Development of optical quality in the infant
monkey (Macaca nemestrina) eye
Rick A. Williams and Ronald G. Boothe
Behavioral measures of the development of spatial vision, such as contrast sensitivity and
acuity, do not distinguish between optical and neural contributions to the emergence of adult
visual sensitivity in primates. The optical contribution to visual development in monkeys was
estimated by measuring retinal image quality in the eyes of seven infant monkeys ranging in age
from 2 days to 9 months. Results from both longitudinally and cross-sectionally tested monkeys
indicate that the optics in infant monkeys are good at birth but that improvements with age can
be found. The optical modulation transfer function shows that contrast transmission through
the optics increases with age at all measurable spatial frequencies. Adult levels of optical
quality are seen by 13 weeks of age. In comparison to the large improvements found, during
development in contrast sensitivity in monkeys, the optical changes are small and probably
pose no major limit to the development of spatial vision in this species. (INVEST OPHTHALMOL
VIS Sci 21:728-736, 1981.)
Key words: modulation transfer function, retinal line spread function,
spatial frequency, contrast sensitivity, retinal image scatter,
contrast ratio, fast Fourier transform
M
ajor progress has been made in the last
few years in describing the postnatal development of acuity and contrast sensitivity in
human and monkey infants. l~3 Such behav-
From the Department of Psychology, Interdisciplinary
Vision and Ophthalmic Research Center, Regional
Primate Research Center, Seattle, Wash., and Child
Development and Mental Retardation Center, University of Washington, Seattle.
This research was supported in part by grants 1 T32
EY02031 to Davida Y. Teller, 1 R02 EY0202510 to
R. G. Boothe, RR00166 to the Regional Primate Research Center, EY01730 to the Interdisciplinary Vision and Ophthalmic Research Center, and NICHD
02274 to the Washington Regional Child Development and Mental Retardation Center.
Some of these results were previously reported at the
Annual Meeting of the Optical Society of America,
October 1980, Chicago, 111.
Submitted for publication Nov. 21, 1980.
Reprint requests: Rick A. Williams, School of Optometry, University of California, Berkeley, Calif.
94720.
728
ioral measures are of obvious usefulness, but
they do not in themselves address the question of whether changes in retinal image
quality contribute to the emergence of spatial
vision in primates.
If the contrast of a visual stimulus is reduced in passing through the eye's optics,
then optical quality could be contributing to
the limitation of visual sensitivity. Campbell
and Green4 have shown, using laser interferometry, that the adult human visual system can resolve finer gratings when the eye's
optics are not used for image formation than
when the retinal image is formed by the eye's
refractive components, thus indicating that
optical quality limits adult sensitivity to some
extent. Whether or not infant visual sensitivity is similarly affected by optical quality is
not known.
We set out to determine the quality of the
optics during development in infant macaque
monkeys, with the goal of separating the con-
0146-0404/81/110728+09$00.90/0 © 1981 Assoc. for Res. in Vis. and Ophthal., Inc.
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Volume 21
Number 5
Optical quality in infant monkeys
729
84 CM
A3 —
—
Fig. 1. Diagram of the optical apparatus used to measure optical quality in infant monkeys.
Light from a xenon arc source (S) is focused by a condenser lens (C) onto the target slit (TS) via
a cold mirror (Ml). The target slit beam passes through photopic correction filter (PF), is
limited by aperture (Al), and is focused onto the monkeys retina with additional spectacle
lenses (LI). An artificial pupil (A2) controls the diameter of the light beam entering the eye. A
pellicle beamsplitter (P) directs the light beam reflected from the retina through lens L2. If
removable mirror M2 is in place, mirror M4 and lens L3 provide a virtual image of the
monkey's retina through aperture A3. This channel provides the experimenter with an
ophthalmoscopic view of the animal's retina and the target slit image. When mirror M2 is
removed, a real image of the retinal image of the target slit is formed in the plane of the
analyzing slit (AS) via mirror M3. Mirror M3, mounted on the shaft of a pen motor, sweeps the
aerial image across the slit, while the output of a photomultiplier (PM) is sampled by a
computer.
tributions of optical factors from those of neural factors toward the development of acuity
and contrast sensitivity in these animals.
