with early age-related macular changes

Smithet al.
Vol. 5, No. 12/December 1988/J. Opt. Soc. Am. A
2113
Color matching and the Stiles-Crawford effect in observers
with early age-related macular changes
Vivianne C. Smith, Joel Pokorny, and Kenneth R. Diddie*
Eye Research Laboratories, The University of Chicago, 939 East 57th Street, Chicago, Illinois 60637
Received April 4, 1988; accepted July 29, 1988
We studied the color-match-area effect and the Stiles-Crawford effect in 10 observers with age-related macular
changes.
Observers were graded on a scale of I to IV according to the Sarks classification, which correlates fundus
appearance and visual acuity with the severity of postmortem histological changes in Bruch's membrane. Observers in group II showed subtle abnormalities of color matching; those in groups III and IV showed more-severe
abnormalities. The Stiles-Crawford effect was abnormal in 9 of 10 eyes tested. Only one observer showed a Stiles-
Crawford effect that had a well-defined peak near the center of the pupil and a near-normal bandpass. The results
suggest that early age-related changes visible in the fundus can be revealed by psychophysical tests of photoreceptor
architecture.
INTRODUCTION
The retinal effects of the aging process become clinically
important as early as the sixth decade. The initial signs are
of a pigmentary disturbance deep in the retina that reflects
hyalinization and thickening of Bruch's membrane.' In
age-related macular degeneration, these changes progress in
one of two typical ways: (1) to senile disciform degeneration
of the retina or (2) to geographic atrophy. Either change
may cause severe reduction of central vision and obliteration
of the overlying sensory retina.
In a clinicopathologic study of 378 eyes, Sarks 2 correlated
fundus appearance during life with the postmortem histological appearance of the pigment epithelium (Table 1).
The clinical sample was from 216 patients ranging in age
from 43 to 97 years. All were patients admitted for long-
term care. Patients with eye diseases including degenerative myopia, retinal vascular disease, and advanced glaucoma were excluded, as were patients for whom an adequate
view of the macula had not been obtained. Sarks noted that
the appearance of the macula ranged from normal to the late
manifestations of age-related macular degeneration (AMD).
In the postmortem material, the earliest evidence of a distur-
degeneration. In addition to the pigment epithelial alterations emphasized by Sarks, there is mounting evidence
(reviewed in Ref. 3) of foveal photoreceptor
age.
dropout with
Our study was designed to investigate the function of the
visual photoreceptors
in observers with age-related changes
and normal or near-normal visual acuity, i.e.,observers within Sarks's grades I-IV who might be judged to be normal for
age or to have early AMD.
We chose two psychophysical
tests, one involving color matching and the other involving
the Stiles-Crawford effect, that were shown4 to be sensitive
to retinal disease and thus to the types of change described
by Sarks to accompany aging. One of the authors, an ophthalmologist, graded each observer according to the Sarks
classification. This grading was performed independently
of the psychophysical testing and without knowledge of the
psychophysical results. The question that we wished to
address was whether we could measure changes in photore-
ceptor function that would mirror the age-related changes in
Bruch's membrane that were postulated by Sarks.
METHODS
bance of Bruch's membrane was an accumulation of a granu-
lar deposit at the base of the cells, which Sarks termed a
"basal linear deposit." The thickness of this deposit was the
feature that was both the most reliable histological criterion
and the best predictor of the clinical findings. For example,
Apparatus
in group I the histology showed no basal linear deposit in
nm in the mixture field; the test field was 589 nm. The field
luminance was -5 cd/M2. Field stops provided circular
fields subtending 30', 10, 20, 40, and 8°.
To measure the Stiles-Crawford effect we used a twochannel apparatus that was described previously.7 The apparatus permits measurement of the Stiles-Crawford effect
with a 620-nm monochromatic center-annulus brightnessmatching procedure. The annulus, subtending 30 38' with a
Bruch's membrane. The group I patients had visual acuities of 6/6-6/9 (Snellen notation) and, in 20% of the cases,
showed small drusen. In comparison, in group III there was
a thin, continuous basal linear deposit in Bruch's membrane.
These patients, with visual acuities of 6/9-6/24, had drusen
and fine pigment clumping. Groups V and VI represented
the late stages of geographic atrophy and disciform degeneration, respectively.
