Download Accommodation demand and deprivation in kitten ocular

Accommodation Demand and Deprivation in Kitten
Ocular Development
Phillip Hendrickson* and William Rosenblumf
The effects of accommodation demand and deprivation on the development of ocular optics was
investigated in four groups of kittens (total n = 29). Group 1 consisted of five normal kittens; group
2 (nine kittens) had monocular radial keratotomy to induce relative hypermetropia and more
accommodation demand as well as to impart interocular refractive differences (anisometropia); group
3 (eight kittens) received daily monocular atropine; and group 4 (seven kittens) had binocular radial
keratotomy combined with daily monocular atropine. Regular examination provided documentation of
ocular development from the first through the sixth months of life. Subsequently, the focal lengths
of the crystalline lenses were determined in vitro. An apparent tendency for kitten eye pairs to grow
toward isometropia, even when anisometropia had been induced early in life, was seen in those eyes
in which the accommodative mechanism had been left intact (groups 1 and 2), but without
accommodation anisometropia resulted (groups 3 and 4). There was relatively more elongation of the
globe (3.08 ± 0.22%) as well as shorter than normal focal lengths of the crystalline lens (—4.91
± 1.62% anterior, —2.78 ± 1.54% posterior) in the eyes of the second group, and the eye pairs
regained isometropia. In those eyes of the third and fourth groups that received atropine daily, there
was relatively less elongation of the globe (—3.09 ± 0.59% and —3.22 ± 0.67%, respectively) and
shorter crystalline lens focal lengths (—3.50 ± 1.18% and —4.62 ± 1.07% anterior, —2.64 ± 1.02%
and —1.59 ± 0.62% posterior, respectively). Response of the eye to excess accommodation demand
(group 2) as well as increased demand with deprivation (groups 3 and 4) was thus seen to be
manifested not only in axial length differences but also in alteration of the focal lengths of the
crystalline lens, and it is demonstrated that these two elements contribute significantly to normal
ocular development toward isometropia. Invest Ophthalmol Vis Sci 26:343-349, 1985
Within a normal population there is a strong
representation of emmetropic individuals, with the
ametropic remainder disproportionately biased toward
myopia. Socio-economic factors1 were long overlooked
in favor of genetic ones.2"4
In 1969 Young5 examined the influence of mandatory schooling following attainment of statehood
in Alaska and reported a relatively high rate of
myopia in Eskimo schoolchildren, although their
illiterate parents and grandparents were, moreover,
emmetropic or even hypermetropic. On the other
hand, Steiger6 studied the distribution of individual
ocular optical components within a normal population
(5,000 eyes) and suggested that the chance combination of randomly distributed optical elements leads
to a relatively normal distribution of normally sighted
individuals.
Chance occurrence, genetic predetermination, or
environmental influence: which actually leads to myopia? The suggestion that accommodation extent
plays a role7"9 was taken into consideration when the
present experimental model was being developed. In
an attempt to elicit increased accommodation demand, the refractive power of the cornea was reduced
by means of radial keratotomy, leaving the accommodative system intact. In other kittens, the accommodative mechanism was eliminated by atropinization, and, in yet further kittens, these two perturbations were combined.
Materials and Methods
Since accommodation was to be the essential experimental feature of this investigation, the model
had to incorporate an animal that is not only highly
visual but also one that has an accommodative range
similar to that of humans. 10 Furthermore, the animal
had to be one that can be bred easily and economically
in colony, and, with these factors in mind, the
developing, mixed-breed kitten was chosen. The
treatment and handling of all animals included in
From the Department of Ophthalmology,* Basle University,
Basle, Switzerland, and the Department of Physiological Optics,f
University of Alabama in Birmingham, Birmingham, Alabama.
Supported in part (at University of Alabama in Birmingham) by
NIH Biomedical Research grant SO-7RR05807.
Submitted for publication: March 23, 1984.
Reprint requests: Dr. Phillip Hendrickson, Wissenschaftliches
Labor I, Universitats-Augenspital, CH-4056 Basle, Switzerland.
343
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INVESTIGATIVE OPHTHALMOLOGY & VISUAL SCIENCE / March 1985
Vol. 26
Table 1. Comparative mean terminal data for all groups (axial lengths and focal lengths)
Axial length
Group
Type
Final
diff*in
retina
1
2
3
4
N
RK
AT
RK + AT
0.02 ± 0.05
0.12 ±0.08
1.94 ±0.94
1.50 ±0.54
Diff. (dAL)
0.08
0.62
-0.64
-0.66
±0.07
±0.05
±0.11
±0.13
Anterior focal length
% Diff.
