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The Absence of So-called Compensatory Ocular Countertorsion
The Response of the Eyes to Head Tilt
Robert S. Jampel, MD, PhD;
Dian X. Shi, MD
Arch Ophthalmol. 2002;120:1331-1340.
ABSTRACT
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Objectives To show that so-called compensatory ocular countertorsion (static ocular
counterrolling) does not exist and to describe the torsional eye movements
that occur while the head is tilting.
Methods Two miniature video cameras, a fiberoptic light source, and a fixation
target were suspended from a headband. The cameras, fixation target, and light
source moved in synchrony with the head. One camera videorecorded iris and
conjunctival landmarks, and the other recorded head movement and position.
The video frames were digitized and analyzed using computer algorithms.
Results The eyes showed no compensatory ocular countertorsion in any stabilized
head tilt position. During head tilt, periodic torsional eye movements occurred.
These movements included a tonic counterlag followed by a saccadic forward
torsion that rotated the eyes prior to the head; this was followed by a saccadic
countertorsion that realigned and synchronized the eyes with the head, bringing
the eyes and head into equilibrium.
Conclusions Compensatory ocular countertorsion does not exist. Torsion occurs only
during head tilt. The eyes are oriented to the brain and not to the horizon.
When the head stabilizes in any tilted position, the retinas assume the same
dynamic state of equilibrium with the brain that they assume in every other
position. The main function of the oblique muscles is to stabilize the retinas
in relation to the brain in all held head positions and directions of gaze.
During head tilt, the oblique muscles produce involuntary torsional movements
of small amplitude (up to approximately 10°) that appear to anticipate
the final head position and prepare the eyes for obtaining retinal correspondence.
These torsional movements may protect the retinas by dampening the effect
of the head movement on this sensitive tissue.
INTRODUCTION
IT IS GENERALLY BELIEVED that the eyes manifest compensatory ocular
countertorsion (COCT) (also known as static ocular counterrolling) around
the visual line when an earthbound person tilts his or her head and holds
it at a steady angle to the shoulder or terrestrial horizon. For example,
when the head is held in a tilted position at about 50°, the eyes undergo
countertorsion around an anterior-posterior axis that is variable but always
less than 50°. Compensatory ocular countertorsion is believed to be caused
by the gravitational and inertial stimulation of the hair cells in the otolith
organs of the vestibular apparatus. Hypothetically, otolith function could
be evaluated by measuring COCT, which may be diminished in a state of weightlessness.
These measurements might also yield information concerning vestibular physiologic
characteristics, the cause of space motion sickness, and the mechanisms of
ocular and neurological abnormalities.1-11
Compensatory ocular countertorsion has been accepted as a foundation
or variable in many scientific studies on vestibular and ocular motor physiologic
characteristics and as a precept in the interpretation of clinical ocular
motor defects.12-26 The
existence of COCT is so universally accepted that there is even a published
history of this phenomenon.27 The Nagel1 law states that any degree of sideways tilt of the
head toward the shoulder produces a torsional rotation of both eyes in the
opposite direction, equal to approximately one sixth of the degree of head
tilt. Although subsequent investigators have demonstrated that COCT is highly
variable and asymmetrical in every position of head tilt, all agree that its
magnitude is directly related to the magnitude of the head tilt.1-26
There are logical reasons to believe in the existence of ocular torsion
as a normal compensatory mechanism for head tilt. Orbital dissection shows
that the eyes move within lubricated ball-and-socket joints and therefore
seem capable of 3 degrees of freedom of motion: horizontal, vertical, and
torsional. This belief is reinforced by the anatomical locations of the insertions
of the oblique extraocular muscles, whose primary function would appear to
be torsion.28 An area for the so-called neural
integration and control of torsional and vertical movements has been identified
in the midbrain nucleus of Cajal.29
Experimental methods with natural and artificial ocular surface landmarks,
astigmatic axes, after images, the blind spot, digital tracking, and cinematography
have been used to demonstrate COCT.30 In recent
studies, the measurement of COCT varied between 7° and 14° depending
on the subject and whether or not astigmatic axes, Maddox rod images, or cinematography
was used to confirmed the existence of this phenomenon.7, 10, 15, 18 The
scleral induction coil method has shown that involuntary torsional movements
occur in the primary position and in different directions of gaze.31-32 Some investigators have observed
static compensatory torsion by watching their eyes in a mirror after tilting
their heads.1, 15
Because the existence of COCT has important implications in ocular motor
physiology and clinical neuroscience, we decided to investigate the effects
of head tilt and head movements on eye movements using video-oculography (VOG)
and computer algorithms.
