Department of Neurology, Zurich University Hospital, CH-8091 Zurich, Switzerland
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ABSTRACT |
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Bergamin, O. and D. Straumann. Three-Dimensional Binocular Kinematics of Torsional Vestibular Nystagmus During Convergence on Head-Fixed Targets in Humans. J. Neurophysiol. 86: 113-122, 2001. When a human subject is oscillated about the nasooccipital axis and fixes upon targets along the horizontal head-fixed meridian, angular eye velocity includes a vertical component that increases with the horizontal eccentricity of the line-of-sight. This vertical eye movement component is necessary to prevent retinal slip. We asked whether fixation on a near head-fixed target during the same torsional vestibular stimulation would lead to differences of vertical eye movements between the right and the left eye, as the directions of the two lines-of-sight are not parallel during convergence. Healthy human subjects (n = 6) were oscillated (0.3 Hz, ±30°) about the nasooccipital axis on a three-dimensional motor-driven turntable. Binocular movements were recorded using the dual search coil technique. A head-fixed laser dot was presented 1.4 m (far head-fixed target) or 0.25 m (near head-fixed target) in front of the right eye. We found highly significant (P < 0.01) correlations (R binocular = 0.8, monocular = 0.59) between the convergence angle and the difference of the vertical eye velocity between the two eyes. The slope of the fitted linear regression between the two parameters (s = 0.45) was close to the theoretical slope necessary to prevent vertical retinal slippage (predicted s = 0.5). Covering the left eye did not significantly change the slope (s = 0.52). In addition, there was a marked gain reduction (~35%) of the torsional vestibuloocular reflex (VOR) between viewing the far and the near targets, confirming earlier results by others. There was no difference in torsional gain reduction between the two eyes. Lenses of +3 dpt positioned in front of both eyes to decrease the amount of accommodation did not further change the gain of the torsional VOR. In conclusion, ocular convergence on a near head-fixed target during torsional vestibular stimulation leads to deviations in vertical angular velocity between the two eyes necessary to prevent vertical double vision. The vertical deviation velocity is mainly linked to the amount of convergence, since it also occurs during monocular viewing of the near head-fixed target. This suggests that convergence during vestibular stimulation automatically leads to an alignment of binocular rotation axes with the visual axes independent of retinal slip.
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INTRODUCTION |
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During head movements, the vestibuloocular reflex
(VOR) serves to stabilize the eyes in space. To keep the line-of-sight
directed to a head-fixed target while the head rotates horizontally or vertically, the VOR must be cancelled; i.e., ideally, its gain becomes
zero (Barnes et al. 1978; Zee 1977
). If
one extends the analysis to all degrees-of-freedom of eye rotations
during vestibular stimulation (horizontal, vertical, and
torsional), the description of the influence by visual fixation
on the VOR cannot be restricted to the dynamic aspects (gain, phase) of
the system, i.e., visual VOR-suppression, but must also consider the
three-dimensional (3D) kinematics of eye rotation.
Misslisch et al. have shown that the angular velocity vector during
visual VOR cancellation is oriented approximately parallel to the
line-of-sight (Misslisch et al. 1996). This is a result of a 3D reorientation of the ocular rotation axes, such that retinal slippage is restricted to rotations about the line-of-sight. For instance, when subjects are oscillated about the nasooccipital axis in
total darkness (=torsional VOR), the angular velocity axis tilts in the
opposite direction to the gaze line by about half the angle
(Misslisch et al. 1994
). However, if the eyes fixate upon a head-fixed light dot, the angular velocity axis tilts toward the
gaze line by roughly the full angle (Misslisch et al.
1996
). Thus the angle between the ocular rotation axes during
pure torsional VOR and during suppression of torsional VOR amounts one
and a half times the gaze angle.