(%dAL)
0.45
3.08
-3.09
-3.22
±0.30
±0.22
±0.59
±0.67
%Diff.
(% dFVF)
Diff. (dFVF)
0.06 ± 0.05
-0.67 ± 0 . 2 1
-0.47 ± 0 . 1 6
-0.62 ± 0 . 1 4
0.44
-4.91
-3.50
-4.62
± 0.36
± 1.62
± 1.18
± 1.07
Posterior focal length
Diff. (dBVF)
-0.04 ± 0 . 1 6
-0.30 ± 0 . 1 8
-0.35 ± 0 . 1 6
-0.21 ± 0.08
%Diff.
(% dBVF)
-0.27
-2.78
-2.64
-1.59
± 1.06
± 1.54
± 1.02
±0.62
* Diff. = difference.
Lengths in millimeters; retinoscopic values in diopters; means ± SD. For
normals (N): difference = greater — lesser. For treated animals: difference
= treated eye - untreated eye.
this investigation conform to the ARVO Resolution
on the Use of Animals in Research.
Kittens develop cortical organization by the end of
the first postnatal month, 11 and adult-like visual
acuity and function have been reported to exist by
the sixth month of life,10 at which time the axial
length of the globe has reached adult-like proportions.12 Therefore, the experimental influence was
exerted from the first through the sixth months of
life of the kittens in this present investigation (n
= 29). There were five normal controls.
days, respectively (mean = 27.3 days). Postoperative
Neosporin ointment in the operated eyes precluded
keratometry for at least a week.
Those kittens in which the extent of anisometropia
imparted by monocular radial keratotomy fell markedly below an arbitrarily defined criterion of 1.5 D
had repeat surgery.
Radial Keratotomy
Other investigators have attempted to induce myopia by means of high minus lenses,13 restrictive
environment, 14 lid-suturing,15"19 as well as opacification. 20 For example, it is popularly assumed that
myopia via lid suture occurs according to the following
process: lid suture causes accommodation; accommodation causes increased intraocular pressure; intraocular pressure causes scleral stretch; and then, scleral
stretch21 causes myopia. This of course is a sequence
of a great many "ifs." Interestingly, lid-sutured macaque monkey eyes do not always lengthen but
sometimes shorten or show no change at all.22
We chose to impart only a mild refractive error by
means of moderate perturbation in one eye in order
to render the experimental model as close to clinically
occurring conditions as possible. To avoid the difficulties inherent in fitting and maintaining appropriate
contact lenses in small animals, the relatively simple
technique of radial keratotomy23 was selected. In each
cornea to be so treated (nine kittens, monocular),
between 16 and 20 incisions through about 50% of
the corneal thickness were made radiating from the
corneal cap (2.5-mm diameter) to 1 mm from the
limbus, resulting in a uniform reduction of refractive
power of the cornea of up to 3 D. Had the incisions
been made deeper, more power could have been
eliminated from the cornea, but a mild effect was
desired. At the time of treatment the ages of the nine
kittens were 32, 32, 30, 30, 28, 28, 28, 19, and 19
Atropinization
It has been proposed24'25 that the mechanical stresses
involved in accommodation 26 (coronally inward) are
conducive to secondary stress generation (longitudinally outward) and elongation of the ocular globe.
Excessive accommodation should lead to excessive
stresses and, thus, to excessive elongation (myopia).
Coleman7 suggested that accommodation causes an
increase in pressure in the vitreous chamber and,
therefore, an increase in stress on the chamber itself.
Estimation of these stresses27 has shown them to be
small, but their significance is yet undetermined.
However, Young28 measured the vitreous pressure
increase in monkeys to be fully 7 mmHg during
accommodation, and Coleman 29 found vitreous pressure increases of 2-4 mmHg in one human volunteer
in spite of cycloplegia (directly measured prior to
enucleation). An additional role played by stresses
exerted by the extraocular muscles during convergence
also has been considered,2425 and it is entirely possible
that both mechanisms combine to cause elongation.
It should follow that the elimination of the accommodative mechanism would lead to less than normal
elongation. The engineering concepts of stress and
strain related to accommodation and ocular growth
have been considered further by Barraquer30 and
Friedman.31
If radial keratotomy causes excessive accommodation and elongation, the elimination of accommodation in eyes having had radial keratotomy should
prevent such excessive growth, as success in bifocal32
and atropine 26 control of developing clinical myopia
(optical or pharmacologic reduction of accommodation) implies.
