vertical gratings when the gratings were paired with homogenous gray fields. They found no difference in the growth of visual acuity for the two orientations. Slater and Sykes (1977), however, found that when horizontal and vertical gratings were themselves paired with one another, a preference could be obtained for the horizontal grating which could be interpreted to mean that the horizontal grating was easier to see. Certainly, no one
50
SHEPHERD,
FAGAN,
AND
KLEINER
has reported data on preterm neonates. The present study thus compared the preterm neonates’ responses to the two stimulus orientations. In summary, few data exist with regard to vision in the premature neonate. Thus, the purpose of the present study was to measure the ability of premature neonates to resolve square-wave gratings of different spatial frequencies which varied in contrast and orientation. METHOD
Subjects The study was undertaken in the nurseries of a local hospital. The sample for the study included 184 infants who were born prior to 40 weeks gestation. The mean gestational age of the sample as estimated by a Dubowitz examination at the time of birth was 34.5 weeks (SD=4.5 weeks). At the time of testing, the infants had a mean postconceptional age (gestational age plus postnatal age) of 37.6 weeks (SD = 3.1 weeks), i.e., the infants were tested approximately 3 weeks after birth, but 2 weeks prior to the usual 40-week term of gestation. Only two of the infants had retrolental fibroplasia. No refractive errors were noted in the hospital records for any of the infants. The mean birthweight of the sample was 2317 g (SD= 1059 g). Seventy-three percent were of appropriate weight for gestational age, while the remaining infants were either small for gestational age (15%) or large for gestational age (12%). The infants in the sample were divided nearly equally between females and males (53 070and 47 % , respectively). The racial composition of the sample included 64% white and 36% black infants. Apparatus and Materials A portable visual preference apparatus similar to that shown in Fagan (1970) was used for testing the visual abilities of the preterm neonates. Essentially, the apparatus consisted of a stimulus presentation chamber which had walls on either side and above so that a minimally distracting environment was provided for testing. The inside of the chamber was painted a uniform gray and was illuminated by two 12-W incandescent bulbs which were placed out of view of the infant and aimed at the stimuli. The testing chamber also had a movable back wall which was attached at a right angle to a small floor in the test chamber, so that when the back wall was pulled away from the infant, the floor rose and prevented the infant from seeing what was happening to the back wall. In effect, the back wall and floor of the test chamber formed a pivoting unit. While the back wall was out of view of the infant, stimulus targets could be attached magnetically to the wall in either of two positions. When the back wall was returned to the view of the infant, the stimulus targets were horizontally aligned and appeared at a distance of approximately 33 cm from the infant’s eyes. The stimulus targets were approximately 30 cm apart from center to center, forming a display that was 78 ’ wide. While the stimulus targets were presented to the infant for viewing, an observer could watch the
VISUAL
PATTERN
DETECTION
51
cornea1 reflections of the targets over the pupils of the infant’s eyes through a .6 cm peephole centered between the two stimulus targets. A digital event recorder timed stimulus presentations and recorded the length of time that the targets were fixated. There were a total of 30 unique stimulus targets produced. The targets contained square-wave gratings and included 8 which were 66% contrast, 6 each at 38% and 22% contrast, and 5 each at 17% and 13% contrast, The stimuli at 66% contrast had spatial frequencies of .06, .ll, .23, .46, .92, 1.9, 3.7, and 7.4 c/deg. At 38% and 22% contrast, frequencies of .06, .ll, .23, .46, .92, and 1.9 c/deg were employed, and at 17% and 13 % contrast, frequencies of .06, .l 1, .23, .46, and .92 c/deg were used. The gratings at 66% contrast were initially mechanically produced and then lithographically reproduced. The remainder were produced by hand by combining various shades of gray (Colormatch) art papers. All contrasts were measured by focusing a spot-light photometer on the light and dark bars of each contrast grating and calculating the contrast by dividing the difference between the values by the sum of the obtained values. Regularity of the gratings was calculated by measuring the distance between stripes at at least 10 points (deemed to be places of greatest error). Overall, the lowest frequency gratings were the most regular. For example, the .23 c/deg target at 13% contrast had a SD of .005 c/deg, while the .92 c/deg target had a SD of .l c/deg. Finally, a 31st target served as the plain comparison stimulus target presented for testing with all of gratings.2 The average luminance of the gratings and the plain target was constant at 130.c/m2 The targets were circular fields 26” in diameter from the infant’s viewing distance. Each of the gratings could be placed either vertically or horizontally for a total of 60 stimulus configurations. Procedure During testing, an infant was held facing the test chamber by an assistant who sat on a chair in front of the testing chamber. An observer, watching through the peephole in the back wall of the chamber, saw the cornea1 reflections of the stimuli on the infant’s eyes and recorded the length of time that the infant fixated the two targets. The pairs of gratings and plain targets were shown to the infant for two trials of 5-s duration. The relative positions of the targets between trials were exchanged so that each target of a pair appeared on both sides of the viewing field (i.e., on the left and right of the back wall). Each infant saw an average of seven randomly ordered pairs (range = 28 pairs) during a test session. The only constraint on randomization was that an attempt was made to test every infant with the same pairs both horizontally 1 An informal pilot study employing a small number of newborns tested in the same apparatus paired a high-frequency grating (14 c/deg) with a plain gray target. The infants did not prefer one target to the other, but we felt that since the high-frequency target had been produced in a manner identical to the 66% contrast gratings, it would be the better choice for the “plain” target in the present study. Thus, the plain target referred to in the text is actually a 14 c/deg grating.
52
SHEPHERD,
FAGAN,
AND
KLEINER
and vertically. Those infants who saw fewer than seven or eight pairs did so due to fussiness or sleepiness. Because there were no systematic differences in pattern preferences as a function of number of test pairs shown, all data were included in the described analysis. Finally, four different observers collected the data in the present study. One observer collected about one third of the data, while the other three collected roughly equal amounts. RESULTS The first step in the data analysis was to determine the percentage fixation score for each target pair by each infant. The percentage fixation score for the grating in each pair was obtained by dividing the fixation time given to the grating by the total fixation time given to both members of the pair during the two test trials. Thus, each infant had one percentage fixation score for each stimulus pair with which he or she was tested. After percentage fixation scores were calculated, the percentage of infants who preferred the grating was calculated for each condition by dividing the number of infants with percentage fixation scores greater than 50% by the total number of infants tested at that condition. Since the percentage of infants preferring the gratings could vary from 0070, when no infants preferred the grating, to lOO%, when all the infants preferred the grating, it was necessary to adopt some criterion for judging when the infants were able to resolve a given grating. The criterion of 75% of infants preferring the grating was chosen for making the judgment of stimulus resolution. The next step was to estimate the reliability of the data from different observers in order to be sure an effect was not due to the presence of a particular observer. An interobserver reliability was calculated by correlating the proportion of infants who preferred the grating at each spatial frequency within a given contrast level across the different observers. The data from the observer who collected the majority of the data was compared to the pooled data from the other three observers. The obtained correlation was .79 @C .Ol). We next examined the data separately for horizontally and vertically oriented gratings by calculating the percentages of infants preferring the grating at each condition for the two orientations of the stimuli. The orientation data are, for the most part, within-subject data, since almost every infant contributed data at each orientation for each condition with which he or she was tested. The results of the analysis for the two orientations are shown in Table 1. Note that the percentages for the comparable conditions are similar for both orientations. The data were then employed to estimate contrast-sensitivity functions for the two orientations. The functions, like all of those to follow, were generated by applying a probit analysis (Finney, 1971) wherever possible to the data at each spatial frequency. When a probit analysis was not possible because all of the preference data at a given spatial frequency were either greater or less than 75070, no attempt was made to estimate the 75%
79(14)
Contrast
13%
the
93(14)
Contrast
17% H V
Note. tested from
Table 1 contains for each condition vertically presented
percqntoges in parentheses. stimuli.
33(9) 75(8)
EO(l5)
71(17)
V
H V
94(16)
80(15)
22% H
Contrast
1 @WV
of infants An “H”
87(15) 60(15)
lOO(16)
94(16)
lOO(9)
lOO(9)
lOO(9)
V
Contrast
preferring indicates
96(28) 1OO(28)
20/5290 1 .I1
30% H
WO)
20/10580 1% .06
lOO(10)
Controst
Equivalent Width (in.)
