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Investigative Ophthalmology & Visual Science, Vol. 30, No. 5, May 1989
Copyright © Association for Research in Vision and Ophthalmology
Optical Constancy of the Chick Lens During Pre- and
Post-Hatching Ocular Development
J. G. Sivok, L. A. Ryall, J. Weerheim, and M. C. W. Campbell
Embryonic and post-embryonic development of the ocular lens is associated with the continual production of new secondary lens fibers by the mitotic activity of equatorial epithelial cells. This continual
development affects lens size and shape and refractive index distribution. Study of embryonic lens
optical function has been largely ignored. The optical characteristics of the developing chick lens,
including paraxial and eccentric focal lengths, were measured during the embryonic period of development and up to 15 days after hatching. Measurements were made with an automated scanning laser
system in which the video image of a helium-neon laser beam refracted by an excised lens in solution is
digitized. Focal length is measured for beams moving in small steps on either side of that center.
Measurements were made on excised lenses as well as with the lens in situ within the anterior segment
of the eye. The results, collected from a study of a total of 80 lenses, indicates that embryo lenses at
6-7 days of incubation have long and very variable focal lengths. At the tenth embryo day, focal length
drops by more than one-half and focal variations, between lenses and for different beam positions
within a single lens, is reduced. Further measures for 14- and 17-day embryo lenses, as well as for
lenses from hatchling and 5-, 10- and 15-day-old chicks, indicate that there is little change in focal
length, either paraxially or for eccentric beam positions. Measures of lens size and shape from frozen
eye sections and from freshly excised lenses indicate that this focal constancy is accompanied by major
changes in lens size and shape. These results indicate that the developing chick lens may be a static
refractive feature of the developing eye. It is suggested that this focal stability simplifies the process of
emmetropization in that ocular refractive state is governed by manipulating the size and shape of only
the ocular globe. Invest Ophthalmol Vis Sci 30:967-974, 1989
The lens of the eye is a cellular structure that develops from the surface ectoderm.1'2 In all vertebrates, the lens initially forms a hollow vesicle which
is filled by the elongation of the cells of the posterior
hemisphere. The newer cells, the primary lens fibers,
are joined by new elongating cells formed around the
equator. These cells, the secondary lens fibers, produce successive layers or shells around the primary
ones.
The continual growth of the lens and the compression of older tissue toward the center results in the
formation of a lens of variable refractive index, the
center being higher than the periphery.3 This factor
has the important optical consequence of affecting
the ability of the lens to control spherical aberration.4-5
While the above developmental sequence is common to all vertebrate lenses, the size, shape and refractive index distribution of the adult lens of each
species will depend on the overall refractive plan of
the eye. Thus in aquatic species such as fish, where
the lens is the only refractive element of the eye, the
lens is usually spherical in shape and has an elevated
refractive index. The lens of terrestrial animals is
often elliptical in shape, softer in consistency and
lower in refractive index.5'6 However, among terrestrials, lens relative size and shape and consistency
may vary considerably, depending on whether the eye
is used in nocturnal or diurnal light conditions.67
Major variations in lens shape have been noted even
among fish.8 These variations in lens shape may have
dramatic effects on lens focal properties.5'9
A recent preliminary study of a limited number of
human embryo lenses suggests that the developing
human lens has an approximately constant focal
length and a minimal amount of spherical aberration.10 In view of the extensive change in size and
shape of the lens during embryo development, this
result is very surprising. The study which follows is an
effort to examine focal variation during lens development in greater detail.
From the School of Optometry, University of Waterloo, Waterloo, Ontario, Canada.
The support of the Medical Research Council of Canada and of
the Natural Sciences and Engineering Research Council of Canada
is gratefully acknowledged.
Submitted for publication: May 9, 1988; accepted October 25,
1988.
Reprint requests: J. O. Sivak, School of Optometry, University of
Waterloo, Waterloo, Ontario, Canada N2L 3G1.
