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Development of Binocular Vision

Development of Binocular Vision

Robert H. Duckman
Jojo W. Du

Binocular vision refers to the condition where the two eyes view a common portion of
visual space. In vertebrates, the size of this overlap ranges from 0° to about 190° in
humans (1). In visual space, objects occupy a three-dimensional space; the x- and y-
dimensions give the object visual direction, and the z-dimension gives the object depth
information. The x- and y-axes information can be obtained from the geometric retinal
image. The z-axes information, however, is not available to a single retina, but requires
the input from two retinae. For humans, the eyes are frontally placed and laterally
separated. This separation is crucial in providing the two eyes with slightly different views
of an object. These small differences in retinal images, known as disparity, provide the
critical z-axes information giving rise to depth perception.

Traditionally, Worth (2) classified binocular function into three hierarchically related
levels:

Bifoveal fixation

Fusion

Stereopsis

In normal adults, the presence of bifoveal fixation is a necessary prerequisite for fusion,
and fusion is essential for stereopsis. It is currently known, however, that bifoveal fixation
is not a sufficient condition for functional fusion or for stereoscopic abilities. This chapter
considers each of these three levels of binocular function to describe the mechanisms
underlying the development of bifoveal fixation and fusion, leading to the pinnacle of
binocular function, stereopsis, the ability to discriminate disparate information giving a
three-dimensional depth percept.

Stereopsis is an acquired ability; thus, newborn babies do not perceive binocular depth
until a sudden onset at age 3 to 5 months. This sudden onset is followed by a period of
rapid maturation that finalizes between 4 and 6 months of age, in which the adultlike
stereo- acuity is achieved. The oculomotor system is not mature at birth, but develops
rapidly in parallel with the anatomic development of the eye, vision, and the visual
pathway. Binocularity and stereopsis can only manifest if the eyes are accurately aligned.
At this early age, infants are very sensitive to conditions that interfere with visual
development. Common vision problems (e.g., uncorrected refractive errors, strabismus,
and visual deprivation) present during this period of plasticity can cause a permanent
reduction of stereoacuity by hampering the development of stereopsis. Early detection of
these anomalies within the critical period carries high potential for recovery and normal
vision development, because the potential to develop normal visual function seem to be
inversely related to age.

Early research on infant binocular vision failed to separate monocular and binocular cues
to depth. Owing to poor experimental design, results described in those initial studies
could be affected by monocular cues of depth or technical artifacts. Based on those
results, consistent conclusions regarding the binocular component of depth perception
could not be delineated. Subsequent studies were designed with the focus of increasing
understanding of binocular cues. Further research was made more accurate by studying
binocular cues in isolation from monocular ones, thus leading to more conclusive
information.

Ocular Alignment and Convergence

As the eyes track an object, they move in synchrony via yoked eye movements. This
results in synchronous retinal images. When both foveae are directed toward the same
target, a condition known as bifoveal fixation results. Similar retinal images and, hence,
bifoveal fixation are thought to be required for binocular fusion and stereopsis. In
preverbal infants, the development of bifoveal fixation has been studied indirectly by
measuring ocular alignment and vergence control. Although ocular alignment and
vergence control improves with age (3), several lines of evidence suggest that this is not
the limiting factor on early binocular function. Early studies of ocular alignment
suggested that infants often exhibit divergence (4,5), indicating a lack of bifoveal fixation
and, thus, accounting for the lack of binocular function and stereopsis. This is in contrast
to more recent findings that most newborn infants are orthotropic (6), thus indicating
that cortical development, rather than ocular alignment, is the limiting factor on early
binocular function.

Early eye alignment experiments conducted by Wickelgren (5) and Maurer and de Graaf
(4) presented visual targets and recorded the relative position of the two pupil centers
using corneal photography (5). Their research concluded that infant visual axes are
generally diverged. This technique had a pitfall, however; it measured eye alignment with
respect to the center of the pupil (optic axis), but did not take into account that the
optical axis did not coincide with the visual axis (line from the target to the fovea). This
optic axis-visual axis discrepancy is called the angle alpha. The results from their
experiments, therefore, could be affected by errors in their methodology. Later in 1975,
Slater and Findlay (7) concluded that binocular fixation was present at birth with a
limited response to static targets (10 and 20 inches). Although the corneal photography
method was used, previous limiting factor of the angle alpha was overcome by using an
average correction method (2).

Interestingly, Aslin (8) provided evidence that inaccuracies in binocular fixation during
early infancy are not the result of a divergence bias. The resting position of binocular
alignment in infants and adults was estimated by obtaining photographic measures of
interpupillary distance in total darkness. The mean dark vergence position in the adult
group corres- ponded to a distance of approximately 100 cm. The mean dark vergence
positions were 25 and 50 cm for infants aged 1 to 4 months and 6 to 18 months,
respectively. Hence, these results provide evidence that young infants’ inade- quate
convergence to near target distances is not the result of a divergence bias. Moreover,
these results suggest that the young infants’ oculomotor system can most easily maintain
binocular fixation at relatively near viewing distances. The correspondence between the
optic-visual axis discrepancy and interocular separation during development and the
validity of the estimates of dark vergence in infants is uncertain, however.