METHODS
Measurements of eye movements in healthy subjects in stable head tilt
positions and during head tilt were obtained using VOG.10, 33 This
technique is noninvasive, free of electronic noise, and independent of electronic
field interference. Unsophisticated, untrained subjects can be tested using
different experimental conditions, and the obtained measurements are direct
because the investigators can see what they are measuring. The calibrations
of the measuring tools in the computer algorithms were easily checked against
common rulers and protractors and were found to be accurate to at least one
tenth of a degree, an accuracy that proved more than adequate for this study.
The limitation of VOG is a low sampling rate of 30 frames per second.
APPARATUS
Two microhead miniature video cameras (GP-KS152 with a 7-mm wide-angle
lens; Panasonic, Secaucus, NJ), a needle-thin fiberoptic light source, and
a rigid, thin 32-cm aluminum rod were suspended from an adjustable headband.
One camera was affixed to a mechanical coupling that allowed 3 degrees of
freedom of movement. This camera could be focused on the eye from different
angles at distances that produced the sharpest possible images. Its function
was to record eye movements. The other camera was attached to the side of
the headband pointing backward and was focused on a black-and-white backlighted,
translucent screen behind the subject. It was used to measure the angle of
head tilt and the velocity of head movement. The fiberoptic light source could
be pointed at the eye from different directions to produce optimum and uniform
illumination of the anterior eye surface. The aluminum rod was used to suspend
a target at various distances (usually about 32 cm) and locations in space.
Thus, the cameras, light source, and target moved simultaneously and synchronously
with the head. The apparatus weighed about 700 g (Figure 1).
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Figure 1. The experimental apparatus.
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The microhead video camera magnified the diameter of the iris about
12 times and its area about 144 times. With this magnification, the micromovements
of the eyes were visible on the computer monitor. Artifacts caused by macromovements
of the eye (version or vergence), the displacement of the headband, forehead
wrinkling, and eye blinking were easily managed because they were seen in
progress.
The VOG images were displayed on a video monitor and split vertically
into 2 parts. The image of the anterior surface of the eye was displayed on
seven eighths of the split screen. The image of the alternating black-and-white
stripes, representing head position, was displayed on one eighth of the screen.
The movements and positions of the eye and head were then simultaneously recorded
on a standard videotape at 30 frames per second.
FRAME CAPTURE
The analog videotapes were reviewed using an editing control unit (RM-86U;
JVC, Wayne, NJ). Selected clips from the analog tapes were then digitized
using a video graphics board (Targa 2000; Truevision, Santa Clara, Calif).
The usual clip was 30 seconds in duration and contained 899 frames. Individual
numbered frames or sequences of frames of the eye, with the head tilted in
the coronal plane and held in different spatial positions (eg, with the body
supine or on one side), were then captured from the larger clips and stored
on the hard drive.
The stored digitized video files were copied to Adobe Photoshop 5.5
software (Adobe Systems Inc, San Jose, Calif) for analysis. The Photoshop
layering tool was used to organize the frames in sequence. The first frame
was selected and displayed as the background layer. The second frame in the
sequence was selected and copied. The first frame was then reselected, and
the second frame was pasted as layer 1 on top of the background layer. The
procedure was repeated until all of the frames were contained in a numbered
sequence in a single graphics-layered document. Empty layers were added at
the end of the sequence, on which various landmarks from the background frame
were traced. These layers could be moved independently and superimposed onto
the other frames of the sequence.
MEASUREMENTS
The eye measurements used in our study were, for practical purposes,
schematic (Table 1). Like all
biological measurements, they encompass a physiological range and vary from
time to time and according to subject. The angular tilt and velocity of the
head were measured from the captured frames at 30-millisecond intervals using
the rectangular bars that contained the alternating black-and-white stripes.
The measuring tool of Adobe Photoshop 5.5 was used for obtaining measurements.
This versatile tool can measure an angle to 0.1° (6 minutes of arc) and
a linear distance between pixels of 0.16° (10 minutes of arc).