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ACCOMMODATION DEMAND AND DEPRIVATION IN KITTENS / Hendrickson and Rosenblum
No. 3
r 1.50
345
r 1.50
roo 5
0.50
0.00
tfl.25
60.0
RADIAL
KERATOTOMY
50.0 5
O
20
40
60
80
AGE
O
0
100 120 140 160 180 200
20
40
60
(days)
80
AGE
100 120 140 160 180 200
(days)
ri.50
1.00 S
0.50 £
0.00
L-0.25
19.0-
J 180
jE 17.0
UJ
RADIAL
KERATOTOMY
16.0
PLUS
< 15.0
X
if 14.0
<
13.0-1
0
20
40
60
80
AGE
100 120 140 160 180 200
0
^0.0
ATROPINE
^0.0
|
O
o
II
20
40
60
(days)
80
AGE
100 120 140 160 180 200
(days)
Fig. 1. Axial length (AL), corneal power (K), and interocular retinoscopic differences (dRET) versus age in a kitten from: A, top left,
normal-, B, top right, radial keratotomy-, C, bottom left, atropine-, and D, bottom right, radial keratotomy plus atropine groups (UE
= untreated eye; RK = occurrence of surgery).
Beginning on about the thirtieth day of life and
continuing every day thereafter, one drop of 1%
atropine was instilled into one eye of each kitten in
groups 3 (eight kittens) and 4 (seven kittens). In the
case of the latter group, in which radial keratotomy
was performed first, atropinization began on the third
postoperative day and continued through the sixth
month of life.
In Vivo Ocular Examination
Examination of all kitten eyes was made prior to
treatment onset and thereafter on a regular weekly
or biweekly basis. When necessitated by extremely
high corneal powers in 1-2-month-old kittens, sup-
plementary lenses of 1.25 or 2.25 D were employed
on the keratometer with appropriate correction. During this and the other ocular examinations, the kittens
were anesthetized with Ketamine HC1 (0.2 mg/kg).
The refractive state of the two eyes was determined
by means of retinoscopy.
Axial lengths as well as the axial extents of the
individual ocular components were determined by
means of A-scan ultrasonography (10 MHz focused
transducer). Propagation velocities for ultrasound in
cornea, aqueous, lens, and vitreous in the kitten
(1.639, 1.486, 1.585, and 1.534 mm//isec, respectively)
were determined 33 using in vitro samples of known
linear dimensions (measure "t"; v = d/t). These values
were used to calculate individual in vivo ocular
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INVESTIGATIVE OPHTHALMOLOGY & VISUAL SCIENCE / Morch 1985
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Table 2. All groups means and standard deviations of interpolated values for ocular components at day 175
Group
Eye
Type
Cornea
Aqueous
Lens
Vitreous
Axial length
dAL§
1
N
OD*
OS|
0.90 ± 0.06
0.90 ± 0.08
3.45 ± 0 . 1 4
3.44 ±0.17
6.72 ± 0.23
6.72 ±0.15
8.27 ±0.21
8.28 ± 0.22
19.34 ± 0.41
19.33 ± 0.37
0.07 ± 0.04
2
RK
RK
UEt
0.92 ± 0.03
0.92 ± 0.03
3.67 ± 0.28
3.59 ± 0.26
6.75 ±0.21
6.79 ±0.14
8.56 ± 0.37
8.04 ± 0.29
19.90 ± 0.63
19.34 ± 0.46
0.56 ± 0 . 1 0
3
AT
AT
UE
0.92 ± 0.03
0.92 ± 0.03
3.70 ± 0 . 1 9
3.78 ± 0 . 1 9
6.63 ± 0.20
6.69 ±0.15
8.00 ± 0.20
8.44 ± 0.23
19.25 ± 0.38
19.84 ±0.35
-0.59 ± 0 . 1 2
4
RK + AT
RK + A T
RK
0.93 ± 0.04
0.93 ± 0.04
3.59 ± 0 . 1 3
3.76 ± 0 . 1 9
6.59 ± 0.20
6.61 ±0.17
7.93 ± 0.33
8.31 ±0.27
19.04 ± 0.44
19.62 ± 0.26
* OD = right eye; fOS = left eye; JUE = untreated eye; £dAL = interocular
axial length difference (dAL for normals = greater — lesser; dAL for treated
component dimensions, the total of which was regarded to be the axial length of a particular eye.
