Abstract
purpose. Poor response rates and/or the confounding of motion and offset
responses make it difficult to interpret results of previous studies of
infant hyperacuity. The aim of the present study was to design a
protocol that overcomes these limitations and to investigate the normal
maturation of hyperacuity.
methods. Hyperacuity of 31 healthy term infants aged 4 to 12 months was measured
using radial deformation of static circular D4 patterns with a
two-alternative, forced-choice, preferential-looking (FPL) protocol and
maximum likelihood threshold estimation. FPL grating resolution acuity
was assessed on the same visit.
results. Both hyperacuity and resolution acuity were 1.1 to 1.2 logMAR (12–16
minutes arc) at 4 months of age. Hyperacuity improved rapidly to
approximately 0.3 logMAR (2.0 minutes arc) by 9 to 12 months of age.
This 0.9 log unit improvement in the hyperacuity still leaves the
12-month-old infant at a level 0.4 log unit poorer than adults’
thresholds. Resolution acuity improved more gradually to approximately
0.7 logMAR (5 minutes arc) by 9 to 12 months of age. This 0.4 log unit
improvement leaves the 12-month-old infant at a level 0.6 log unit
poorer than adults’ resolution acuity.
conclusions. Hyperacuity measured via radial deformation thresholds matures very
rapidly between 4 and 6 months of age and continues to mature more
slowly throughout infancy and into early childhood. The radial
deformation protocol may provide a sensitive index for detecting and
monitoring abnormalities in spatial vision in cases of infantile
esotropia.
Strabismic amblyopia often begins during the first year of life.
However, there are currently no good quantitative methods for early
detection of strabismic amblyopia or for monitoring the effectiveness
of amblyopia treatment during infancy. Infant grating acuity test
protocols are insensitive to strabismic amblyopia; strabismic infants
with strong fixation preference consistent with amblyopia often show
little or no grating acuity deficit during the first year of
life.
1 2 3 For example, in a recent analysis of various
interocular grating acuity difference criteria for detection of
amblyopia, accurate detection of amblyopia ranged from a low of 0% to
a high of 60% for forced-choice preferential looking and swept visual
evoked potential data sets.
4 During occlusion therapy for
strabismic amblyopia, grating acuity may even show reversals, that is,
poorer preferred eye grating acuity and improved nonpreferred eye
grating acuity, which are inconsistent with fixation preference and
recognition acuity measures of amblyopia.
5 6
Adults with strabismic amblyopia show more profound impairment of
vernier acuity than grating acuity with a consequent large reduction in
the resolution/vernier ratio.
7 8 Greater impairment of
vernier acuity than grating acuity has been interpreted as evidence for
spatial undersampling and/or irregular sampling in strabismic
amblyopia.
9 10 The relatively greater impairment in
vernier than grating acuity provides a basis for the hypothesis that
vernier acuity test protocols may have higher sensitivity than
resolution acuity for detecting and monitoring spatial vision deficits
in infantile strabismic amblyopia.
Several infant vernier acuity tests have been reported in the
literature.
11 12 13 14 15 16 17 18 19 20 However, these electrophysiological and
psychophysical studies of vernier acuity in normal infants have been
limited by poor response rates and/or confounding of motion and offset
responses. In those vernier acuity protocols that used static
offsets,
11 13 14 19 20 many infants were unable to
complete the test protocol and many of those who were able to complete
testing provided low upper asymptote or a small number of trials
(yielding poorly defined psychometric functions). In an effort to
better capture the infant’s visual attention, some paradigms added
temporal jittering to the offsets.
12 15 16 17 18 19 The addition
of temporal jitter did have the intended effect of yielding higher test
success rates and better upper asymptotes for psychometric functions.
However, there remained some infants were unable to complete the test
protocol and the addition of jitter to the stimulus had the unwanted
effect of making it difficult to unambiguously interpret responses as
mediated by detection of spatial offsets rather than detection of
motion cues.
Recently, a paradigm for detection of static radial deformation of D4
(fourth derivative of a Gaussian) circular contours has been
described.
21 Adults perform this task as a hyperacuity;
for example, for a 5 c/deg peak spatial frequency D4 pattern of 0.5°
radius, the radial deformation threshold is less than 10 seconds
arc.
21 Over large ranges of D4 peak frequencies, radii,
and radial deformation frequencies, radial deformation threshold is a
constant Weber fraction of the D4 radius (∼0.3%).
21 Evidence suggests that discrimination of static radial deformation of
D4 circular contours, unlike more traditional vernier acuity tasks, is
performed as a global shape detection task.
