Download Interocular alignment following visual deprivation in the cat.

Interocular alignment following visual
deprivation in the cat
Max Cynader
Kittens were placed in the dark just after birth and then removed at various ages for the study
of interocular alignment. It was found that kittens dark-reared for 4 months or longer were
characteristically incyclotorted with respect to normal animals. Deprivation periods of less
than 2 months were ineffective in producing these changes. Divergence of the visual axes was
also observed in some dark-reared cats. Pupillary constriction in response to light was much
more pronounced in dark-reared cats than in normal cats. This enhanced pupillary reaction
persisted for at least 3 weeks after the deprived animals were brought into an illuminated,
environment. When dark-reared cats were allowed a recovery period, in a normally lit visual
environment, their ocular alignment changed markedly. The incyclotorsion and divergence of
the visual axes disappeared, and instead, cats allowed recovery from deprivation could, display
excyclotorsion and/or convergence of the visual axes. These anomalies of ocular alignment
associated with the recovery from visual deprivation could, occur following periods of initial,
deprivation as short as 30 days or as long as 2 years. The mechanisms and. possible significance
of such anomalies are considered.
Key words: interocular alignment, cyclotorsion, strabismus, cat,
visual deprivation, recovery of vision
I t has been known since Wheatstone's1 original demonstrations that stereoscopic depth
perception depends on the neural integration
of slightly dissimilar images on the two
retinas. A necessary prerequisite for this
achievement is accurate alignment of the two
eyes. In strabismus, a condition in which the
visual axes of the two eyes do not intersect on
the object of regard, inappropriate alignment
results in double vision (diplopia) or suppression of the input from one eye.2"4
A wealth of data has accumulated in both
From the Department of Psychology, Dalhousie University, Halifax, N. S., Canada.
Supported by Research Grants EY 02248 (National Institutes of Health) and MT 5201 (Medical Research
Council of Canada).
Submitted for publication Aug. 14, 1978.
Reprint requests: Dr. Max Cynader, Department of
Psychology, Dalhousie University, Halifax, N. S.,
Canada.
726
the clinical and experimental literature2 6
indicating that abnormal visual experience
can lead to marked anomalies in both the development of the visual system and in development of visuomotor coordination. In particular, several investigators have reported
abnormal alignment of the eyes in association
with various deprivation conditions.7"10 In
view of the evidence indicating a role for visual experience in the development of eye
alignment, this report examines the consequences of rearing animals in darkness and of
subsequent exposure in light for the development of interocular alignment.
Previous studies of strabismus in kittens
have concentrated on horizontal misalignment of the eyes. It is clear, however, that
ocular deviations may be present in the vertical dimension (hypertropias) and that torsional anomalies, in which the eyes are misaligned in the plane about the line of sight,
0146-0404/79/070726+16$01.60/0 © 1979 Assoc. for Res. in Vis. and Ophthal., Inc.
Downloaded From: http://iovs.arvojournals.org/pdfaccess.ashx?url=/data/journals/iovs/933085/ on 06/12/2017
Volume 18
Number 7
Interocular alignment after visual deprivation
may also have severe consequences for the
organism's ability to construct a stereoscopic
representation of three-dimensional space.
This report emphasizes anomalies of torsional
alignment associated with visual deprivation
and its aftermath.
Methods
Subjects. The interocular alignment of 75 cats
was examined in these experiments which took
place over a period of 4 years. Twenty-six normal
cats served as control subjects against which
data from experimental animals were compared.
Twenty-nine cats were studied on emergence into
the light after having been reared in darkness from
before the time of natural eye opening until 4
months of age. Twelve cats were deprived of vision for 8 to 24 months before their ocular alignment was examined on emergence from the dark,
and eight kittens were light-deprived for short
periods of time, starting at or near birth and continuing until there were 30 to 60 days of age. Some
of the animals which had been reared in the dark
were further studied after varying durations of exposure in a normal visual environment. Over 1200
photographs were examined to provide the data
reported in this paper. Data from some of these
animals have been presented elsewhere. 11
Measurement of ocular alignment. To assess interocular alignment in awake animals, cats were
held upright and the eyes brightly illuminated
with a small light source located 1 meter from the
cats eyes behind the shoulder of the experimenter. We made strenuous efforts to keep the cat
in an erect position and to photograph the animal
while it looked straignt ahead at the camera,
whose film plane was 0.5 meter from the animal.
These photographs provided information about
torsional and verge nee alignment of the eyes. By
torsional alignment, we refer to the correspondence between the eyes in the frontal plane
(i.e., about the line of sight). This was measured
by simply extending the lines formed by the streak
pupils of the two eyes and measuring the angle at
which they intersected. In normal cats (Figs. 1 and
2) this angle averages 12°. Cats were called incyclotorted if this angle of intersection was greater
than that of normal cats and exajclotorted if angles
of intersection were less than those of normal cats,
or negative in some instances. Since mediolateral
and/or torsional alignment of the eyes may vary
with the elevation of gaze, photographs in which
the subject's gaze was not directed approximately
straight ahead were excluded from analysis.
727
Although torsional alignment may be measured
with ease and precision in alert cats, assessment of
the relative horizontal positions of the eyes in alert
cats poses several problems. Efforts to develop a
procedure equivalent to the cover test used in the
assessment of strabismus in human subjects2' '
have proved unreliable, since cats will not fixate
stimuli as readily as human subjects. Rough estimates of the vergence alignment of the eyes are
possible with the corneal reflex technique. 2 ' 4i 7i !>
When the eyes are illuminated by a small light
source, spots of light (the reflection of the light
source) are visible on the anterior corneal surfaces
of the eyes. In the normal cat in the center of
Fig. 1, the reflex is not perfectly centered in the
pupils but falls medial to the constricted pupils. In
normal human subjects, studied with the same
methods, the reflex would appear to be well centered in both pupils. A miscentered reflex would
imply either divergence or convergence, depending on whether it fell medial or lateral to the centers of the pupils. These observations in man
imply that the normal cat of Fig. 1, in which the
reflex is miscentered, exhibits a divergent strabismus. It has, however, been shown9- 12- |:! that in
the cat the optical axis of the eye (i.e., the axis of
optical symmetry) is not aligned with visual axis,
the line between the posterior nodal point of the
eye and the area centralis of the eye. The angle
between the optical and visual axes is such that
normal cats appear slightly diverged.13> !) This
angle "alpha" varies from cat to cat, 13 and this variability inevitably limits the accuracy with which
horizontal interocular alignment can be inferred
from corneal reflex measurements.