Estimates of retinal image quality were obtained in infant monkeys (Macaca nemestrina) ranging in age from 2 days to 9 months.
Two main points emerge from our results. (1)
Although optical quality is good at birth,
small age changes are present, and adultlike
optics do not emerge until several weeks
after birth. (2) Optical development seems to
precede neural development by such a large
factor that the quality of the retinal image is
probably good enough to support the level of
neural processing available at all stages of development. Thus the improvements in optical quality during development probably
have little effect on measured acuity or contrast sensitivity.
Methods
We estimated retinal image quality in monkeys
using the double-pass ophthalmoscopic technique
that has been used previously to measure optical
quality in human eyes 3 and cat eyes. 6 The assumptions and limitations of this method have
been thoroughly discussed by others. 5 ' 6 Our optical system is diagrammed in Fig. 1.
A target slit (0.2 min arc wide by 35 min arc
long) illuminated with white light from a 150 W
xenon arc source is imaged on the retina by the
optics of the eye. A small fraction of the image
light is reflected from the retina back through the
eyes optics. With a pellicle beamsplitter and converging lens, an aerial image of the light distribution on the retina is focused in the plane of an
analyzing slit (0.6 min arc wide by 35 min arc long)
after reflection from the sweep mirror, M3. Since
the amount of light reflected out of the eye is extremely small, an averaging technique is needed
to produce a reliable aerial image luminance
profile. We used the small mirror, M3, mounted
on the shaft of a pen motor to sweep the image
repeatedly across the analyzing slit. The motor
was driven by the digital-to-analog output of a
PDP 11/10 computer.
The signal from a photomultiplier mounted directly behind the slit was sampled by the com-
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Invest. Ophthalmol. Vis. Sci.
November 1981
730 Williams and Boothe
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Fig. 2. Data analysis sequence, a, Averaged aerial image luminance profile (200 sweeps),
2-month-old monkey, 4 mm artificial pupil. Luminance is normalized to unity at the peak of
the function. Data are sampled at intervals of 0.12 min arc. b, Optical MTF derived (as
described in text) from data of a. Amplitude of the MTF is normalized to unity at zero
frequency. Linear truncation through high-frequency noise region is shown as dashed portion
of the MTF. c, Retinal LSF resulting from inverse FFT of function in b. Luminance is
normalized to unity at the peak of the LSF. Data points are shown at intervals of 0.24 min arc.
puter 1024 times within each 2-degree sweep of
the mirror. Each sweep took about 0.5 sec to
complete, so that a typical 100-sweep data record
required about 1 min of averaging time. A photopic correction filter was inserted in the light
beam to reduce the intensity at wavelengths outside the visible spectrum. Calibration of the optical system with a first-surface mirror in place of
the eye yielded significant power in the frequency
spectrum at 110 cycles/degree. The measurements were nonetheless corrected for the
finite widths of the target and analyzing slits, as
discussed below.
Mirror M2 in Fig. 1 is movable and can be
swung into the light path so that an ophthalmoscopic view of the retinal image is provided at
aperture A3, via mirror M4 and lens L3. This
channel is used by the experimenter to initially
position and focus the slit image on the retina. The
mirror is moved out of the light path during data
recording.
In order to record line spread profiles the monkeys were first anesthetized (ketamine, intramuscularly), and in most cases their eye movements
were paralyzed with a retrobulbar block (0.05 ml
of lidocaine [Xylocaine; Astra Pharm. Products,
Inc., Worcester, Mass.]). A clear, zero-power contact lens of appropriate base curvature was fitted
to the cornea of the eye being studied. The animal
was secured in a restraining chair, and its head was
positioned so that the target light entered the eye
through the approximate center of the dilated
pupil. Three drops of a 1% solution of cyclopentolate (Cyclogyl; Alcon Laboratories, Inc., Ft.
