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Dissociated Vertical Divergence
Perceptual Correlates of the Human Dorsal Light Reflex
Michael C. Brodsky, MD
Arch Ophthalmol. 2002;120:1174-1178.
ABSTRACT
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Background Dissociated vertical divergence (DVD) has been attributed to a human
dorsal light reflex that emerges when single binocular vision is precluded
in infancy. If this is the case, then DVD should be associated with a subjective
sensation of tilt.
Methods Prospective examination of 9 patients with DVD and 9 control subjects
to determine whether monocular occlusion and alternate occlusion induces a
subjective sensation of visual tilt or body tilt.
Results Alternate occlusion disclosed a tilt in the subjective visual vertical
in 8 of the 9 patients with DVD and in none of 9 control subjects. On occlusion
of the fixating eye, a vertical pencil positioned in the sagittal plane was
perceived as instantaneously tilted, with its upper pole tipped toward the
side of the covered eye. This visual tilt was quickly followed by a perceived
rotation back to vertical, which coincided with the dorsally directed drift
of the covered eye.
Conclusion In patients with DVD, monocular occlusion is associated with a subjective
visual tilt that is annulled by a cyclovertical divergence movement of the
eyes. This observation supports the notion that DVD is a human dorsal light
reflex, which functions to restore vertical visual orientation when unequal
binocular visual input evokes a subjective sensation of visual tilt.
INTRODUCTION
IN LIVING ORGANISMS, light from the sky above and gravity from the earth
below have led to the evolution of sensory organs for vision and balance.
The bright sky serves as a hemispheric light source that provides a stable
visual reference for which way is up. In lower animals, the central vestibular
system integrates visual input from the 2 eyes and graviceptive output from
the 2 labyrinths to modulate postural and extraocular muscle tonus and maintain
vertical orientation.1-3
Although visual input is usually subordinate to vestibular input in establishing
postural orientation, some lateral-eyed animals also maintain vertical orientation
by equalizing visual input to the 2 eyes.4
Many fish and insects exhibit a dorsal light reflex in which illumination
from one side evokes a reflex body tilt toward the light.4-7
When a light is shined down from the right side, for example, the right eye
receives greater visual input than the left eye (Figure 1). This binocular disparity would only exist in nature if
the animal were tilted with its right side toward the sky. This visual imbalance
causes the central vestibular system to register a leftward body tilt relative
to the body position that would be necessary for the 2 eyes to receive equal
binocular visual input, and to reflexively alter postural tonus to correct
the tilt1-4
(Figure 1). In a vertically stabilized
fish, the same stimulus evokes a vertical divergence of the eyes to reorient
the interpupillary axis relative to the new light source, causing the eye
with lesser visual input to shift dorsally, and the eye with greater visual
input to shift ventrally3 (Figure 1).
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Figure 1. In the fish, increasing luminance
to the right eye by shining a light from the 1-o'clock position (as seen by
the animal) shifts subjective vertical clockwise toward the 1-o'clock position
(as seen by the animal). Visual objects aligned with the gravitational vertical
are therefore misregistered as being tilted counterclockwise toward the 11-o'clock
position relative to the animal's subjective vertical. A, Vertical objects
and the animal's body are subjectively misregistered as being tilted counterclockwise,
necessitating a clockwise body tilt toward the body position that is necessary
for equal binocular visual input. B, When a corrective body tilt is prevented,
the ocular component of this righting reflex evokes a vertical divergence
of the eyes to rotate the interpupillary axis toward a position that is perpendicular
to the altered subjective vertical.
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The term dorsal pertains to the back or upper
aspect of an animal. The dorsal aspect of the head in fish, quadrupeds, and
bipeds corresponds to the top of the head. In bipeds such as humans, the back
retains its phylogenetic dorsal orientation, although it is no longer the
upper aspect in the upright position. Humans with congenital strabismus who
never develop single binocular vision exhibit an atavistic resurgence of the
dorsal light reflex in the form of dissociated vertical divergence (DVD).8 When these strabismic humans fixate monocularly, the
nonfixating eye exhibits a slow dorsal rotation termed dissociated vertical deviation. This dorsal rotation can be elicited
by optically or mechanically reducing visual input to either eye. It can also
occur spontaneously when there is a fluctuating degree of sensory suppression
in one or both eyes.8 Eye movement recordings
have confirmed that DVD comprises a cyclovertical divergence in which the
fixating eye depresses and intorts while the nonfixating eye elevates and
extorts.9-11 Thus,
the alternative term, dissociated vertical divergence,
provides a more accurate mechanistic description of this movement.8
In fish, abrupt fluctuations in binocular visual input cause the central
vestibular system to register a tilt, and the ensuing dorsal light reflex
serves to annul this tilt by realigning the eyes and body to new a orientation
that the brain interprets as vertical. If DVD is a human dorsal light reflex,
then humans with DVD might be expected to experience a perceived visual tilt
(ie, a sensation that the visual environment is tilted) when the gradient
of visual input to the 2 eyes is abruptly altered. In this case, the cyclovertical
divergence associated with DVD should serve to reduce or eliminate the perception
of tilt. Alternatively, if DVD is not a human dorsal light reflex, then the
torsional component of DVD might be expected to induce a perception of visual
tilt. In this case, patients should perceive no visual tilt prior to the onset
of DVD, but a perceived visual tilt should be present after the DVD has occurred.