A second difficulty with measures of interocular
alignment in alert animals is that the subject is free
to binocularly fixate stimuli at different distances.
Hence uncontrolled vergence movements can add
variability to the assessment of interocular alignment. Since the cat has a moderate range of disjunctive eye movement, 14 this is a potential contaminant for any measure of interocular alignment
in alert animals. To fully remove this contaminant
would require extensive behavioral training of
each cat. In the assessment of eye position, efforts
were made to keep the cat attentive to the experimenter or to the light source, both of which were
a known distance from the animal. Repeated measures of ocular alignment in the same cat on the
same day suggest that uncontrolled vergence cannot play a major role in the in the results. The
technical problems described above, however,
make the corneal reflex technique a relatively
crude one, with probable accuracy of no more than
Downloaded From: http://iovs.arvojournals.org/pdfaccess.ashx?url=/data/journals/iovs/933085/ on 06/12/2017
728
Invest. Ophthalmol. Visual Sci.
July 1979
Cynader
Fig. 1. Interocular alignment of a normal 4-month-old kitten (center) compared with that of
two dark-reared kittens (left-hand side and right-hand side). The reflections of the light source
on the corneal surfaces fall medial to the centers of the streak pupils in both normal and
dark-reared kittens. In both dark-reared kittens, but especially the subject illustrated on the
left, the tops of the streak pupils of both eyes are rotated inward relative to the normal kitten
in the center.
5°. Hence small ocular deviations would not be
observed with this measure. Due to these difficulties with the corneal reflex measure, quantitative
assessment of horizontal eye position was made
only in paralyzed cats, where much more accurate
assessments of ocular alignment could be made.
Measurement of ocular alignment in paralyzed! anesthetized cats. Animals were anesthesized with intravenous Pentothal and prepared for
single-unit recording by methods which have been
described elsewhere." 1 >h After initial paralysis
with Flaxedil (10 mg/kg), a continuous infusion of
Flaxedil (10 mg/kg/hr) and 5% lactated dextrose in
Ringer's was begun and maintained throughout
the recording session. Neo-Synephrine (1 drop of
10% solution) was instilled into each eye, and contact lenses were inserted to protect the corneas. In
most cases, the animal was held in a specially modified stereotaxic instrument so that eye bars,
which could distort the measurement of ocular
alignment, were unnecessary. Eye bars were,
however, employed in some of the earlier experiments. After initial paralysis, lA hr was allowed
before the cat was photographed with the same
methods as described for "alert" cats. From measures like this, it has become clear that cats become incyclotorted (about 4° to 6° in each eye)
under paralysis13 and that some divergence or
convergence of the visual axes may also occur. On
the whole, however, we have found that the horizontal ocular alignment as assessed in the paralyzed state is representative of that of the alert
animal. Similar conclusions have been reached in
a quantitative study of this problem. 16
The slit pupils having been photographed,
ophthalmic atropine was instilled to paralyze accommodation and dilate the pupils. Retinoscopy
was performed, and contact lenses with 4 mm diameter artificial pupils were selected to ensure
that images were in good focus on a tangent screen
1.5 meters distant. At least 1 hr was then allowed
for the eyes to fully stabilize before retinal landmarks were plotted with a reversing ophthalmoscope. The procedure involved plotting the locations of the areae centrales of each eye on the
tangent screen as well as the location of the optic
discs.
One possible contaminant of this method for
assessing interocular alignment is the well-known
uncertainty in plotting the area centralis in the
cat.12' 13 Where possible, the locations of the
ophthalmoscopically plotted areae centrales were
validated by recording responses from several
binocularly driven single cells in the central representation of the striate cortex. In cats with a normal complement of binocularly driven neurons,
the receptive field location through each eye could
be determined. The separation between the two
receptive fields corresponded well with the
plotted separation between the areae centrales of
the two eyes.
Results
Interocular alignment in dark-reared cats.
Fig. 1 illustrates the interocular alignment of
two dark-reared cats in comparison with that
of a normally reared animal. At least two features distinguished the interocular alignment
of these two groups of subjects. In both
Downloaded From: http://iovs.arvojournals.org/pdfaccess.ashx?url=/data/journals/iovs/933085/ on 06/12/2017
Volume 18
Number 1
Interocular alignment after visual deprivation 729
INTEROCULAR
TORSION
DARK-REARED
CATS
INTORTED
•
•
NORMAL
Normal Cats
4 Months
Dark-reared
8-10 Months
Dark-reared
40° 38
36
34
32
30
28
26
24
INTEROCULAR
22
20
TORSION
18
16
IN
DEGREES
14
12
10
8
6
4
2°
Fig. 2. Distribution of interocular torsion for normal cats in comparison with that of kittens
deprived of vision for 4 months or 8 to 10 months, starting just after birth. Each square
represents one kitten, although the data for one kitten in this and subsequent figures may
represent the mean of up to five photographs. Interocular torsion is defined as the angle of
intersection formed by extending the lines of the streak pupils. The mean of the distribution
for normal cats is 11.2° (S.D. 3.0°) and that for the 4-month dark-reared group is 22.3°
(S.D. 6.0°). The mean interocular torsion angle for cats dark-reared for 8 to 10 months is 27°
(S.D. 4.7°).
MEDIOLATERAL
OCULAR
ALIGNMENT
Nor tial
6 -
Cats
Dar (-Reared Cats
;;" y
4 -
•
•
2 -
Hi
7
6
5
— CONVERGED
4
1 0
1
SUPERIMPOSED
2
6
7
m
^^ H
8
9
10
list
15°
DIVERGED
Fig. 3. Comparison of the horizontal positions of the areae centrales in normal cats under
paralysis with those of dark-reared cats studied under the same conditions. To derive these
data, the cats were paralyzed and then the locations of the areae centrales of the two eyes were
plotted on a tangent screen 57 inches away with a reversing opthalmoscope. In many cases,
these measurements were further checked by determining the location of the two receptive
fields of binocularly driven units. Each square represents one cat and the abscissa is in
degrees. In normal cats, the areae centrales are more frequently crossed on paralysis than
uncrossed (mean = 0.8° crossed; S.D. = 2.9°). The dark-reared group displays more variability than the normal population (S.D. = 5.3°) and the areae centrales are, on average, diverged
relative to the normal group (mean = 4.6° uncrossed).
