 |
 Previous Article | Next Article 
The Journal of Neuroscience, February 15, 2003, 23(4):1104
BRIEF COMMUNICATION
Foveal Versus Full-Field Visual Stabilization Strategies
for Translational and Rotational Head Movements
Dora E.
Angelaki,
Hui-Hui
Zhou, and
Min
Wei
Department of Neurobiology, Washington University School of
Medicine, St. Louis, Missouri 63110
 |
ABSTRACT |
Because we view the world from a constantly shifting platform when
our head and body move in space, vestibular and visuomotor reflexes are
critical to maintain visual acuity. In contrast to the phylogenetically
old rotational vestibulo-ocular reflex (RVOR), it has been proposed
that the translational vestibulo-ocular reflex (TVOR) represents a
newly developed vestibular-driven mechanism that is important for
foveal vision and stereopsis. To investigate the hypothesis that the
function of the TVOR is indeed related to foveal (as opposed to
full-field) image stabilization, we compared the three-dimensional
ocular kinematics during lateral translation and rotational movements
with those during pursuit of a small moving target in four rhesus
monkeys. Specifically, we tested whether TVOR rotation axes tilt with
eye position as in visually driven systems such as pursuit, or whether
they stay relatively fixed in the head as in the RVOR. We found a
significant dependence of three-dimensional eye velocity on eye
position that was independent of viewing distance and viewing
conditions (full-field, single target, or complete darkness). The
slopes for this eye-position dependence averaged 0.7 ± 0.07 for
the TVOR, compared with 0.6 ± 0.07 for visually guided pursuit
eye movements and 0.18 ± 0.09 for the RVOR. Because the torsional
tilt versus vertical gaze slopes during translation were slightly
higher than those during pursuit, three-dimensional eye movements
during translation could partly reflect a compromise between the two
different solutions for foveal gaze control, that of Listing's law and
minimum velocity strategies. These results with respect to
three-dimensional kinematics provide additional support for a
functional difference in the two vestibular-driven mechanisms for
visual stability during rotations and translations and establish
clearly the functional goal of the TVOR as that for foveal visual acuity.
Key words:
eye movement; binocular; vestibular; vestibulo-ocular; vergence; kinematics; torsion; stereopsis
| |
Introduction |
For an eye movement whose functional
goal is to keep images stable on the fovea, such as during visual
tracking of a small target, only the horizontal and vertical components
of gaze direction need to be specified. In general, the eyes could
assume an infinite number of torsional orientations and still foveate
the target, because ocular torsion remains unspecified. Among the
different possible orientations that the eyes could assume (each of
which would have a different consequence for optic flow on the
peripheral retina), three strategies have been described as providing
unique, although distinct, advantages (see Fig. 1). On one extreme, the eye could always rotate about an axis that is anchored to the head and
is independent of the direction of gaze. This is the optimal strategy
for minimizing slip on the peripheral retina, thus providing for a
full-field (FF) image stabilization solution [see Fig.
1A, full-field strategy]. On the other extreme, the rotation axis of the eye could remain eye-fixed, and thus, in head
coordinates, rotate similarly as gaze [see Fig. 1B,
right, minimum rotation (MR) strategy]. The advantage of
this solution is that the eye follows the shortest possible path to
acquire the target but results in the largest slip of images on the
peripheral retina. The third strategy rotates the eye about axes that
are in between a head-fixed and an eye-fixed coordinate system. Its unique advantage is that, contrary to the first two solutions, ocular
torsion is minimized [see Fig. 1B, left,
Listing's law (LL) strategy]. It is now well established that smooth
pursuit, and in general all conjugated, visually guided,
foveal-specific eye movements, obey LL (Tweed and Vilis, 1987 , 1990;
Haslwanter et al., 1991; Tweed et al., 1992).