Worth, Texas), administered topically to the eye 5
min apart, paralyzed accommodation and dilated
the pupil. An artificial pupil placed in front of the
eye, approximately 3 to 5 mm from the corneal
pole, acted to restrict target light to a paraxial
area. The displacement of the pupil from the corneal pole increases the size of the exit pupil, so
that our results cannot be directly compared to
those of studies in which the pupil was placed on
the contact lens. However, as the results show,
our modulation transfer functions (MTFs) for older
monkeys were very similar to adult human MTFs
measured under nearly identical experimental
conditions.5
Viewing the retinal image through the ophthalmoscope channel of the optical system (Fig. 1),
we could achieve a well-focused retinal image by
placing trial lenses of various power just in front of
the monkey's eye until a sharp image of the slit
was observed. Focus was further optimized by recording line spreads for a series of lenses differing
by 0.25 diopters until an objective optimum was
found.
Application of the contact lens will reduce substantially any corneal astigmatism which might be
present. At the same time, we are paralyzing ac-
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Volume 21
Number 5
commodation and artificially inducing a focused
retinal image with external lenses. Therefore the
presence of astigmatism and the accuracy of accommodation in infant monkeys in the normal
awake state are factors that we have intentionally
eliminated from our analysis. The incidence and
amount of astigmatism as well as the accommodative response in infant monkeys are not known
at present. Their effects on image quality during behavioral testing of vision should be investigated.
If the monkey retina approximates a diffusing
screen in its reflecting properties, as is the case in
humans and cats,5"(i then the MTF can be derived
from the Fourier transform of the aerial line
spread image profile. The raw data plots in Fig. 2
illustrate the sequence of data analysis. The plot in
Fig. 2, a, is an averaged aerial image luminance
profile measured from the eye of a 2-month-old
monkey with a 4 mm artificial pupil. These data
were first digitally smoothed to reduce the obvious
high-frequency photomultiplier noise. From the
numerous line spread profiles we have analyzed,
we found that the luminance in the skirts of our
line spreads decays as l/(x3/2) beyond about
x = 0.25 degrees from the image center. By extrapolating the aerial line spread using this function beyond 0.25 degrees, we could further improve the signal-to-noise ratio in the data without
altering the form of either the aerial image or the
computed MTF. 7
The smoothed, extrapolated aerial image data
were then Fourier transformed with a fast Fourier
transform (FFT) computer routine. The resulting
amplitude spectrum was corrected for both the
target and analyzing slit widths by dividing the
amplitude spectrum by the FFTs of the line
weighting functions of the two slits. The MTF
(Fig. 2, b) was derived by taking the square root of
this last spectrum to correct for double passage
through the eye's optics.
Before inverse transforming the MTF to generate the retinal line spread function (LSF), the
spatial frequency beyond which noise dominates
the MTF was determined as the frequency where
the MTF amplitude first falls below twice the
high-frequency (greater than 60 cycles/degree)
noise level.7 The amplitude of the MTF was assumed to fall linearly to zero above this frequency
limit at the same rate at which its amplitude was
declining just below the frequency limit. This
method of truncating the MTF resulted in a monotonically declining MTF amplitude and avoided
truncation artifacts in the inverse transform.
In Fig. 2, c, the retinal line spread function
Optical quality in infant monkeys 731
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Fig. 3. Contrast transmission of the optics for a
single infant monkey (VF) is plotted in terms of
contrast ratio (image/object) for six spatial frequencies between 1 and 32 cycles/degree. Data
points were taken from MTFs for which contrast
ratio was determined in 0.5 cycle/degree steps.
resulting from the inverse FFT of the MTF in Fig.