Downloaded From: http://iovs.arvojournals.org/pdfaccess.ashx?url=/data/journals/iovs/933085/ on 06/12/2017
730
Invest. Ophthalmol. Visual Sci.
July 1979
Cynader
Fig. 4. Interocular alignment of three cats which have been kept in darkness for prolonged
periods starting just after birth and then allowed a recovery period in the light after the
deprivation period. The cat on the left-hand side was maintained in darkness for 24 months and
then allowed a 4-month recovery period before this photograph was taken. A marked esotropia
is indicated by the lateral location of the light reflex relative to the center of the streak pupils.
This cat has been kept in the light for 2 years since this photograph was taken without obvious
alteration in interocular alignment. The center cat is the same animal as illustrated on the
right-hand side of Fig. 1, but with 2 months of exposure in a normal environment. Comparison
of interocular alignment before and after the recovery period reveals a change from incyclotorsion to excyclotorsion and from normal vergence alignment to esotropia. The cat on the right
represents an extreme example of the excyclotorsion associated with recovery from visual
deprivation. The medial location of the light reflex relative to the streak pupils indicates,
however, that vergence alignment is approximately normal in this cat.
dark-reared cats, the streak pupils were incyclotorted relative to those of the normal
subject. The cat on the left of Fig. 1 represents an extreme case of this torsional anomaly. In this case, the angle between the
pupils was 34°, compared with that of 12° for
the normal cat in the center of Fig. 1. Incyclotorsion was less marked (21°) in the cat
pictured on the right but was still greater
than that of the normal cat in the center.
Only a few dark-reared cats overlapped with
the normal population in their torsional
alignment. Fig. 2 illustrates the distribution
of interocular torsion in the populations of
dark-reared and normal cats which have been
examined. The range of interocular torsional
angles was much greater in dark-reared cats
than in the normal cats. As well, a marked
trend toward incyclotorsion was clearly visible. This trend appeared especially marked
among the animals which had been deprived
for longer periods (8 to 10 months). The additional incyclotorsion in kittens deprived for
4 months averaged 11° relative to normal subjects, whereas the animals deprived for 8 to
10 months were, on average, 16° incyclotorted relative to the normal group.
The trend toward incyclotorsion of the
optic axes was the most consistent anomaly
observed in the dark-reared group but not
the only one. Several authors have commented on the tendency toward divergence
among dark-reared cats,7" IOr n and the cat
illustrated on the left of Fig. 1 exemplifies
this trend. Examination of the positions of
the corneal reflex in the two eyes of the normal cat revealed that it was somewhat medial
to the streak pupils in the both eyes. In normal cats the reflex is typically miscentered by
1.25 to 1.75 mm on the corneal surfaces.7 By
contrast, the reflex is markedly miscentered
in both eyes of the left-hand side dark-reared
subject, implying a divergence of the optic
axes. Cats with obvious divergence did not,
however, dominate the population of darkreared subjects. In the dark-reared cat on the
right-hand side of Fig. 1, the reflex appeared
to fall just medial to the pupil in each eye.
This value falls within the range of ocular
alignment in normal cats. On paralysis (see
Downloaded From: http://iovs.arvojournals.org/pdfaccess.ashx?url=/data/journals/iovs/933085/ on 06/12/2017
Volume 18
Number 7
Interocular alignment after visual deprivation 731
INTEROCULAR TORSION DARK-RECOVERY
-INTORTED
CATS
NORMAL
EXTORTED
|::: 11 :| NORMAL CATS
L
DARK-REARED
^ H
DARK - RECOVERY
6
I 1
CO
*.
-L
-
-
r-.
1
ro
NUMBER OF
5
5
II
1
[
I I I
I
1
40° 38
36
34
32
30
28
26
24
22
20
18
16
I
:
14
12
10
8
6
4
2
0
2
4°
INTEROCULAR TORSION IN DEGREES
Fig. 5. Comparison of interocular torsional alignment among normal cats, dark-reared cats,
and dark-recovery cats. Conventions are as in Fig. 2. The mean of the distribution of interocular torsion angles is 9.8° for the dark-recovery group, which is similar to that of normal cats
(11.2°). The standard deviation is however much greater for the dark-recovery group
(S.D. = 10.3°) than for normal cats (S.D. = 3.0°).
Methods) of the subject shown on the right of
Fig. 1, the relative positions of the areae centrales in two eyes indicated a convergence of
3°. This value is well within the range observed in normal cats under the same conditions (Fig. 3).
It is evident, especially in the cat on the
left of Fig. 1, that conclusions about divergence or convergence of the optic axes will be
markedly influenced by the elevation of the
corneal reflex in the two eyes. If the reflex is
positioned on the inferior corneal surface, all
dark-reared cats would appear markedly divergent. By contrast, positioning the reflex
on the superior surface would result in apparent convergence of the optic axes in many
cases. Inattention to the elevation of the
reflex when the cat is photographed may account for some of the discrepant results
which have been reported in the literature.7' I0- n
As discussed in Methods, the many difficulties associated with the corneal reflex
measure render it unsuitable for quantitative
evaluation of the relative horizontal position
of the eyes. Much more accurate assessments
can be made by paralyzing the subject and
determining the projections of the areae centrales either by the use of a reversing ophthalmoscope or by plotting the receptive
fields of centrally located, binocularly driven
single units. Both of these methods were
employed and resulted in data which were in
good agreement. Fig. 3 summarizes the data
obtained with these measures for a population of normal cats as compared -with visually
deprived subjects. It is evident that the range
of interocular misalignment was much greater
among the group of dark-reared cats than
among normal animals. Dark-reared cats as a
group also appeared somewhat divergent
with regard to the normally reared population. It is clear, however, that exceptions to
this rule were not uncommon and that the
trend toward divergence of the visual axes
was less consistent than was the trend toward
incyclotorsion observed among dark-reared
cats.