In contrast to foveal-specific eye movements, the rotational
vestibulo-ocular reflex (RVOR), whose goal is to stabilize images on
the entire retina and whose sensory input can uniquely specify all
three degrees of freedom of the eye, best complies with the FF
strategy (Crawford and Vilis, 1991; Misslisch et al., 1994; Misslisch
and Hess, 2000). However, unlike the role of the RVOR in FF visual
stabilization, it has been proposed that the translational vestibulo-ocular reflex (TVOR) function is tightly coupled with foveal
vision and stereopsis (Miles, 1993, 1998). To date, two experimental
results have provided support for this hypothesis. First, it has been
shown that the TVOR anticipates and accounts for the motion parallax
associated with viewing targets at different depth planes during
translation, because eye velocity changes in inverse proportion
to viewing distance (Schwarz et al., 1989; Paige and Tomko, 1991;
Schwarz and Miles, 1991; Telford et al., 1997; Miles, 1998). Second,
the horizontal and vertical components of the evoked eye movement
depend on heading (movement) direction and eye position, as
expected according to the geometrical dependencies associated with
keeping images stable on the fovea (McHenry and Angelaki, 2000;
Angelaki and Hess, 2001).
Indeed, if the functional goal of the TVOR is to assist and extend
foveal tracking, then it must be modulated as a function of gaze
similar to smooth-pursuit eye movements. Thus, in the present
study, we have compared the three-dimensional kinematics associated
with the TVOR with those of the RVOR and pursuit eye movements as a
simple test for a more general conceptual property regarding the
functional role of vestibular-evoked eye movements during translation.
| |
Materials and Methods |
Binocular eye movements were recorded in four rhesus monkeys
during 0.5 Hz (± 3°) pursuit, 0.5 Hz (± 0.08 gm), or 4 Hz (± 0.25 gm) lateral translation and 4 Hz (±1-3°) yaw rotation. Two of the
animals were implanted with dual coils on each eye for three-dimensional eye-movement recordings (Hess, 1990). In the remaining two animals, only one eye was implanted with a dual three-dimensional coil. Because the other eye was implanted with a
traditional two-dimensional coil, binocular responses were used for
behavioral control (and reinforcement of the appropriate vergence angle
for each target distance; see below), although quantitative analysis
was performed only on the data recorded in the eye with the
three-dimensional coil. All animals were trained to fixate or follow
targets (<0.5°) at distances of 12, 18, 32, or 100 cm in a softly
illuminated room. Targets were back-projected onto one of four screens
and were presented either as single targets using a laser/mirror
galvanometer system (General Scanning, Watertown, MA) in a dimly
illuminated room or as a computer-generated, red target within
full-field, white, random-dot patterns using a projector (Mirage 2000;
Christie Digital, Cypress, CA). Eye movements were calibrated by
requiring the animals to monocularly fixate far targets at different
horizontal and vertical eccentricities (Angelaki et al., 2000; Angelaki
and Hess, 2001).
During translation, rotation, and pursuit, the eye-position dependence
of eye velocity was tested by requiring the animals to fixate targets
in the midsagittal plane at different vertical eccentricities (up to
±25°). During 4 Hz motion, periods of target presentation were
alternated with periods in total darkness. With the 0.5 Hz stimuli, the
target was on throughout the experimental run. Trained animals were
required to keep their eyes within binocular behavioral windows of
<1.5° (during pursuit) or <3° (during motion), even in darkness.
The vergence angle was monitored throughout the experiment. Only data
for which the actual vergence angle was within 10% of the "ideal"
values (based on target distance and eccentricity, as well as the
monkey's interocular distance) (Angelaki et al., 2000) were included
in the analyses. This was important to investigate any potential effect
of different vergence angles on the kinematic rules followed by
pursuit, TVOR, and RVOR.