We asked whether these kinematical principles could also be applied to ocular movements during torsional VOR while the eyes converge on near head-fixed targets. Our hypothesis was that the binocular angular velocity vectors are no longer oriented in parallel, but align with the lines-of-sight. We predicted that the combination of convergence and torsional VOR results in a physiological "dissociation" of vertical eye movements when described in a head-fixed coordinate frame. In other words, the "correct" vertical deviation of movements between the two converging eyes during torsional VOR would produce "purely torsional" movements in eye-fixed coordinates to prevent double vision.
To test our hypothesis on convergence-induced reorientation of ocular rotation axes during vestibular roll stimulation, we measured the 3D movements of both eyes in healthy head-restrained human subjects during whole-body oscillation about the nasooccipital axis on a motorized turntable. During stimulation, subjects had to fix upon a head-fixed light dot at near or far distances.
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METHODS |
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Subjects
Six healthy human subjects (2 female, 4 male; 32-55 y) gave consent and participated in this study after being informed of the experimental procedures. Protocols adhered to the Declaration of Helsinki for research involving human subjects (adopted by the 18th World Medical Assembly, Helsinki, Finland, 1964, and revised last in Hong Kong in 1989), and were approved by the local Ethical committee.
Experimental setup
Subjects were tested on a turntable with three servo-controlled motor-driven axes (Acutronic, Jona, Switzerland). The head was restrained with an individually molded thermoplastic three-point-mask (Sinmed BV, Reeuwijk, The Netherlands). The subject's head was positioned such that the center of the interaural line was at the intersection of the three axes of the turntable. Evacuation pillows and safety belts minimized body movements. The head was surrounded by an aluminum coil frame (side length 0.5 m) by which three orthogonal magnetic fields with frequencies of 55.5, 83.3, and 41.6 kHz were produced. The synchronous detection of the amplitude-modulated signals yielded instantaneous voltages induced by the three magnetic fields (system built by A. Lasker, Baltimore, MD).
Eye movement recordings
Three-dimensional eye movements were recorded binocularly with
dual scleral search coils (Skalar Instruments, Delft, The Netherlands) (Collewijn et al. 1985; Robinson 1963
).
For calibration, the voltage offsets of the system were zeroed by
placing the search coils in the center of a metal tube to shield them
from the magnetic fields. Then the relative gains of the three magnetic
fields were determined with the search coils on a gimbal system placed
in the center of the coil frame. Details of the calibration procedure can be found in detail elsewhere (Straumann et al.
1995
).
After conjunctival and corneal local anesthesia with oxybuprocaine 0.4%, the search coil annuli were placed around the cornea of both eyes. Eye and chair movements were digitized at a frequency of 1,000 Hz with a 16-bit resolution and stored on a computer hard disk for off-line processing. The peak-to-peak noise levels of calibrated position signals were 0.2° in the torsional and 0.1° in the horizontal and vertical directions.
Experimental protocol
On the 3D turntable, subjects were seated in the upright position. The axis about which the turntable was oscillated during the subsequent paradigms coincided with the x-axis of the coil frame, i.e., the torsional or nasooccipital axis. During all paradigms, the turntable was sinusoidally rotated with a frequency of 0.3 Hz and an amplitude of ±30°. A head-fixed laser dot was projected onto screens 0.25 or 1.4 m in front of the right eye. The center of the right eye and these two targets formed a straight line that was parallel to the vestibular stimulation axis (Fig. 1). To make sure that the near target was exactly on the line through the center of the right eye parallel to the stimulation axis, the screen for the near target was transparent, and the subjects had to indicate on the screen the position that was precisely in front of the far target. This location was then marked with a circular non-transparent paper (3 mm diam), in the center of which a head-fixed laser was projected to serve as the near target.
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Subjects were instructed to fixate and focus onto the far or near light
dot such that it did not appear blurred. When both eyes converged on
the far or near target, the line-of-sight of the left eye pointed
1 = 2.5° or
2 = 13.5°
inward, respectively. An additional far laser dot (again at a distance
of 1.4 m), positioned along the straight line between the center
of the left eye and the near target, could be switched on.