To elucidate the perceptual correlates of DVD, I examined visual tilt perception
in 9 patients with DVD and 9 normal control subjects.
PATIENTS AND METHODS
Nine patients with bilateral DVD were examined prospectively and consecutively.
Children who had been treated with previous cyclovertical muscle surgery were
excluded from the study since the resulting fundus torsion could influence
the perception of tilt. Dissociated vertical divergence was diagnosed when
occlusion of either eye evoked a dorsal rotation of the occluded eye. The
amplitude of the DVD was measured in both eyes using the vertical prism under
cover test. Visual acuity was measured in each eye, versions were examined,
field measurements were obtained, and a dilated retinal examination was performed
to look for static torsion.
To determine whether patients experienced a perceived visual tilt (ie,
a perceived tilt of the visual environment without any sensation of body tilt)
or subjective tilt (ie, a perceived tilt of the body) under monocular conditions,
each patient was instructed to view a pencil held vertically in the sagittal
plane midway between the 2 eyes during occlusion of each eye and during alternate
occlusion of the eyes. The patient's head was maintained in the upright position
before and during testing. Care was taken to assure that the pencil was not
slanted forward or backward in the sagittal plane, as a slant would optically
induce a monocular image tilt. Each patient was instructed to hold up his
or her index finger and to move this finger to demonstrate any perceived movement
of the pencil as each eye was occluded. The cover test and alternate cover
test were repeated 3 to 4 times in each patient to assure that perceptual
responses were consistent from one trial to the next. When a perceived motion
was noted, the patient was specifically asked whether the pencil appeared
to move sideways or to tilt. The patient was then asked, "does it look like
the pencil is moving, or does it feel like you are moving?" A labyrinthine
imbalance such as that brought on by spinning or by disease of the semicircular
canals, is generally perceived as a sensation of body movement in space. Thus,
a perceived sensation of body movement in space would suggest that unequal
visual input is inducing a labyrinthine imbalance, while perceived visual
tilt with no sensation of body movement would suggest that the neural pathways
activated by unequal visual input do not directly alter the relative output
of the 2 labyrinths. This test was also performed in 9 control subjects who
had normal stereopsis and no history of strabismus.
RESULTS
Patient ages ranged from 4 to 51 years. All but 1 patient was
younger than 15 years. Seven patients had a history of congenital strabismus
that had been treated with only horizontal muscle surgery. One child with
prominent DVD had a history of perinatal bruising of both eyelids, but had
never developed congenital esotropia, latent nystagmus, or nasotemporal asymmetry.
(The term nasotemporal asymmetry refers to a disparity
in monocular nasally directed and temporally directed optokinetic responses,
with normal nasal optokinetic responses, and impaired temporal optokinetic
responses. This asymmetry is normal within the first 6 months of life and
is retained throughout life in patients with congenital esotropia.) One adult
with no history of horizontal strabismus also had bilateral DVD with no latent
nystagmus or nasotemporal asymmetry. All patients were neurologically normal
except for one prematurely born child with congenital esotropia and delayed
walking who probably had periventricular leukomalacia.
The amplitude of the DVD in the 2 eyes was symmetrical in 5 patients
and asymmetrical in 4 patients. Six patients had grossly visible latent nystagmus.
Three patients had bilateral inferior oblique muscle overaction with a "V"
pattern and bilateral static extorsion of the globes. The one patient with
a history of prematurity had bilateral superior oblique muscle overaction
with an "A" pattern and intorsion of the globes.