TABLE
1
the
Frequency
each of the horizontally
gl(32) 55(31)
~(32)
72(29)
gt?(16) gl(16)
lOO(12) 80(15)
93(15) 46(13)
20/ I320 % .46
the grating for data set from
73(15) 86(14)
73(15) t36(14)
tll(16) 75(16)
93(14) 80(15)
94(18) Et9(18)
20/2640 % .23
Spatial
60 possible presented
69(16) 59(17)
53(17)
44(1l3)
~(29)
ww
59(29) 68(28)
66(29)
69(20)
20/650 ‘/s .92
of Infants Preferring Gratings Over a Plain at Various Spatial Frequencies and Contrasts
V
66% H
Stripe C/Des
Snellen
Percentage
64(14)
43(14)
64(14)
36(14)
54(35)
6804)
20/330 %6 1.85
conditions followed stimuli, and a “V”
Target
33(24) 25(24)
20/8 1 ‘/64 7.38
by the n of infants indicates the data set
46(13) 45(11)
20/162 !A2 3.69
54
SHEPHERD,
FAGAN,
AND
KLEINER
criterion. Instead, the last contrast tested was taken as the best estimate possible for that spatial frequency. In the figures that follow, such points are indicated by arrows in the appropriate direction. Only the five lowest frequencies tested were used to draw the contrast sensitivity functions shown in the present paper, because too little data were available for the higher frequencies. The functions for the data presented in Table 1 are shown in Fig. 1. In Fig. 1 and all of the figures to follow, the ordinate is labeled Spatial Frequency in c/deg and the abscissa is labeled Contrast Threshold on the left and Log Sensitivity on the right. All scales are log scales. As seen in Fig. l’, the horizontal and vertical functions were not very different. Acuities were extrapolated by applying linear regression on semi-log coordinates. When the data points for .92 c/deg were estimates, the acuities given were found by calculating regression lines both with and without the .92 c/deg data, resulting in a range of acuity estimates rather than a single value. For the orientation data then, the estimated acuities were .92-l .03 c/deg for the horizontal gratings and .92-l .02 c/deg for the vertical gratings. Because the data for the horizontal and vertical orientations were not different, the data were subsequently combined into one score for each infant for the second analysis. The second analysis examined the preterm neonates’ resolution of the various gratings when the horizontal and vertical data were combined into one score for each infant. The resulting data set is presented in Table 2. Note that, in comparing the data shown in Table 1 and Table 2, there appears to be some contradictions in the percentages (see, e.g., 1.85 c/deg at 38% contrast). The apparent difficulty is due to combining the horizontal and vertical preference scores from an infant into one score for a given infant. The differences between Tables 1 and 2 do not result in a change in interpretation of the data, however. .05 .06
-horizontal - - - - - -veftlcal
squarawave squarewave
1.25
gratings gratings
.06 .lO
t
Spatial
Figure 1. Preterm neonates’ tal or vertical square-wave
frequency
estimated grotings.
1.00
(cldeg)
contrast-sensitivity
functions
for
horizon-
55
SHEPHERD,
56
FAGAN.
AND
KLEINER
Overall, it appears that the infants were able to resolve the detail contained in a grating at least as fine as .46 c/deg at the highest contrast employed and that the infants were able to resolve some gratings at a contrast at least as low as 13%. An unexpected finding, that of an unusually low preference for the highest spatial-fre.quency grating presented at 66% contrast (7.4 c/deg), indicating a preference for the plain target rather than for the grating, is also seen in Table 2. A binomial test demonstrated that the infants’ preference for the plain target was statistically significant (PC .OOl). We will return to a consideration of this anomalous finding later in the Discussion section. Since one objective of the present study was to consider the infants’ responsiveness to a range of contrast and spatial frequencies, the data shown in Table 2 were used to estimate the sample’s contrast sensitivity function. The function generated from the data in Table 2 is shown in Fig. 2, which clearly demonstrates a high-frequency fall-off as the gratings become very fine and difficult to resolve. In other words, as the gratings become finer, preterm neonates need more contrast in order to resolve them, eventually reaching a frequency where no amount of contrast will allow the grating to be seen, i.e., the point of contrast is 100% and acuity is measured. Visual acuity was estimated from the function by plotting the high-frequency fall-off on a semi-logarithmic scale and extrapolating to 100% contrast. The resulting acuity estimate was .92-1.02 c/deg or a Snellen acuity estimate of approximately 20/650 to 20/586. Note that no low-frequency fall-off is evident in Fig. 2. In fact, the absolute difference between the highest point on the function and the lowest point for the low-frequency gratings is only 6% contrast. Since the data set was so large and considerable variability existed with respect to age at birth and at test, we decided to undertake several subsidiary analyses to find out if differences in responding among subsets of the infants were obscured by the pooling of all of the data. .05* .06 ..
J- 1.25
06..lO
_.
20
-.
_. 100
z 2 5 z z :,
--
.30--
.75
..
50
..
25
25 E 2 % f
” .40-.50-.60-.a0
--
1.00
7
--0.00 .05
.lO
20
Spatial Figure wave
2. Preterm grotings.
neonotes’
.30
frequency
estimated
40
.50
100
(cldeg)
contrast-sensitivity
function
for
square-
VISUAL
PATTERN
DETECTION
57
The first of the secondary analyses concerned the effect of the infants’ age at test on the measures of acuity and contrast sensitivity for the squarewave gratings. The sample of infants was therefore divided into two groups, those who were tested prior to 36 weeks postconceptional age and those who were tested after 36 weeks postconceptional age. Subjects in the former group (n =63) were tested approximately three weeks after birth (M=34 weeks, SD = 1.4 weeks). The infants had an average gestational age at birth of 3 1.1 weeks (SD= 2.3 weeks) and an average birthweight of 1593 g (SD =470 g). Eighty-nine percent were appropriate for gestational age with the remainder either small or large for gestational age (6% and 5%, respectivelyj. Subjects in the latter group (n = 121) were also tested approximately three weeks after birth (M postconceptional age at test = 39 weeks, SD = .9 weeks). The infants had an average gestational age at birth of 36.7 weeks (SD=3.5 weeks) and an average birthweight of 2674 g (SD = 826 g). Of the subjects in the latter group, 64% were appropriate for gestational age with the rest either small or large for gestational age (20% and 16070, respectively). The results of the comparison between the two groups are shown in Table 3. Overall, the performance of the youngest group of neonates was slightly poorer relative to the older subsample. This is shown graphically in Fig. 3, which presents the two estimated contrast sensitivity functions drawn from the data. The high-frequency fall-off for the younger subsample begins at a lower frequency than it does for the older subsample. Acuity was estimated from the two contrast-sensitivity functions and found to be .66-l .04 c/deg or a Snellen equivalent estimate of approximately 201920 to 20/575 for the younger infants, and 1.13 c/deg or a Snellen equivalent of approximately 20/529 for the older infants. .05 -4. .06 -.
_____
.ffl--
infants infants
>36 <36
.- 1.25
-- 1.00
.lO -. % 2 f z 5 6 0
-_ .75
JO-.30 -_
..
.m
.f p 5 ,B
.40-so -.60 --
-. .25
.60-1.00
-0.00 .OS
.lO Spatial
.20
.30
.40 .50
1.00
frequency(c/deg)
Figure 3. Estimated contrast-sensitivity functions far square-wave gratings from twa subsamples of preterm neonates. One subsample is comprised of infapts tested after.36 weeks pastconception, the second subsample includes only those neonates tested prior to 36 weeks postconception.
Contrast
Contrast
Contrast
Contrast
Etjuivalent (in.)
Width
Note. The data obtained fants tested after 36-weeks in parentheses.