967
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INVESTIGATIVE OPHTHALMOLOGY & VISUAL 5CIENCE / May 1989
0.0
2.0
4.0
6.0
8.0
10.0
Fig. 1. Sample focal
length measurements for
single lens from a 15-dayold chick. Focal length
(mm) on abcissa, eccentricity (mm) from optic axis
(0.0) on ordinate. Note
characteristic
negative
spherical aberration. Data
points (+) indicate axial
crossover point for each eccentricity.
FOCAL LENGTH (mm)
Materials and Methods
Chick embryo lenses were obtained from eggs
(Cobb Arbor Acres, New Hamburg, Ontario, Canada) incubated for specific numbers of days at a local
hatchery. The eggs were opened and the embryos
transected close to the anterior aspect of the spinal
column. Lenses were carefully removed from the
embryo eyes and placed in physiological saline. All
animal tissue used in this study was obtained in a
manner in keeping with the ARVO Resolution on the
Use of Animals in Research.
Chick lenses were also obtained from hatchling
chicks (Cobb Arbor Acres) of various ages. These
chicks were collected on the day of hatching from the
same hatchery. The chicks were housed in stainless
steel chick brooders for varying periods, up to 15
days. Brooder temperatures were kept at 32°C for the
first week and 20°C for the second week, as necessary. The chicks were fed commercial chick starter
and water ad libitum. A fluorescent light schedule of
14 hr light and 10 hr dark was maintained. Chicks
were sacrificed at 5, 10 and 15 days after hatching by
CO2 asphyxiation. Lenses were carefully removed
from the enucleated eyes and placed in physiological
saline.
The optical (focal) properties of the excised lenses
(embryo and post-hatching) were determined with an
automated laser scanner." The scanner consists of a
low-power helium-neon laser mounted on a computer-controlled X-Y table, and a television camera
with video frame digitizer. The laser is programmed
to scan across the chick lens in predetermined steps
while the digitizer determines the position of the
beam after it is refracted by the lens. In practice, the
device first locates the optical center of the lens by
locating the position of zero or minimal refraction for
both the X and Y direction. It then determines focal
lengths for beam positions on either side of the
center. Scanning step sizes of 0.05 to 0.10 mm were
used in this experiment (Fig. 1).
The principal plane is the surface of unit magnification defined by the intercept of the path of the
incoming ray with the path of the existing ray. The
focal length is measured from this intercept to the
intercept of the ray with the optic axis along a path
parallel to the optic axis. Changes in this distance
with ray eccentricity are influenced by the presence of
coma and spherical aberration, but spherical aberration is the dominant factor. Focal variations are
therefore referred to as spherical aberration.
Each lens was placed in a special lens cell on a ring
of Duxseal® (Johns-Manville, Asbestos, Quebec,
Canada), a soft pliant material used to minimize lens
damage or deformation. Each lens was maintained in
physiological saline (0.9% NaCl) in the cell i for the
duration of the scan. Lenses were scanned within 3 hr
after excision. Tests indicate little or no change in
lens focal properties or transparency for 12 hr after
being placed in saline.
To provide an overview of change in lens shape
and size during development, frozen sections were
made of two eyes of each incubation stage studied.
This involved freezing the eyes rapidly in acetone and
dry ice (-80°C) and mounting each eye in a position
appropriate for axial sectioning on a freezing microtome head. As thin sections (10-20 /urn) of the central
portion of the eye were removed, photographs were
taken of the remaining block of tissue with a singlelens reflex camera mounted above the preparation.
The photograph showing the greatest lens dimensions
(to an accuracy of ±0.025 mm) was assumed to represent an axial section of the lens. A photograph of a
millimeter rule provided the control for magnification.
As an indication of the possible effect of freezing on
lens shape and size, as well as the effect of le|ns removal from the eye on its shape, the axial and equatorial diameters of a small number of freshly excised
embryo lenses of various ages were measured with a
vernier caliper to an accuracy of ±0.05 mm.
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CHICK LENS DEVELOPMENT / Sivok er a\
No. 5
969
7 DAY CHICK EMBRYOS
Fig. 2. Average focal
lengths for 7-day-old chick
embryo lenses. Focal length
(mm) on ordinate, eccentricity from (mm) optic axis
(0.0) on abcissa. Bars denote
standard error of the mean.