Three paradigms (I-III) were used during torsional vestibular
stimulation: I, fixation of the far target in front the right eye (left
eye pointing to the right by the angle 1); II, fixation of the far target on the right (left eye pointing to the right by the
angle
2); and III, fixation of the near target in front of the right eye (left eye pointing to the right by the angle
2 again). Each paradigm lasted 34 s.
Figure 1 schematically explains why we chose these target locations:
the position of the right eye was the same in paradigms I and III,
while the position of the left eye was the same in paradigms II and
III. Hence the eye movements recorded during paradigms I and II served
as control data for the eye movements recorded during paradigm III. In
all three paradigms, subjects were tested during binocular fixation (I,
II, and III) and during monocular fixation with the right viewing
(IR, IIR, and IIIR). In addition,
paradigm III was repeated with the subjects wearing glasses of +3 dpt
in front of each eye (binocular: IIIg; monocular:
III
Data analysis
The data analysis was performed with an interactive program
written with MATLAB Version 5.3. Three-dimensional eye positions were
expressed as rotation vectors. A rotation vector r = (rx, ry,
rz) describes the instantaneous orientation of a
body as a single rotation from the reference position; the vector is
oriented parallel to the axis of this rotation, and its length is
defined by tan (/2), where
is the rotation angle. The three
head-fixed orthogonal axes of the coil frame defined the coordinate
system of rotation vectors with the x-axis pointing forward,
the y-axis leftward, and the z-axis upward. The
signs of rotations about these cardinal axes were determined by the
right-hand rule; i.e., clockwise, leftward, and downward rotations, as
seen by the subject, were positive.
From the rotation vectors r, 3D velocity vectors were
computed, using the formula (Hepp 1990
)
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Geometric considerations
Figure 2 depicts the rotation axes of the eyes during binocular fixation of far and near head-fixed targets during torsional vestibular stimulation in upright position. In this hypothetical scheme we assumed that the ocular motor system succeeds in stabilizing the head-fixed target point on the fovea in all three paradigms (I, II, and III).
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Figure 2A shows the retina of both eyes from behind during ocular counterrolling in the clockwise direction (gray-shaded arrow). If the line-of-sight is parallel to the vestibular stimulation axis while fixating the far head-fixed target straight ahead, both eyes rotate about the line-of-sight, i.e., no additional vertical or horizontal movement is necessary for the stabilization of the head-fixed target point on the fovea (paradigm I). During binocular fixation of the far head-fixed target in right gaze, the same counterroll would move the fovea mainly upward (dotted arrow), unless there is a corrective downward movement component of the eyes. Without this vertical correction, the head-fixed target would slip vertically on the retina of both eyes (paradigm II). If a near head-fixed target is precisely in front of the right eye on a line that is parallel to the vestibular stimulation axis (paradigm III), the right eye must rotate as in paradigm I and the left eye as in paradigm II, in order to stabilize the head-fixed target on both eyes' fovea for binocular fixation.
Figure 2B illustrates the top view of the angular velocity vectors during the three paradigms. During binocular fixation of the far head-fixed target straight ahead, the angular velocity vectors of both eyes are aligned with the lines-of-sight and parallel to the vestibular stimulation axis (paradigm I). When the eyes fix upon the far head-fixed target to the right, both angular velocity vectors coincide again with the line-of-sights but deviate from the vestibular stimulation axis (paradigm II). Provided the gain (gain is eye velocity divided by turntable velocity) of counterroll is the same as in paradigm I, the torsional component of the angular velocity vectors remains the same, but an additional component has to be vectorially added for the appropriate vertical movement. If the subject fixes upon the near head-fixed target in front of the right eye and stabilizes the head-fixed target on both eyes' fovea (paradigm III), the angular velocity vector of this eye must point straight ahead and be purely torsional (as in paradigm I), while the angular velocity vector of the left eye must point to the right (as in paradigm II). Note that the components of the angular velocity vectors (horizontal, vertical, torsional) are in a head-fixed coordinate frame (see above). In an eye-fixed coordinate frame, however, the movements of both eyes in all paradigms would be named "purely torsional."