Interocular alignment in dark-recovery
cats. When cats are first removed from the
darkroom following prolonged visual deprivation, they give the appearance of total
blindness. The animals fail to react to threatening visual stimuli, they bump into objects
Downloaded From: http://iovs.arvojournals.org/pdfaccess.ashx?url=/data/journals/iovs/933085/ on 06/12/2017
732
Invest. Ophthalmol. Visual Sri.
July 1979
Cynader
TIME COURSE DARK RECOVERY
14
CO
DC
O
UJ
12
8
o
en
cc
2 2
0
1
2
3
4
WEEKS IN LIGHT
5
6
Fig. 6. Time course of torsion changes when kittens previously deprived from just after birth
are brought into the light at 4 months of age. The kittens' torsional alignment at the end of
deprivation was assigned a value of 0 and represents the origin of the graph. Changes of
alignment toward excyclotorsion are assigned positive values. The error bars represent one
standard error.
as they skitter about the floor, and they fail
to pursue moving visual stimili. If such animals are maintained in a normally lit environment for the next few weeks, their capacity for visually guided behavior improves
markedly.18> 19 Pari passu with the improvement in visual behavior, the ocular alignment
of these animals changes. Fig. 4 illustrates
the interocular alignment of three cats after
they have been allowed a period of recovery
in a normal visual environment following prolonged dark-rearing.
A comparison of Figs. 1 and 4 reveals two
major differences between the ocular alignment of these cats and subjects which have
just been removed from the darkroom. First,
the marked incyclotorsion characteristic of
the dark-reared population was no longer
evident, and the cat on the right of Fig. 4
was, in fact, markedly excyclotorted. Second,
divergence of the visual axes disappeared,
and instead convergent strabismus was observed (left-hand side subject in Fig. 4). The
middle subject in Fig. 4 is the same kitten
as illustrated on the right of Fig. 1. The 8
weeks of exposure intervening between the
two photographs resulted in a change of 19°
in the torsional alignment of the eyes. This
animal was now clearly excyclotorted with
regard to the normal cat in Fig. 1. Furthermore, the medial location of the corneal
reflex in the two eyes of the dark-reared kitten has been replaced by the symmetric location of the reflex in the same animal after
recovery. On paralysis, shortly after this photograph was taken, the relative positions of
the areae centrales in this dark-recovery subject indicated an esotropia of 14°. The esotropia observed in the dark-recovery cats was
clearly visible under paralysis as well, indicating that active contraction of the eye muscles was not necessary for its manifestation.
These two alterations of interocular alignment, i.e., from incyclotorsion towards excyclotorsion and from exotropia toward
esotropia, constituted the major changes observed in the interocular alignment of darkrecovery cats.
Fig. 5 adds torsional data derived from the
study of dark-recovery cats to the comparison
Downloaded From: http://iovs.arvojournals.org/pdfaccess.ashx?url=/data/journals/iovs/933085/ on 06/12/2017
Volume 18
Interocular alignment after visual deprivation 733
Number 7
MEDIOLATERAL OCULAR ALIGNMENT
j ; : : : : | NORMAL CATS
[ | ^ | DARK-REARED CATS
DARK RECOVERY CATS
CONVERGED
SUPERIMPOSED
DIVERGED
Fig. 7. Horizontal interocular alignment of normal cats, dark-reared cats, and cats allowed a
prolonged recovery period in the light following visual deprivation. Conventions and methods
are the same as those for Fig. 3. The dark-recovery cats display a clearly measurable esotropia
under paralysis. The mean of the distribution for dark-recovery cats is 10° crossed
(S.D. = 4.2°) compared with 0.8° crossed for normal cats and 4.6° uncrossed for dark-reared
cats which have not been allowed a recovery period.
between normal and dark-reared subjects
made in Fig. 2. The data indicate that cats
allowed a recovery period in a normal environment were consistently excyclotOrted
relative to dark-reared cats. The mean interocular torsional alignment in the population of dark-recovery cats was not significantly different from that of normal cats,
but the range of torsional values was much
larger among the dark-recovery group. It is
particularly striking that in some cases the
dark-recovery cats developed a marked excyclotorsion of the visual axes. The righthand side subject in Fig. 4 represents an extreme example of excyclotorsion associated
with the recovery of vision following prolonged deprivation.
The time course of the alterations in interocular alignment among the dark-recovery
cats has been studied in eight animals which
were maintained in darkness until 4 months
of age. They were then photographed at
weekly intervals following their emergence
from the dark. The rate of change of interocular torsion for these animals is plotted in
Fig. 6. To produce this figure, interocular
torsion for each animal at the time of
emergence from the dark was normalized to
zero. In subsequent measures, a change to-
ward excyclotorsion was assigned a positive
value. The graph indicates that alterations in
torsional alignment began within a few days
and that the change toward excyclotorsion
appeared to be largely complete within 3
weeks. It should be noted that although the
smooth curve of Fig. 6 represents the mean
of data derived from eight animals, intersubject variability, both in the exact timing and
in the degree of torsion change with visual
experience, was considerable. The variability
associated with repeated measures of the
same kitten on the same day was also increased during this recovery period relative
to normal cats. In two of the eight cats followed in this series, torsional alignment of
the eyes remained essentially unchanged
during the recovery period, although clear
changes in vergence alignment were observed. The source of this interanimal variability is as yet unclear. Since some of the
animals were subject to single-unit analysis
during the same period, it is possible that the
paralysis, anesthesia, and cycloplegia associated with recording may have influenced the
recovery process. It has been a consistent observation, however, that the animals which
have the least marked incyclotorsion when
they first emerge from the dark tend to de-
Downloaded From: http://iovs.arvojournals.org/pdfaccess.ashx?url=/data/journals/iovs/933085/ on 06/12/2017
734
Invest. Ophthalmol. Visual Sri.