-1.0
-0.3
-O'.O'
015'
DISTANCE FROM OPTIC CENTRE (mm)
For a more sensitive indication of the effect of removal of the lens on its optical properties, a limited
number of laser scans were made with the lens in
place in its suspensory apparatus. In this case the
posterior one-third of the globe was removed. The
rest of the eye was placed in a lens cell and immersed
in physiological solution. Since the refractive power
of the cornea is virtually eliminated when its external
surface is in water the refractive effect measured by
the scanner may be assumed to be that of the lens
alone.12 This procedure was used with 5- and 15-day
chicks and 17-day embryos. The procedure was not
possible for earlier embryos because of the excessive
flexibility of the developing globe.
Results
The results are based on the study of a total of 39
chick embryo lenses (6-21 days of incubation) and 22
post-hatching chick lenses (0-15 days). The lower
limit of embryo incubation age, 6 days, resulted from
difficulty experienced in handling and orienting
smaller lenses (<0.7 mm diameter) as well as to mechanical and software limits of the scanning laser
system.
At 6 and 7 days of incubation chick embryo lenses
have long and variable focal lengths (Fig. 2). This is
true both for axial and eccentric measures of focal
length. Spherical aberration, as indicated by the dif-
ference in focal length between paraxial and eccentric
lens positions, varies non-monotonically between
positive (undercorrected) and negative (overcorrected) values. This finding is probably not the result
of handling deformation since the lens at this age has
a more rigid consistency than lenses from older embryos (eg, 21 days) which show monotonic focal
length variation even though they are softer and more
difficult to handle.
After a few more days of incubation (10th day of
incubation) the chick embryo lens demonstrates a
precipitous drop in focal length (from 30-35 mm to
14 mm) as well as a much smaller variation in focal
length between lenses (Fig. 3). The variations between paraxial and eccentric focal lengths (spherical
aberration) is reduced. The aberration that exists increases continuously in the direction of negative
(overcorrected) spherical aberration. Thus eccentric
focal lengths, particularly those near the edge of the
scan are longer (about 20 mm) than near axial ones
(about 10 mm).
• • •
Lenses from 14 day, 17 day and 21 day embryos
demonstrate optical characteristics very similar to
those which have been incubated for 10 days (Fig. 4).
This is true of axial focal length, interlens focal variation and the appearance of negative spherical aberration. Paraxial focal lengths average between 12 to 14
mm while focal lengths for rays refracted by the edge
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INVESTIGATIVE OPHTHALMOLOGY & VISUAL SCIENCE / May 1989
10 DAY CHICK EMBRYOS
N=6
Fig. 3. As Figure 2for10day-old chick embryo
lenses.
-0.5
-O'.O'
0l5'
DISTANCE FROM OPTIC CENTRE (mm)
21 DAY CHICK EMBRYOS
N=7
Fig. 4. As Figure 2 for 21 day-old chick embryo
lenses.
-1.0
-0.5
-0.0
0.5
1.0
DISTANCE FROM OPTIC CENTRE (mm)
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071
CHICK LENS DEVELOPMENT / Sivok er ol
No. 5
Fig. 5. Frozen hemi-sectionsofchick embryo eyes at (A) day 7, (B)day 10, (C)day 14, (D) day 21. Note changing size and shape of the lens.
Magnification X9. The unilateral appearance of a lens in (A) is a result of the fact that the two eyes were not sectioned in the same plane.
of the lens average about 20 mm (ie, negative spherical aberration). Lenses from the eyes of chicks at
hatching as well as lenses from 5-, 10- and 15-day-old
chicks show similar characteristics (ie, paraxial focal
length, interlens focal variation and negative spherical aberration).
While the frozen sections are limited in number to
one or two eyes of each incubation age (7, 10, 14, 17
and 21 days), they clearly indicate that the developing
lens is undergoing significant change in size and
shape (Fig. 5).