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RESULTS |
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Figures 3 and
4 show the data of a typical example
(subject AK) during paradigms I (Figs. 3, I and 4, I) and
III (Figs. 3, III and 4, III). In both figures, the panels depict in
descending order: torsional turntable position multiplied by (1) and
the three components of eye movement (torsional, vertical, horizontal).
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Figure 3 represents the torsional turntable position (top panel), and the torsional (rx), vertical (ry), and horizontal (rz) components (bottom 3 panels) of eye position (rotation vectors) during vestibular stimulation (0.3 Hz, ±30°). Traces of the right (solid line) and the left (dashed line) eye are plotted. In Fig. 3, I, during fixation of the far head-fixed target in front of the right eye, the ocular response to the turntable oscillation is mainly torsional, i.e., aligned with the stimulus axis, and nearly in phase. There are frequent torsional quick phases in the opposite direction of the slow phases (=vestibular nystagmus). Clearly, the amplitudes of the torsional traces (rx) of the two eyes are not exactly equal. Also there are small divergent movements of the vertical (ry) positions traces.
In Fig. 3, III, the component with the largest modulation is again torsional (rx), but now the divergent movement of the vertical traces (ry) have increased (arrows) compared to the situation when the subject fixed upon the far head-fixed target in front of the right eye. The horizontal position (rz) of the right eye is approximately zero, and the left eye points 12° to the right, as both eyes converge upon the near head-fixed target in front of the right eye. There was a small offset of 2-3° between the torsional traces of the right and left eye.
Figure 4 depicts the turntable movement and the deviation between the
two eyes in the velocity domain. The angular velocity of ocular
deviation was defined by the difference between the angular
velocity vectors of the right and left eye
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To further process the data, the following sine function (s)
with two harmonics was fitted to the torsional, vertical, and horizontal components of angular deviation velocity
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Figure 5 summarizes the amplitudes of the
angular deviation velocity (A) computed
from the data of the same subject on which the three previous figures
were based. The abscissa contains the three conditions of fixation (I:
far head-fixed target in front of the right eye; II: far head-fixed
target to the right; III: near head-fixed target in front of the right
eye). Values for the binocular (
- - -
) and right-eye
(
) viewing conditions show a similar pattern in all
panels: the torsional deviation velocity
[A
(x); top panel]
did not change between paradigms I and II, but decreased in paradigm
III. For the vertical deviation velocity
[A
(y); middle panel], paradigms I and II again lead to similar values, while in
paradigm III the velocity showed a striking increase. The values for
the horizontal deviation velocity
[A
(z); bottom
panel] were roughly the same in all three paradigms.
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To visualize to what extent the different components of the angular
deviation velocity (A) were influenced by
the convergence angle (
), we plotted these two parameters against each other in Fig. 6. In all three
panels, the four data points at a convergence angle
= 0°
stem from paradigms I and II (monocular:
; binocular:
). The data
point at
= 6.5° convergence corresponds to the monocular
viewing condition (IIIR), and the data point at
= 11.5° to the binocular viewing condition (III) in paradigm III.1 Clearly, only the
vertical deviation velocity (middle panel) increased as a
function of the convergence angle. Two lines (dashed and dotted) were
added to the middle panel of the figure.