21 22 Adults
with strabismic amblyopia show radial deformation threshold deficits in
this protocol consistent with the severe losses shown in more
traditional hyperacuity tasks.
22
The aim of the present study was to develop a protocol for evaluating
infant vernier acuity that has high response rates and is free from the
confounding effects of motion so that we can define the normal
maturation of hyperacuity during the first year of life. Our hope was
that the static radially deformed D4 patterns would be sufficiently
attractive to infants that the infants would prefer to look at them
rather than at the plain circular contours. We found a strong
preference for looking at the radially deformed D4 patterns. The
achievement of this aim is the first step toward a paradigm for the
study of the earliest stages of infantile strabismic amblyopia.
Thirty-one healthy term infants aged 4, 6, 9, or 12 months
participated. In addition, six healthy adults aged 24 to 47 years
participated to provide comparison groups. Informed consent was
obtained from one or both parents before the child’s participation.
This research protocol observed the tenets of the Declaration of
Helsinki and was approved by the Institutional Review Board of the
University of Texas Southwestern Medical Center.
A sample circular D4 stimulus pair is shown in
Figure 1 . The patterns are defined by four parameters: D4 peak spatial
frequency, radius, radial frequency, and modulation amplitude. Peak
spatial frequency, which defines the width of the circular contour, was
set to 1 c/deg to be well within the grating acuity limit for even the
youngest infants tested in the present study. Radius, which defines the
size of the circle, was set to 3°, based on pilot data from infants
that suggested that the stimuli of this size were attractive to the
infants yet could still be presented with sufficient spatial separation
on a video monitor to allow for reliable forced-choice preferential
looking responses. Radial frequency, which defines the number of
deformations present around the circumference of the pattern, was set
to 8 based on pilot data from infants that suggested that this
frequency elicited robust preferential looking responses. The peak
spatial frequency, radius, and radial deformation frequency used in the
present study are within the range over which the adult Weber fraction
is constant and 0.3% of D4 radius.
21 Mean luminance was
1.52 log cd/m
2.
On each trial the infant was presented a static circular D4
pattern deformed by radial sinusoidal modulation paired with an
undeformed static D4 pattern. When the deformation was large, infants
consistently preferred to look at the deformed circle. Radial
deformation thresholds were assessed using a 2-down-1-up staircase
forced-choice preferential looking protocol,
23 varying
modulation amplitude. An observer, who was unaware of the left-right
location of the two patterns, watched the infant and made a
forced-choice decision on each trial regarding which pattern was
preferred by the infant. When the observer indicated the decision by
joystick, the trial ended. When the deformation was large, infants
consistently preferred to look at the deformed circle. On average, a
complete staircase included 33 trials (SD = 7 trials). Thresholds
were determined by performing maximum likelihood estimation on the
staircase data sets using a three-parameter model of the psychometric
function
24 :
\[R(x){=}{\gamma}P(x){+}0.5{[}1-P(x){]}\]
in which γ is the upper asymptote of
R(
x)
and
\[P(x){=}1-2^{-(x/{\alpha})^{{\beta}}}\]
where α is threshold and β controls slope.
Grating acuity was assessed during the same visit using Teller
acuity cards and a 2-down-1-up staircase forced-choice
preferential-looking protocol.
23 Mean luminance of the
acuity cards was 1.60 log cd/m
2. Thresholds were
determined by performing maximum likelihood estimation on the staircase
data sets using a three-parameter model of the psychometric
function.
24
The success rate for the test protocol was high, with only 2
(6.5%) of 31 infants (one 4-month-old and one 12-month-old) failing to
complete both the radial deformation and grating acuity protocols.
Three typical examples of radial deformation psychometric functions are
shown in
Figure 2 . At low modulation amplitudes, infants show no consistent preference
for either pattern, and the observer’s performance is at chance level
(50% correct). At moderate modulation amplitudes, performance
increases above chance and, in general, reaches an upper asymptote of
100% correct. Overall, infant psychometric functions had high upper
asymptotes (means = 0.98, 0.98, 0.99, and 0.98 for the 4-, 6-, 9-,
and 12-month-old groups, respectively) and steep slopes (means =
20.3, 8.4, 28.3, and 14.8 for the 4-, 6-, 9-, and 12-month-old groups,
respectively).
As shown in
Figure 3 , both radial deformation and resolution thresholds were 1.1 to 1.2
logMAR (12–16 minutes arc; 6.7–8.9% D4 radius) at 4 months of age.