According to Sarks, 2 groups I and II
constitute the natural aging process, groups III and IV constitute the development and progression of pathologic
changes, and groups V and VI constitute the end-stages of
0740-3232/88/122113-09$02.00
For color matching we used a modified5 Moreland anomaloscope,6 providing a bipartite colorimetric field to assess the
color-match-area
effect.
We used primaries of 545 and 670
field luminance of 130 cd/m 2 , was centered on the optic axis
of the observer's pupil. The central circle, subtending 55',
was provided by a movable beam that could be shifted hori-
zontally in the plane of the observer's pupil. A neutral© 1988 Optical Society of America
2114
Table 1. Sarks Classification of Age-Related Macular
Changes"
Usual
Grade
I
II
III
IV
Histological
Visual Acuity
Description
Range
Fundus Appearance
No basal linear
deposit in Bruch's
6/6-6/9
Small drusen
(20% of cases)
6/6-6/12
Drusen (20%)
6/9-6/24
Drusen, fine
pigment clumping
(50%)
6/12-6/24
Drusen, coarse
membrane
Patchy basal
linear deposit in
Bruch's membrane
Thin continuous
basal linear deposit in Bruch's
membrane
Thick continuous
basal linear de-
pigment clumping
posit in Bruch's
membrane
V
VI
Late stage of geo-
Severely
graphic atrophy
reduced
Late stage of dis-
ciform degeneration
a
Smithet al.
J. Opt. Soc. Am. A/Vol. 5, No. 12/December 1988
Severely
reduced
Geographic atrophy
Disciform degen-
eration
See Ref. 2.
density wedge in this channel could be used to match the
brightness of the central circle to that of the annulus. Ophthalmic lenses were used to correct for off-axis aberrations.
A telescopic viewing device 8 was used to align and monitor
the position of the observer's eye throughout the course of
the experiment.
Observers
We studied 10 observers who ranged in age from 50 to 78
years. Two observers (observers 1 and 5) had responded to
an advertisement for research subjects in the University of
Chicago student newspaper. Five observers came to the
ophthalmology clinic for a routine eye examination. Two of
these observers (observers 6 and 9) had no complaints, two
(observers 3 and 10) complained of difficulty with near vision, and one (#4) complained of left-eye blurring. This
observer was noted to have left-eye punctate lenticular opac-
ities. Two of the observers came to the ophthalmology clinic with symptoms consistent with a diagnosis of AMD; one
(observer 2) reported right-eye metamorphopsia (distortion
of visual space), and the other (observer 7) reported righteye dimming. Observer 8 came on a routine visit with a
previous diagnosis of right-eye AMD. Observers 2, 7, and 8
all showed evidence of a neovascular membrane in the affected eye.
Procedure
The ophthalmologic evaluation included measurement of
the visual acuity, color screening, and ophthalmoscopy.
Fundus photography was obtained from eight observers.
Two did not return for the follow-up visit. Fluorescein
angiography was performed on the three patients who had
fundus photographs and fluorescein angiographs to give independent confirmation of the fundal abnormalities noted
in the chart and to evaluate the presence of neovascular nets
and leakage. Each patient was given a grade based on the
visual acuity and the fundus appearance, obtained from
both the notes from the chart and the evaluation of the
photographs. The grading was performed by one of the
authors (Diddie), and the result was not revealed until the
completion of the psychophysical testing. The eyes were
not graded separately; the grading reflected the overall impression. Since the age of each observer is contained in the
chart notes and Diddie had personally examined the observers, the grading was not masked to age.
The procedure for evaluation of color matching followed
published protocols.9 The Moreland anomaloscope has an
adjustable eye lens. This lens was adjusted for each observ-
er until the thin black line separating the test and mixture
fields was in best focus. If the observer could not see the
division of the bipartite field, the next largest field stop was
presented. The matching range was evaluated for each field
stop. The 2° field was tested first, followed by the 1°, 30',
40, and 8° fields. Both eyeswere tested. Data were reported as the logarithm of the green/red ratio (log G/R) at the
extremes of the matching range. Color-match-area effect
data were obtained from nine observers. Observer 7, a deuteranomalous trichromat, did not participate in this measurement because of his poor chromatic discrimination.