From five measurements made on each eye at each
examination session, the longest was accepted as most
closely representing the actual axial dimension.
In Vitro Ocular Examination
Following the sixth month and the last in vivo
ocular measurements, each kitten was killed, and the
eyes were enucleated and prepared for focal length
determination of the crystalline lenses. Here, the
anterior and posterior ends are removed, leaving the
lens suspended within its capsule and the central
coronal section (as in vivo). Described in detail
elsewhere,34 this interferogrammetric technique permits maintenance of the lens to be examined in a
saline solution through which the optical pathway
passes. Repeated measurements demonstrated a precision of about 1/10 mm. Focal lengths were measured
to both the anterior and posterior vertices of the lens.
Results
Comparative mean terminal data for all four groups
of kittens is given in Table 1. From each group a
typical animal has been chosen to demonstrate axial
growth, development of corneal power, and the refractive states of the eye pairs in the respective group,
seen in Figures 1A-D.
By regularly examining the ocular status of the
developing eyes, it was possible to assess the extent
of temporal variation within the growth history of
each ocular component. However, due to organizational considerations, the ages at which the examinations took place could not be maintained uniform
for all animals, and comparisons between groups at
exactly the same age were not directly available. To
provide such comparisons, values for the ocular components were interpolated for day 175 from the
growth data gathered, shown in Table 2 and Figure 2.
-0.58 ±0.17
animals = treated eye — untreated eye or RK + AT — RK); All lengths in
millimeters.
Discussion
Axial Length and Crystalline Lens
Focal Length Development
In normal developing kittens the ocular axial length
at 1 month of life is about 13 mm, extending to
about 20-22 mm by the sixth month. Interocular
differences in axial length are only slight (about 1/10
mm) if present at all. In all three treatment groups
the interocular growth differences in axial length and
crystalline lens focal length were obvious when compared with those seen in the normal group (Table 1).
Essentially two types of refractive deficiency were
imparted to the treated eyes. The first, imparted to
the nine radial keratotomy kittens (group 2), consisted
solely of reduced corneal power, while the accommodative mechanism was left undisturbed. Accommodation then could provide an immediate and
almost constant correction of the resulting hypermetropia. The fact that all kittens subjected to monocular
radial keratotomy exhibited large interocular differences in axial length provides strong support for the
suggestion that excessive demand upon accommodation may lead to an increased axial length (group
2 mean interocular difference = 0.62 ± 0.25 mm).
Monocular relative hypermetropia of, for example, 3
D in an eye of approximately 20-mm axial length
should be only partially corrected by an axial length
excess of about 6/10 mm (equivalent to approximately
2 D), but these eye pairs were seen to have regained
isometropia during the growth period (group mean
terminal extent of anisometropia = Vs D). The remainder of the adjustment might be found in the
differences in crystalline lens focal lengths in the
treated and untreated eyes of this group (Table 1).
The lenses of these eyes were seen to have developed
a shorter focal length, which would be the appropriate
compensation.35 A possible contralateral response to
monocular perturbation is considered below in the
section, "Axial Component Composition."
The second type of refractive deficiency imparted
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ACCOMMODATION DEMAND AND DEPRIVATION IN KITTENS / Hendrickson ond Rosenblum
175-DAY
OCULAR COMPONENTS
.56±.1O
21
20
MS
PODOS
RK
• T UE
-.58±.12
-.58 ±.17
ATi£iRK+ATRK
19 CSD
~^18
i"
W
I
Fig. 2. Group mean ocular component
composition of values gained by interpolation: C = cornea; A = aqueous; L = lens;
V = vitreous; MSD = monocular axial
length standard deviation; and CSD
= component SD. The range of kitten
weights interpolated for day 175 = 9622,860.
16
15
O14
LJJ
13
12
11
LU
10
9
CL
8
5 7
O
RK
AT RK+AT
GROUP
(group 3) was that achieved by means of atropinization, eliminating accommodation. Absence of the
accommodative mechanism in the kittens treated
with atropine would go unnoticed if they had only
to view distant objects at six meters or more. However,
in the case of a kitten growing up in a birthing box
approximately '/? X xh X % m, then with its mother
and siblings in a cage approximately I X 1 xh X 1'/?
m, and finally in a group colony approximately 1'/?