<36 >36
13% Contrast
<36 >36
17%
<36 >36
22%
>36
<36
38%
>36
66% <36
C/Des
Stripe
Snellen
3
70(10) ao(20)
a3(18)
W11)
W’) w4
1w(a)
1oo(4)
71(7) 1oo(5)
20/ I320 % .46
Spatial
7)
age ore indicated The n of infants
M)(5) SO(10)
67(6) 30(10)
36(14) 92(13)
aa(i
by the participating
50(4) 57(7)
20/162 %2 3.69
2o(5) 16(19)
20/a I L 7.38
symbol “<36”: the data from inat each data point are shown
67(6) 50(a)
25(a)
3W
68(22)
50(10)
58(12)
20/330 %6 1.85
6306)
Target
67(12)
20/650 # .92
Over a Plain Contrasts
Frequency
and
to 36-weeks postconceptional indicated by the symbol ” >36:’
aw
from the infants postconceptional
6o(5)
6o(5) wa)
57(7) 1oo(9)
92(12)
low
20/2640 x .23
50(6) tested prior oge are
W) 1 wa)
w9)
1 oo(7)
1 oo(7)
1W2)
1 W9) loo(19)
20/5290 1 .II
at
TABLE of Infants Preferring Gratings Various Spatial Frequencies
1ow)
WV
71(7)
aaiai
lW2) 1W6)
lW3) 1 W5)
20/10580 1% .06
Percentage
VISUAL
PATTERN
DETECTION
59
In summary, the secondary analysis resulting from a split of the large sample into those infants tested prior to 36-weeks postconceptional ‘age and those tested after 36-weeks postconceptional age indicated slightly poorer acuity and contrast sensitivity for square-wave gratings on the part of the younger infants. The infants in the analysis differed, however, not only in age at test but also in gestational age at birth. Either variable could have accounted for the obtained differences in group performance. One way to equate two groups of infants on one of the variables was to make them equivalent for age at test and allow the gestational age at birth to vary. Thus, a subsequent analysis was done to determine if, for infants roughly equated for age at test, a difference in performance would still be discerned. Infants tested after 38 weeks postconceptional age were therefore divided into those who were born prior to 36 weeks and those born after 36 weeks. Subjects in the former group (n = 48) had an average gestational age of 32.4 weeks (SD = 3.2 weeks) at birth and were tested at an average postconceptional age of 38.3 weeks (SD= 2.1 weeks). Subjects in the latter group (n =73) had an average gestational age of 39.5 weeks (SD = 1.4 weeks) at birth and were tested at an average postconceptional age of 40.2 weeks (SD = 1.5 weeks). The difference in age at test for the two subsamples created by this split was not significant. The data obtained are shown in Table 4. Overall, the data for the two groups are highly similar and estimated contrast sensitivity functions, shown in Fig. 4, are also similar. Apparently, maturation accounts for the increased ability to see higher-frequency gratings. The estimated visual acuities for the two groups were not different at .92-1.03, or 1.05 c/deg for both. .05 J. .06 ..
____-
horizontal vertical
square-wave square-wave
gratings gratings
-- 1.25
.06-. -. l.00
.lO .. : 5 t C 1 il s 0
-- .?5 .20-.30--
.. so
li ,B
.40-SO-.60--
-. .25
.60 --
l.OO$ :
;
:
.05
.lO
.20 Spatial
Figure
4 p
4. Estimated contrast-sensitivity two subsamples of preterm neonates. to 36 weeks postconception and tested second subsample consists of infants tested after 38 weeks postconception
frequency
; : : .30
.40 so
:
)o.oo
1.00
(cldeg)
functions for square-wave gratings from One subsample includes infants born prior after 38 weeks postconception (-----); the born after 36 weeks postconception and (-1.
Contrast
Contrast
Contrast
Contrast
Frequency
‘36(7) the gratings infants born
lW2)
6X4 57(7)
lW(5)
low)
10(x4)
1 f-w)
1W1) g6(7)
75(4)
W)
50(4)
17(6)
g3(6) lOO(7)
75(4) 92(13)
Target
tested to the
O(2) W)
3.69
‘h,
20/162
by then infants age: ” >36” refers
40(5)
67(3)
O(3) 40(5)
70(10) 73(10)
1.85
‘II 6
20/330
for each of the 60 conditions, followed prior to 36 weeks postconceptional
75(B) 75(12)
89(9)
78(9)
1 OO(4)
8OW
1W1) lOO(7)
70(10)
5’W
lOO(4)
no data
.92
56
20/650
W5)
.46
%
20/ J320
Spatlaf
1W(7)
33(3)
loo($)
1 OO(3)
75(4)
1 W5)
1 OO(3) lOO(4)
1W8) lOO(11)
.23
‘h
20/2640
WV
5W)
lOO(5)
lOO(3)
‘3’35)
lOO(3) 1OO(3)
lOO(4)
1Wl)
Note. Table 4 presents the percentages of infants preferring condition in parentheses. “<36” indicates the data set from from infants born after 36 weeks postconceptional age.
c36 >36
13%
~36 >36
i7%
>36
22% ~36
~36 >36
38%
~36 >36
Controst
.JJ
.06
C/Deg
66%
1
20/5290
1 %
20/10580
TABLE 4 of Infants Preferring Gratings Over a Plain at Various Spatial Frequencies and Contrasts
Snellen Equivalent Stripe Width (in.)
Percentage
for each data set
W6) 8(12)
7.38
54
20/B J
VISUAL
PATTERN
DETECTION
61
DISCUSSION
In the present study, prematurely born neonates were tested for their ability to resolve gratings which varied in spatial frequency, contrast, and orientation. It was shown that neonates, born an average of 5.2 weeks prior to a 40-week fullterm gestation and tested an average of three weeks after birth, had a visual acuity estimate from their group contrast sensitivity function of approximately 1 .O c/deg, equivalent to a Snellen estimate of approximately 20/600. This estimate is congruent with previous studies for infants of similar ages (Miranda, 1970; Morante et al., 1982) and fits well with estimates derived for older infants (Baraldi, Ferrari, Fonda, & Penne, 1981; Dobson &Teller, 1978; Gwiazda, Brill, Mohindra, & Held, 1978). In addition, the neonates demonstrated that they could see some square-wave gratings at a contrast at least as low as 13%. The finding of differential sensitivity to contrast is in keeping with results for older infants for diverse stimuli including checkerboards (Adams, 1982), and sine-wave gratings (Atkinson et al., 1979; Banks & Salapatek, 1981). In agreement with the results of others who have examined contrast sensitivity in infants under two months of postnatal age, we did not find a low-frequency fall-off for the preterm neonates tested in the present study. Finally, it did not appear from our data that horizontal gratings were seen any better than were vertical gratings. There are two methodological issues that must be addressed. The first concerns the way some of the stimuli were produced. The 66%-contrast stimuli are not a problem, because they were mechanically produced. The remaining gratings were hand-produced, however, resulting in some variability in the width of the stripes making up the gratings, a factor which would cause some “frequency splattering” (see Fig. 14 in Banks & Salapatek, 1981). The effect of the splattering would be to overestimate the contrast sensitivity at high frequencies. The second methodological issue concerns the use of square-wave gratings to measure contrast sensitivity. Usually, contrast sensitivity is estimated not with square-wave gratings, as in the present study, but with gratings whose luminance varies sinusoidally. The effect of using square-wave gratings as ‘opposed to sine-wave gratings in adult subjects is to overestimate contrast sensitivity at intermediate and high frequencies by a small amount (27%) for most of the contrast sensitivity function and by a larger amount at very low spatial frequencies (i.e., less than 1.0 c/deg) (Campbell & Robson, 1968). Since the employment of square-wave and sine-wave gratings at low frequencies results in different estimates of contrast sensitivity, our failure to find a low-frequency fall-off using square-wave gratings is relatively uninformative. Together, these methodological issues make it reasonable to interpret the present data conservatively with respect to contrast sensitivity and expect that perhaps the estimates are somewhat higher than one would obtain from sinewave gratings. The acuity estimates may therefore also be slightly inflated. That any inflation was small, however, can be inferred from the fact that, except for the
62
SHEPHERD,
FAGAN,
AND
KLEINER