2, b, is depicted. This function represents the retinal light distribution that would be predicted for
the image of an infinitesimally thin, bright line
target.
Results
Seven infant monkeys were tested, four of
them longitudinally and three others at a
single age each. One of the longitudinally
tested animals, VF, was tested six times between the ages of 2 days and 13 weeks. Results obtained at three representative ages
from monkey VF are shown in Fig. 3. The
contrast ratio (image/object), i.e., the amplitude of the MTF, is plotted as a function of
spatial frequency in cycles per degree. Frequency is plotted on a Iog2 scale to show the
Downloaded From: http://arvojournals.org/pdfaccess.ashx?url=/data/journals/iovs/933099/ on 06/17/2017
Invest. Ophthalmol. Vis. Sci.
November 1981
732 Williams and Boothe
SUMMARY
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Fig. 4. Contrast transmission of the optics is
shown averaged for all infant monkeys studied
within three age groups: 1 to 2 weeks, 4 animals; 4
to 6 weeks, 4 animals; and 9 to 13 weeks, 5 animals. Some animals were tested at more than one
age. Error bars indicate ±1 S.D. of the observations within each age group.
low-frequency range in detail. The data obtained with a 6 mm pupil (Fig. 3, a) showed
consistent improvement in contrast transmission between 1 and 6 weeks, and between
6 and 13 weeks up to 32 cycles/degree. With
a 6 mm pupil, contrast transfer increased by a
factor of about 1.5 between 1 and 13 weeks at
4 cycles/degree. At 16 cycles/degree, it more
than doubled, from about 0.10 to nearly 0.25.
In Fig. 3, b, the data obtained with a 4 mm
pupil showed the same general trend.
For a 4 mm pupil (Fig. 3, b) the contrast
ratio improved, relative to the 6 mm pupil
data, over the entire spatial frequency range
at all ages. The age-related increases in con-
trast ratio are superimposed on the improvement with the smaller pupil. However,
for this smaller pupil size the decreased light
level available in the aerial image increased
the noise level, so that interpretation of agerelated changes above 16 cycles/degree is
difficult.
In order to summarize our results from all
the infant monkeys studied between 1 and 13
weeks of age, we have collapsed the MTF
results into three age groups: 1 to 2 weeks, 4
to 6 weeks, and 9 to 13 weeks. Within each
age group, the mean and standard deviation
of the amplitude of the MTF were calculated
at each of six spatial frequencies. The results
are shown in Fig. 4 for data obtained with a 6
mm pupil (Fig. 4, a) and a 4 mm pupil (Fig.
4, b). The error bars associated with each
point represent ± 1 S.D. Within age groups
the standard deviation increased from less
than 10% of the mean at low spatial frequencies to about 20% of the mean at higher frequencies. Although these individual differences in optical quality between monkeys
seem large, the same general trends as observed in the individual data of Fig. 3 were
present in the summary MTF results. Contrast transmission increased between 1 to 2
and 9 to 13 weeks of age for spatial frequencies between 1 and 32 cycles/degree, with
proportionally more improvement at higher
frequencies. The summary results for a 4 mm
pupil (Fig. 4, b) indicate that cross-sectionally among our animals, optical quality
may not have changed substantially after 6
weeks of age. However, individual animals
tested longitudinally did show improvement
between 6 and 13 weeks.
MTF data obtained from two 36-week-old
monkeys were within the range of variability
indicated by the error bars for the 13-week
curves plotted in Fig. 4. It therefore appears
that the contrast transmission characteristics
of the infant monkey eye are essentially
adultlike by about 13 weeks of age.
From the optical MTF one can derive the
retinal light distribution of any known target
light distribution. Since an infinitesimally
thin luminous line contains equal power at all
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Volume 21
Number 5
spatial frequencies, the corresponding retinal
light distribution, called the retinal LSF,
provides a fundamental description of the
optical quality of an eye. It can be shown that
the LSF is just the inverse Fourier transform
of the optical MTF.