During experiments, the monkeys were seated in a primate chair that was
secured inside the inner frame of a rotator/sled motion delivery system
(Neurokinetics, Pittsburgh, PA). Both stimulus presentation and
data acquisition were controlled with custom-written scripts within the
Spike2 software environment using the Cambridge Electronics Design
(CED, model 1401; Cambridge, UK) data acquisition system. Data
were anti-alias-filtered (200 Hz, six pole Bessel), and digitized by
the CED at a rate of 833.33 Hz (16 bit resolution). Off-line,
eye-movement data were converted into rotation vectors, using straight
ahead as the reference position. In addition, angular velocity was
computed and fast phases were removed from the velocity records using a
semi-automated procedure based on higher derivatives of eye velocity
(Hepp, 1990; Angelaki et al., 2000). Angular velocities were expressed
using the right-hand rule (if you point your right thumb in the
direction of the vector, then your fingers curl around in the direction
of spin). Positive directions were leftward, downward, and clockwise
for the horizontal, vertical, and torsional components, respectively.
For example, a forward-pointing vector represents a clockwise rotation
(from the animal's viewpoint). The amount of axis tilt in the
animal's sagittal plane was evaluated by plotting the elicited
eye-velocity vector in head coordinates and fitting a line in three
dimensions. A "torsional tilt angle" was then computed from the
direction cosines of the three-dimensional line, as the angle between
the line and the positive horizontal axis in the sagittal plane.
Subsequently, torsional tilt angles were plotted versus vertical eye
position, and regression lines were used to quantitatively describe
this dependence. For the 4 Hz motion stimuli, the analysis was
performed separately for cycles with the target on and in total
darkness. All statistical comparisons used repeated-measures
ANOVA (for both the effects of distance and
RVOR/TVOR/pursuit).
For a direct comparison, experimental conditions were similar during
rotation, translation, and pursuit, other than the frequency of
stimulation, which was 0.5 Hz for pursuit but 4 Hz for the TVOR/RVOR.
We considered it important to test the TVOR at a frequency that is more
functionally relevant (Paige and Tomko, 1991; Telford et al., 1997)
than in the low-frequency range to be directly comparable with pursuit.
Nevertheless, in two of the animals we also collected data during
lower-frequency (0.5 Hz) translation. Because the results during
low-frequency translation were the same as those at 4 Hz, the data
presented in Results focus on the higher-frequency stimulus.
Furthermore, because the orientation of Listing's plane depends on the
vergence angle (Mok et al., 1992; Van Rijn and Van den Berg, 1993;
Minken and Van Gisbergen, 1994; Misslisch et al., 2001), it was
important that a direct comparison with pursuit be made for each
viewing distance.
| |
Results |
If image stability on the peripheral retina is important for the
TVOR (as is the case for the RVOR), we would expect little or no
torsional eye velocity during lateral translation at vertically eccentric eye positions ("zero-angle rule") (Fig.
1A). In contrast, a
kinematic requirement for both the MR and LL strategies is a specific
eye-position dependence of the axis of rotation of the eye, in which
the eye velocity axis is expected to tilt by the same or half the angle
of gaze ("full-angle rule" and "half-angle rule," respectively)
(Fig. 1B) (Tweed and Vilis, 1987, 1990; Tweed et al.,
1992; Misslisch et al., 1994). As is explained below, contrary to the
RVOR, eye velocity in the TVOR exhibited a large and systematic
dependence on vertical gaze position.
View larger version (27K):
[in this window]
[in a new window]
|
Figure 1.
Geometrical expectations based on different
strategies for image stabilization. A, For FF image
stabilization (FF strategy), the axis of rotation of the eye [shown as
the arrow indicating eye velocity
(EV)] should always remain head-fixed (e.g.,
head horizontal) and be independent of the direction of gaze.
B, For foveal image stabilization, the axis of rotation
of the eye is not anchored to the head. According to the LL strategy,
the axis of rotation of the eye is neither head-fixed nor eye-fixed,
but rather rotates in the same direction of gaze through one-half the
angle of gaze ( /2; half-angle rule). According to the MR strategy,
the axis of rotation of the eye remains eye-fixed (i.e., rotates in the
same direction and through the same angle as gaze, ; full-angle
rule). Dotted lines represent the head vertical and
horizontal directions.
|
|
Let us first consider the three-dimensional eye velocity organization
during horizontal pursuit at different vertical eccentricities. During
horizontal smooth pursuit with the gaze straight ahead, for example,
the elicited eye movement is purely horizontal, with negligible
modulation in torsional eye velocity (Fig.