Although clinical observational reports indicate newborn infants often exhibit substantial
eye turns, mostly exotropia (9), Hainline and Riddell (3) proposed that some eye turns
were caused by the confusion of versions and vergences (as evaluated from a single
photograph taken of an off-axis infant) as well as the large angle kappa of newborn
infants. Angle kappa is the angle between the visual line, which connects the point of
fixation with the nodal points and the fovea, and the pupillary axis, which is a line
through the center of the pupil perpendicular to the cornea.

Thorn et al. (6) used the Hirschberg test to examine the ocular alignment in 34 healthy
infants; they reported that most infants are orthotropic in the first month. This is in
contrast with previous large sample (N = 1031–3316) studies that used the examiner’s
face as a fixation target as infants attend to a face better than to a light (10,11,12).
Besides the large angle kappa of newborn infants, Thorn et al. (6) have found the task of
judging the position of their own reflection from an infant’s cornea to be far more difficult
than the Hirschberg test. Another confounding factor, when using the examiner’s face as
a fixation target, is that the facial features on which the infant fixates change with age
(3). In any case, all studies concur that a substantial proportion of newborns are
orthotropic and that this proportion increases with age (13). Owing to the limited
cooperation of infants, methods available to test ocular alignment prove to be
insufficient. Hence, examiners have resorted to an indirect measure of ocular alignment.

To successfully fixate bifoveally, not only do the eyes need to be relatively well aligned in
the stationary state, but they also need to be capable of changing its alignment in the
appropriate direction should the object of interest move. To determine whether bifoveal
fixation is a limiting factor for stereopsis, a number of researchers measured the ability of
young infants to change their vergence in response to static and dynamic targets.

Using corneal photography, Aslin (14) recorded changes in binocular eye alignment in
infants 1, 2, and 3 months of age in response to a luminous target that moved along the
infant’s midline. In his experiments, angle alpha was not affected by changes in the
target distance because the light creating the corneal reflection was created by the
moving target itself, and was not a fixed light source as in previous experiments (5). The
results indicated that infants have the ability to converge and diverge in the appropriate
direction as early as 1 month of age, but they cannot consistently converge to near
targets until 2 months of age. Moreover, as age increases, the ability to respond
appropriately to faster target motion also increases (14).

Because disparity is a likely cue for the visual system to indicate the necessity for a
change in convergence, Aslin (14) also observed the saccadic refixation response to
wedge prisms, clinically known as the four-prism diopter base out test commonly used to
test for foveal suppression. The introduction of a prism during bifoveal fixation induces a
shift in the image of the target as viewed by the affected eye, thus creating diplopia. A
typical response to the four prism-diopter base out test consists of biphasic eye
movements: a saccade followed by a convergent movement. If the affected eye is
suppressed, the disparity created by the prism is not detected, and no eye movement
occurs. If suppression is not present, the affected eye detects the disparity created by
the prism and diplopia results. Eye movements will then be initiated to realign the foveae
to reattain fusion. A five- or ten-prism diopter wedge prism, which displaces the image
2.5° and 5° nasally, respectively, was placed alternately in front of each eye of infants 3,
4.5, and 6 months of age. Refixational eye movements in response to disparity induced
by wedge prisms were not present consistently until 6 months of age. This agreed with
earlier results by Parks (15), whose clinical reports indicate that saccadic response to a
prism test was not present in infants until 4 to 6 months of age.

Birch et al. (16) examined the hypothesis of whether the development of vergence
accounts for the onset of stereopsis by comparing the ages of onset for stereopsis with
and without vergence requirements. The presentation of stimuli near the horopter, which
is a geometric surface in visual space that passes through the point of bifoveal fixation
and contains all corresponding retinal points where single vision results (Fig. 7.1), did not
significantly alter the age of onset of stereopsis. Hence, the development of accurate
vergence is not the limiting factor in the development of stereopsis, but rather, the onset
of stereopsis is dependent on the development of neural mechanisms (16).

Moreover, Hainline and Riddell (3) measured monocular and binocular eye positions of
631 infants (aged 17–120 days) from photographic images of eyes when static targets
were presented (25–200 cm). Many of even the youngest infants showed good ocular
alignment, both monocularly and binocularly, although the youngest infants displayed the
greatest variability in vergence. This suggests that oculomotor constraints are not a
significant barrier to the development of higher forms of binocularity.