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Schematic Measurements Used in the Experiments
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The number of pixels in an iris image was related to its magnification
and ranged from 360 to 480 pixels. Thus, each pixel was between 7.5 and 10
arc minutes in length. The iris was about one sixth of the circumference of
the globe, or approximately 60°. If the number of pixels in the diameter
of the iris was 360 and the iris diameter was 12 mm, each pixel was approximately
0.16° or 10 arc minutes.
To measure velocity and change in position, the limbus was bracketed
using guidelines selected from the view menu of Adobe Photoshop 5.5. Guidelines
appear to float over the entire image and can be moved independently from
frame to frame. They were used to measure in pixels the amount of eye movement
that occurred in 30-millisecond intervals.
LANDMARKS
The anterior surface of the eye has iris, limbal, and conjunctival landmarks.
At first, 2% pilocarpine hydrochloride was instilled to control iris movement.
This proved unnecessary because iris landmarks are displaced radially and
limbal landmarks are not displaced at all by iris movement. In addition, because
the light source moved with the head, the iris was evenly illuminated, which
also minimized iris movement. Conjunctival vessels proved to be suitable landmarks.
Even though the conjunctiva is fixed at the limbus and loose over the scleral
surface, there was no distortion of the conjunctival vessels during eye movement.
SUBJECTS
The eye and head movements of 15 subjects (7 men and 8 women) were recorded.
All were healthy adults who ranged in age from 21 to 74 years. Visual acuity
in all subjects was 20/25 OU or better without correction, with contact lenses,
or following refractive surgery. All had clinically normal-appearing conjunctivas,
irises, and retinas and clinically normal eye and head movements. All subjects
gave informed consent for this study, which was approved by the Human Investigation
Review Committee of Wayne State University School of Medicine (Detroit, Mich).
RESULTS
EYE ORIENTATION WITH THE HEAD HELD STEADY AT DIFFERENT ANGLES OF HEAD
TILT
Six landmarks were traced on images of a greatly magnified (approximately
x144) segment of the iris (Figure 2A). The landmarks were traced using the Adobe Photoshop 5.5 pencil
tool with a line 1 pixel thick. Each landmark was drawn in a separate layer
using the Photoshop layering tool. The tracings could be moved independently
of each other or merged in varying combinations and were shifted away from
the landmarks to show their configurations. Iris segments were further enlarged
to show details (Figure 2B and C).
The tracings could be moved to outline the landmarks with a precision greater
than 10 arc minutes.
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Figure 2. A, Tracings of 6 iris landmarks
in a greatly magnified iris segment. The tracings are drawn in separate moveable
layers using Adobe Photoshop 5.5 (Adobe Systems Inc, San Jose, Calif) and
can be superimposed with micrometerlike precision (± 10 arc minutes)
onto the landmarks (B and C).
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The head was tilted to the left shoulder from 0° to 90° and
held for about 5 seconds at randomly selected angles (Figure 3). The magnitude and velocity of the head tilt were measured
from the alternating black-and-white stripes. Eye frames were obtained from
the video clips for analysis at 3°, 12°, 33°, 46°, 60°,
and 90°. The outlines of the tracings of the selected iris landmarks were
superimposed individually in each frame. The superimposed tracings were precise
and identical in each frame. If COCT was present, it was less than 10 arc
minutes.
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Figure 3. Six video frames of the iris with
the head held tilted to the shoulder and horizon from 3° to 90°. Superimposition
was precise and identical in all frames. There was no compensatory ocular
countertorsion. Striped bars indicate the degree of head tilt.
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Two other methods were used to determine eye orientation in different
positions of head tilt (Figure 4).
A rectangular segment of the conjunctiva containing conspicuous blood vessels
was selected from the initial frame and placed in its own layer. Its opacity
was then reduced to 60%. Thus, when this layer was superimposed, the conjunctival
vessels in the frame were seen through the rectangular conjunctival segment
(Figure 4B). Insets of the segment
of conjunctiva were placed on top of the striped bar that indicated the angle
of head tilt. Although the conjunctiva adheres relatively loosely to the sclera,
the superimposition of the tracings was precise in different head tilt positions.
No COCT was measured.
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Figure 4. Six video frames of the iris with
the head held tilted to the shoulder from 6° to 57°. B, Conjunctival
vessel tracing proved adequate for measuring eye orientation. C, Pixel color
values also provided a means of measuring eye orientation. Striped bars indicate
the degree of head tilt.