2, smooth pursuit). However, because of
the kinematic constraints of LL, a combination of both horizontal and
torsional eye movements is observed during pursuit of a target that is
moving horizontally in eccentric positions. During horizontal pursuit
with gaze up, for example, a negative (counterclockwise relative to the
animal, as viewed from the right ear) torsion accompanies the positive (leftward) component of pursuit. The opposite is true for down gaze
(Fig. 2). As a result, the instantaneous axis of rotation of the eye
tilts away from a purely head-horizontal axis in the same direction as
gaze and through approximately one-half the gaze angle, as illustrated
when eye velocity is plotted in head coordinates (Fig. 2, smooth
pursuit).
View larger version (48K):
[in this window]
[in a new window]
|
Figure 2.
Dependence of smooth pursuit and ocular responses
during translation on vertical gaze. From top to
bottom, Three-dimensional eye position
(Etor,
Ever, and
Ehor) and angular velocity
( tor, ver,
hor) for up, center, and down gaze during 0.5 Hz
(± 3°) pursuit and 4 Hz (± 0.25 gm) lateral translation (distance
of 32 cm). Tg, Target on and off; H, head
motion acceleration. Fast phases have been eliminated.
|
|
A similar dependence of eye velocity on gaze angle was also observed
during lateral translation (Fig. 2, translation). Similar to pursuit
responses, the amount of axis tilt was evaluated by plotting eye
velocity in head coordinates and fitting a line in three dimensions
(Fig. 2, white lines). The torsional tilt angle was
then computed from the direction cosines of the three-dimensional line
as the angle formed with the positive horizontal axis in the sagittal
plane. Torsional tilt angles were plotted versus vertical gaze, and
regression lines were used to describe this dependence quantitatively
(Fig. 3A). Similar to pursuit,
significant correlations were observed between torsional tilt angles
and vertical gaze during translation. Regression lines for the gaze
dependence of pursuit were consistent with the half-angle rule of LL.
However, regression slopes for the TVOR were typically >0.5, as
illustrated by the data points falling between the lines corresponding
to half-angle and full-angle (unity) slopes (Fig. 3A,
middle, dotted lines). Similar to previous
reports in humans and monkeys (Misslisch et al., 1994; Misslisch and
Hess, 2000), the torsional tilt angle as a function of vertical gaze
during rotation was significantly lower (Fig. 3A,
bottom).
View larger version (37K):
[in this window]
[in a new window]
|
Figure 3.
A, Calculated torsional tilt angles
of eye velocity as a function of vertical gaze during pursuit,
translation, and rotation as the animal followed a target at a distance
of 18 cm. Solid lines represent linear regressions;
dotted lines illustrate the full- and half-angle rules
of three-dimensional kinematics. B, The torsional eye
velocity tilt versus vertical gaze angle slopes for the TVOR
(solid symbols) and RVOR (open symbols)
from four animals (6 eyes) at different viewing distances.
Dotted lines illustrate the unity-slope line (diagonal).
C, The corresponding zero-intercepts for the TVOR
regressions plotted versus the corresponding values for pursuit. Other
than the farthest distance (squares), data fall along
the unity (dotted) line.
|
|
Data from all four animals have been summarized in Figure
3B,C. For each animal, the torsional tilt versus gaze angle
slope during rotation, translation, and pursuit were computed
separately for four target distances (12-100 cm). When compared
directly with the corresponding values during pursuit, TVOR slopes lie along or slightly above the unity-slope line (Fig. 3B,
solid symbols and diagonal dotted line). The
torsional tilt versus gaze angle slopes averaged 0.7 ± 0.07 during translation and 0.6 ± 0.07 (means ± SD) for
visually guided pursuit eye movements (difference not significant;
F(1,4) = 0.15; p > 0.05). In contrast, RVOR slopes were smaller, averaging 0.18 ± 0.09. Results were similar during the actual fixation of either a
space-fixed single target or a full-field random dot pattern, as well
as in intermingled periods of complete darkness
(F(1,15) = 1.3; p > 0.05).