For measurement of the Stiles-Crawford effect, we used a
procedure that had been optimized for use with patients
with eye diseases.4 The pupil was dilated with 10%phenylephrine hydrochloride; an adequate pupil diameter was obtained in all cases. A bite bar was prepared by using dental
impression wax. The observer was then aligned with the
optical path. For each pupil entry position, ophthalmic
lenses were used to correct for refractive error, maintaining
the image of the center circle within the annulus. The
observer then adjusted the luminance of the center circle so
that annulus and center appeared to be a uniform light field.
The experimenters monitored the corneal reflex from the
annulus by using the telescopic viewing device, to ensure
that the same eye position was maintained
for the course of
the measurement. Measurements started on the optic axis
and moved nasally and temporally until a match could not
be made or until the center beam fell on the iris. Five
matches were made at each pupil entry position, and the
three central values were taken as the matching range. Data
were reported as the logarithm of the relative efficiency of
the central movable beam for various pupil entry positions.
Stiles-Crawford
effect measurements
were obtained from 7
of the 10 observers. Three observers did not participate:
two did not wish to perform the test, and the third broke the
neutral-density wedge drive; the data for that observer were
not usable.
RESULTS
Ophthalmologic Evaluation
The results of the ophthalmologic evaluation are summa-
been diagnosed as having early AMD to look for evidence of
rized in Table 2, in which the observers are numbered in
neovascular membranes. A retinal surgeon evaluated the
order of age. The visual acuities ranged from 6/6 to 6/18.
Smithet al.
Vol. 5, No. 12/December 1988/J. Opt. Soc. Am. A
2115
Table 2. Summary of Clinical Findings for 10 Observers
Observer
Number
Sarks Grade
1
III
IV
Sex
Age
Eye
Visual
Acuity
F
50
Left
Right
Left
Right
Left
Right
Left
Right
Left
6/6
6/6
6/6
6/6
6/9
5/6
6/9
6/6
6/6
Right
6/12
Left
Right
Left
Right
Left
6/6
6/9
6/6
5/6
6/9
DA
DA
Right
6/6
116
Left
5/6
Right
5/6
Left
6/18
Right
6/9
5
F
55
10
M
78
3
M
53
4
F
53
6
M
59
9
M
72
2
M
52
7
8
M
F
68
70
FM 100-Hue
Test Resulta
Fundus Appearance
75
149
Pigmentary changes,
drusen
Pigmentary changes
92
116
165
199
36
Pigmentary changes
(right eye)
Pigmentary changes,
drusen
Pigmentary changes,
30
116
96
punctate lenticular
opacities (left eye)
Drusen (left eye),
pigmentary changes
Pigmentary changes
Pigmentary changes,
neovascular membrane
(right eye)
Pigmentary changes,
drusen, neovascular membrane,
(right eye)
Pigmentary changes,
neovascular membrane
(right eye)
a Farnsworth-Munsell
100-huetest. DA, deuteranomalous trichromacy.
One observer (observer 7) was a deuteranomalous
trichro-
mat; the remainder had normal color vision. The results of
the Farnsworth-Munsell 100-hue test were within normal
Color Matching
The color-match-area effect results are displayed in Fig. 2, in
which the matching ranges (shown as filled rectangles) are
limits for age for the seven observers who performed this
plotted as a function of field size. A horizontal line is drawn
test.10
through the midpoint of each observer's 80 match. The
large bar at the right of each graph indicates the expected
Grade II was assigned to three observers (observers 1, 5
and 10) who showed only pigmentary changes and visual
acuities better than 6/9. Grade III was assigned to four
observers (observers 3, 4, 6, 9). These observers showed
pigmentary changes and drusen.
Their visual acuities
ranged from 6/6 to 6/12. Grade IV was assigned to three
observers (observers 2, 7, and 8). Each of these observers
had a neovascular membrane in one eye. The membrane in
the eye of observer 2 was of recent origin, and fluorescein
angiography did not reveal leakage. Both eyes showed pig-
mentary changes and drusen. For observer 7, both eyes had
many drusen; the left eye was affected more seriously than
the right eye. However, the right eye had a neovascular
membrane just inferior to the fovea, which showed minimal
population range of 80 matches in young adult observers.