anomalous treatment of a very high-frequency grating (7.4 c/deg), the data at 66% contrast corroborate the acuity estimated from the contrast sensitivity functions. That the estimates of acuity from,fhe contrast sensitivity functions were slightly higher than those obtained from the 66%-contrast gratings is perfectly reasonable (the former estimate assumes 100% contrast) and probably accounts for the slightly higher estimates made from our data relative to others, whose estimates were apparently taken directly from their lowercontrast stimuli. Returning to the finding of a pronounced shift in the infants’ preference from grating over plain, to plain over grating at ‘the highest spatial frequency (7.38 c/deg), and contrast tested (66%) shown (e.g., in Table 2), it would be tempting to conclude that the shift reflects the detection of the very fine lines in the grating. Stimulus artifacts may, in fact, be the explanation, however, owing to the choice of “plain” comparison stimulus, in actuality a high-frequency (14 c/deg) grating. That is, the neonates may have shifted their attention to some unrecognized low-frequency information contained in the “plain” target (perhaps due to uneven distribution of ink or irregularity of lines in the grating) when they could no longer resolve the opposing grating. Given that the shift was found for only one stimulus, it probably would be wise to withhold further speculation until the finding is replicated. Posthoc analyses were also performed to see the effects of age at test and age at birth, when age at test was held constant, on contrast sensitivity and visual acuity estimates. It appeared that when the sample was divided by age at test, their contrast sensitivity and acuity was reduced for the younger -infants relative to the older infants, a finding in keeping with the apparently rapid growth of visual function in early postnatal life. However, a comparison of infants born at different gestational ages but tested at the same postconceptional age found little difference in visual function, suggesting that the visual processes tested in the present study develop somewhat independently of the environmental stimulation available at the time of birth. In sum, we have shown that preterm neonates are able to detect coarse, square-wave gratings across a limited range of contrast. The results of the present study agree with and substantially extend previous findings of vision in similar infants. The present study has several limitations, however. Unfortunately, we could test only part of the range of contrasts to which preterm neonates appear to be sensitive. Second, the use of hand-produced squarewave gratings not only adds noise to the stimuli, thus requiring that the estimates of contrast sensitivity and acuity be rather broad, but also limits the inferences that can be made about visual sensitivity for other stimuli. Third, the present study can only account for the ability of healthy, preterm neonates to see, not infants who are too sick for testing or those with suspected eye problems, because those infants were of necessity excluded from the present design. However, despite the limitations of the present work, some knowledge has been gained about how preterm neonates obtain preliminary information
VISUAL
PATTERN
DETECTION
63
through their use of vision. Future research should improve on the present study and extend the present findings in order that we might better understand the earliest functioning of the human visual system. REFERENCES Adams, R. J. (1982, March). Newborn’s detection of visual contrast. Paper presented at The International Conference on Infant Studies, Austin, TX. Atkinson, J., Braddick, O., & French, J. (1979). Contrast sensitivity of the human neonate measured by the visual evoked potential. Investigative Ophthalmology and Visual Sciences, IS, 210-213. Atkinson, J., Braddick, O., & Moar, K. (1977). Development of contrast sensitivity over the first 3 months of life in the human infant. Vision Research, 17, 1037-1044. Banks, M. S., & Salapatek, P. (1981). Infant pattern vision: A new approach based on the contrast sensitivity function. Journal of Experimental Child Psychology, 31, l-45. Banks, M. S., & Salapatek, P. (1983). Infant visual perception. In P. Mussen (Ed.), Handbook of child psychology: Vol. II. Infancy and developmental psychobiology. New York: Wiley. Baraldi, P., Ferrari, F., Fonda, S., & Penne, A. (1981). Vision in the neonate (full-term and premature): Preliminary result of the application of some testing methods. Documenta Ophthalmologica, 51, 101-112. Campbell, F. W., & Robson, J. G. (1968). Application of fourier analysis to the visibility of gratings. Journal of Physiology, 197, 551-566. Dobson, V., & Teller, D. Y. (1978). Visual acuity in human infants: A review and comparison of behavioral and electrophysiological studies. Vision Research, 18, 1469-1483. Fagan, J. F. (1970). Memory in the infant. Journal of Experimental Child Psychology, 9, 217226. Fantz, R. L., Ordy, J. M., & Udelf, M. S. (1962). Maturation of pattern vision in infants during the first 6 months. Journal of Comparative Physiological Psychology, 55, 907-917. Finney, D. J. (1971). Probit analysis (3rd ed.). Cambridge, England: Cambridge University Press. Gwiazda, J., Brill, S., Mohindra, I., & Held, R. (1978). Infant visual acuity and its meridional variation. Vision Research, I8, 1557-1564. Gwiazda, J., Brill, S., Mohindra, I., &Held, R. (1980). Preferential looking acuity in infants from two to fifty-eight weeks of age. American Journal of Optometry and Physiological Optics, 57(7), 428-432. Miranda, S. B. (1970). Visual abilities and pattern preferences ofpremature infants and full-term neonates. Journal of Experimental Child Psychology, IO, 189-205. Miranda, S. B., & Hack, M. (1979). The predictive value of neonatal visual-perceptual behavior. In T. Field, A. M. Sostek, S. Goldberg, & H. H. Shuman (Eds.), Infants born at risk. Jamaica, NY: Spectrum. Morante, A., Dubowitz, L. M. S., Levene, M., & Dubowitz, V. (1982). The development of visual function in normal and neurologically abnormal preterm and full-term infants. Developmental
Medicine
and Child
Neurology,
24, 771-784.
Slater, A., & Sykes, M. (1977). Newborn infants’ visual responses to square-wave gratings. Child Development,
48, 545-554. 22 August
1983;
Revised
29 August
1984
n
BEHAVIOR
AND
DEVELOPMENT
8,
47-63
(1985)
Visual Pattern Detection in Preterm Neonates* PATRICIA ANN SHEPHERD, JOSEPH F. FAGAN, III, AND KATHLEEN
A. KLEINER
Case Western Reserve University The purpose of the present study was to test the ability of preterm neonates to resolve square-wave gratings varying in spatial frequency, contrast, and orientation. The sample included 184 infants born prematurely at an average of 34 weeks, 6 days who were tested at a mean postconceptional age of 37 weeks, 4 days. The preferential looking procedure was employed for testing the neonates’ resolution of the gratings. Spatial frequencies included .06, .ll, .23, .46, .92, 1.85. 3.69, and 7.30 cycles/degree. Controsts were 66%. 38%. 22%. 17%. and 13%. The major results were that detection of the gratings varied as a function of contrast and spotial frequency. Higher spatial frequencies required more contrast to be resolved and, on an absolute basis, the infants were able to detect spatial frequencies OS high as .92 to 1.02 c/deg and contrast as low as 13%. Horizontal and vertical gratings did not differ in detectability. In general, the present results indicate much more refined pattern-detection capacities in the preterm neonate than has previously been demonstrated. visual
acuity
contrast
sensitivity
preterm
neonates
pattern
detection
Whether the visual system of the healthy human newborn is functional has ceased to be a subject for debate since research in recent years has conclusively demonstrated that some visual perception is present even in preterm neonates (Miranda, 1970; Morante, Dubowitz, Levene, & Dubowitz, 1982). Instead, debate now focuses on how well the human newborn can see. For the most part, work has been conducted with full-term newborns (e.g., Adams, 1982). There has been very little study of visual perception in prematurely born neonates, i.e., infants born prior to a term gestation of 38-40 weeks postconception. In the present study, therefore, we examined three aspects of the premature neonates’ visual perception: their sensitivity to contrast differences in stimuli, their ability to see fine patterns at high contrast, i.e., their visual acuity, and their ability to resolve patterns presented in either a horizontal or a vertical orientation. Visual acuity and contrast sensitivity were chosen for study because they provide a widely accepted description of visual functioning across all ages of subjects. Orientation was included as a variable simply because it was easy to obtain and would add to our information about how premature neonates perceive form. * We wish to thank Drs. Velma Dobson and Ronald Boothe for their help with data analyses in preparation of this manuscript. We are indebted to our reviewers who gave such thoughtful and extensive comments on earlier drafts of this manuscript. Requests for reprints should be made to the first author at The Child Development and Mental Retardation Center, University of Washington, WJ-10, Seattle, WA 98195. 47
48
SHEPHERD,
FAGAN.