As shown in Figure 3B, the closer the target, the
larger the RVOR slope (F(3,24) = 11.7 ;
p < 0.05). In contrast, the slopes of the eye-position
dependence for the TVOR (and pursuit) were independent of viewing
distance (F(3,12) = 0.03;
p > 0.05). However, the zero-intercepts of the TVOR
regressions (i.e., the torsional tilt angle at zero vertical elevation)
depended on viewing distance (Fig. 3C)
(F(3,12) = 33.7; p < 0.05). This was not so for pursuit, for which both the slopes and the
zero-intercepts remained independent of target distance. Only for near
targets (at 12, 18, and 32 cm) were the zero-intercepts for TVOR and
pursuit similar (F(1,5) = 0.04;
p > 0.05). In contrast, for small vergence angles
(i.e., far targets), the zero-intercept values were larger than those of pursuit (F(1,4) = 30.6;
p < 0.05; compare the squares with the unity-slope dotted line in Fig. 3C).
| |
Discussion |
Because translational displacements could result in a differential
optic flow across the retina, no single eye movement could generally
result in stabilization of the entire visual field. Theoretically, the
brain has a choice between two extreme strategies: it can eliminate
optical flow entirely over the fovea, or it can minimize the average
optical flow over the entire retina, with no special concern for the
fovea. Alternatively, it could do something in between, keeping optical
flow over the fovea somewhat smaller than the average flow elsewhere.
If the TVOR represents an eye-movement system whose function is linked
to foveal image stabilization, it must also be characterized by
three-dimensional kinematics that are similar to those during other
foveal-specific ocular responses, such as pursuit, and different from
those in the RVOR. This expectation was verified here by showing that
the three-dimensional kinematics of the TVOR are more similar to those
during pursuit and unlike those of the RVOR.
In a previous study in which torsion was quantified during
high-frequency translation while maintaining fixation on a near target,
a systematic dependence of TVOR eye velocity on vertical gaze angle was
reported, with a slope of 0.7 (Angelaki et al., 2000). The possibility
that TVOR might follow LL was addressed then, although because the
target was visible during motion and because corresponding data for
pursuit and the RVOR were not available, a direct comparison could not
be made. Thus, the present study was specifically designed to compare
directly the eye-position dependence of the TVOR, RVOR, and pursuit at
different target distances and under different viewing conditions. The
present results clearly support the hypothesis (Miles, 1993, 1998) that the RVOR and TVOR are functionally distinct processes, although they
both arise from signals originating in the labyrinth. Specifically, for
near-target viewing (<32 cm) when the TVOR is functionally important,
we found its three-dimensional kinematics to be statistically indistinguishable from those of pursuit, in contrast to those for the
RVOR. Nevertheless, because the torsional tilt versus vertical gaze
slopes during translation were slightly higher than those during
pursuit (means of 0.7 vs 0.6, respectively), three-dimensional eye
movements during translation might partly reflect a compromise between
the two different strategies for gaze control, that of LL and MR
strategies (Misslisch et al., 1994).