X 2 X 3 m with other kittens of various ages and
freedom of interaction, such loss of the ability to add
power for near objects (accommodation deprivation)
may be considered a refractive defect. Atropine treatment also dilates the pupil and, thereby, reduces
depth of field, thus increasing the need for exact
dioptric adjustment to focus on near objects of regard
and enhancing the deprivation effect.
The kittens of group 3, following long-term monocular atropinization, showed less axial length development in those eyes receiving atropine than in the
untreated fellow eyes, a finding interestingly similar
to the clinical control of developing myopia (atropine
reduces accommodation, less myopia develops).36 The
same was seen in the kittens in group 4 (binocular
radial keratotomy with monocular atropine) but to a
slightly greater extent. Relative lengthening of the
radial keratotomy-treated eye (with no atropine) and
relative shortening of the atropine- and radial keratotomy-treated fellow eye could have led to this
slightly greater interocular axial length difference.
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INVESTIGATIVE OPHTHALMOLOGY & VISUAL SCIENCE / Morch 1985
Anisometropia imparted in the kittens of groups 3
and 4 (Table 1, Figures 1C, D) was not relieved
during the course of development studied. Crystalline
lens focal length differences in these eyes were approximately the same as those of the radial keratotomy
group. In all three treated groups, the interocular
differences were greater for the anterior focal length,
especially in the fourth group in which the ratio of
differences anterior to posterior was almost 3:1 (Table
1). This finding would seem reasonable since it is in
the anterior surface curvature that most of the changes
of the crystalline lens occur during accommodation. 37
These in vitro focal length measurements demonstrate only relative differences and do not necessarily
represent actual in vivo values at any particular
accommodative state. As such they cannot be used
directly to model the kitten eye.
Axial Component Composition
Seen in Table 2 and in Figure 2, the linearly
interpolated 175-day axial component lengths are
similar to those of the terminal measurements at
various ages (Table 1), the mean values for the former
being only slightly less than those of the latter.
Normalization of growth data for one particular
age permits two further considerations:
(1) The ocular component compositions in Figure
2 indicate that the strongest contribution to induced
interocular axial length differences in all groups in
this investigation is made by differences in vitreous
depth, the other dimensions being consistently similar
in extent. This conforms to the increased vitreous
chamber pressure aspect of Coleman's model.7
(2) In monocularly treated kittens, eyes receiving
no treatment have been referred to as "untreated"
since they no longer existed in an absolutely normal
environment, consisting of two untreated, normally
developing fellow eyes, which become isometropic
and attain binocularity. Furthermore, the untreated
eye in a monocularly atropine-treated kitten may not
be isolated completely from possible systemic communication with the drug.
Percent Ocular Component Growth
For organizational reasons, uniformity of initial
(31 ± 6 days) and terminal (199 ± 29 days) examination ages could not be maintained, but normalizing
the data by linear interpolation to an initial age of
35 days and a terminal age of 184 days can provide
a general insight into the percent component growth
extents of all kitten eyes in this study.
In all groups (29 kittens), percent ocular component
growth from 35 to 184 days was moreover uniform
Vol. 26
in extent except for that of the depth of the anterior
chamber. Whereas the corneal thickness, lens thickness
and the depth of the vitreous increased only 29
±11%, 30 ± 9%, and 20 ± 7%, respectively, the
increase in the anterior chamber depth had a mean
value of 183 ± 53%.
Since anterior chamber depth is thus by far the
site of greatest percentage growth during the first 6
months of kitten ocular development, its growth,
providing separation of the refractive elements of the
eye, might be considered to be one possible means
by which the total refractive power of the eye is
adjusted during development.38 Recalling our own
finding that only the developing vitreous depth contributes significantly to interocular axial length differences that occur following induced anisometropia,
we even might suggest further that coarse developmental adjustment of the optics of the eye occurs in
the anterior chamber depth while fine adjustment
takes place in the depth of the vitreous.
The findings of this investigation are consistent
with the idea39 that ocular growth may be a selfregulating process guided by visual experience and
dependent upon intact accommodative function.
Key words: accommodation, anisometropia, deprivation,
development of kitten ocular optics, radial keratotomy
Acknowledgments
The authors would like to express their appreciation to
Dr. Graeme Wilson, Dr. Carl Graves, Dr. Martin McCutcheon, and Dr. Thomas Norton for their helpful criticism
and advice. For her tireless assistance in handling and
examining the kittens, Ms. Madeleine Holzer has earned
the authors' sincere gratitude.
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