As a rough comparison, the two measures, frozen
eye (frozen lens in frozen eye) and fresh lens diameters, show considerable agreement in terms of lens
size and shape (Table 1). The lens flattens considerably from the embryo age of 10 days onward. Curiously, frozen and fresh lenses appear to be rounder on
the tenth embryo day than on day 7.
Measures of lens focal length, with the lens suspensory apparatus intact, indicate that the focal length of
the excised lens is shorter in the periphery than it is
when the anterior eye is intact (Fig. 6). The difference
Table 1. Fresh lens and frozen lens dimensions. Number in brackets refers to number of lenses tested.
R = equatorial diameter/axial diameter
Fresh lens diameter (mm)
Embryo age
(days)
7
10
14
17
19
21
'
Frozen lens diameter (mm.)
Equatorial
Axial
R
Equatorial
Axial
R
1.34(3)
1.88(4)
2.25 (4)
0.62 (3)
1.24 (4)
1.40(4)
2.16
1.52
1.61
1.35(2)
1.68(1)
2.45 (2)
2.87 (2)
0.83 (2)
1.36(1)
1.45(2)
1.50(2)
1.63
1.24
1.69
1.91
3.16(4)
1.56(4)
2.02
3.30 (2)
1.73(2)
1.90
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INVESTIGATIVE OPHTHALMOLOGY & VISUAL SCIENCE / May 1989
Vol.
30
15 DAY POST HATCHING
N=g
oenudeated lens
• non-enucleated lens
E
X
o
-2.0
-1.0
-0.0
Fig. 6. Focal length measurements on either side of
the optic axis for enucleated
and nonenucleated 15-dayold chick lenses. In the latter
case the eye is intact except
for the removal of the posterior and sclera, choroid and
retina. Corneal refractive
power is eliminated by immersion in water. Bars denote standard error of the
mean.
1.0
DISTANCE FROM OPTIC CENTRE (mm)
is minimal paraxially and larger (to 3 mm) at more
eccentric locations. In other words, the difference between paraxial and eccentric focal lengths is decreased by lens excision. These differences are presumed to be the result of changes in shape of the
excised lens. However, this assumes that the immersed cornea does not contribute to spherical aberration. Since the difference was found at the three
ages studied (5- and 15-day embryos and 17-day embryos), it may also be assumed that the constancy of
optical properties referred to in this study is true of
both conditions.
Discussion
The results of this study are consistent with earlier
work on human embryo lenses in that they suggest
that lens focal length, and therefore lens refractive
power, is relatively constant (Fig. 7) during most of
the period of lens embryonic development.10 The
wide range in focal length between lenses and within
a single lens at the 6 to 7 day incubation period indicates that lens ultrastructure and molecular organization is irregular until after this point. The lack of focal
constancy may be related to local variations in refractive index within the matrix of lens tissue. The
significant drop in focal length from the 6th and 7th
day of incubation to the 10th day indicates that the
overall refractive index of the developing lens is in-
creasing at a rate beyond the tendency for an increase
in focal length due to the marked increase in anterior
and posterior lens radii of curvature. In this context it
is of interest to note that the presence of various
classes of lens crystallins varies with age and location
in the embryo and post-hatching chick lens13 and in
the mammalian lens.14
From the 1 Oth day of incubation onwards, change
in lens size and shape and/or refractive index distribution, does not affect its axial focal characteristics.
This is true for both paraxial and eccentric lens positions, indicating that spherical aberration (the (difference in focal length for paraxial and eccentric positions) does not increase with development, a finding
opposite to that of the developing rat lens.15 The fact
that this constancy is carried over into the post-hatching period of lens development supports the existence
of a mechanism which predetermines lens refractive
power in isolation from other ocular refractive developments and regardless of whether light rays enter the
eye or not.
In third-order aberration theory, minimum blur
will occur three-quarters of the distance between the
paraxial and marginal focal points.16 Since the^ lens
paraxial focal points are constant and marginal focal
points are similar, the position of minimum blujr will
not change with age. Of course total ocular refractive
power will depend on both the cornea and the lens.