We calculated this range from population studies of Rayleigh matches 10 and centered the range on the average 100
matches of young observers in our laboratory. The young
adult observer (age 20-40 years) can make color matches at
all field sizes, showing a continuous decline in log G/R. 5
Prototypical data for an adult of age 37 years are shown in
the top panel in the left-hand column of Fig. 2. There is a
minor discrimination improvement for the 80 field size, but
all the matching ranges are narrow. The size of the colormatch-area effect from 30' to 80 is 0.12 log unit for this
normal observer. The average 30'-8° color-match-area ef-
leakage on fluorescein angiography. For observer 8, there
was a previous diagnosis of AMD with neovascular mem-
fect in the 10 normal observers 5 of ages 20-40 was 0.16
[standard deviation (SD), 0.06; range, 0.10-0.28]. The average 1°-8° color match-area effect was 0.104 (SD, 0.04; range,
brane in the right eye and previous laser treatment. This
0.055-0.128). The correlation of the 30'-8° and 1°-8° color-
eye continued
match-area effects was 0.9.
to show problems; there was no sign of a
neovascular membrane in the left eye. A neovascular membrane is an immediate precursor of disciform degeneration,
The majority of the experimental observers made matches
which in an advanced stage would parallel Sarks's grade VI.
At the time of testing we judged observers 2, 7, and 8 to be
more characteristic of grade IV than of grade VI. Had we
at all field sizes. Three observers were unable to make a
color match with the 30' field, and one observer (observer 8, a
grade IV patient) could not make matches even with the 10
or 20 fields. The 80 matches of all observers were within the
graded the eyes separately, the right eye of observer 8 might
expected population range for Rayleigh matches at this field
well have been assigned to grade VI. Figure 1 shows fundus
photographs of examples of grades II-IV.
size for young adults.
The three lower panels in the left-hand column of Fig. 2
2116
J. Opt. Soc. Am. A/Vol. 5, No. 12/December 1988
Smith et al.
(a)
(c)
(b)
give data for the three observers assigned to grade II. These
color matches showed a continuous decrease in log G/R for
field sizes of 1°-8°.
However, data for the 30' field size
obtained for observers 1 and 5 were displaced toward the red
Fig. 1. Fundus photographs of selected observers as examples of
the grading system: (a) grade II, observer 5, age 55 years, right eye;
(b) grade III, observer 4, age 53 years, left eye; (c) grade IV, observer
7, age 68 years, left eye.
right eye, 0.06) and below the normal range (0.038-0.052) in
the remaining four eyes.
The panels in the middle column of Fig. 2 show data for
observers assigned to grade III. These data showed abnor-
primary and, in the case of observer 1, showed discrimination loss. A 30' match was not reported for observer 5 (left
eye). She reliably reported the mixture field to be too green
malities similar to those noted for grade II observers. The
or too red but could not find a match point. The estimated
30' match point was at the midpoint of her 2° match, suggesting a function similar in appearance to her right-eye
normal adults in five of the six eyes tested.
data. Observer 10 was unable to resolve the line separating
the bipartite field. The field appeared all one color, and we
did not attempt to assess a matching range. The 1°-8°
color-match area effect was at the low end of the normal
range for two eyes (observer 1, right eye, 0.0066; observer 10,
30' matches showed a shift to a smaller log G/R value and/or
enlarged matching widths compared with data for young
For observer 3,
the 1°-8° color-match-area effect was less than normal
(0.04) in the left eye and flat in the right eye. Observer 4
showed a 1°-8° color-match-area effect well within the normal range (left eye,0.113; right eye,0.082). For observer 10
the 1°-8° color-match-area effect was flat in the left eye and
0.02 in the right eye.
The panels in the right-hand column of Fig. 2 show data
Smithet al.
Vol. 5, No. 12/December 1988/J. Opt. Soc. Am. A
for observers assigned to grade IV. These observers each
had one eye with a neovascular membrane adjacent to the
fovea of one eye. Observer 2 showed a low-normal 1°-8°
color-match-area effect (left eye, 0.065; right eye, 0.07). The
30' matching range was displaced to larger log G/R values in
the right eye, but the left eye showed a 30'-8° color-matcharea effect of 0.08, just below the normal range. The other
two observers showed severe abnormalities
with a negative
color-match area effect. These color-matching abnormalities are typical of those seen in patients with neovascular
membranes resulting from other eye disorders.4 For observer 8 there was a discrimination loss for the 20 field, and for
observer 9 the 10 matching range was displaced to a smaller
log G/R value. Additionally, observers 7 and 8 showed evi-
dence of pseudoprotanomaly in the affected eye, results that
were consistent with the minimal leakage of dye observed on
fluorescein angiography. For observer 7, who had a neovas-
cular membrane just inferior to the fovea, pseudoprotanomaly was revealed in the match width widened to red for
the 30' target.