AND
KLEINER
In an early study of infant visual perception, Fantz, Ordy, and Udelf (1962) paired high-contrast, square-wave gratings (i.e., patterns with uniform, sharply contrasting black-and-white stripes) with plain gray targets of equal luminance.’ Since infants typically prefer to look longer at patterned than at plain targets, the assumption made was that the gratings would be preferred to the unpatterned gray targets, so long as the stripes in the gratings were resolvable by the infants. The finest grating (i.e., that grating with the highest spatial frequency or number of stripes) preferred to gray was then taken to indicate the infants’ estimated level of minimum separable acuity. Since 1962, numerous studies have explored the development of minimum separable acuity in infants (e.g., Dobson & Teller, 1978; Gwiazda, Brill, Mohindra, & Held, 1978, 1980). At present, infant visual acuity is believed to improve from approximately 1 .O cycle/degree (c/deg) or a Snellen acuity of about 201600 at birth to 5.0 c/deg or a Snellen of about 20/120 at 6 months in normal, full-term infants, although some disagreement exists regarding the acuity estimates given for newborns and l-month-old infants (Banks & Salapatek, 1983; Dobson & Teller, 1978). The only data on minimum visual separable acuity that exist for newborn premature infants are two published reports (Miranda, 1970; Morante et al., 1982) and studies briefly mentioned in a chapter on neonatal visual perception (Miranda & Hack, 1979). Miranda (1970) reported that the visual acuity of infants averaging 35 weeks from conception at the time of testing was roughly the same acuity as full-term newborns, with both groups of infants resolving a vertically oriented .5 c/deg square-wave grating but not resolving a .9 c/deg grating. Morante et al. (1982) similarly reported that newborns born between 35 and 41 weeks who were tested for visual acuity within one week of birth were able to resolve vertical .5 c/deg square-wave gratings but not .9 c/deg gratings. Moreover, they found that infants younger than 35 weeks at test were only able to resolve a grating if it contained no more than .2 c/deg. Finally, Miranda and Hack (1979) commented that 30-week postconceptional-age infants whom they had tested were able to resolve gratings of .2 c/deg or less. Unfortunately, none of the studies report any details about the contrast at which acuity was tested, making it difficult to judge the accuracy and reliability of their estimates. Despite that, the studies demonstrate that visual acuity is a measurable attribute even of premature newborns, that newborns 35-41 weeks of postconceptional age can resolve gratings at least as fine as .5 c/deg, and that premature newborns younger than 35 weeks may have poorer acuity than older newborns. One purpose of the present study, therefore, was to replicate and extend the previous findings for premature neonates. ’ Gratings are typically describedin terms of their spatial frequencyand contrast. Spatial J-equency is defined asthe number of cyclescontainedin one degreeof visual angle, wherea cycle consistsof an adjacent light and dark stripe and visual angle is that formed by the grating at the eyeof the observer.Contrust is defined asthe maximum minus the minimum luminance of the grating divided by the sum of the two luminances. Contrast is thus a measureof the intensity differencesbetweenelementsip. the grating. Contrust sensifivity is defined as the reciprocalof contrast at the observer’sthreshold.
VISUAL
PATTERN
DETECTION
49
The measurement of vision is not limited to the study of responses to high-contrast stimuli, however. Measurement of sensitivity to contrast for a variety of spatial frequencies provides an improved description of the visual system because it addresses the question of the range of stimulation which can be detected visually. At high spatial frequencies, contrast sensitivity and acuity become similar so that visual acuity can be estimated from data regarding the least contrast necessary to detect a set of high spatial frequencies. In short, finding the minimun contrast that an infant requires to detect gratings of different frequencies adds considerably more information than that obtained by the measurement of visual acuity alone. In addition, contrast sensitivity has been evaluated in older infants (e.g., Atkinson, Braddick, & French, 1979; Atkinson, Braddick, & Moar, 1977; Banks & Salapatek, 1981), allowing comparisons with the present study. The function that relates the minimum contrast necessary to see a sample of different frequency gratings ranging from coarse to fine is termed a contrast sensifivify function. For the function, sensitivity to contrast is graphed as a function of spatial frequency. From work conducted with infants so far, it has been determined that young infants, 1 to. 3 months postnatal age at test, are sensitive to a much smaller range of contrasts and spatial frequencies than are adults (Banks & Salapatek, 1981, 1983), although after 2 months of postnatal age, the shapes of the contrast sensitivity functions for infants and adults are grossly similar. That is, the infants’ and adults’ contrast sensitivity functions demonstrate that intermediate frequencies require less contrast to be seen than do lower or higher frequencies, so that the resulting functions appear to have an inverted U-shape. Prior to 2 months postnatal age, however, the functions differ in that they do not show a low-frequency fall-off characteristic of the functions for older subjects, a phenomenon believed to be due to the immaturity of lateral inhibition processes in the young infants (e.g., Banks & Salapatek, 1983). To date, few reports have been presented with regard to sensitivity to contrast in infants less than 1 month old at the time of testing. The most recent report, and the one providing the best estimate of contrast sensitivity in newborns, was by Adams (1982), who found that newborns tested from 1 to 5 days postnatally were able to see checkerboard elements of .13 c/deg at 11% contrast. Adams, however, tested only one stimulus size. The present study there fore sought to estimate preterm neonates’ responsiveness to contrast for a variety of stimuli over a range of spatial frequencies. Finally, the data on the relative resolution of vertical and horizontal gratings is contradictory for older infants. Gwiazda et al. (1980) measured resolution of horizontal and vertical gratings when the gratings were paired with homogenous gray fields. They found no difference in the growth of visual acuity for the two orientations. Slater and Sykes (1977), however, found that when horizontal and vertical gratings were themselves paired with one another, a preference could be obtained for the horizontal grating which could be interpreted to mean that the horizontal grating was easier to see. Certainly, no one
50
SHEPHERD,
FAGAN,
AND
KLEINER
has reported data on preterm neonates. The present study thus compared the preterm neonates’ responses to the two stimulus orientations. In summary, few data exist with regard to vision in the premature neonate. Thus, the purpose of the present study was to measure the ability of premature neonates to resolve square-wave gratings of different spatial frequencies which varied in contrast and orientation. METHOD
Subjects The study was undertaken in the nurseries of a local hospital. The sample for the study included 184 infants who were born prior to 40 weeks gestation. The mean gestational age of the sample as estimated by a Dubowitz examination at the time of birth was 34.5 weeks (SD=4.5 weeks). At the time of testing, the infants had a mean postconceptional age (gestational age plus postnatal age) of 37.6 weeks (SD = 3.1 weeks), i.e., the infants were tested approximately 3 weeks after birth, but 2 weeks prior to the usual 40-week term of gestation. Only two of the infants had retrolental fibroplasia. No refractive errors were noted in the hospital records for any of the infants. The mean birthweight of the sample was 2317 g (SD= 1059 g). Seventy-three percent were of appropriate weight for gestational age, while the remaining infants were either small for gestational age (15%) or large for gestational age (12%). The infants in the sample were divided nearly equally between females and males (53 070and 47 % , respectively). The racial composition of the sample included 64% white and 36% black infants. Apparatus and Materials A portable visual preference apparatus similar to that shown in Fagan (1970) was used for testing the visual abilities of the preterm neonates. Essentially, the apparatus consisted of a stimulus presentation chamber which had walls on either side and above so that a minimally distracting environment was provided for testing. The inside of the chamber was painted a uniform gray and was illuminated by two 12-W incandescent bulbs which were placed out of view of the infant and aimed at the stimuli. The testing chamber also had a movable back wall which was attached at a right angle to a small floor in the test chamber, so that when the back wall was pulled away from the infant, the floor rose and prevented the infant from seeing what was happening to the back wall. In effect, the back wall and floor of the test chamber formed a pivoting unit. While the back wall was out of view of the infant, stimulus targets could be attached magnetically to the wall in either of two positions. When the back wall was returned to the view of the infant, the stimulus targets were horizontally aligned and appeared at a distance of approximately 33 cm from the infant’s eyes. The stimulus targets were approximately 30 cm apart from center to center, forming a display that was 78 ’ wide. While the stimulus targets were presented to the infant for viewing, an observer could watch the
VISUAL
PATTERN
DETECTION
51
cornea1 reflections of the targets over the pupils of the infant’s eyes through a .6 cm peephole centered between the two stimulus targets. A digital event recorder timed stimulus presentations and recorded the length of time that the targets were fixated. There were a total of 30 unique stimulus targets produced. The targets contained square-wave gratings and included 8 which were 66% contrast, 6 each at 38% and 22% contrast, and 5 each at 17% and 13% contrast, The stimuli at 66% contrast had spatial frequencies of .06, .ll, .23, .46, .92, 1.9, 3.7, and 7.4 c/deg. At 38% and 22% contrast, frequencies of .06, .ll, .23, .46, .92, and 1.9 c/deg were employed, and at 17% and 13 % contrast, frequencies of .06, .l 1, .23, .46, and .92 c/deg were used. The gratings at 66% contrast were initially mechanically produced and then lithographically reproduced. The remainder were produced by hand by combining various shades of gray (Colormatch) art papers. All contrasts were measured by focusing a spot-light photometer on the light and dark bars of each contrast grating and calculating the contrast by dividing the difference between the values by the sum of the obtained values. Regularity of the gratings was calculated by measuring the distance between stripes at at least 10 points (deemed to be places of greatest error). Overall, the lowest frequency gratings were the most regular. For example, the .23 c/deg target at 13% contrast had a SD of .005 c/deg, while the .92 c/deg target had a SD of .l c/deg. Finally, a 31st target served as the plain comparison stimulus target presented for testing with all of gratings.2 The average luminance of the gratings and the plain target was constant at 130.c/m2 The targets were circular fields 26” in diameter from the infant’s viewing distance. Each of the gratings could be placed either vertically or horizontally for a total of 60 stimulus configurations. Procedure During testing, an infant was held facing the test chamber by an assistant who sat on a chair in front of the testing chamber. An observer, watching through the peephole in the back wall of the chamber, saw the cornea1 reflections of the stimuli on the infant’s eyes and recorded the length of time that the infant fixated the two targets. The pairs of gratings and plain targets were shown to the infant for two trials of 5-s duration. The relative positions of the targets between trials were exchanged so that each target of a pair appeared on both sides of the viewing field (i.e., on the left and right of the back wall). Each infant saw an average of seven randomly ordered pairs (range = 28 pairs) during a test session. The only constraint on randomization was that an attempt was made to test every infant with the same pairs both horizontally 1 An informal pilot study employing a small number of newborns tested in the same apparatus paired a high-frequency grating (14 c/deg) with a plain gray target. The infants did not prefer one target to the other, but we felt that since the high-frequency target had been produced in a manner identical to the 66% contrast gratings, it would be the better choice for the “plain” target in the present study. Thus, the plain target referred to in the text is actually a 14 c/deg grating.