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Iris areas were selected based on the similarity in color of adjacent
pixels using the Adobe Photoshop magic wand tool (Figure 4C). The iris collarette of this subject is shown in detail.
The collarette layer was superimposed onto each frame. No COCT was measured.
The left eye of this subject is focused upward and slightly outward
(Figure 5A). The configuration of
conjunctival vessels near the limbus remained the same at head tilts of 3°
to 80°. The superimposition of the layer of conjunctival vessels was precise
in all frames. No COCT was measured. All 15 subjects had the same findings
as described previously.
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Figure 5. A, The configuration of conjunctival
vessels remained the same at all positions of head tilt (indicated by the
striped bars) with the eye held elevated and slightly abducted. The superimposition
of the conjunctival vessels was precise in all frames. B, Conjunctival vessels
at 3° of tilt. C, Conjunctival vessels at 80° of tilt.
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EYE MOVEMENTS DURING HEAD TILT WITH THE FIXATION TARGET MOVING WITH
THE HEAD
During head tilt, the eyes underwent involuntary, unconscious movements
around an anterior-posterior axis. These periodic eye movements had 3 phases.
The first was a small-amplitude tonic countertorsional movement. The second
was a forward-torsional saccade that accelerated prior to the head. The third
was a counter-decelerating saccade that allowed the head to catch up to the
eye. The cycle repeated itself until the eyes and the head came to rest and
achieved a dynamic equilibrium that was devoid of torsion.
Although the amplitude of the eye movement varied from subject to subject,
the pattern of alternating tonic and saccadic movements was consistent. The
amplitude of the saccade was directly related to the velocity of the head
movement (Figure 6 and Figure 7). Active (attentive) fixation caused
a decrease in the amplitude of the movement (ie, a blurred target produced
visible eye movements of relatively large amplitude), and a clear target produced
small-amplitude movements (Figure 7B).
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Figure 6. The measurement of ocular torsion
during head tilt (indicated by the striped bars). The head was tilted to the
left shoulder at about 30°/s. Three frames of the left eye were obtained
at 30-millisecond intervals and were captured between 32° and 34°
of head tilt. A, The eye lags behind the head. B, The eye makes a saccade
in the direction of the head tilt in less than 30 milliseconds, as shown by
the blurriness of the frame. The sampling rate was not fast enough to record
the saccade in detail. C, The eye has moved prior to the head. D, The angle
of saccadic torsion was 4° at about 34° of head tilt. Circle indicates
initial position of iris; X, center of pupil; and E, rotation of iris after
30 milliseconds. Together they form the angle of forward rotation of approximately
4°.
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Figure 7. A, The eye lags behind the head
and periodically makes a saccade to catch up to the head. When the head ceases
tilting and holds its position, the eye and head are in synchrony. B, The
amplitude of the saccade is determined by the velocity of the head tilt.
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The location of the anterior-posterior axis usually did not correspond
with the visual line. Head tilt generally was not "pure" but was associated
with a vertical (pitch) and/or horizontal (yaw) rotation of the head. These
rotations caused a shift of the anterior-posterior rotational axis away from
the visual line. Rotation around such an eccentric axis added a vertical and/or
horizontal component to the head tilt.28
When the head moved slowly (<10°/s) and the subject held fixation,
the magnitude of these movements was minimal. When the head tilted rapidly
(>10°/s), the torsional eye movements were visible, but in no instance
did the magnitude of the torsional saccades exceed approximately 12°.
POSSIBLE CAUSES OF ARTIFACTUAL COCT
It is difficult to produce pure head tilt and prevent small-scale lateral
and vertical head movements. A slight amount of head movement may cause a
significant shift of the eye in the orbit or a shift of the head from a stable
frontal plane. For example, a vertical or horizontal head movement of only
1 mm may cause a 1-mm shift of the eye in the orbit. This small shift could
produce an angular error of 5° (1 mm on the retinal surface is about 5°
or 900 µm). When projected onto a flat surface and recorded on photographic
film or videotape, these shifts cause the landmarks to show a measurable angular
deviation, which may be interpreted as COCT. In addition, the fixation target,
if not in a constant location relative to the head tilt, may cause an eye
shift in the orbit (Figure 8 and Figure 9).34
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Figure 8. The illusion of torsion results
when the eye does not maintain the same position in the orbit during head
tilt. During a head tilt from 2° to 90°, the eye gradually shifts
its position in the orbit about 12°. The landmarks, indicated by the black
dots, form an angle of 7° at 2° of head tilt and an angle of 12°
at 90° of head tilt, a difference of 5°.