July 1979
Cynader
Fig. S. Top photograph compares the size of the
pupils of a normal kitten (left) with those of a visually deprived kitten (right) under the same lighting conditions. It is evident that the normal kitten's pupils are markedly more dilated than those
of the dark-reared kitten. Lower photograph compares the area of the pupils in two littermate kittens. The kitten on the right was dark-reared until
3 weeks before this photograph was taken; the kitten on the left was treated normally from birth.
Under the same illumination conditions, the
pupils of the previously deprived kitten are markedly constricted relative to those of the normal cat.
The level of illumination under which these photographs were taken was 1.3 log ft. lamberts.
velop the most marked excyclotorsion of the
visual axes following light exposure. By contrast, kittens with marked incyclotorsion to
begin with tend to remain strongly incyclotorted despite light exposure, showing less
torsion change than other dark-reared kittens.
Vergence changes in interocular alignment.
At the same time as interocular torsion
changes during recovery from visual deprivation, both eyes turn medialward, resulting
in convergent strabismus. Fig. 7 compares
horizontal ocular alignment among normal
cats, dark-reared cats, and cats which have
been allowed a recovery period in a normal
visual environment following prolonged deprivation. The data indicate that the dark-recovery group ot cats was markedly convergent, relative both to dark-reared cats
immediately after deprivation and also to
normal cats. As with the torsional measures
reported in such cats (Fig. 5), the range of
interocular vergence values among the darkrecovery population was much larger than
that of normal cats.
The time course of the alterations in mediolateral interocular alignment on exposure
to light was similar to that previously described for torsion changes, and in some animals, these alterations in eye position in the
horizontal and torsional planes occurred together, suggesting a common basis. In other
subjects, however, including the two described above, the recovery process consisted mainly of alterations in vergence
alignment, with little or no torsional change.
In the subject on the left of Fig. 4, a marked
esotropia can be observed in the presence of
normal torsional alignment. In other cases,
typified by the cat shown on the right of
Fig. 4, the recovery process consisted of
marked torsional changes accompanied by
only a small vergence change.
Pupillary reactions in dark-reared cats. If
a previously dark-reared cat is brought into a
moderately well-lit room and allowed a few
minutes to settle down, it can be observed
that the pupils are much more constricted
than those of normal kittens under the same
conditions. Fig. 8 (top) compares pupillary
reactivity of a normal kitten with that of a
dark-reared kitten of similar age. It is immediately evident that the pupils in the
dark-reared kitten on the right are only one
fifth as large in area as those of the normal
kitten under the same lighting conditions.
This increased pupillary constriction under
conditions of moderate illumination (1.3 log
foot-lamberts) has been observed in virtually
all dark-reared animals which have been
examined.
The enhanced pupillary reactions of dark-
Downloaded From: http://iovs.arvojournals.org/pdfaccess.ashx?url=/data/journals/iovs/933085/ on 06/12/2017
Volume 18
Number 1
Interocular alignment after visual deprivation 735
INTEROCULAR
TORSION
SHORT-TERM
DEPRIVATION
Normal
NORMAL
INTORTED
Cats
30-60 Days
Dark Reared
28° 26
24
22
20
18
INTEROCULAR
16
14
TORSION
12
IN
10
8
6
4
2°
DEGREES
Fig. 9. Distribution of interocular torsion for kittens dark-reared for 30 to 60 days in comparison with normal kittens. Conventions as in Fig. 2. The mean interocular torsion for the
short-term dark-reared cats is 13.5° (S.D. = 4.8°). This is not significantly different from that
of the normal group (mean = 11.2°; S.D. = 3.0°).
reared cats described above diminished with
time but could be readily observed for as long
as 2 to 3 weeks after the animal was brought
into the light. The lower part of Fig. 8 illustrates the relative degree of pupillary constriction in a normally reared kitten and its
littermate which had spent 3 weeks in the
light following 4 months of dark-rearing. It is
evident that pupillary area was reduced by a
factor of 3 in the previously deprived kitten
relative to the normally reared kitten, even
after the 3-week recovery period. Our methods are not adequate to determine whether
the hyperreactive pupillary reflex which
characterizes dark-reared cats eventually
subsides to the level of normal or whether a
small increase in excitability persists indefinitely despite continued exposure in the
normal environment.
Age-dependent process in interocular alignment. Several aspects of interocular alignment observed in these experiments appeared to depend on the animal's age. Fig. 9
compares the torsional alignment of kittens
kept in darkness from just after birth until 60
days (or less) with that of normal cats. The
data indicate that subjecting kittens to a short
deprivation period did not result in the
characteristic torsional anomalies observed
with longer term deprivation. A comparison
of the data presented in Fig. 9 with those of
Fig. 2 suggests that these anomalies developed between 2 and 4 months of age. The
difference between the 4 month and 8 to 10
month deprivation conditions in Fig. 2 indicates that incyclotorsion of the visual axes
may increase progressively with prolonged
deprivation.
Although the torsional anomaly which
characterizes dark-reared cats appeals to exhibit a well-defined critical period, the alterations in interocular alignment which occur
when dark-reared subjects are brought into
the light are, to some extent, independent of
the animal's age. One animal maintained in
the dark for 2 years developed a marked esotropia on subsequent exposure in a normal
visual environment (Fig. 4). Similarly, esotropia and excyclotorsion were noted in two
of three kittens which were visually deprived
from just after birth until only 30 days of age.
The main difference between the effects of
short vs. long periods of deprivation starting
at birth appears to be the speed with which
the alignment of the eyes changes when the
animal is brought into the light. The time
Downloaded From: http://iovs.arvojournals.org/pdfaccess.ashx?url=/data/journals/iovs/933085/ on 06/12/2017
Invest. Ophthalmol. Visual Set.
July 1979
736 Cynader
A
A
5°;
.DR
c-
-D
CR
Fig. 10. Consequence of rotating each eye inward through 5° about the line of sight. The lines
AB and CD represent the projections of the vertical and horizontal meridia of both eyes onto a
screen under conditions of appropriate torsional alignment. With incyclotorsion of each eye
through 5°, ALBL and ARBR represent the vertical meridia of the left and right eyes, respectively. C,DL and C R D R represent the horizontal meridia. The horizontal separation of the
vertical meridia of the two eyes increases with distance from the areae centrales. In the upper
visual fields, the left and right vertical nieridia are crossed, indicating convergence, whereas
they are uncrossed in the lower visual fields, indicating divergence. Similarly the vertical
separation of points along the horizontal meridia of the two eyes increases with increasing
eccentricity.
course for alignment changes described in
Fig. 6 for kittens kept in the dark for 4
months, which required several weeks, is
compressed into 3 to 4 days if kittens are deprived for just 30 days.