52
SHEPHERD,
FAGAN,
AND
KLEINER
and vertically. Those infants who saw fewer than seven or eight pairs did so due to fussiness or sleepiness. Because there were no systematic differences in pattern preferences as a function of number of test pairs shown, all data were included in the described analysis. Finally, four different observers collected the data in the present study. One observer collected about one third of the data, while the other three collected roughly equal amounts. RESULTS The first step in the data analysis was to determine the percentage fixation score for each target pair by each infant. The percentage fixation score for the grating in each pair was obtained by dividing the fixation time given to the grating by the total fixation time given to both members of the pair during the two test trials. Thus, each infant had one percentage fixation score for each stimulus pair with which he or she was tested. After percentage fixation scores were calculated, the percentage of infants who preferred the grating was calculated for each condition by dividing the number of infants with percentage fixation scores greater than 50% by the total number of infants tested at that condition. Since the percentage of infants preferring the gratings could vary from 0070, when no infants preferred the grating, to lOO%, when all the infants preferred the grating, it was necessary to adopt some criterion for judging when the infants were able to resolve a given grating. The criterion of 75% of infants preferring the grating was chosen for making the judgment of stimulus resolution. The next step was to estimate the reliability of the data from different observers in order to be sure an effect was not due to the presence of a particular observer. An interobserver reliability was calculated by correlating the proportion of infants who preferred the grating at each spatial frequency within a given contrast level across the different observers. The data from the observer who collected the majority of the data was compared to the pooled data from the other three observers. The obtained correlation was .79 @C .Ol). We next examined the data separately for horizontally and vertically oriented gratings by calculating the percentages of infants preferring the grating at each condition for the two orientations of the stimuli. The orientation data are, for the most part, within-subject data, since almost every infant contributed data at each orientation for each condition with which he or she was tested. The results of the analysis for the two orientations are shown in Table 1. Note that the percentages for the comparable conditions are similar for both orientations. The data were then employed to estimate contrast-sensitivity functions for the two orientations. The functions, like all of those to follow, were generated by applying a probit analysis (Finney, 1971) wherever possible to the data at each spatial frequency. When a probit analysis was not possible because all of the preference data at a given spatial frequency were either greater or less than 75070, no attempt was made to estimate the 75%
79(14)
Contrast
13%
the
93(14)
Contrast
17% H V
Note. tested from
Table 1 contains for each condition vertically presented
percqntoges in parentheses. stimuli.
33(9) 75(8)
EO(l5)
71(17)
V
H V
94(16)
80(15)
22% H
Contrast
1 @WV
of infants An “H”
87(15) 60(15)
lOO(16)
94(16)
lOO(9)
lOO(9)
lOO(9)
V
Contrast
preferring indicates
96(28) 1OO(28)
20/5290 1 .I1
30% H
WO)
20/10580 1% .06
lOO(10)
Controst
Equivalent Width (in.)
TABLE
1
the
Frequency
each of the horizontally
gl(32) 55(31)
~(32)
72(29)
gt?(16) gl(16)
lOO(12) 80(15)
93(15) 46(13)
20/ I320 % .46
the grating for data set from
73(15) 86(14)
73(15) t36(14)
tll(16) 75(16)
93(14) 80(15)
94(18) Et9(18)
20/2640 % .23
Spatial
60 possible presented
69(16) 59(17)
53(17)
44(1l3)
~(29)
ww
59(29) 68(28)
66(29)
69(20)
20/650 ‘/s .92
of Infants Preferring Gratings Over a Plain at Various Spatial Frequencies and Contrasts
V
66% H
Stripe C/Des
Snellen
Percentage
64(14)
43(14)
64(14)
36(14)
54(35)
6804)
20/330 %6 1.85
conditions followed stimuli, and a “V”
Target
33(24) 25(24)
20/8 1 ‘/64 7.38
by the n of infants indicates the data set
46(13) 45(11)
20/162 !A2 3.69
54
SHEPHERD,
FAGAN,
AND
KLEINER
criterion. Instead, the last contrast tested was taken as the best estimate possible for that spatial frequency. In the figures that follow, such points are indicated by arrows in the appropriate direction. Only the five lowest frequencies tested were used to draw the contrast sensitivity functions shown in the present paper, because too little data were available for the higher frequencies. The functions for the data presented in Table 1 are shown in Fig. 1. In Fig. 1 and all of the figures to follow, the ordinate is labeled Spatial Frequency in c/deg and the abscissa is labeled Contrast Threshold on the left and Log Sensitivity on the right. All scales are log scales. As seen in Fig. l’, the horizontal and vertical functions were not very different. Acuities were extrapolated by applying linear regression on semi-log coordinates. When the data points for .92 c/deg were estimates, the acuities given were found by calculating regression lines both with and without the .92 c/deg data, resulting in a range of acuity estimates rather than a single value. For the orientation data then, the estimated acuities were .92-l .03 c/deg for the horizontal gratings and .92-l .02 c/deg for the vertical gratings. Because the data for the horizontal and vertical orientations were not different, the data were subsequently combined into one score for each infant for the second analysis. The second analysis examined the preterm neonates’ resolution of the various gratings when the horizontal and vertical data were combined into one score for each infant. The resulting data set is presented in Table 2. Note that, in comparing the data shown in Table 1 and Table 2, there appears to be some contradictions in the percentages (see, e.g., 1.85 c/deg at 38% contrast). The apparent difficulty is due to combining the horizontal and vertical preference scores from an infant into one score for a given infant. The differences between Tables 1 and 2 do not result in a change in interpretation of the data, however. .05 .06
-horizontal - - - - - -veftlcal
squarawave squarewave
1.25
gratings gratings
.06 .lO
t
Spatial
Figure 1. Preterm neonates’ tal or vertical square-wave
frequency
estimated grotings.
1.00
(cldeg)
contrast-sensitivity
functions
for
horizon-
55
SHEPHERD,
56
FAGAN.
AND
KLEINER
Overall, it appears that the infants were able to resolve the detail contained in a grating at least as fine as .46 c/deg at the highest contrast employed and that the infants were able to resolve some gratings at a contrast at least as low as 13%. An unexpected finding, that of an unusually low preference for the highest spatial-fre.quency grating presented at 66% contrast (7.4 c/deg), indicating a preference for the plain target rather than for the grating, is also seen in Table 2. A binomial test demonstrated that the infants’ preference for the plain target was statistically significant (PC .OOl). We will return to a consideration of this anomalous finding later in the Discussion section. Since one objective of the present study was to consider the infants’ responsiveness to a range of contrast and spatial frequencies, the data shown in Table 2 were used to estimate the sample’s contrast sensitivity function. The function generated from the data in Table 2 is shown in Fig. 2, which clearly demonstrates a high-frequency fall-off as the gratings become very fine and difficult to resolve. In other words, as the gratings become finer, preterm neonates need more contrast in order to resolve them, eventually reaching a frequency where no amount of contrast will allow the grating to be seen, i.e., the point of contrast is 100% and acuity is measured. Visual acuity was estimated from the function by plotting the high-frequency fall-off on a semi-logarithmic scale and extrapolating to 100% contrast. The resulting acuity estimate was .92-1.02 c/deg or a Snellen acuity estimate of approximately 20/650 to 20/586. Note that no low-frequency fall-off is evident in Fig. 2. In fact, the absolute difference between the highest point on the function and the lowest point for the low-frequency gratings is only 6% contrast. Since the data set was so large and considerable variability existed with respect to age at birth and at test, we decided to undertake several subsidiary analyses to find out if differences in responding among subsets of the infants were obscured by the pooling of all of the data. .05* .06 ..