1)
The dashed line (straight line) represents the prediction of vertical deviation velocity based on the following assumptions. A) The vertical deviation velocity is zero in the absence of convergence. B) Both eyes rotate such that the head-fixed target always stays on the fovea. C) The gain of ocular counterroll during convergence is the same as during viewing of the far target. In this subject, the average torsional vestibuloocular gain of both eyes during binocular viewing of the far target was gx = 0.56. This corresponds to a torsional angular velocity of Ax = 31.7°/s at a maximal chair velocity of 56.5°/s (0.3 Hz, ±30°). From these three assumptions, the first-order linear regression relating the convergence angle (
) and the average torsional velocity of both eyes [A
(x)] with the angular deviation velocity [A
(y)] is
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The data points in the middle panel of Fig. 6
are oriented more parallel to the theoretical regression, that takes
into account the decrease of the torsional gain with convergence
(dotted line), and less parallel to the regression that is based on a
constant torsional gain. Thus the amount of vertical deviation velocity seems to depend on the torsional gain and the convergence
angle. The offset of the data points at zero degree convergence
probably represents the known small skew deviation observed during
torsional VOR of healthy human subjects (Jauregui-Renaud et al.
1998).
Figure 7 demonstrates the effect of the
different paradigms on the gain of the torsional VOR in subject
CB (Fig. 7, A and B) and in all six subjects
measured (Fig. 7, C and D). The gains of the
right () and the left (
) eyes are plotted separately. The
left panels (Fig. 7, A and C) depict
the gains during binocular, and the right panels (Fig. 7,
B and D) the gains during monocular fixation of
the head-fixed target. On the top panels (Fig. 7, A and B) the lines connect the single data
points; on the bottom panels (Fig. 7, C and
D), the lines connect the medians. The gains of both eyes
were very similar. In both the binocular and monocular viewing
conditions, fixation of the far head-fixed target in front of the right
eye (I, IR) during torsional VOR resulted in the highest
gains. Note, however, that the gains during binocular straight-ahead
far viewing (Fig. 7C, I; median gains right eye: 0.49; left
eye: 0.51) were considerably higher than during monocular straight-ahead far viewing (Fig. 7D, IR; right
eye: 0.42; left eye: 0.40). These gain differences were significant in
the paired t-test (P < 0.001).
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Already fixing with both eyes upon the far head-fixed target 13.5° to
the right led to a decrease of the gain during both binocular (Fig.
7C, II; right eye: 24.6%; left eye: 23.8%) and monocular
viewing (Fig. 7D, IIR; right eye: 16.6%; left
eye: 8.5%). These numbers were much higher than one would have
expected if the gain vector had only changed its orientation by 13.5°
to the right, but not its length; in this case the torsional gain would have only decreased by 1 cos (13.5°) = 2.8%. During
convergence on the near head-fixed target in front of the right eye, we
measured an additional decrease of the gain; the gain reduction
compared to fixation of the far head-fixed target in front of the right eye (100%) was more prominent in the binocular (Fig. 7C,
III; right eye: 34.2%; left eye: 34.4%) than in the monocular (Fig. 7D, IIIR; right eye: 20.7%; left eye: 12.5%)
viewing condition. There was no further decrease of torsional gains
when the subjects wore the glasses with +3 dpt (Fig. 7, C
and D, IIIg and III
So far we have shown that the different paradigms influenced both the
vertical deviation velocity and the gain of the torsional VOR. We asked
whether there was a linear correlation between the convergence angle
(independent variable) and the vertical deviation velocity (dependent
variable). To explore this question, we pooled the data of all six
subjects collected during the four different paradigms into two
datasets: one from the binocular (I, II, III, IIIg) and the
other from the monocular (IR, IIR,
IIIR, III) and vertical deviation velocity
[A
(y)]. The correlation for
the binocular viewing conditions (Fig. 8A) was superior
compared to the monocular viewing conditions (Fig. 8B). In
part, this was due to the fact that during monocular fixation upon the
near head-fixed target convergence angles typically did not reach
values above 10°.