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Figure 9. A, The illusion of compensatory
ocular countertorsion is explained schematically with the projection of a
line from a curved to a flat surface. Line AB indicates the diameter of the
iris in the primary position that projects to A'B' on a flat screen
(EF), which measures 1.77 U. Line CD indicates the diameter of the iris rotated
23° from the primary position. It projects on EF to C'D',
which measures 1.51 U. Circle indicates center of rotation. B, A schematic
drawing of the iris is shown in the primary position and in lateral and oblique
gaze. A line connects limbal landmarks G and H. The iris landmark (IRL) is
a designated linear fold or crypt. The angle formed with the dotted line by
GH and IRL varies with the iris position. The angle also varies with the position
and configuration of the landmark. These variations in the angles may be interpreted
as torsion. To study uncomplicated head tilt, it is necessary to eliminate
these movements and maintain the eye in a steady position in the orbit.
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To prevent horizontal and vertical rotation of the head during tilt,
researchers have used fitted plastic head and body shells and casts, alginate
dental material, straps, and the so-called human disorientation device. However,
the scalp is moveable over the underlying skull, and even when a plastic cast
or headband is tightened to the point of discomfort, slippage of the device
is possible. Despite restraint with a mechanical device, the head tends to
make small lateral and/or vertical movements when tilted. Bite bars, which
may be slightly askew, limit the head movement to the axis of the bar. They
are generally uncomfortable, and when the head is tilted, slight slippage
is possible no matter how carefully the bite bar is fitted.
The failure to distinguish between what happens during head tilt and
what happens when the head is held steady may be a source of artifact. The
intermittent torsional movements that occur during head tilt may be interpreted
as COCT. The scleral induction coil technique has the sensitivity to record
these movements.29-32,35-36 Other
possible causes are the nonuniform illumination of iris crypts and folds,
which cast shadows of varying depths and sizes, and the displacement of fixation
targets. Artifact may also be caused by the slippage of contact lenses, variations
in intraocular pressure, or ocular pulsations and blinking.
COMMENT
STEADY HEAD TILT
When the head is held steady in any position tilted to the horizon or
shoulder, healthy subjects affected by earthbound gravity show no COCT. The
gravitational force on the extraocular muscles, supposedly mediated by impulses
from the otolith apparatus, is counterbalanced by impulses that probably arise
from the reticular activating system of the brain stem, the contralateral
otoliths, the visual cortex (possibly the fusion reflex), or all 3. The eye
weighs between 7 and 8 g, and the head weighs about 2800 g. Thus, the head
weighs approximately 360 times more than the eye. The headband and suspended
cameras add an additional 700 g to the head. Despite this extra weight, which
should add increased inertial and gravitational stimulation to the otoliths,
no COCT results. We conclude that the eyes (retinas) are oriented to the head
(brain) and not to the terrestrial horizon and that the effects of gravity
are neutralized by the tonus in the extraocular muscles.
DURING HEAD TILT
During head tilt, the eyes undergo intermittent, involuntary torsional
tonic and saccadic movements that are not conscious. These torsional movements
take place around an anterior-posterior axis that is determined by the complexity
of the head movement (ie, whether the head while tilting also has a horizontal
and/or vertical component). When the axis of rotation does not correspond
to the visual line, the anterior pole of the axis (the index point for all
eye movement) transcribes a small circle of latitude that adds vertical and
horizontal movements to the torsional movement (an eccentric torsion, a skewlike
deviation).37-42
The torsional movements have alternating, intermittent tonic and saccadic
phases. In the tonic phase, the eyes appear to lag behind the head. In the
saccadic phase, the eyes accelerate prior to the head and then decelerate,
allowing the head to catch up to the eyes. The movements have the same amplitude
and duration in both eyes. The amplitude of the saccades increases and their
number decreases as the head tilts faster. When the head tilts rapidly or
the image is blurred, the saccades are visible without magnification. When
the head tilts slowly, the torsional movements are of small amplitude and
may require magnification to be seen. Conscious attention to a fixation target
decreases the amplitude of the torsional movements. The peak velocity and
duration of the saccades depend on their amplitudes. Torsional saccades have
been measured from about 2° for sharply focused images to about 12°
for indistinct images.37-42
OBLIQUE MUSCLES
The consensus is that the functions of the oblique muscles are to produce
torsion, to provide COCT to compensate for head tilt, to produce vertical
eye movements in synergy with the vertical rectus muscles, and by co-contraction,
to supplement the abduction produced by the lateral rectus muscle. The absence
of COCT suggests that the principal function of the oblique muscles is to
provide a servomechanism for the inhibition of ocular torsion, thus allowing
ocular stability in all held head positions in space and in all gaze directions.