Discussion
Torsional and horizontal alignment of the
eyes. Two major features distinguish the ocular alignment of dark-reared cats from that of
normal subjects: incyclotorsion of the visual
axes and a tendency toward divergence. We
have treated horizontal and torsional alignment of the eyes separately in our descriptions of dark-reared cats. This separation is
based on several considerations. First, the
characteristics of the adequate visual stimuli
for the elicitation of vergence or cyclotorsional eye movements are quite different.
The adequate stimulus for eliciting vergence
eye movements has been shown to be a
stimulus movement and/or offset perpendicular to the fixation plane.20' 2I This stimulus would demand alterations in lateral
alignment of the eyes without necessitating
torsional changes. By contrast, the adequate
stimulus for the system producing opposed
cyclotorsional eye movements would be a rotation about the fixation plane (see below).
Such a stimulus would demand no net vergence change, since the upper and lower
field signals for vergence would counteract
each other.
A second reason for treating these aspects
of interocular alignment separately is the observation that torsional or vergence alignment of the eyes may be altered independently during recovery from visual depriva-
Downloaded From: http://iovs.arvojournals.org/pdfaccess.ashx?url=/data/journals/iovs/933085/ on 06/12/2017
Volume 18
Number 7
Interocular alignment after visual deprivation
737
Fig. 11. The relationship between incyclotorsion and the plane over which binocular fusion is
possible. If the cats eyes are aligned such that a vertical screen (solid line) is in binocular
correspondence at a fixation distance of 50 cm., incyclotorsion of each eye by 2° would require
that the screen be tilted toward the subject by 49° in order for binocular correspondence to be
maintained. If each eye were incyclotorted by 5°, a 71° tilt of the plane (top toward the subject)
would be required to negate the horizontal and vertical disparities shown in Fig. 10.
tion (Fig. 4). In the various experimental
conditions reported here and in the companion paper, 22 incyclotorsion has been
found in association with either esotropia or
exotropia and in kittens with normal vergence alignment.
Torsional anomalies. At first glance, the
significance of the torsional anomalies observed in the dark-reared animals in this
study appears unclear. However, several
geometric consequences for fused binocular
vision follow immediately from alterations in
interocular torsional alignment. With incyclotorsion, the degree of horizontal ocular
misalignment will vary with the elevation of
the visual stimulus. The deprived cats of
Fig. 1 would be markedly more divergent for
stimuli presented in the lower visual fields
than for stimuli presented in the upper fields.
A vergence movement would alter the relative horizontal position of the eyes and would
also change the elevation of the retinal areas
in which fused binocular overlap could occur
if the cat faces a vertical screen. The situation
is illustrated in Fig. 10, for a cat facing a tangent screen. If the torsional alignment of the
eyes is appropriate, as in a normal cat, the
vertical and horizontal meridia of the two
eyes will line up (solid lines) so that an object
falling anywhere along them will fall on corresponding retinal points. The dotted lines
illustrate the consequences of rotating each
eye inward through 5° about the area centralis. This is about the size of the torsional
anomaly observed in the deprived kittens. It
can be seen that horizontal disparities between the two eyes arise for stimuli presented along the vertical meridia and that the
sign of these disparities is opposite in the
upper and lower fields. Convergence of the
visual axes would allow stimuli presented
along the vertical meridian of the lower fields
Downloaded From: http://iovs.arvojournals.org/pdfaccess.ashx?url=/data/journals/iovs/933085/ on 06/12/2017
Invest. Ophthalmol. Visual Set.
July 1979
738 Cynader
to fall on corresponding retinal points, the
degree of convergence determining the retinal elevation at which binocular overlap occurred. Similarly, divergence would permit
binocular overlap in the upper fields. Horizontal vergence movements would, however,
be unable to compensate for the vertical disparities arising for stimuli presented along
the horizontal meridian, or for the vertical
component of the disparities arising for
stimuli which fall on neither the horizontal
nor the vertical meridian. These geometric
considerations make it evident that inappropriate torsional alignment of the eyes presents an impediment to binocular fusion
which may be as severe as that associated
with inappropriate vergence alignment.
In order to re-establish binocular correspondence in the face of the 5° incyclotorsion
of each eye which characterizes the darkreared kitten, the top of the screen which the
animal faces would have to be rotated toward
him (about its center) through an angle which
depended on the fixation distance. This relationship between interocular torsion and the
inclination of the plane of regard was first
treated by Helmholtz.23 The equation
tan y =
tan 6
(1)
where y is the monocular torsion angle in
degrees, 21 is the interpullary distance, F is
the fixation distance, and d is the angle of
inclination of the plane which is viewed, is
derived from Helmholtz and is illustrated in
Fig. 11. For a given fixation distance (50 cm
in Fig. 11) and assuming a 3 cm interpupillary distance for the cat, incyclotorsion of
each eye through 5° would require a 71° rotation of the plane being viewed toward the
animal in order to retain binocular correspondence. Even 2° of incyclotorsion of each
eye would require a 49° tilt of the plane being
viewed in order for objects on that plane to
continue to fall on corresponding retinal
points.
One would naturally assume that the plane
which is in correspondence for subjects with
normal torsional alignment is upright. In fact,
however, recent evidence indicates that the
plane which is in binocular correspondence
(the vertical horopter) is tilted away from subjects with normal torsional alignment.24' 25
These data, which appear similar for cats,
owls, and humans, indicate that the degree of
tilt of the vertical horopter depends on the
fixation distance. At the fixation distance described above, the horopter would be tilted
away from the normal subject by about 70°. It
has been suggested that the inclination of the
vertical horopter away from the organism
may serve the function of keeping the terrain
which is being traversed in binocular correspondence as the subject locomotes. The
consequence of incyclotorsion, as in the case
of the dark-reared cat, would be to tilt the
vertical horopter, so that it was approximately upright, rather than tilted away from
him, as in the normal cat. In this sense, the
alterations of torsional alignment observed in
the dark-reared cats may represent a "best
guess" of the inclination of the plane of
binocular correspondence made in the absence of visual input.