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The hypothesis that led to these experiments was that, at a specific
convergence angle, an increase in counterroll gain should directly lead
to an increase of the vertical deviation velocity if the head-fixed
target is kept on the foveae of both eyes. But since the gain of ocular
counterroll was different between subjects and also decreased with
convergence, the direct relation between the convergence angle and the
vertical deviation velocity could better be shown by normalizing the
data to a constant gain of ocular counterroll. In line with our
hypothesis, the predicted vertical deviation velocity
[A(y)] and
the measured counterroll gain (gx) by
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DISCUSSION |
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This study in healthy human subjects demonstrates that convergence upon a near head-fixed target during torsional head oscillation about the nasooccipital axis leads to ocular movements that are different in the two eyes. The convergence-induced reorientation of the ocular rotation axes during the torsional VOR ensures that the lines-of-sight of both eyes remain directed onto the visual target, i.e., the axes about which the two eyes rotate during the torsional vestibular stimulation are parallel to the respective lines-of-sight. As a consequence, the vertical velocity (expressed in head-fixed coordinates) differs between the two eyes. This vertical deviation velocity depends on the gain of the dynamic ocular counterroll and the convergence angle, but not on accommodation. In addition, by lowering the gain of the torsional VOR during convergence, the CNS reduces the vertical deviation velocity needed for directing both lines-of-sight to the visual target.
So far, little was known about the kinematical changes of eye movements
induced in the context of visual VOR cancellation. Most investigations
on how the CNS suppresses ocular responses during vestibular
stimulation were focused on the dynamical aspects of the relation
between vestibular input and ocular motor output (Barnes et al.
1978; Gauthier and Vercher 1990
; Robinson
1982
). When the technology to measure eye movements about all
principal axes of rotation (horizontal, vertical, torsional) was
established, it became possible to study the effect of visual
suppression on the orientation of the ocular rotation axes
(Collewijn et al. 1985
; Robinson 1963
).
The first series of experiments concentrated on whether the torsional
VOR could be suppressed by vision, even though the pursuit system
operates only in two dimensions (horizontal and vertical). In rhesus
monkeys, postrotatory torsional nystagmus could not be cancelled during
the first few seconds, i.e., there was only a late suppressive effect,
which was attributed to the optokinetic system (Straumann et al.
1992
). In humans who actively oscillated their heads at about
0.5 Hz, the gain of the torsional VOR dropped from 0.61 in the dark to
0.46 when subjects were viewing a visual display (Leigh et al.
1989
). Thus despite the fact that the pursuit system is not
sensitive for rotations about the line-of-sight and despite the very
low torsional optokinetic gain in upright position (Collewijn et
al. 1985
), visual suppression was able to reduce the torsional
VOR gain by 25%.
The next step was to elicit the VOR in all directions (horizontal,
vertical, torsional) and, at the same time, to present fixation targets
at different horizontal and vertical positions. Misslisch et al. found
that the angular velocity vectors of the eyes were always aligned with
the line-of-sight (Misslisch et al. 1996). Thus the
pursuit system cancelled the horizontal and vertical components of
retinal velocity. In addition, the remaining angular
velocity vector, which was oriented parallel to the ocular rotation axis, was decreased in length. This again suggested the existence of a second mechanism of VOR cancellation in addition to the
mechanism by the pursuit system.
In the present experiments, which were restricted to visual suppression of the torsional VOR, we demonstrated that the same principles that apply to the fixation of far targets could be extended to convergence. We chose to study the effect of visual fixation during the VOR in the torsional direction, because, in this paradigm, it was easiest to demonstrate the effect of the direction of the line-of-sight on the kinematics of eye rotation. The angular velocity vectors of the two eyes were parallel with their lines-of-sight, and thus the rotation axes of the two eyes formed an angle that was close to equal to the convergence angle.
The results of our study demonstrate that, under the described
conditions, the ocular system is successful in directing the rotation
axes of the two eyes toward the fixation target during ongoing
vestibular stimulation, even in the absence of visual feedback. This
result agrees well with the reported high precision of binocular
vertical alignment of fixations and saccades during convergence in
tertiary positions (Collewijn 1994; Schor et al. 1994
; Ygge and Zee 1995
). The gain reduction of
the torsional VOR induced by convergence, a phenomenon that has already
been reported by earlier studies (Averbuch-Heller et al.