On monocular occlusion, 8 patients reported an instantaneous tilt of
the pencil with its top tipped toward the side of the covered eye (Figure 2). This immediate perception of a
tilt seemed to precede any motor movement of the uncovered eye and was probably
caused by a change in perception only. This visual tilt was followed quickly
by a perceived rotation of the pencil back to vertical, which coincided with
a dorsally directed drift of the covered eye. (Note that if the fixating eye
is making a torsional movement, the subject will perceive the pencil as moving
in the opposite direction that the eye is rotating. Thus, if the subject sees
the rotation of the pencil such that the top goes from being nasally tipped
to straight up, this means that the 12-o'clock meridian of the cornea is rotating
nasally. So an apparent extorsional movement of the pencil would correspond
to an intorsional movement of the globe. This intorsional movement in the
fixating eye begins the phenomenon known as DVD.9-11)
The one patient who did not report a perceived tilt was the adult who had
idiopathic DVD and no other history of strabismus.
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Figure 2. Visual tilt evoked by monocular
occlusion in the strabismic human with dissociated vertical divergence. Gray
image of the pencil denotes perceived visual tilt immediately following occlusion
of one eye. Curved arrows denote the perceived rotation of the tilted visual
image back to vertical, coinciding with the appearance of dissociated vertical
divergence. On occlusion of either eye, the vertical pencil positioned in
the sagittal plane is perceived as instantaneously tilted, with its upper
pole tipped toward the side of the covered eye. This subjective visual tilt
is quickly followed by a perceived rotation back to vertical that coincides
with the cyclovertical divergence of the eyes.
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In patients who had markedly asymmetrical DVD, the visual tilt was usually
observed only when the dominant eye was covered. All 8 patients who reported
a sensation of visual tilt denied any sensation of head or body tilt. No spontaneous
head tilting was observed during alternate cover testing. Three patients also
perceived a sideways movement of the pencil during alternate occlusion. One
adult with DVD perceived no visual tilt or sideways movement on occlusion
of either eye. All 9 control subjects reported a horizontal movement of the
pencil without tilt on alternate occlusion.
COMMENT
In DVD, monocular occlusion evokes a subjective tilt of the visual environment,
which is followed by a cyclovertical divergence of the eyes and a perceived
rotation of the tilted visual environment back to the vertical. This sequence
of perceptual changes suggests that the cycloversional component of the DVD
functions to correct a perceived tilt and to thereby reestablish vertical
orientation under conditions of monocular fixation. In this discussion, I
adhere to the convention in vestibular research of describing subjective visual
tilt from the point of view of the subject rather than the examiner, although
figures are shown from the perspective of the examiner to facilitate clinical
application. According to this convention, when a patient looks "to the right,"
it is to the patient's right rather than the examiner's right, and so a clockwise
rotation of visual environment or a torsional rotation of the patient's eyes
must also be defined as clockwise from the patient's perspective.
True vertical corresponds to the gravitational
vertical. Our perception of true vertical is influenced by graviceptive input
to the 2 labyrinths and visual input to the 2 eyes. Subjective
vertical applies to an individual's internal vertical orientation relative
to true earth coordinates. When the subjective vertical is altered by neurologic
disease or abnormal binocular vision input, the patient will experience a subjective visual tilt, which is a percieved tilt of the
visual environment relative to the subjective vertical.8
As shown in Figure 1, increased
luminance input to the right eye of a fish tilts the subjective vertical clockwise
(as viewed by the animal), so that a vertical visual stimulus would then appear
to be tilted counterclockwise relative to the subjective vertical. The direction
of perceived visual tilt in DVD corresponds to the postural responses of lateral-eyed
animals that exhibit a dorsal light reflex. The same perceptual shift is reported
by strabismic humans with DVD when a binocular visual imbalance is induced
by occlusion of one eye (Figure 2).
Thus, with occlusion of the left eye, a right eye predominance would shift
the subjective vertical clockwise (as seen by the patient), so that true vertical
then appears to be rotated counterclockwise relative to the patient's altered
subjective vertical (Figure 3).
This counterclockwise tilt of the visual world, which is seen monocularly
with the uncovered right eye, evokes a cyclovertical divergence movement of
the eyes to erase the perceived tilt (Figure
3).
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Figure 3. Depiction of perceived visual
tilt following monocular occlusion in patients with dissociated vertical divergence.
SV indicates the subjective vertical (the patient's internal representation
of vertical). A perceived tilt of the visual environment (a tilt of the subjective
visual vertical) is determined by the position of vertical objects in the
visual world relative to the internal representation of vertical (ie, relative
to the subjective vertical). Left, Occlusion of the left eye evokes a monocular
tilt in the subjective vertical. Since the visual environment is perceived
in relation to the tilted subjective vertical, which the patient perceives
as vertical, the monocular visual environment, as viewed with the right eye,
is now perceived as tilted counterclockwise relative to the patient's subjective
vertical. Right, The human dorsal light reflex is a twofold movement consisting
of a primitive vertical divergence, which realigns the interpupillary axis
with the tilted subjective vertical (as in fish), and a newer cycloversional
movement that rotates both eyes torsionally in the direction of the tilted
visual environment. This counterclockwise cycloversional movement (ie, intorsion
of the right eye and extorsion of the left eye) produces a clockwise rotation
in the subject's tilted visual environment to realign it with the tilted subjective
vertical (which the subject perceives as vertical), thereby annulling the
subjective visual tilt.