J- 1.25
06..lO
_.
20
-.
_. 100
z 2 5 z z :,
--
.30--
.75
..
50
..
25
25 E 2 % f
” .40-.50-.60-.a0
--
1.00
7
--0.00 .05
.lO
20
Spatial Figure wave
2. Preterm grotings.
neonotes’
.30
frequency
estimated
40
.50
100
(cldeg)
contrast-sensitivity
function
for
square-
VISUAL
PATTERN
DETECTION
57
The first of the secondary analyses concerned the effect of the infants’ age at test on the measures of acuity and contrast sensitivity for the squarewave gratings. The sample of infants was therefore divided into two groups, those who were tested prior to 36 weeks postconceptional age and those who were tested after 36 weeks postconceptional age. Subjects in the former group (n =63) were tested approximately three weeks after birth (M=34 weeks, SD = 1.4 weeks). The infants had an average gestational age at birth of 3 1.1 weeks (SD= 2.3 weeks) and an average birthweight of 1593 g (SD =470 g). Eighty-nine percent were appropriate for gestational age with the remainder either small or large for gestational age (6% and 5%, respectivelyj. Subjects in the latter group (n = 121) were also tested approximately three weeks after birth (M postconceptional age at test = 39 weeks, SD = .9 weeks). The infants had an average gestational age at birth of 36.7 weeks (SD=3.5 weeks) and an average birthweight of 2674 g (SD = 826 g). Of the subjects in the latter group, 64% were appropriate for gestational age with the rest either small or large for gestational age (20% and 16070, respectively). The results of the comparison between the two groups are shown in Table 3. Overall, the performance of the youngest group of neonates was slightly poorer relative to the older subsample. This is shown graphically in Fig. 3, which presents the two estimated contrast sensitivity functions drawn from the data. The high-frequency fall-off for the younger subsample begins at a lower frequency than it does for the older subsample. Acuity was estimated from the two contrast-sensitivity functions and found to be .66-l .04 c/deg or a Snellen equivalent estimate of approximately 201920 to 20/575 for the younger infants, and 1.13 c/deg or a Snellen equivalent of approximately 20/529 for the older infants. .05 -4. .06 -.
_____
.ffl--
infants infants
>36 <36
.- 1.25
-- 1.00
.lO -. % 2 f z 5 6 0
-_ .75
JO-.30 -_
..
.m
.f p 5 ,B
.40-so -.60 --
-. .25
.60-1.00
-0.00 .OS
.lO Spatial
.20
.30
.40 .50
1.00
frequency(c/deg)
Figure 3. Estimated contrast-sensitivity functions far square-wave gratings from twa subsamples of preterm neonates. One subsample is comprised of infapts tested after.36 weeks pastconception, the second subsample includes only those neonates tested prior to 36 weeks postconception.
Contrast
Contrast
Contrast
Contrast
Etjuivalent (in.)
Width
Note. The data obtained fants tested after 36-weeks in parentheses.
<36 >36
13% Contrast
<36 >36
17%
<36 >36
22%
>36
<36
38%
>36
66% <36
C/Des
Stripe
Snellen
3
70(10) ao(20)
a3(18)
W11)
W’) w4
1w(a)
1oo(4)
71(7) 1oo(5)
20/ I320 % .46
Spatial
7)
age ore indicated The n of infants
M)(5) SO(10)
67(6) 30(10)
36(14) 92(13)
aa(i
by the participating
50(4) 57(7)
20/162 %2 3.69
2o(5) 16(19)
20/a I L 7.38
symbol “<36”: the data from inat each data point are shown
67(6) 50(a)
25(a)
3W
68(22)
50(10)
58(12)
20/330 %6 1.85
6306)
Target
67(12)
20/650 # .92
Over a Plain Contrasts
Frequency
and
to 36-weeks postconceptional indicated by the symbol ” >36:’
aw
from the infants postconceptional
6o(5)
6o(5) wa)
57(7) 1oo(9)
92(12)
low
20/2640 x .23
50(6) tested prior oge are
W) 1 wa)
w9)
1 oo(7)
1 oo(7)
1W2)
1 W9) loo(19)
20/5290 1 .II
at
TABLE of Infants Preferring Gratings Various Spatial Frequencies
1ow)
WV
71(7)
aaiai
lW2) 1W6)
lW3) 1 W5)
20/10580 1% .06
Percentage
VISUAL
PATTERN
DETECTION
59
In summary, the secondary analysis resulting from a split of the large sample into those infants tested prior to 36-weeks postconceptional ‘age and those tested after 36-weeks postconceptional age indicated slightly poorer acuity and contrast sensitivity for square-wave gratings on the part of the younger infants. The infants in the analysis differed, however, not only in age at test but also in gestational age at birth. Either variable could have accounted for the obtained differences in group performance. One way to equate two groups of infants on one of the variables was to make them equivalent for age at test and allow the gestational age at birth to vary. Thus, a subsequent analysis was done to determine if, for infants roughly equated for age at test, a difference in performance would still be discerned. Infants tested after 38 weeks postconceptional age were therefore divided into those who were born prior to 36 weeks and those born after 36 weeks. Subjects in the former group (n = 48) had an average gestational age of 32.4 weeks (SD = 3.2 weeks) at birth and were tested at an average postconceptional age of 38.3 weeks (SD= 2.1 weeks). Subjects in the latter group (n =73) had an average gestational age of 39.5 weeks (SD = 1.4 weeks) at birth and were tested at an average postconceptional age of 40.2 weeks (SD = 1.5 weeks). The difference in age at test for the two subsamples created by this split was not significant. The data obtained are shown in Table 4. Overall, the data for the two groups are highly similar and estimated contrast sensitivity functions, shown in Fig. 4, are also similar. Apparently, maturation accounts for the increased ability to see higher-frequency gratings. The estimated visual acuities for the two groups were not different at .92-1.03, or 1.05 c/deg for both. .05 J. .06 ..
____-
horizontal vertical
square-wave square-wave
gratings gratings
-- 1.25
.06-. -. l.00
.lO .. : 5 t C 1 il s 0
-- .?5 .20-.30--
.. so
li ,B
.40-SO-.60--
-. .25
.60 --
l.OO$ :
;
:
.05
.lO
.20 Spatial
Figure
4 p
4. Estimated contrast-sensitivity two subsamples of preterm neonates. to 36 weeks postconception and tested second subsample consists of infants tested after 38 weeks postconception
frequency
; : : .30
.40 so
:
)o.oo
1.00
(cldeg)
functions for square-wave gratings from One subsample includes infants born prior after 38 weeks postconception (-----); the born after 36 weeks postconception and (-1.
Contrast
Contrast
Contrast
Contrast
Frequency
‘36(7) the gratings infants born
lW2)
6X4 57(7)
lW(5)
low)
10(x4)
1 f-w)
1W1) g6(7)
75(4)
W)
50(4)
17(6)
g3(6) lOO(7)
75(4) 92(13)
Target
tested to the
O(2) W)
3.69
‘h,
20/162
by then infants age: ” >36” refers
40(5)
67(3)
O(3) 40(5)
70(10) 73(10)
1.85
‘II 6
20/330
for each of the 60 conditions, followed prior to 36 weeks postconceptional
75(B) 75(12)
89(9)
78(9)
1 OO(4)
8OW
1W1) lOO(7)
70(10)
5’W
lOO(4)
no data
.92
56
20/650
W5)
.46
%
20/ J320
Spatlaf
1W(7)
33(3)
loo($)
1 OO(3)
75(4)
1 W5)
1 OO(3) lOO(4)
1W8) lOO(11)
.23
‘h
20/2640
WV
5W)
lOO(5)
lOO(3)
‘3’35)
lOO(3) 1OO(3)
lOO(4)
1Wl)
Note. Table 4 presents the percentages of infants preferring condition in parentheses. “<36” indicates the data set from from infants born after 36 weeks postconceptional age.
c36 >36
13%
~36 >36
i7%
>36
22% ~36
~36 >36
38%
~36 >36
Controst
.JJ
.06
C/Deg
66%
1
20/5290
1 %
20/10580
TABLE 4 of Infants Preferring Gratings Over a Plain at Various Spatial Frequencies and Contrasts
Snellen Equivalent Stripe Width (in.)