For observer 8, pseudoprotanomaly
was re-
vealed by the large interocular difference in the 8° matches.
The left-eye match at a log G/R value of -0.0045 was at the
green end of the population scale, consistent with the high
lens density that this 70-year-old observer had. The righteye match was at -0.1143. Although this match is within
the population range for Rayleigh matches, the interocular
difference is not.
In our experience, interocular differences
are not greater than ±0.03 in normal eyes.
In summary, none of the observers showed a color-matcharea effect typical of a young adult eye. The first abnormality was difficulty with the 30' field size,with matching ranges
displaced to smaller log G/R values. The 1°-8° colormatch-area effect was in the low-normal range. A more
severe abnormality was seen among some grade III observers, who showed a zero color-match-area effect. A negative
color-match-area effect occurred with two grade IV observers.
Stiles-Crawford Effect
The Stiles-Crawford effect data are shown in Fig. 3, in which
the logarithm of the relative luminous efficiencyis plotted as
a function of pupil entry position relative to the optic axis.
In a young adult, the function shows a well-defined peak for
a given pupil entry position, with a decrease on either side of
the peak. The function shows a 50% reduction within ±2.5
mm of its peak." The average position of the peak is at a
point 0.5 mm nasal to the optic axis, and in 90% of eyes the
peak falls within ±1.5 mm of the average.'2 Control data,
obtained by using our apparatus and identical procedures on
2117
for two observers assigned to grade III and two assigned to
grade IV. The Stiles-Crawford effect functions were qualitatively abnormal in 9 of 10 eyes. The abnormalities included enlargement of the half-height bandpass, displacement of
the maximum from the optic axis, and the appearance of
multiple subpeaks. The half-height bandwidths could not
be computed for eight eyes. For the grade II observers, the
half-height bandwidth was computed in only one of six eyes
(observer 5, 5.7 mm). All six functions did include a peak
that was near the optic axis but was accompanied by other
subpeaks. For grade III observers, the half-height bandwidths were computed for two of three eyes. The function
for observer 6 (left eye) appeared close to normal, with a
half-height bandwidth of 5.7 mm; however, the function in
the left eye was flat. Observer 4 showed a half-height band-
width of 5.7 mm (right eye), and this function showed two
distinct peaks at +1 and -2 mm from the optic axis. These
abnormalities may reflect a displacement of the peak on the
vertical axis or some random disarray of the photoreceptors.
The most-severe abnormalities occurred for observers in
grade IV, with functions that showed no defined peak within
±2 mm of the optic axis.
DISCUSSION
We believe that the abnormalities of color-matching and
Stiles-Crawford effect results that we found can be attributed to abnormalities in the orientation of the photoreceptor
layer rather than to other abnormalities that are known to
accompany aging, such as lens changes, cloudy media, and
head and eye tremor. Although a subclinical lens opacity
might alter the Stiles-Crawford function,'4 it would not
have a profound effect on the Rayleigh match or on the
color-match-area effect. An increase in the matching range
on the Rayleigh equation may be attributed to poor focus,
cloudy media, receptoral abnormality,
4
or generalized neural
discrimination loss. A shift in the midmatching point to a
smaller log G/R value, as is well known from the Von Kries
laws, is indicative of either prereceptoral or receptoral
change. Increased lens density shifts the Rayleigh equation
to larger log G/R values.' 0 A shift to a lower log G/R value
with or without an increased match width must be attributed to a change in the photopigment absorption spectrum.
In a number of studies a clear-cut correlation was demonstrated between a decrease in the log G/R value and a
decrease in the optical density of the visual photopigments. 4 "15"16 Further, it has been demonstrated
that a common cause of such decreases is photoreceptor
disorientation.4
Similarly, abnormalities of the Stiles-
seven laboratory observers ranging in age from 9 to 38 years,
were published previously. 4 All showed well-peaked func-
Crawford effect may be attributed to numerous causes, including thickening of the lens and also scatter. However,
tions with normal half-height bandwidths of 5.0-5.3 mm.
frequent abnormalities of the Stiles-Crawford effect, correlated with receptor disorientation in macular disease, were
documented in a previous study. Despite our relatively
small sample and the considerable interobserver variability
in both color-matching and Stiles-Crawford effect results,
we believe that the most economical explanation of our data
The average half-height bandwidth was 5.13 mm (SD, 0.14).