1997
), facilitates the vertical alignment during fixation of a
near target in the presence of a vestibular roll stimulation.
Can our findings be explained by the action of the smooth pursuit
system during VOR cancellation? The following speaks against this
hypothesis: for each eye, one would have to postulate a separate pursuit system, both for the afferent (detection of retinal velocity) and efferent (eye movement) pathways. To our knowledge there are no
experimental findings that would support this assumption. Moreover, the
fact that covering one eye does not lead to a change of its rotation
axis also speaks against a significant role of the smooth pursuit
system in VOR cancellation during convergence. It is more likely that
the ocular motor system explicitly computes the correct 3D kinematics
from the relevant parameters, i.e., the horizontal-vertical direction
and depth of the target, and the gain of the torsional VOR at a given
frequency. Such an algorithm of VOR cancellation is certainly able to
stabilize the lines-of-sight of the two eyes on the target but also
allows for a certain amount of torsional retinal slip that is equal in
the two eyes. If such a mechanism is implemented, the question arises
whether the impact of the pursuit system on VOR cancellation is rather
weak. In fact, there are experimental findings that support a
non-pursuit suppression mechanism of VOR cancellation; rarely one finds
patients with disordered smooth pursuit, but intact VOR cancellation
(Chambers and Gresty 1983). Similarly, some patients
with deficient smooth pursuit eye movements can still smoothly track a
moving target when both eye and head are moving (Grant et al.
1992
). Probably the segregation of smooth pursuit and VOR
cancellation is already implemented at the level of the cerebellum: in
patients with spinocerebellar ataxia type 6, horizontal smooth pursuit
was impaired, but the cancellation of the horizontal VOR was not
affected (Takeichi et al. 2000
). These behavioral data
agree with lesional studies in squirrel monkeys: muscimol
microinjections into the floccular region impaired ocular pursuit, but
had little effect on VOR cancellation (Belton and McCrea
1999
). Our finding that the torsional VOR gain during
cancellation was reduced and even further decreased during convergence
also indicates that other mechanisms than the pursuit system are
involved in the visual cancellation of the VOR. How exactly the
kinematical changes of the torsional VOR induced by convergence is
implemented remains unclear. Possibly, active muscle pulleys play an
important role in reorienting the ocular rotation axes during
convergence (Demer et al. 2000
).
The roll stimulus we applied in our experiments was not purely angular
but also included a vertical linear component, because the rotation
about the nasooccipital axis through the center of the head caused the
labyrinths to be vertically translated in opposite directions
(Seidman et al. 1995). Therefore it is possible that the
vertical movement of the left eye, that points its line-of-sight toward
the target in front of the right eye, is enhanced by the linear VOR.
Future experiments must try to quantify the contribution of the linear
VOR during torsional vestibular stimulation by applying head roll in
total darkness about different axes through the head and varying
convergence angles with (earth-horizontal axis) and without
(earth-vertical axis) otolith activation.
In conclusion, ocular convergence on a head-fixed target during the VOR
requires a substantial modification of binocular kinematics to prevent
double vision. We have demonstrated this phenomenon for a frequency of
0.3 Hz, which is well below the natural frequencies of the head
(Grossman et al. 1988). Thus it will be necessary to do
the same analysis on the convergence-induced reorientation of ocular
rotation axes at higher frequencies.
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ACKNOWLEDGMENTS |
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We thank A. A. Kori for valuable comments and help in part of the experiments, and A. Züger for technical support.
This work was supported by the Swiss National Science Foundation (3231-051938.97/3200-052187.97), the Betty and David Koetser Foundation for Brain Research, and the Freiwillige Akademische Gesellschaft, Basel.
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FOOTNOTES |
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Address for reprint requests: D. Straumann (E-mail: dominik{at}neurol.unizh.ch).
1
The convergence angle was smaller during
monocular viewing than during binocular viewing in all but one subject
(OB).
Received 13 October 2000; accepted in final form 23 March 2001.
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REFERENCES |
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