What is the functional advantage for the eye-position dependence
exhibited by the TVOR? Although several suggestions about the
functional significance of LL have been made, one important aspect is
keeping the eyes near the center of their motor range (by minimizing
torsion), thus improving motor efficiency (von Helmholtz, 1867; Hering
1868; Hepp, 1990, 1995; Tweed and Vilis, 1990; Tweed et al., 1992). The
three-dimensional kinematic rules outlined in Figure 1 also make
distinct predictions about how three-dimensional visual scenes project
onto the retina. Specifically, if the eye were to follow the zero-angle
rule, in which eye axes remain anchored to the head and independent of
gaze (Fig. 1A, FF strategy),
space-horizontal lines do not remain parallel with the horizontal
meridian of the eye at eccentric eye positions. A
space-horizontal line appears to turn clockwise when the eye looks
right and counterclockwise when it looks left (Klier and Crawford,
1998; Crawford et al., 2000). Although this geometrical problem is
eliminated with a full-angle rule, in which eye axes move 100% with
gaze (Fig. 1B, right), the MR strategy has
never been observed for the eye. Instead, visually guided eye rotations lie in between these two extremes in terms of a mismatch between space
and retinal line orientations (Crawford et al., 2000). Thus, the TVOR
0.7 angle rule might represent an efficient compromise between
the need to enhance motor performance by keeping the eyes near the
center of their motor range and the need to minimize the lack of
correspondence between spatial and retinal coordinates.
When viewing targets at various depths, the three-dimensional rotations
of the two eyes are yoked in accordance with a recently discovered
geometric rule that has been referred to as the binocular extension of
LL, or LL2 (Mok et al., 1992; Tweed, 1997; Misslisch et al., 2001).
Briefly, the Listing's planes of the two eyes rotate temporally as the
eyes converge, such that the eyes incyclorotate when looking up and
excyclorotate when looking down (Mok et al., 1992; Van Rijn and
Van den Berg, 1993; Minken and Van Gisbergen, 1994; Misslisch et al.,
2001). The functional significance of this rotation lies in the fact
that it tends to reduce torsional disparities in the two eyes: When
Listing's planes rotate temporally by as much as the eyes converge,
horizontal lines at the fovea stay parallel to the horizontal of the
eye (Tweed, 1997). Moreover, the search zones for retinal
correspondence necessary to achieve stereoscopic vision are
retina-fixed and independent of gaze direction, although the epipolar
lines (the retinal bands where corresponding image features project in
the two eyes) migrate on the retinas when the eyes change position
(Schreiber et al., 2001). Thus, the reason that the eyes twist about
their lines of sight in compliance with LL2 is to reduce the motion of
the epipolar lines, allowing for easier and more efficient stereopsis.
Accordingly, it has been proposed that LL and LL2 represent important
contributors to binocular vision (Schreiber et al., 2001).
The fact that the TVOR follows the three-dimensional kinematic
strategies consistent with foveal vision and stereovision provides strong support for a phylogenetically novel role of the primate vestibular system regarding its contribution to a postulated crucial function of the oculomotor system in depth vision. How this
phylogenetically novel vestibulo-ocular system is implemented within
the premotor circuitry and how it interacts with the phylogenetically
"old" RVOR remain unresolved. Recent neurophysiological recordings
suggest a differential premotor processing of vestibular signals in the TVOR and RVOR (Angelaki et al., 2001), although details about the
underlying circuitry, physiology, and computations are still in the
very early stages of exploration.
| |
FOOTNOTES |
Received Oct. 16, 2002; revised Nov. 25, 2002; accepted Nov. 26, 2002.
The work was supported by National Institutes of Health Grants EY12814
and DC04260 and by the McDonnell Foundation for higher brain function.
Correspondence should be addressed to Dr. Dora Angelaki, Department of
Anatomy and Neurobiology, Box 8108, Washington University School of
Medicine, 660 South Euclid Avenue, St. Louis, MO 63110. E-mail:
angelaki{at}thalamus.wustl.edu.
| |
References |
-
Angelaki DE,
Hess BJM
(2001)
Direction of heading and vestibular control of binocular eye movements
Vision Res
41:3215-3228[Web of Science][Medline].
-
Angelaki DE,
McHenry MQ,
Hess BJM
(2000)
Primate translational vestibulo-ocular reflexes. I. High frequency dynamics and three-dimensional properties during lateral motion.
J Neurophysiol
83:1637-1647[Abstract/Free Full Text].
-
Angelaki DE,
Green AM,
Dickman JD
(2001)
Differential sensorimotor processing of vestibulo-ocular signals during rotation and translation.