When the dark-reared cat is brought into a
normally illuminated environment and allowed a recovery period, the incyclotorsion
which characterizes the recently deprived
animal disappears. During the change from
incyclotorsion toward excyclotorsion of the
visual axes, the inclination of the plane over
which binocular correspondence can be maintained alters as well. The vertical horopter
tilts away from the animal as incyclotorsion
lessens, and in the kittens which become
excyclotorted relative to normal cats, the
vertical horopter may come to lie almost
horizontal.
It is tempting to regard the torsion changes
of the dark-recovery kittens as an adaptive
modification, i.e., to surmise that the kitten
is attempting to compensate for the presumed diplopia induced by the different
orientations of visual stimuli on the retinas. If
these torsional alterations represent efforts to
reduce diplopia, however, they must be singularly unsuccessful. Few of the dark-recovery animals eventually achieve normal
Downloaded From: http://iovs.arvojournals.org/pdfaccess.ashx?url=/data/journals/iovs/933085/ on 06/12/2017
Volume 18
Number 7
Interocular alignment after visual deprivation
torsional alignment. Individual subjects may
pass through a period of normal alignment
during the recovery process only to continue
past this point toward excyclotorsion of the
visual axes. The significance of this overshoot
is still unclear. The results from the darkrecovery cats may be placed in context, however, by noting that the time course of the
alterations in torsional alignment during recovery from visual deprivation correlates well
with the time course of the recovery of feature specificity by neurons in the visual cortex of kittens which have been dark-reared
until 4 months of age and then allowed a
recovery period in a normal visual environment.2(i> 27
Vergence anomalies. A trend toward increased divergence in dark-reared cats has
been noted by some authors, 7 ' l7 although
others have not consistently observed this
phenomenon in such animals.10> I6 It should
be noted that the corneal reflex measures
used in most of these studies are relatively
inaccurate. Moreover, the systematic torsional misalignment of the visual axes in
dark-reared cats must complicate corneal
reflex measures of esotropia since the distance between the center of the pupil and the
reflex would vary with the elevation of the
light source and the cat's angle of regard in
the vertical plane. For these reasons, our
quantitative date for vergence alignment in
dark-reared cats have been gathered by determining the positions of the areae centrales
in paralyzed and anesthetized cats. These
data agree with those of other workers in indicating that dark-reared cats are on average
divergent with regard to normal cats but
show that there is considerable overlap between the two populations in this regard.
Though the development of esotropia following exposure to light in previously darkreared kittens has been a consistent observation (Figs. 4 and 5), the mechanism underlying this phenomenon remains uncertain. Our
working hypothesis is, however, that esotropia is associated with the pupillary anomalies exhibited by dark-reared animals. It has
been established for man, cats, and monkeys
739
that the occurrence of pupillary constriction
is often associated with convergence of the
visual axes and with accommodation. These
three reactions occur together when an object approaches the observer, and so have
been referred to collectively as the "near
reflex."28 This triadic response is the basis for
the well-known observation that stimuli demanding accommodation elicit convergence
and pupillary constriction as well as the
appropriate accommodative response. The
linkage between these accommodative and
vergence reactions during normal usage
provided the basis for Donders' 29 explanation
of the relationship between hypermetropia
and esotropia. It was known, even in his
time, that hypermetropic subjects often developed convergent strabismus. Donders'
view was that the constant accommodative
effort required for clear vision in hypermetropia would result in tonically increased convergence as well. This tonically
increased convergence would lead ultimately
to esotropia. It may be that a similar mechanism leads to esotropia in the dark-recovery
kittens. According to this view, constant demands to constrict the pupil (due to the kittens' increased reactivity to light) would demand tonically increased convergence. This
would result eventually in convergent strabismus. This hypothesis is a tentative one
and requires many further experiments before it can be accepted. It does, however,
enable us to account for the divergence
which occurs in dark-reared cats in the same
terms as the convergence associated with recovery from deprivation. According to this
hypothesis, the initial exotropia results from
an absence of stimulation to the pupillary system while the animal is in the dark, whereas
the esotropia which develops when the animal is brought into the light is a result of
overstimulation of this system.
The esotropia which characterizes the darkrecovery cats can be observed both in alert
animals (Fig. 4) and in the paralyzed and
anesthetized subjects (Fig. 7). Since paralysis
removes any active contribution of the muscles to eye position, this finding implies that
Downloaded From: http://iovs.arvojournals.org/pdfaccess.ashx?url=/data/journals/iovs/933085/ on 06/12/2017
Invest. Ophthalmol. Visual Sri.
July 1979
740 Cynader
the anatomical position of rest of the eyes can
be altered by the unusual exposure history.
The resting length of the relaxed muscles
may thus be subject to modification under
these circumstances.
Time-dependent processes in the development of ocular misalignment. In recent years
much attention has been directed toward the
concept of the critical period, with reference
to the idea that the visual system is especially
sensitive to environmental manipulation at
certain stages in its development. Several aspects of interocular alignment appear to depend on the age of the subject. The incyclotorsion characteristic of dark-reared cats has
not been observed consistently in kittens less
than 60 days of age (Fig. 9). On the other
hand, kittens reared in the dark for 8 to 10
months seem, as a group, more incyclotorted
than kittens maintained in darkness for 4
months. These data suggest that the torsional
alignment of visually deprived kittens is initially normal and remains so until 60 to 120
days of age. During this period the incyclotorsion appears and is then maintained (and
may increase progressively) as deprivation is
prolonged. Similar conclusions have been
reached by Olson and Freeman16 in a longitudinal study of the development of ocular
alignment in dark-reared kittens.