The retinal LSFs shown in Fig. 5 for infant
VF have been derived by taking the inverse
FFT of the MTFs from which the data of Fig.
3 were taken. In Fig. 5, a, the relative illuminance in the retinal image of a thin
luminous line is plotted as a function of distance on the retina in minutes of arc of visual
angle. These data for a 6 mm artificial pupil
show that the LSF became narrower at all
illuminance levels between 1 and 13 weeks of
age.
Two parameters of the LSF are useful in
evaluating retinal image quality. The widths
of the function where relative illuminance
has fallen to 50% (L50) and 10% (L10) correspond to the sharpness of the image core and
the degree of scatter or veiling glare in the
image, respectively. From the plots in Fig. 5,
a, it appears that L10 decreased more dramatically than did L50 during the early postnatal
weeks. In Fig. 5, b, this effect is shown
quantitatively. The circles plot Li0 and the
squares plot L50 as a function of age for the 6
mm pupil data obtained from monkey VF.
The dotted lines were fit to the data points
with a least-squares criterion. The downward
trend with age evident in both the L50 and
the L10 data indicate that the major developmental changes in the optics of this monkey's eye were a decrease in the amount of
scattered light in the retinal image, with
some edge sharpening. These image changes
correspond to the general increase in contrast transmission at all spatial frequencies
that was seen in the MTF data of Fig. 3.
Retinal LSFs derived from the 4 mm pupil
data for monkey VF show age changes that
are consistent with the changes noted in the 6
mm pupil data. L10 values decreased from
about 9 min arc at 2 days of age to about 4
min arc at 13 weeks. Values for L50 decreased
only slightly between 2 days and 13 weeks of
age, from about 2 to about 1.5 min arc.
Optical quality in infant monkeys
733
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Fig. 5. a, Retinal LSFs for infant monkey VF, with
a 6 mm artificial pupil calculated by taking the
inverse FFT of the MTFs for this monkey (Fig. 3,
a). Data are normalized to unity amplitude at 0
min arc. b, Widths of the LSF at half-height (L50)
and tenth-height (L10) are plotted as a function of
age in weeks for infant VF. Dotted lines through
the data were fits from a least-squares criterion.
Discussion
The developmental changes in optical quality evident in our data are small. As early as 2
days after birth the cutoff frequency of the
MTF is greater than 32 cycles/degree. Given
this quantitative evidence of excellent optical
quality in newborn monkeys, the optical contribution to the development of spatial vision
can be evaluated. Recent behavioral measures of contrast sensitivity and acuity in
monkeys during the early postnatal weeks 3
indicate that behavioral cutoff frequency may
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Invest. Ophthalmol. Vis. Sci.
November 1981
734 Williams and Boothe
Behavioral CSF = optical MTF X neural CSF
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Fig. 6. a, Optical MTF data replotted from Fig. 3
on log-log axes to facilitate comparison with behavioral contrast sensitivity', b, Evaluation of the optical contribution to the development of behavioral
contrast sensitivity in infant monkeys. Behavioral
CSFs were obtained from one infant monkey at 5
and 13 weeks of age; optical MTFs from a different
infant monkey obtained at 5 and 13 weeks of age
were used to calculate retinal contrast at behavioral threshold; the two were used to plot the estimated curves for contrast sensitivity of the neural
visual system.
be substantially lower than the optical cutoff
that we have measured at corresponding
ages. Therefore optical quality probably
poses no major limit to behaviorally measured spatial vision during infancy. The optical MTFs and behavioral contrast sensitivity
functions (CSFs) shown in Fig. 6 illustrate
this point.