A secondary function is to produce the torsional movements during head tilt
that compensate for the inertia of the head. (The head weighs at least 360
times more than the eye.) The magnitude of these involuntary torsional movements
is directly related to the velocity and amplitude of the head movements, but
they rarely exceed 10°. In vertical and oblique movements, the oblique
muscles act synergically with the rectus muscles to prevent torsion.43 Thus, a constant equilibrium between the retinas
and the brain is maintained, and retinal correspondence is preserved in all
head positions in space.
OTOLITHS
Otolith ablation in cats causes alterations in the extensor muscle tonus
of both the homolateral limbs and contralateral cervical musculature. The
head-righting reflex is diminished, and there is a loss of the compensatory
eye movements that result from the alteration of head positions in space.
Experimental evidence suggests that the otoliths detect changes in gravitational
and inertial forces and are responsible for the orientation of the head and
body in space and for the nystagmus produced by linear acceleration; however,
an extensive literature search found no experimental evidence to support the
general belief that the otoliths are responsible for COCT.44
Electrical stimulation of the cat's otolith apparatus and utricular
nerve produced torsional movements, smooth vertical or horizontal movements,
and horizontal nystagmus.45-46 Stimulation
of the utricle produced horizontal eye movements, whereas stimulation of the
saccule caused vertical eye movements. In these experiments, the eye movements
could not be correlated with those of the head. An alternative interpretation
of these findings is that the eye movements resulting from unilateral utricular
stimulation are part of a stabilizing mechanism that keeps the eyes and head
in equilibrium in all positions of head tilt. The midbrain's so-called neural
integrator for torsional movements may also have an inhibiting and stabilizing
function rather than an excitatory function.29
CONCLUSIONS
The function of the intermittent torsional movements is probably to
dampen the possible harmful effects of head movement on the retinas, thereby
allowing the retinas to rapidly and precisely orient to new head positions.
When head or body tilt causes the fixation object to be out of view, the saccades
anticipate a new orbital position and fixation object.47
Torsional eye movements have the same characteristics as movements induced
by rotation of the head around a horizontal or vertical axis.41 The
difference is that torsional movements take place around an anterior-posterior
axis. They are probably caused by stimulation of the semicircular canals and
not the otoliths. The otoliths may counteract the effects of gravity and contribute
to the stability of the eyes and head in space. In any sequence of head movement,
the vestibular apparatuses act as integrated wholes.45, 48-49 When
the head comes to rest in any position tilted to the shoulder or horizon on
earth, the eyes and head establish a dynamic equilibrium in which there is
no COCT. In this state of equilibrium, the large-scale, visible (macroscopic)
eye movements are absent. Although the eyes do not appear to be moving during
fixation, they are moving microscopically back and forth across the foveolae
in flicks, drifts, and tremors.49 This dynamic
equilibrium between the retinas and the brain is the same in all positions
of steady head tilt (and in all steady head positions). Imagine the computational
burden placed on the brain if for each position of the brain in space, there
were varying retinal correspondence. The absence of static COCT provides additional
evidence for the validity of the Donders law.50
AUTHOR INFORMATION
Submitted for publication September 18, 2001; final revision received
May 20, 2002; accepted June 3, 2002.
This study was supported in part by Research to Prevent Blindness Inc,
New York, NY.
Corresponding author and reprints: Robert S. Jampel, MD, PhD, Kresge
Eye Institute, 4717 St Antoine St, Detroit, MI 48201 (e-mail: rjampel{at}comcast.net).