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I have proposed that DVD is an atavistic resurgence of the dorsal light
reflex that is evoked by a binocular visual disparity in humans with early-onset
strabismus.8 Since the eyes retain some of
their primitive function as balance organs in humans, unequal visual input
induces a central vestibular imbalance in which the internal sense of vertical
no longer corresponds to the gravitational vertical (Figure 3).8 Some patients with DVD
also have a head tilt away from the side of the hyperdeviated eye,12-13 which corresponds to the postural
component of the dorsal light reflex in fish.14
This head tilt, which is not compensatory for binocular vision,12-13
may serve to align the head to the tilted internal vertical representation
(ie, the subjective vertical).14
Under monocular viewing conditions, patients with DVD may experience
a "schizophrenic" perceptual situation in which the eyes tell the brain that
the external world and the body are tilted relative to the altered internal
representation of vertical, while the otoliths tell the brain that the head
is upright.8 A similar sensory conflict is
induced when humans view a tilted visual world under experimental conditions.15 Under the latter circumstances, the brain strikes
a compromise, and the subjective visual vertical is tilted to an intermediate
position between what the eyes and labyrinths are telling the brain.15
In DVD, the dorsal rotation of the visually deprived eye corresponds
to the vertical divergence induced by the primitive dorsal light reflex. Although
the deviating eye is said to drift "upward" in humans with DVD, the direction
of rotation is not necessarily upward in space but always dorsal relative
to the head, regardless of whether the patient is positioned in the upright,
supine, or head-hanging position.16 Humans
with DVD also display a phylogenetically newer cycloversional movement that
corrects the perceived tilt of the visual environment.17
This ipsidirectional cycloversional movement can also be evoked by viewing
torsional optokinetic stimuli or by inducing a static visual tilt of the visual
environment.18-22
All of these visual stimuli evoke a reflex cycloversional movement, which
serves to align the tilted visual environment with the tilted internal representation
of vertical.22
Thus, the human dorsal light reflex comprises a twofold movement—a
vertical divergence to realign the interpupillary axis of the eyes relative
to the altered internal representation of the vertical, and a cycloversional
movement that torsionally rotates the eyes in the direction of the tilted
visual world to correct the perceived visual tilt (Figure 3). The vertical component of the human dorsal light reflex
is a primitive adaptation that corresponds to the purely vertical divergence
in fish. The phylogenetically newer cycloversional component conforms to Stephen
Jay Gould's definition of an exaptation, which is
a feature that did not arise as a primary adaptation, but one that was subsequently
co-opted or grafted on to meet the newer demands of evolution (in this case,
frontally placed eyes).23 According to Gould,
exaptations are features that were not originally built by natural selection
for their current role, but that now enhance fitness (in this case, by restoring
vertical orientation under monocular viewing conditions in the frontal-eyed
human).23
The human dorsal light reflex demonstrates how the central vestibular
system can uncouple the vertical and torsional components of a cycloversional
movement to allow each component to subserve its corrective function relative
to specific conditions of a perceived tilt. During head or body tilt in humans,
altered otolithic tone (ie, unbalanced input from the 2 labyrinths rather
than from the 2 eyes) stimulates elevation and intorsion of the lower eye
in space, and depression and extorsion of the higher eye in space.24 This stimulus forms the basis of the Bielschowsky
Head Tilt Test.25 In DVD, however, the elevating
eye extorts, and the depressing eye intorts, producing a cyclovertical divergence
in which the torsional eye movements are opposite to those evoked by head
tilt.8 This dissociation could occur only if
the central vestibular system separately processes visual disparity input
and graviceptive input from the trunk and otoliths, then integrates them to
establish subjective vertical orientation as it does in fish.1, 8
The central ocular motor command centers must be at liberty to implement separate
commands for vertical divergence and cycloversion in humans, although the
2 signals produce a single integrated extraocular movement.
This study needs to be viewed in light of its inherent limitations.