In the spatial frequency domain, optical
and neural components of the behavioral
CSF are related by multiplication:
The optical contribution to the development
of the behavioral CSF can be factored out to
yield an estimate of the neural developmental components. Since optical and behavioral
data are not available for the same monkey,
we have assumed that general trends in both
optical and behavioral development do not
vary substantially between animals. The behavioral data used in the analysis shown in
Fig. 6 are from an infant monkey whose contrast sensitivity development proceeded at
the most advanced rate of any animal tested
to date in our laboratory.3 Thus any optical
limitation of behaviorally measured spatial
vision during development would be most
evident for the data of this animal.
In Fig. 6, a, optical MTF data for infant VF
are replotted from Fig. 3 on log-log axes to
facilitate comparison with contrast sensitivity
results (Fig. 6, b), which are usually plotted
in terms of log contrast sensitivity as a function of log spatial frequency. For the optical
data this produces an apparent reduction in
low-spatial-frequency age-changes relative
to high-frequency changes in contrast ratio.
The behavioral CSFs shown in Fig. 6, b, as
the solid curves fit through the data points
were obtained from another infant monkey,
with the use of an operant forced-choice pattern discrimination technique that has been
described previously.3' 8 The dashed curves
were generated by correcting the threshold
contrast values for the contrast attenuation of
the optics, as described above. These curves
plot the reciprocal of retinal contrast at
threshold as a function of spatial frequency
and therefore represent the estimated contrast sensitivity of the neural visual system.
These results suggest that optical contributions are relatively unimportant to the
development of spatial vision. The optical
changes between 6 and 13 weeks are minor
compared to the large changes in behavioral
and neural contrast sensitivity that take place
between 5 and 13 weeks. Furthermore, at 5
weeks the difference between the behavioral
and neural CSFs, i.e., the optical contribution, is particularly small. At this early age
the visual system is sensitive only to very low
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Volume 21
Number 5
spatial frequencies, where optical demodulation is smallest. At 13 weeks the optical contribution is larger, but this is primarily due to
the shift of the CSF to a higher spatial frequency range, where optical attenuation increases markedly with frequency. Thus, although the optical MTF changes postnatally,
the magnitude of optical development is
small relative to the developmental changes
observed in the behavioral and neural CSFs.
The parallel changes in the neural and behavioral CSFs between 5 and 13 weeks of age
indicate that changes in neural information
processing are primarily responsible for the
changes in the form taken by the behavioral
CSF throughout development.
In making these comparisons between optical and behavioral data, we are assuming
comparable spectral composition in the retinal light distributions of the optical slit and
sinusoidal gratings. The P31 phosphor of the
cathode ray tube (CRT) used to generate the
gratings for the behavioral experiment peaks
near 530 nm. The yellow photopic filter used
in the MTF optical system brings the spectral
response of the optical apparatus near the
photopic spectral sensitivity curve, which
peaks near 550 nm. Thus the situation in the
optical experiments mimics as closely as possible the spectral composition of visual targets to which a monkey eye might normally
be exposed, including the CRT.
We have also assumed comparable pupil
size during the behavioral and optical experiments. Under the stimulus conditions of the
behavioral experiment, the monkeys view
the display with natural pupils of between 5
and 6 mm diameter. The optical data used in
the analysis depicted in Fig. 6 were obtained
with a 6 mm artificial pupil.
Other optical factors, ones which we have
not addressed in the present study, may also
contribute to the development of behavioral
CSFs and visual acuity. We have been extremely careful to ensure well-focused retinal
images in our evaluation of optical quality.
However, if the accommodative system of an
infant is not functioning to achieve optimal
retinal image focus during development,
then defocus could affect a behaviorally measured acuity value. More evidence regarding
Optical quality in infant monkeys 735
accommodation in infant monkeys9 and quantitative study of the effects on the retinal
image of varying amounts of defocus are
needed before complete identification of optical factors in the development of spatial vision can be achieved.