The average midpoint was 0.14 mm temporal, and all observ-
ers showed a peak within ± 1 mm of the average. These
values correspond closely to those calculated for foveal mea-
surements of other studies in the literature.' 2"13 Data from
one of our observers (age 37 years) is shown in the upper left-
hand panel of Fig. 3.
The three lower panels in the left-hand column of Fig. 3
show the Stiles-Crawford data for the observers assigned to
grade II, and the panels in the right-hand column show data
is that abnormalities of the photoreceptor layer develop in
the aging eye.
Since the original report of Stiles and Crawford in 1933,'3
there have been more than 200 papers"" 7 devoted to the
measurement and analysis of photoreceptor directional sen-
2118
J. Opt. Soc. Am. A/Vol. 5, No. 12/December 1988
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Vol. 5, No. 12/December 1988/J. Opt. Soc. Am. A
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Fig. 3. Stiles-Crawford effect functions. Log relative efficiency is plotted as a function of pupil entry position relative to the optic axis. The
top panel (two graphs per panel) in the left-hand column shows data for a young adult (37 years). The remaining panels in the left-hand
column show data for observers assigned to grade II. The panels in the right-hand column show data for observers assigned to grades III and
IV. RE, Right eye; LE, left eye.
Fig. 2 (opposite).
Color-match-area effect. Each panel shows the matching range for log G/R plotted as a function of field size. A horizontal
line is drawn through the midmatching point for the 80 field. The error bar to the right of each graph shows the spread of midmatching points
for a 2° field in 12 laboratory observers. The top panel in the left-hand column shows data for a young adult observer (age 37 years). The remaining panels in the left-hand column show data for observers assigned to grade II. The panels in the center column show data for observers
assigned to grade III; the panels in the right-hand column show data for observers assigned to grade IV. RE, Right eye; LE, left eye.
2120
J. Opt. Soc. Am. A/Vol. 5, No. 12/December 1988
sitivity. A striking feature in this literature is the paucity of
data on older observers.
There is good reason for this. The
measurements are demanding, requiring good head stabilization and the ability to yield meaningful psychophysical
data. Dental impressions are usually used as a way of stabilizing eye position; this precludes measurement for a large
proportion of observers in older age groups who have lost a
significant number of their natural teeth. Psychophysical
procedures can be demanding, requiring concentration for
an extended period of time. Spatial inhomogeneity in lens
transmission (as with the formation of a nuclear cataract'4 )
distorts the Stiles-Crawford function. Our methodology
includes the mouthbite but uses a psychophysical task,
brightness matching, that is easy to understand and for
which the observer does not feel any time pressure. After
alignment, the total time required to measure a Stiles-Crawford function is usually less than 10 min. With minimal
instruction and practice, data were collected successfully
from observers as young as 9 years of age' 8 and from 16
patients with acquired and inherited chorioretinal diseases.4
The efficacy of measurement can be shown in patients with
disease confined to or predominantly limited to one eye.
Such patients show unilateral Stiles-Crawford abnormalities. 4" 6
In distinct contrast to the difficult Stiles-Crawford measurements, color matches are relatively easy psychophysical
tasks that are suitable for use with older people. Color
matches were used previously for diverse purposes in aging
populations.' 9 -2 ' An analysis of changes in red-green color
matches that accompany photoreceptor disorientation was
given previously.4"15"16 The color-matching technique that
we used has the advantage of being insensitive to small
spatial variations in lens transmission. The major rationale
for including the Stiles-Crawford measurements is to exclude mechanisms other than photoreceptor disorientation
that may change color matches, e.g., a decrease in the path
length through the photopigment, caused by a decrease in
axial length, 22 or a photopigment kinetic defect. 23
The clinical classification was based on the Sarks 2 classifi-
cation. We found this classification relatively easy to use.