First, it is a qualitative and subjective study that was performed in a clinic
setting. The advantage of this simple method is that it enables the practicing
ophthalmologist to confirm or refute these results without the need for special
instrumentation. This disadvantage is that, because eye movement recordings
were not obtained, a precise and quantitative temporal relationship between
the appearance of DVD and the resolution of the subjective visual tilt could
not be confirmed. Second, it is well recognized that both eyes normally extort
in convergence.26 One could therefore question
whether the perceived image intorsion when the dominant eye is uncovered might
result from each eye being in an extorted convergent position relative to
the vertical object. If this were the case, however, one would expect the
control group to have experienced the same perceptual changes since their
eyes would also extort during convergence. However, this did not occur. Third,
von Helmholtz27 determined that the subjective
vertical retinal meridian is tilted approximately 1° in each eye, with
its top tipped temporally.27 This subjective
tilt could cause the top of a vertical line to appear to be tipped nasally
(ie, tilted toward the side of the covered eye, as shown in Figure 2). 28 As such, it could be
argued that this small degree of extorsional tilt in the subjective vertical
retinal meridians of each eye could potentially contribute to the perception
that the monocular image appears instanteously intorted when either eye is
uncovered. If this were the case; however, one would again expect the control
group to have perceived a similar visual tilt. Yet, only patients with DVD
perceived a visual tilt under monocular conditions, suggesting that this effect
did not influence the results of this study. Furthermore, the original von
Helmholtz measurements of the subjective retinal vertical, like standard horopter
measurements, were obtained using isolated visual stimuli in the absence of
any surrounding contextual cues. In this study, normal background contextual
cues were present, so one would not expect patients in either group to detect
this small vertical bias. Fourth, it is not clear why the group of patients
with DVD were less likely than the control group to report a perceived lateral
movement of the pencil when the cover was switched from one eye to the other.
It could be that the perception of tilt overrides the perception of lateral
movement in these patients; that surgically corrected congenital esotropia
is associated with an altered perception of visual space under monocular conditions;
or that I was more attuned to elucidating the direction and sequential changes
of the perceived tilt in patients with DVD, and that verbal or nonverbal cues
could have influenced patient responses. Last, one could argue that if DVD
is not a human dorsal light reflex, this cyclovertical divergence could be
the cause rather than the result of the observed perceptual changes. In other
words, extorsion of the covered eye in DVD could cause the vertical pencil
to appear momentarily intorted when the either eye is uncovered. As the eye
intorts to fixate, the image would extort, producing a similar sequence of
perceptions as observed. If this were the case, one would expect patients
with DVD to report that the image of the pencil shifted from an initial position
of intorsion to a final position of extorsion. However, all patients with
DVD stated that the tilted image of the pencil appeared vertical following
its rotation, which would only occur if this reflex cycloversional movement
served to correct the monocular visual tilt. This perceptual response suggests
that this complex cyclovertical movement must function to reestablish vertical
visual orientation when binocular vision is preempted.
In conclusion, DVD is associated with a subjective tilt of the visual
environment and a reflex cyclovertical divergence of the eyes. This subjective
visual tilt appears to drive both components of the resulting cyclovertical
divergence. These perceptual correlates add to the accumulating body of evidence
that DVD is a human dorsal light reflex, which serves to restore vertical
visual orientation under monocular conditions. In DVD, a subjective sensation
of visual tilt under monocular viewing conditions evokes 2 compensatory eye
movements—a phylogenetically older vertical divergence movement (ie,
a primitive adaptation) to realign the eyes relative to the altered internal
representation of vertical, and an exaptive cycloversion movement that torsionally
rotates the eyes in the direction of the tilted visual environment to restore
vertical visual orientation by neutralizing the perceived visual tilt. The
vertical component of this movement corresponds to the ancestral dorsal light
reflex in fish, while the cycloversional component of the human dorsal light
reflex appears to be an exaptation that functions to annul the subjective
visual tilt under monocular conditions when the eyes are frontally placed.
This twofold reflex movement corresponds both in theory and in actuality to
the ocular motor response that would result from a tilted internal representation
of the visual vertical. In the human dorsal light reflex, the direction of
the cycloversion movement relative to the vertical divergence is opposite
to that observed during a head tilt in space, demonstrating that the vertical
divergence and the cycloversional component of visual tilt are independently
programmed, and that these 2 extraocular movements can be dissociated by unequal
visual input to the 2 eyes in humans with congenital strabismus.
AUTHOR INFORMATION
Submitted for publication October 12, 2001; final revision received
April 11, 2002; accepted May 23, 2002.
Supported in part by a grant from Research to Prevent Blindness Inc,
New York, NY.
Reprints: Michael C. Brodsky, MD, Arkansas Children's Hospital, 800
Marshall St, Little Rock, AR 72202.
From the Departments of Ophthalmology and Pediatrics, University of
Arkansas for Medical Sciences, Little Rock.
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