Another physical factor which should be
considered is the fact that the eye grows in
size during development. For M. nemestrina
monkeys the axial length increases from
about 14 mm at birth to about 20 mm in the
adult (F. A. Young, personal communication). The retinal image is therefore increasing in size during the same period that contrast sensitivity and optical quality are improving. Over the age range covered by our
optical quality measurements, the retinal
image changed from about 0.21 to about 0.24
mm/degree, based on changes in the posterior nodal distance. If one were to plot both
MTF and CSF data in terms of cycles per
millimeter rather than cycles per degree, this
increase in retinal image size would not substantially change the impact of the curves
shown in Fig. 6.
Our results represent the "worst case" estimate of infant monkey optical quality. Measurements obtained with another technique
that might avoid the troublesome assumptions of perfect reversibility of the optics and
diffuse reflection from the retina may yield
better optical quality estimates. However,
the technique used here is totally noninvasive and allows longitudinal study of a single
animal.
In another sense, the double-pass method
may underestimate the amount of scattered
light present in the retinal image as a result of
the vignetting effect of the pupil as the
reflected light leaves the eye.7 Our measurements in monkeys indicate that the
amount of scatter is small and decreases over
the first few weeks of life, so that the error in
our estimates is likely to be small. In order to
settle this issue, however, direct measurements of optical scatter in the monkey eye
are needed.
In summary, the present data strongly
suggest that although small developmental
changes in optical quality can be found in
infant M. nemestrina monkeys over the early
Downloaded From: http://arvojournals.org/pdfaccess.ashx?url=/data/journals/iovs/933099/ on 06/17/2017
Invest. Ophthalmol. Vis. Sci.
November 1981
736 Williams and Boothe
postnatal weeks, optical quality is not a major
limiting factor in the spatial vision of these
infants. Previous studies have established a
striking similarity in the time course of visual
development in human and macaque monkey
infants1' 2 and strong similarities in visual
sensitivity in adults of the two species.8' 10
These results, together with the present optical data, suggest that in humans as well as
monkeys, neural rather than optical factors
probably provide the major limitations to
spatial vision in infancy.
We thank Ralph Tigre for construction of optical and
electronic components of the apparatus; Gerald Ruppenthal, Dr. W. M. Morton, and Larene Kuller for continued assistance with the monkeys and their survival;
A. B. Bonds for valuable discussions on problems of
measuring optical quality in monkeys; Davida Teller,
Marty Banks, A. B. Bonds, and Howard Howland for
helpful comments on the manuscript; and Marjorie
Zachow for secretarial assistance.
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REFERENCES
1. Dobson V and Teller DY: Visual acuity in human
infants: a review and comparison of behavioral and
electrophysiological studies. Vision Res 18:1469,
1978.
Teller DY and Boothe RG: Development of vision in
infant primates. Trans Ophthalmol Soc UK 99:333,
1979.
Boothe RG, Williams RA, Kiorpes L, and Teller DY:
Development of contrast sensitivity in infant Macaca
nemestrina monkeys. Science 208:1290, 1980.
Campbell FW and Green DG: Optical and retinal
factors affecting visual resolution. J Physiol 181:576,
1965.
Campbell FW and Gubisch RW: Optical quality of
the human eye. J Physiol 186:558, 1966.
Bonds AB: Optical quality of the living cat eye. J
Physiol 243:777, 1974.
Robson JG and Enroth-Cugell C: Light distribution
in the cat's retinal image. Vision Res 18:159, 1978.
Williams RA, Boothe RG, Kioipes L, and Teller DY:
Oblique effects in normally reared monkeys (Macaca
nemestrina): meridional variations in contrast sensitivity measured with operant techniques. Vision
Res (in press).
Banks MS: The development of visual accommodation during early infancy. Child Dev 51:646, 1980.
DeValois R, Morgan H, and Snodderly D: Psychophysical studies of monkey vision III. Spatial
luminance contrast sensitivity tests of macaque and
human observers. Vision Res. 14:75, 1974.
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