J Neurosci
21:3968-3985[Abstract/Free Full Text].
-
Crawford JD,
Vilis T
(1991)
Axes of eye rotation and Listing's law during rotations of the head.
J Neurophysiol
65:407-423[Abstract/Free Full Text].
-
Crawford JD,
Henriques DY,
Vilis T
(2000)
Curvature of visual space under vertical eye rotation: implications for spatial vision and visuomotor control.
J Neurosci
20:2360-2368[Abstract/Free Full Text].
-
Haslwanter T,
Straumann D,
Hepp K,
Hess BJM,
Henn V
(1991)
Smooth pursuit eye movements obey Listing's law in the monkey.
Exp Brain Res
87:470-472[Web of Science][Medline].
-
Hepp K
(1990)
On Listing's law.
Commun Math Phys
132:285-292.
-
Hepp K
(1995)
Theoretical explanations of Listing's law and their implication for binocular vision.
Vision Res
35:3237-3241[Web of Science][Medline].
-
Hering E
(1868)
Die Lehre vom binocularen Sehen (Bridgeman B, translator).
In: The theory of binocular vision (Bridgeman B,
Stark L,
eds). New York: Plenum.
-
Hess BJM
(1990)
Dual search coil for measuring 3-dimensional eye movements in experimental animals.
Vision Res
30:597-602[Web of Science][Medline].
-
Klier EM,
Crawford JD
(1998)
Human oculomotor system accounts for 3-D eye orientation in the visual-motor transformation for saccades.
J Neurophysiol
80:2274-2294[Abstract/Free Full Text].
-
McHenry MQ,
Angelaki DE
(2000)
Primate translational vestibulo-ocular reflexes. II. Version and vergence responses to fore-aft motion.
J Neurophysiol
83:1648-1661[Abstract/Free Full Text].
-
Miles FA (1993) The sensing of rotational and translational
optic flow by the primate optokinetic system. In: Visual motion and its
role in the stabilization of gaze. Rev Oculomot Res
5:393-403.
-
Miles FA
(1998)
The neural processing of 3-D visual information: evidence from eye movements.
Eur J Neurosci
10:811-822[Web of Science][Medline].
-
Minken AWH,
Van Gisbergen JAM
(1994)
A three-dimensional analysis of vergence movements at various levels of elevation.
Exp Brain Res
101:331-345[Web of Science][Medline].
-
Misslisch H,
Hess BJM
(2000)
Three-dimensional vestibuloocular reflex of the monkey: optimal retinal image stabilization versus Listing's law.
J Neurophysiol
83:3264-3276[Abstract/Free Full Text].
-
Misslisch H,
Tweed D,
Sievering D,
Koenig E
(1994)
Rotational kinematics of the human vestibuloocular reflex. III. Listing's law.
J Neurophysiol
72:2490-2502[Abstract/Free Full Text].
-
Misslisch H,
Tweed D,
Hess BJM
(2001)
Stereopsis outweighs gravity in the control of the eyes.
J Neurosci
21:RC126(1-5).
-
Mok D,
Ro A,
Cadera W,
Crawford JD,
Vilis T
(1992)
Rotation of Listing's plane during vergence.
Vision Res
32:2055-2064[Web of Science][Medline].
-
Paige GD,
Tomko DL
(1991)
Eye movement responses to linear head motion in the squirrel monkey. I. Basic characteristics.
J Neurophysiol
65:1170-1182[Abstract/Free Full Text].
-
Schreiber K,
Crawford JD,
Fetter M,
Tweed D
(2001)
The motor side of depth vision.
Nature
410:819-822[Medline].
-
Schwarz U,
Miles FA
(1991)
Ocular responses to translation and their dependence on viewing distance. I. Motion of the observer.
J Neurophysiol
66:851-864[Abstract/Free Full Text].
-
Schwarz U,
Busettini C,
Miles FA
(1989)
Ocular responses to translation are inversely proportional to viewing distance.