Percentage
for each data set
W6) 8(12)
7.38
54
20/B J
VISUAL
PATTERN
DETECTION
61
DISCUSSION
In the present study, prematurely born neonates were tested for their ability to resolve gratings which varied in spatial frequency, contrast, and orientation. It was shown that neonates, born an average of 5.2 weeks prior to a 40-week fullterm gestation and tested an average of three weeks after birth, had a visual acuity estimate from their group contrast sensitivity function of approximately 1 .O c/deg, equivalent to a Snellen estimate of approximately 20/600. This estimate is congruent with previous studies for infants of similar ages (Miranda, 1970; Morante et al., 1982) and fits well with estimates derived for older infants (Baraldi, Ferrari, Fonda, & Penne, 1981; Dobson &Teller, 1978; Gwiazda, Brill, Mohindra, & Held, 1978). In addition, the neonates demonstrated that they could see some square-wave gratings at a contrast at least as low as 13%. The finding of differential sensitivity to contrast is in keeping with results for older infants for diverse stimuli including checkerboards (Adams, 1982), and sine-wave gratings (Atkinson et al., 1979; Banks & Salapatek, 1981). In agreement with the results of others who have examined contrast sensitivity in infants under two months of postnatal age, we did not find a low-frequency fall-off for the preterm neonates tested in the present study. Finally, it did not appear from our data that horizontal gratings were seen any better than were vertical gratings. There are two methodological issues that must be addressed. The first concerns the way some of the stimuli were produced. The 66%-contrast stimuli are not a problem, because they were mechanically produced. The remaining gratings were hand-produced, however, resulting in some variability in the width of the stripes making up the gratings, a factor which would cause some “frequency splattering” (see Fig. 14 in Banks & Salapatek, 1981). The effect of the splattering would be to overestimate the contrast sensitivity at high frequencies. The second methodological issue concerns the use of square-wave gratings to measure contrast sensitivity. Usually, contrast sensitivity is estimated not with square-wave gratings, as in the present study, but with gratings whose luminance varies sinusoidally. The effect of using square-wave gratings as ‘opposed to sine-wave gratings in adult subjects is to overestimate contrast sensitivity at intermediate and high frequencies by a small amount (27%) for most of the contrast sensitivity function and by a larger amount at very low spatial frequencies (i.e., less than 1.0 c/deg) (Campbell & Robson, 1968). Since the employment of square-wave and sine-wave gratings at low frequencies results in different estimates of contrast sensitivity, our failure to find a low-frequency fall-off using square-wave gratings is relatively uninformative. Together, these methodological issues make it reasonable to interpret the present data conservatively with respect to contrast sensitivity and expect that perhaps the estimates are somewhat higher than one would obtain from sinewave gratings. The acuity estimates may therefore also be slightly inflated. That any inflation was small, however, can be inferred from the fact that, except for the
62
SHEPHERD,
FAGAN,
AND
KLEINER
anomalous treatment of a very high-frequency grating (7.4 c/deg), the data at 66% contrast corroborate the acuity estimated from the contrast sensitivity functions. That the estimates of acuity from,fhe contrast sensitivity functions were slightly higher than those obtained from the 66%-contrast gratings is perfectly reasonable (the former estimate assumes 100% contrast) and probably accounts for the slightly higher estimates made from our data relative to others, whose estimates were apparently taken directly from their lowercontrast stimuli. Returning to the finding of a pronounced shift in the infants’ preference from grating over plain, to plain over grating at ‘the highest spatial frequency (7.38 c/deg), and contrast tested (66%) shown (e.g., in Table 2), it would be tempting to conclude that the shift reflects the detection of the very fine lines in the grating. Stimulus artifacts may, in fact, be the explanation, however, owing to the choice of “plain” comparison stimulus, in actuality a high-frequency (14 c/deg) grating. That is, the neonates may have shifted their attention to some unrecognized low-frequency information contained in the “plain” target (perhaps due to uneven distribution of ink or irregularity of lines in the grating) when they could no longer resolve the opposing grating. Given that the shift was found for only one stimulus, it probably would be wise to withhold further speculation until the finding is replicated. Posthoc analyses were also performed to see the effects of age at test and age at birth, when age at test was held constant, on contrast sensitivity and visual acuity estimates. It appeared that when the sample was divided by age at test, their contrast sensitivity and acuity was reduced for the younger -infants relative to the older infants, a finding in keeping with the apparently rapid growth of visual function in early postnatal life. However, a comparison of infants born at different gestational ages but tested at the same postconceptional age found little difference in visual function, suggesting that the visual processes tested in the present study develop somewhat independently of the environmental stimulation available at the time of birth. In sum, we have shown that preterm neonates are able to detect coarse, square-wave gratings across a limited range of contrast. The results of the present study agree with and substantially extend previous findings of vision in similar infants. The present study has several limitations, however. Unfortunately, we could test only part of the range of contrasts to which preterm neonates appear to be sensitive. Second, the use of hand-produced squarewave gratings not only adds noise to the stimuli, thus requiring that the estimates of contrast sensitivity and acuity be rather broad, but also limits the inferences that can be made about visual sensitivity for other stimuli. Third, the present study can only account for the ability of healthy, preterm neonates to see, not infants who are too sick for testing or those with suspected eye problems, because those infants were of necessity excluded from the present design. However, despite the limitations of the present work, some knowledge has been gained about how preterm neonates obtain preliminary information
VISUAL
PATTERN
DETECTION
63
through their use of vision. Future research should improve on the present study and extend the present findings in order that we might better understand the earliest functioning of the human visual system. REFERENCES Adams, R. J. (1982, March). Newborn’s detection of visual contrast. Paper presented at The International Conference on Infant Studies, Austin, TX. Atkinson, J., Braddick, O., & French, J. (1979). Contrast sensitivity of the human neonate measured by the visual evoked potential. Investigative Ophthalmology and Visual Sciences, IS, 210-213. Atkinson, J., Braddick, O., & Moar, K. (1977). Development of contrast sensitivity over the first 3 months of life in the human infant. Vision Research, 17, 1037-1044. Banks, M. S., & Salapatek, P. (1981). Infant pattern vision: A new approach based on the contrast sensitivity function. Journal of Experimental Child Psychology, 31, l-45. Banks, M. S., & Salapatek, P. (1983). Infant visual perception. In P. Mussen (Ed.), Handbook of child psychology: Vol. II. Infancy and developmental psychobiology. New York: Wiley. Baraldi, P., Ferrari, F., Fonda, S., & Penne, A. (1981). Vision in the neonate (full-term and premature): Preliminary result of the application of some testing methods. Documenta Ophthalmologica, 51, 101-112. Campbell, F. W., & Robson, J. G. (1968). Application of fourier analysis to the visibility of gratings. Journal of Physiology, 197, 551-566. Dobson, V., & Teller, D. Y. (1978). Visual acuity in human infants: A review and comparison of behavioral and electrophysiological studies. Vision Research, 18, 1469-1483. Fagan, J. F. (1970). Memory in the infant. Journal of Experimental Child Psychology, 9, 217226. Fantz, R. L., Ordy, J. M., & Udelf, M. S. (1962). Maturation of pattern vision in infants during the first 6 months. Journal of Comparative Physiological Psychology, 55, 907-917. Finney, D. J. (1971). Probit analysis (3rd ed.). Cambridge, England: Cambridge University Press. Gwiazda, J., Brill, S., Mohindra, I., & Held, R. (1978). Infant visual acuity and its meridional variation. Vision Research, I8, 1557-1564. Gwiazda, J., Brill, S., Mohindra, I., &Held, R. (1980). Preferential looking acuity in infants from two to fifty-eight weeks of age. American Journal of Optometry and Physiological Optics, 57(7), 428-432. Miranda, S. B. (1970). Visual abilities and pattern preferences ofpremature infants and full-term neonates. Journal of Experimental Child Psychology, IO, 189-205. Miranda, S. B., & Hack, M. (1979). The predictive value of neonatal visual-perceptual behavior. In T. Field, A. M. Sostek, S. Goldberg, & H. H. Shuman (Eds.), Infants born at risk. Jamaica, NY: Spectrum. Morante, A., Dubowitz, L. M. S., Levene, M., & Dubowitz, V. (1982). The development of visual function in normal and neurologically abnormal preterm and full-term infants. Developmental
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Slater, A., & Sykes, M. (1977). Newborn infants’ visual responses to square-wave gratings. Child Development,
48, 545-554. 22 August
1983;
Revised
29 August
1984
n