The characteristic response of the deprived
organism to light exposure, namely, increased convergence and excyclotorsion of
the visual axes, can be observed following
deprivation periods as short as 30 days or as
long as 2 years. These data indicate that there
can be no tight "critical period" in early
development during which interocular misalignment, including esotropia and excyclotorsion, can be induced. At first glance this
would appear inconsistent with observations
in the clinical literature which indicate that
certain types of strabismus develop only at
particular ages.2"4' 30 There is evidence,
however, that one effect of maintaining animals in darkness is to allow the visual system
to retain its capacity for modifiability beyond
the duration of the naturally occurring critical
period.11' 27 The data showing that eye alignment is modifiable even in adult cats after 2
years of visual deprivation may be understood in the context of the persisting immaturity retained by the visual system so
long as deprivation is continued. Despite the
fact that esotropia and excyclotorsion may
develop in dark-reared cats of any age after
exposure to light, the speed with which ocular alignment changes depends on the age of
the animals. Following 30 to 60 days of darkrearing, marked alterations in ocular alignment may occur within a few days after the
animal is exposed to a normally lit environment, whereas longer term deprived cats
manifest similar changes only over weeks or
months.
I thank Dr. K. I. Beverly for valuable discussion and
Colleen Clattenburg for assistance in the preparation of
this report.
REFERENCES
1. Wheatstone, C : Contributions to the physiology of
vision. Part the first: On some remarkable and
hitherto unobserved phenomena of binocular vision,
Philos. Trans. R. Soc. Lond. 11:371, 1838.
2. Duke-Elder, S., and Wybar, K.: Ocular motility and
strabismus. In System of Ophthalmology, St. Louis,
1973, The C. V. Mosby Co., vol. 6.
3. Alpern, M.: Movements of the eyes. In Davson, H.,
editor: The Eye, New York, 1969, Academic Press,
Inc., vol. 3.
4. Burian, H.M., and Von Noorden, G.K.: Binocular
Vision and Ocular Motility: Theory and Management of Strabismus, St. Louis, 1974, The C. V.
Mosby Co.
5. Hubel, D.H., and Wiesel, T.N.: The period of susceptibility to the physiological effects of unilateral
eye closure in kittens, J. Physiol. 206:419, 1970.
6. Barlow, H.B.: Visual experience and cortical development, Nature 258:199, 1975.
7. Sherman, S.M.: Development of interocular alignment in cats, Brain Res 37:187, 1972.
8. Blake, R., Crawford, M.L.J., and Hirsch, H.V.B.:
Consequences of alternating monocular deprivation
on eye alignment and convergence in cats, INVEST.
OPHTHALMOL. 13:121, 1974.
9. Olson, C , and Freeman, R.: Development of eye
alignment in cats, Nature 271:446, 1978.
10. Kalil, R.: Dark rearing in the cat: Effects on visuomotor behaviour and cell growth in the dorsal lateral
geniculate nucleus, J. Comp. Neurol. 178:451,
1978.
11. Cynader, M., Berman, N., and Hein, A.: Recovery
of function in cat visual cortex following prolonged
deprivation, Exp. Brain Res. 25:139, 1976.
12. Vakkur, J.G., and Bishop, P.O.: The schematic eye
in the cat, Vision Res. 3:357, 1963.
Downloaded From: http://iovs.arvojournals.org/pdfaccess.ashx?url=/data/journals/iovs/933085/ on 06/12/2017
Volume 18
Number 7
Interocular alignment after visual deprivation 741
13. Bishop, P.O., Kozak, W., and Vakkur, J.G.: Some
quantitative aspects of the cat's eye: axes and plane
ol relerence, visual field coordinates and optics, J.
Physiol. 163:466, 1963.
14. Stryker, M.P., and Blakemore, C.: Saccadic and disjunctive eye movement in cats, Vision Res. 12:2005,
1972.
15. Cynader, M., and Berman, N.: Receptive-field organization of monkey superior colliculus, J. Neurophysiol. 35:187, 1972.
16. Olson, C , and Freeman, R. D.: Eye alignment in
kittens, J. Neurophysiol. 41:848, 1978.
17. Pettigrew, J. D.: The effect of visual experience on
the development of stimulus specificity by kitten
cortical neurones, J. Physiol. 237:49, 1974.
18. Van Hof-Van Duin, J.: Development of visuomotor
behaviour in normal and dark-reared cats, Brain
Res. 104:233, 1976.
19. Timney, B., Mitchell, D.E., and Giffin, F.: The development of vision in cats after extended periods of
dark-rearing, Exp. Brain Res. 31:547, 1978.
20. Rashbass, C., and Westheimer, G.: Disjunctive eye
movements, J. Physiol. 159:149, 1961.
21. Westheimer, G., and Mitchell, D.E.: The sensory
stimulus for disjunctive eye movements, Vision Res.
9:749, 1969.
22. Cynader, M.: Role of visual cortex in interocular
alignment, INVEST. OPHTHALMOL. VISUAL SCI.
23.
24.
25.
26.
27.
28.
29.
30.
18:
742, 1979.
v. Helmholtz, H.: In Southall, P., editor: Treatise
on Physiological Optics, New York, 1962, Dover
Publications, vol. Ill, p. 349.
Nakayama, K.: Geometry of binocular vision. Paper
presented at third annual Interdisciplinary Conference on Vision, Jackson Hole, Wyo., Jan. 1978.
Cooper, M., and Pettigrew, J.D.: A Neurophysiological determination of the vertical horopter in the
cat and owl, J. Comp. Neurol. 184:1, 1979.
Mustari, M., and Cynader, M.: Rapid recovery from
the effects of visual deprivation in cat parastriate
cortex. Neuroscience 3:570, 1977 (abst).
Cynader, M.: Extension of the critical period in cat
visual cortex. Presented at Association for Research
in Vision and Ophthalmology, April, 1977.
Jampel, R.S.: Representation of the near response
on the cerebral cortex of the macacque, Am. J.
Ophthalmol. 48:573, 1959.
Donders, F.C.: On the Anomalies of Accommodation and Refraction of the Eye, London, 1864, The
New Syndenham Society.
Taylor, D. M.: Is congenital esotropia functionally
curable? Trans. Am. Ophthalmol. Soc. 70:529,
1972.
Downloaded From: http://iovs.arvojournals.org/pdfaccess.ashx?url=/data/journals/iovs/933085/ on 06/12/2017