Science
245:1394-1396[Abstract/Free Full Text].
-
Telford L,
Seidman SH,
Paige GD
(1997)
Dynamics of squirrel monkey linear vestibuloocular reflex and interactions with fixation distance.
J Neurophysiol
78:1775-1790[Abstract/Free Full Text].
-
Tweed D
(1997)
Visual-motor optimization in binocular control.
Vision Res
37:1939-1951[Web of Science][Medline].
-
Tweed D,
Vilis T
(1987)
Implications of rotational kinematics for the oculomotor system in three dimensions.
J Neurophysiol
58:832-849[Abstract/Free Full Text].
-
Tweed D,
Vilis T
(1990)
Geometric relations of eye position and velocity vectors during saccades.
Vision Res
30:111-127[Web of Science][Medline].
-
Tweed D,
Fetter M,
Andreadaki S,
Koenig E,
Dichgans J
(1992)
Three-dimensional properties of human pursuit eye movements.
Vision Res
32:1225-1238[Web of Science][Medline].
-
Van Rijn LJ,
Van Den Berg AV
(1993)
Binocular eye orientation during fixations: Listing's law extended to include eye vergence.
Vision Res
33:691-702[Web of Science][Medline].
-
von Helmholtz H
(1867)
In: Handbuch der Physiologischen Optik, Vol 3, Ed 1. Hamburg, Germany: Voss.
Copyright © 2003 Society for Neuroscience 0270-6474/03/2341104-05$05.00/0
This article has been cited by other articles:
|
|
|
|
 
K. L. McArthur and J. D. Dickman
Canal and Otolith Contributions to Compensatory Tilt Responses in Pigeons
J Neurophysiol,
September 1, 2008;
100(3):
1488 - 1497.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
F. F. Ghasia, H. Meng, and D. E. Angelaki
Neural Correlates of Forward and Inverse Models for Eye Movements: Evidence from Three-Dimensional Kinematics
J. Neurosci.,
May 7, 2008;
28(19):
5082 - 5087.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Haque, M. Zakir, and J. D. Dickman
Recovery of Gaze Stability During Vestibular Regeneration
J Neurophysiol,
February 1, 2008;
99(2):
853 - 865.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. Tchelidze and B. J. M. Hess
Noncommutative Control in the Rotational Vestibuloocular Reflex
J Neurophysiol,
January 1, 2008;
99(1):
96 - 111.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. F. Walker, J. Tian, and D. S. Zee
Kinematics of the Rotational Vestibuloocular Reflex: Role of the Cerebellum
J Neurophysiol,
July 1, 2007;
98(1):
295 - 302.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
E. M. Klier, H. Meng, and D. E. Angelaki
Three-dimensional kinematics at the level of the oculomotor plant.
J. Neurosci.,
March 8, 2006;
26(10):
2732 - 2737.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Haque and J. D. Dickman
Vestibular Gaze Stabilization: Different Behavioral Strategies for Arboreal and Terrestrial Avians
J Neurophysiol,
March 1, 2005;
93(3):
1165 - 1173.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. Adeyemo and D. E. Angelaki
Similar Kinematic Properties for Ocular Following and Smooth Pursuit Eye Movements
J Neurophysiol,
March 1, 2005;
93(3):
1710 - 1717.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. E. Angelaki
Eyes on Target: What Neurons Must do for the Vestibuloocular Reflex During Linear Motion
J Neurophysiol,
July 1, 2004;
92(1):
20 - 35.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. J. M. Hess and D. E. Angelaki
Vestibular Contributions to Gaze Stability During Transient Forward and Backward Motion
J Neurophysiol,
September 1, 2003;
90(3):
1996 - 2004.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. E. Angelaki
Three-Dimensional Ocular Kinematics During Eccentric Rotations: Evidence for Functional Rather Than Mechanical Constraints
J Neurophysiol,
May 1, 2003;
89(5):
2685 - 2696.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
TOP
ABSTRACT
Introduction