When infants are tested using tasks that require dynamic changes in vergence, a
different picture emerges. Ling (17) moved a target consisting of a black disc (2 inches in
diameter) along the infant’s midline from a distance of 3 to 36 in (at 2 inches/second);
she concluded that systematic vergence eye movements throughout the range of target
distances employed do not appear until 7 weeks postnatally. Aslin (14) also reported that
infants do not consistently converge to dynamic targets until 2 months of age, and do
not converge without delay until 3 months. This is in agreement with the Coakes et al.
(18) study where their results showed that convergence is well established by 3 months.

Figure 7.1 A schematic of an observer bifoveally fixating a point in space and the
resulting specification of the horopter, Panum’s fusion area, the region of
stereopsis and the region of diplopia.

This discrepancy could result from the use of static versus dynamic targets. Studies that
employ static targets (3) report good eye movement control, even in early infancy. When
dynamic targets are used (14,17), however, few report good eye movement control,
especially in the youngest infants. This suggests that different mechanisms could mediate
static versus dynamic vergence and that these may have different developmental time
courses during infancy. It is important to note that, although appropriate vergences are
made in response to a near target, it is by no means suggestive of bifoveal fixation, but
merely that the infant is fixating with consistent retinal points, which may or may not
correspond to the fovea. Nevertheless, it appears that neural mechanisms, not bifoveal
fixation (although necessary, but not limiting), are the limiting factor in the development
of stereopsis.

Fusion
Fusion is the combining of two retinal images into a single percept. When the two foveae
are aimed toward the same object in visual space, each eye receives similar stimulation
and, thus, gives rise to a fused percept of an object. Beside the foveae, many retinal loci
can yield fusion. These loci comprise the horopter. Single vision, however, can also occur
at areas around the horopter, known as Panum’s fusion area (Fig. 7.1). This area for
single vision is wider at the periphery. Any object located in front or behind Panum’s
fusion area does not stimulate corresponding retinal points, resulting in diplopia.

The development of binocular single vision is accompanied by the development of

oculomotor systems that function to keep images from the two eyes aligned. Binocular
single vision is composed of sensory fusion and stereopsis. Fusion is often referred to as
unification—a process by which the images formed on the retinas of the two eyes are
combined into a single percept. As a prerequisite to achieve fusion, the eyes must be
able to align themselves in such a manner that the retinal images of the fixated object
can be easily placed and maintained on the fovea of the two eyes. Any object located
outside of Panum’s fusion area while the subject is fixating on a target, does not
stimulate corresponding retinal points, resulting in diplopia in the absence of suppression.
As demonstrated by psychophysical and electrophysiologic measurements, human infants
display a rapid onset of fusion at 3 to 5 months of age, which correlates with the
development of stereopsis (19). To determine whether fusion is a prerequisite for
stereopsis, fusion has been measured in normal healthy infants as well as in those with
stra- bismus.

In normal healthy infants, fusion is not present at birth, but develops at approximately 3
months of age, corresponding to the development of stereopsis. To study the
development of binocular function in infancy, Braddick and Atkinson (20) examined visual
evoked potential (VEP) induced by random dot patterns that alternated between
correlated (fusible) and anticorrelated (rivalrous) states and found the median age at
which binocular VEP first could be detected to be 11.4 weeks. Gwiazda et al. (21)
determined the age of onset of fusion preference to be 12.4 weeks, and that female
infants (9.9 weeks) developed fusion-rivalry discrimination earlier than male infants (13.8
weeks). In concordance with Gwiazda et al. (21), Thorn et al. (6) used forced-choice
preferential looking (FPL) and found similar ages of onset of fusion (12.8 weeks) and that
the shift of preference from rivalrous to fusible stimuli occurred during a brief period,
often less than 2 weeks. Using both FPL and VEP protocols, which showed high
concordance, Birch and Petrig (22) reported that few infants aged 2 to 3 months
demonstrated fusion; most infants aged 5 months and older demonstrated fusion and
reached adult levels by 6 to 7 months of age in 149 healthy, full-term infants. Together,
studies on the ages of onset of fusion show close agreement. These findings suggest
that sensory fusion is not present at birth but develops rapidly over the first 6 months of
life.

To determine the effect of anomalous visual experience on fusion capabilities, a number

of studies examined fusion in children with early-onset infantile esotropia to gain insights
into the sequence of events that lead to strabismus. Eizenman et al. (23) measured VEP
responses to dynamic random dot correlograms (RDC) in children with early-onset
esotropia before and after surgical alignment. Before surgical alignment, 38% of children
showed detectable VEP responses (significantly different to age-matched normals),
compared to 85% after surgery (not significantly different to age-matched normals),
suggesting that children with early-onset esotropia have the capacity for fusion and that
a congenital sensory fusion defect is not the cause of esotropia (23). Although the critical
period for fusion development is longer than that of stereopsis (24

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Jun 5, 2016 | Posted by drzezo in OPHTHALMOLOGY | Comments Off on Development of

Binocular Vision

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