Radial deformation thresholds improved rapidly to approximately 0.3
logMAR (2.0 minutes arc; 1.1% D4 radius) by 9 to 12 months of age.
Although this represents 0.9 log unit improvement in the radial
deformation thresholds, 12-month-old infants still remained 0.5 log
unit poorer than adults’ thresholds (−0.2 logMAR; 0.6 minutes arc;
0.33% D4 radius). Resolution thresholds improved more gradually to
approximately 0.7 logMAR (5 minutes arc) by 9 to 12 months of age. With
this 0.4 log unit improvement in resolution thresholds, the
12-month-old infants still remain 0.6 log unit poorer than mean adult
resolution threshold (0.1 logMAR; 1.2 minutes arc).
Individual radial deformation and resolution threshold data are shown
in
Figure 4 . The youngest infants (those with the poorest resolution acuities) do
not show hyperacuity; that is, radial deformation and resolution
thresholds are comparable and fall near or above the diagonal line that
represents a resolution to radial deformation threshold ratio of 1:1.
Older infants (those with better resolution acuities) consistently show
hyperacuity; that is, radial deformation and resolution thresholds fall
below the 1:1 ratio line.
Mean resolution/radial deformation threshold ratios are shown as a
function of age in the inset of
Figure 3 . At 4 months of age, the ratio
is slightly below 1.0; that is, resolution threshold is approximately
0.5 octave better than radial deformation threshold. At 6 months of
age, the ratio is somewhat more mature, but shows further maturation
between 6 and 9 months. Although both resolution and radial deformation
thresholds continue to improve beyond 9 months of age, the
resolution/radial deformation threshold ratios of 9- and 12-month-olds
and of adults are comparable.
Infant sensitivity to radial deformation develops rapidly from 1.4
log unit poorer than adult levels at 4 months to within 0.5 log unit of
adult level by 12 months. Maturation of this form of hyperacuity is
extremely rapid between 4 and 6 months of age, improving by 0.75 log
unit during these 2 months. Evaluation of sensitivity to radial
deformation is successful in more than 90% of infants aged 4 to 12
months, is not confounded by response to offset motion, and yields
excellent discrimination performance.
A comparison with other data from recent studies of the
maturation of hyperacuity is provided in
Figure 5 . Because the absolute level of hyperacuity depends on the spatial and
temporal characteristics of the stimulus, only studies in which
adult performance was reported under the same test conditions are
included in the figure so that the data could be normalized. Although
there is some scatter in the 4-month-old data despite normalization,
the data from the present study generally agree with previous reports.
However, at 6, 9, and 12 months, the data from the present study show
substantially more mature hyperacuity than other studies have. As
previously reported by Gwiazda et al.
25 and by Carkeet et
al.,
26 it is clear that maturation is not complete
by 12 months of age and that the maturation of hyperacuity continues
beyond the first year of life.
There is some evidence that global form units like those reported by
Gallant et al.
27 28 in primate V4 may underlie sensitivity
to the radial deformation used to measure hyperacuity in the present
study. Units in this extrastriate area have large receptive fields and
are optimally responsive to stimuli with circular structure. Thus, the
radial deformation hyperacuity task used in the present study may
reflect the maturation of higher visual areas that encode global object
shape.
29 On the other hand, radial deformation thresholds
are severely disrupted by strabismic amblyopia as are more standard
offset detection measures of hyperacuity.
22 Strabismic
amblyopia is believed to have major effects in V1, including changes in
ocular preference of cells in favor of the fixating eye and reduced
binocularity.
30 31 32 Therefore, it is possible that the
elevations in radial deformation threshold observed in amblyopia may
not represent alterations in V4 function but, instead, may reflect
changes in the V1 input to the extrastriate site.
22 During
infancy, then, the critical immaturity in hyperacuity also may be in V1
even though an extrastriate area underlies performance on the radial
modulation task.
Hyperacuity measured via radial deformation thresholds matures very
rapidly between 4 and 6 months of age and continues to mature more
slowly throughout infancy and into early childhood. Because adults with
strabismic amblyopia show more profound impairment of hyperacuity than
grating, the radial deformation protocol may provide a sensitive index
for determining abnormalities in spatial vision in cases of infantile
esotropia. Moreover, it may provide a better method than grating acuity
for evaluating response to amblyopia therapy during infancy.
Software to generate static circular D4 patterns and to deform them
by radial sinusoidal modulation was provided by Hugh R. Wilson and
modified to permit two-alternative forced-choice preferential-looking
testing of infants.