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970
CHICK LENS DEVELOPMENT / Sivok er ol
No. 5
CHICK DEVELOPMENT
AVERAGED VALUES
Fig. 7. Summary plot of
average focal lengths for all
laser beam positions for preand post-hatching chick
lenses indicating fairly constant focal lengths from day
10 of the developing embryo. Bars denote standard
error of the mean.
(PRE- AND POST-HATCHING)
Z
LU
<
O
o
10
15
20
25
AGE OF EMBRYO/CHICK
The developmental isolation of the lens, in the refractive sense, is suggested by a variety of other evidence. For example, recent studies, in which myopia
is produced in hatchling chicks by depriving the eye
of form vision, show that the gross anatomy, biochemistry and focal characteristics of the lens are not
altered.16"19 These findings are contrary to those of
Coulombre and Coulombre who note that lens
growth and development is largely tied in with globe
development.20 However, the possible independence
of lens development is not ruled out entirely, even in
the latter work.
Efforts to analyze age-related change of the refractive components of the living human eye yield conflicting data. Gordon and Donzis use corneal and
axial measurements of the eye to calculate lens refractive power.21 Their results show that the refractive
power of the human lens varies from 34.4 diopters in
the newborn to 18.8 in the adult eye. Grosvenor,22 on
the other hand, used Sorsby's data23 to show that age
related change in human lens refractive power is
small (1.0 to 1.5 diopters).
While the data presented here and earlier have
raised the possibility that the lens maintains a constant focal profile,10 it is clear that this cannot be a
universal property of the vertebrate lens. For example, the typical fish lens, the only refractive element of
the fish eye has a never-changing spherical shape.6 In
30
35
(DAYS)
Haplochromis burtoni, a cichlid fish, focal length has
been shown to scale with lens size.24 However, the
control of lens spherical aberration can be shown to
vary with age and with species in accord with visual
need.5 The shape and focal nature of the rat lens has
also been shown to vary considerably during the immediate (2 week) post-natal period.14 In this case, the
lens of the newborn, which is elliptical in shape and
more or less free of spherical aberration, rapidly assumes the large and nearly spherical proportions of
the adult rat lens. Large and characteristic amounts of
negative spherical aberration develop as well.
In the avian eye, the ciliary body (and muscle) is in
direct contact with the lens by way of ciliary folds.6 It
is, therefore, important to note that the shape of the
excised bird lens may be influenced by the absence of
contact with the ciliary body. It is noted that this
study shows relatively little difference between the
excised lens and the lens in situ. However, little is
known regarding the development of the avian accommodative mechanism nor is it even certain
whether accommodation in chickens involves lens
change only or change in curvature of the lens and
the cornea. 122526
Despite the uncertainty regarding the effect of excision, it is clear from the frozen sections and measures of fresh lenses representing the various developmental stages of the eye that lens size is changing
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INVESTIGATIVE OPHTHALMOLOGY G VISUAL SCIENCE / May 1989
dramatically. Despite the rounder appearance of the
10-day embryo lens (Table 1) the change in shape of
the chick lens is more or less in accordance with that
expected from the study of lens development. The
pre- and post-natal human lens is commonly described as changing from a more spherical to a more
elliptical shape.1-2-27 This change is inferred to result
from the continued equatorial development of new
lens cells and their tapered anterior and posterior
growth.
Thus it appears that the chick lens (and possibly the
human embryo lens) may be a static refractive feature
in an otherwise complex and changing optical system. Whether this constancy is a coincidental development resulting from a balance between size and
shape of the lens and refractive index distribution or
whether it is a genetically programmed characteristic
may be difficult to ascertain. A spherical distribution
of refractive index within a lens can give rise to the
same axial optics as an ellipsoidal refractive index
distribution.28 Thus, it is important to note that even
if the lens changes in shape and refractive index in
such a way as to keep focal length and spherical aberration constant, the off-axis optical properties of the
lens may be expected to change. Nevertheless it is
tempting to suggest that the focal stability of the lens
simplifies the process of emmetropization; for rather
than coping with two independent variables, lens and
globe, the refractive state of the eye is controlled by
manipulating the size and shape of the globe (sclera
and cornea) alone.
Key words: chick, lens, focal length, embryo, post-hatching
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