Given the limited sample, the clinical grading of each ob-
server was reflected in the severity of abnormality in the
color-match-area effect and to a lesser extent in the StilesCrawford effect. We conclude that the early age-related
changes described by Sarks 2 do have correlates in visual
function. We suggest that hyalinization of Bruch's membrane is accompanied by subtle disorientation of the photoreceptor layer. This is initially manifest in the center of the
fovea. Both the color-match-area effect and the StilesCrawford effect are sensitive tests of such early age-related
changes because both are critically dependent on the normal
architecture of the macula. 4
Other aspects of visual func-
tion, e.g., visual acuity, are not critically dependent on photoreceptor architecture.
For example, an acuity of 6/6 was
reported for 10 eyes assigned to grades II-IV. The Sarks
classification makes use of both the visual acuity and the
fundus appearance.
Following the method of Sarks, we consider the grade II
observers to be normal, grade III observers to show preclinical age changes or early age-related maculopathy, and grade
IV observers to have AMD. As noted above, we did not find
previous reports of the Stiles-Crawford effect in normal
Smith et al.
adult observers over the age of 45, but the color-match-area
effect was the topic of an extensive cross-sectional study.2 '
Eisner et al. 2 1 used rigid exclusion criteria and reported data
only for observers with a visual acuity of 6/6 or better.
Three of our grade III observers and two of our grade IV
observers would not have met their criteria. In their study,
the color-match-area effect was assessed by comparing 1.10
and 5.80 matches. Our data are consistent with their results, in which a minimal color-match-area
effect (<0.03)
was found in almost half of their observers. Since they did
not use a 30' target, they did not see the most frequent
abnormality that we noted. Our data for the grade III observers are consistent with those of other studies of early
AMD (see, for example, Refs. 24-26 and references cited
therein). In those studies a sensitivity loss in the fovea was
noted at the absolute threshold of vision for low-frequency
temporal modulation and for isolated short-wavelength-sensitive cone sensitivity.
Our data are similarly in general
agreement with the results of a previous study27 of the
Stiles-Crawford effect in patients with AMD. This report
included only two patients, one described with "essentially
normal," the other with "anomalous" (i.e., broad) StilesCrawford-effect functions.
In this paper we have avoided the question of what constitutes a normal observer. The impetus for this research was
the desire to collect control data for the color-match-area
effect on observers of ages 45 and greater for comparison
with patients referred to the Eye Research Laboratories
Ophthalmology Clinic. Of ten such observers who responded to an advertisement in the student newspaper, seven
showed abnormalities of the color-match-area effect. Two
of these seven (observers 1 and 5) were subsequently avail-
able to participate in the present study, including the StilesCrawford effect test and ophthalmologic evaluation. The
difficulty of studying visual function in older age groups is
one that has defied solution. The problem can be succinctly
stated thus: The population under study is itself changing
with age, leading to an age-cohort confound in cross-sectional studies and an age-time confound in longitudinal studies.28 In the choosing of norms, the data base depends on
the inclusion-exclusion criteria. If rigid criteria for normality are stressed, then the norms represent a different proportion of the population in each decade of age. The paradoxical situation can arise in which, for observers 80 years old or
older, a given function may seem normal (e.g., as discussed in
Ref. 29) or even to have improved, albeit few observers
satisfying the exclusion criteria can be found. If no exclu-
sion criteria are enforced, the sample is contaminated by
large and uncontrolled sources of variability. This issue was
addressed by Johnson and Choy,'30 who distinguished be-
tween whether the control population should be typical or
healthy.
In studies of the effects of aging, it is better to have
a typical population.
ACKNOWLEDGMENTS
This study was supported in part by the National Institutes
of Health under National Eye Institute research grant
EY00901 to J. Pokorny. Kenneth R. Diddie was supported
by a Heed fellowship.
Data for this study were originally
presented at the Sloan Symposium, "Visual Psychophysics
and Disorders of the Visual System," November 12-14,1981,
Vol. 5, No. 12/December 1988/J. Opt. Soc. Am. A
Smith et al.
and were scheduled to be included in the proceedings edited
by R. Massof and D. Finkelstein. Publication of this book
has been postponed indefinitely.
Crawford effect in patients with cataracts," in Digest of Topical
Meeting on Noninvasive Assessment of the Visual System (Optical Society of America, Washington, D.C., 1985), paper WA6.
15. V. C. Smith, J. Pokorny, J. T. Ernest, and S. J. Starr, "Visual
* Present address, Westside Retinal Consultants, Suite
720E, 2021 Santa Monica Boulevard, Santa Monica, California 90404.
16.
17.
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