From the Kresge Eye Institute and the Department of Ophthalmology,
Wayne State University School of Medicine, Detroit, Mich.
REFERENCES
 |  |
1. Nagel Über das Vorkommen von Vahren Rollungen Des Auges um die
Gesichtslinic. A16 V Graefes Arch f Ophth 1871;17:237-264.
Taken from: Simonsz HJ, trans. Strabismus. 2000;8:33-38.
FULL TEXT
| PUBMED
2. Graybiel A, Woellner RC. A new and objective method for measuring ocular torsion. Am J Ophthalmol. 1959;47:349-352.
3. Miller EF. Counterrolling of the human eyes produced by head tilt with respect
to gravity. Acta Otolaryngol. 1962;54:479-501.
4. Linwong M, Herman SJ. Cycloduction of the eyes with head tilt. Arch Ophthalmol. 1971;85:570-573.
ISI
| PUBMED
5. Krejcova H, Highstein S, Cohen B. Labyrinthine and extra-labyrinthine effects on ocular counter-rolling. Acta Otolaryngol. 1971;72:165-171.
PUBMED
6. Diamond SG, Markham CH, Furuya N. Binocular counterrolling during sustained body tilt in normal humans
and in a patient with unilateral vestibular nerve section. Ann Otol Rhinol Laryngol. 1982;91:225-229.
ISI
| PUBMED
7. Kushner BJ, Kraft S. Ocular torsional movements in normal humans. Am J Ophthalmol. 1983;95:752-762.
ISI
| PUBMED
8. Diamond SG, Markham CH. Ocular counterrolling as an indicator of vestibular otolith function. Neurology. 1983;33:1460-1469.
FREE FULL TEXT
9. Young LR. Looking around: 35 years of oculomotor modeling. Ann Biomed Eng. 1995;23:456-466.
ISI
| PUBMED
10. Groen E, Bos JE, Nacken PF, de Graaf B. Determination of ocular torsion by means of automatic pattern recognition. IEEE Trans Biomed Eng. 1996;43:471-479.
FULL TEXT
|
ISI
| PUBMED
11. Nelson JR, House WF. Ocular countertorsion as an indicator of otolith function: effects
of unilateral vestibular lesions. Trans Am Acad Ophthalmol Otolaryngol. 1971;75:1313-1321.
PUBMED
12. Miller EF, Graybiel A. Effect of gravitoinertial force on ocular counterrolling. J Appl Physiol. 1971;31:697-700.
FREE FULL TEXT
13. Nelson JR, Cope D. The otoliths and the ocular countertorsion reflex. Arch Otolaryngol. 1971;94:40-50.
PUBMED
14. Young LR, Lichtenberg BK, Arrott AP, Crites TA, Oman CM, Edelman ER. Ocular torsion on earth and in weightlessness. Ann N Y Acad Sci. 1981;374:80-92.
ABSTRACT
15. Kushner BJ, Kraft SE, Vrabec M. Ocular torsional movements in humans with normal and abnormal ocular
motility, I: objective measurements. J Pediatr Ophthalmol Strabismus. 1984;21:172-178.
PUBMED
16. Simonsz HJ, Crone RA, van der Meer J, Merckel-Timmer CF, van Mourik-Noordenbos AM. Bielschowsky head-tilt test, I: ocular counterrolling and Bielschowsky
head-tilt test in 23 cases of superior oblique palsy. Vision Res. 1985;25:1977-1982.
FULL TEXT
|
ISI
| PUBMED
17. Vogel H, Kass JR. European vestibular experiments on the Spacelab-1 mission, VII: ocular
counterrolling measurements pre- and post-flight. Exp Brain Res. 1986;64:284-290.
ISI
| PUBMED
18. Kushner BJ. Ocular torsional movements in humans with normal and abnormal ocular
motility, II: subjective observations. J Pediatr Ophthalmol Strabismus. 1986;23:4-11.
PUBMED
19. Vogel H, Thümler R, von Baumgarten RJ. Ocular counterrolling. Acta Otolaryngol. 1986;102:457-462.
PUBMED
20. Enright JT. The aftermath of horizontal saccades: saccadic retraction and cyclotorsion. Vision Res. 1986;26:1807-1814.
FULL TEXT
|
ISI
| PUBMED
21. Diamond SG, Markham CH. Prediction of sp |