| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
Report
Department of Neurology, University Hospital Zürich, CH-8091, Switzerland; and Department of Neurobiology, Washington University School of Medicine, St. Louis, Missouri 63110
Submitted 24 February 2003; accepted in final form 13 April 2003
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
|---|
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
|---|
;
Helmholtz 1867;
Tweed and Vilis 1987). It
implies that there exists a unique ocular orientation, called primary eye
position, from which any other accessible eye positions at a constant vergence
angle can be reached by a combination of horizontal and vertical rotations.
Eye positions with zero torsion lie in a plane, called Listing's plane.
Saccadic, fixation, and smooth pursuit eye positions have all been shown to be
confined to this plane (Crawford and Vilis
1991; Haslwanter et al.
1991,
1992;
Tweed and Vilis 1987;
Tweed et al. 1992).
When statically tilted away from the upright orientation, primary position
and Listing's plane during saccades and fixations were shown to change in both
humans and monkeys (Bockisch and Haslwanter
2001; Crawford and Vilis
1991; Furman and Schor
2003; Haslwanter et al.
1992; Suzuki et al.
1997). Specifically during static roll tilts, a constant amount of
torsion is added to all eye positions, resulting in a shift of Listing's plane
along the torsional axis. Similarly, during static pitch tilts, there is a
corresponding upward or downward rotation of Listing's plane. In both cases,
the direction of shift or rotation, amounting to only about 10% of the tilt,
is in opposite direction to the static tilt, such that Listing's plane does
not remain fixed in head coordinates. Other eye movement systems, such as
smooth pursuit, have been shown to follow Listing's law
(Haslwanter et al. 1991;
Tweed et al. 1992). Although
these effects of head position on Listing's plane orientation hold true for
saccadic eye movements with or without visual guidance, it is presently
unknown whether the same relations also hold true for smooth pursuit eye
movements. Since burst neurons, whose firing rates reflect this
gravity-dependent modulation (Scherberger
et al. 2001), do not modulate during smooth pursuit eye movements,
such information is important for understanding these otolith-dependent
effects and the neural organization of 3D eye movements in general. The aim of
this work was to study the 3D ocular orientation during smooth pursuit eye
movements as a function of static head orientation relative to gravity.
|
METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
|---|
Data were obtained from two rhesus monkeys (Macaca mulatta), which
were chronically prepared with scleral dual-search coils for three-dimensional
(3D) eye movement recordings and skull bolts for restraining head motion
during the experiments. Details of fabrication and implantation of the
dual-search coil have been reported elsewhere
(Hess 1990). The dual coil was
implanted on the left eye of one animal and the right eye of the other animal.
All surgeries and animal handling were in accordance with the National
Institutes of Health Guide for the Care and Use of Laboratory Animals and were
approved by the Veterinary Office of the Canton of Zurich. 3D eye position was
measured with a two-field search coil system (Eye Position Meter 3000, Skalar,
Delft, The Netherlands). The search coil signals were calibrated as described
in Hess et al. (1992). In
brief, an in vitro calibration prior to implantation yielded the coil
sensitivities and the angle between the two search coils. The orientation of
the dual coil on the eye was determined from the four coil output signals
during fixation of a series of vertically arranged target lights relative to
straight ahead. Horizontal, vertical, and torsional eye positions were
digitized at a sampling rate of 833 Hz and stored on a computer for off-line
data analysis. Eye positions were expressed as rotation vectors, E =
tan (
/2)u, where u is a unit vector pointing along the axis
of rotation that brings the eye from the reference position to current
position, and is the angle of rotation about u
(Haustein 1989). 3D eye
positions were expressed relative to a right-handed coordinate system. A
positive torsional, vertical, or horizontal eye position component
(Etor, Ever, Ehor)
corresponded to a clockwise, downward, or leftward rotation of the eye (from
the subjective viewpoint). Listing's plane and primary eye position were
determined from spontaneous eye movements in the light with the head upright
and stationary. All rotation vectors in tilted head orientations were
expressed relative to primary position that was calculated in an upright
position as the unique eye orientation with gaze direction normal to Listing's
plane (see Data analyses).
Experimental protocols
During the experiments, animals were seated in a primate chair with their head restrained in a position of 15° nose-down relative to the stereotaxic horizontal (defined as "upright" position) to place the lateral semicircular canals approximately earth-horizontal. The animals were placed inside the inner frame of a superstructure consisting of two motor-driven gimbaled axes. The effects of static changes in head orientation relative to gravity on visually guided saccades and smooth pursuit eye movements were studied while the monkey was sitting inside a sphere, which completely surrounded the animal (inner diameter, 80 cm). The inner wall of the sphere was covered with a random dot pattern. Using the outmost gimbaled axis of the super-structure, the animal could be tilted relative to earth-vertical without changing its orientation relative to its visual surround (i.e., the optokinetic sphere).
The experimental protocols consisted of the following two visual stimulation protocols that were each tested with the animal in upright, 30°, and 90° left or right ear-down position as well as in 30° and 90° nose up and nose down position. 1) Projection of a laser spot at random locations on the inner wall of the sphere to elicit visually guided saccades. Data were also collected during spontaneous saccades that typically occurred over a range of approximately 35° x 35° (re: straight ahead). 2) Projection of a horizontally or vertically oscillating laser spot at various elevations and eccentricities relative to straight ahead (0°, ±10°, ±15°) at frequencies and amplitudes of 0.1 Hz, ±15° (corresponding to ±9.4°/s) or 0.5 Hz, ±8° (corresponding to ±25.1°/s). Trained animals maintained their eye position within a 2° behavioral window for fluid reward. Due to the eccentric mounting of the system (35 cm up and 15 cm forward relative to the center of the optokinetic sphere) the projected laser spot moved only approximately on iso-elevation and iso-azimuth curves. As a result, target movement during vertical pursuit generated large vertical but also small horizontal eye movements (Fig. 1B and 2B).
|
|
Data analyses
At the beginning of each experimental session, primary position was
determined from spontaneous eye movements while the animal was looking around
in the normally lit laboratory, as follows. First, a planar surface was fitted
to the pooled eye positions by minimizing the least-squares error according to
the equation: Etor = a +
bEver + cEhor, where
Etor, Ever, and
Ehor denote the torsional, vertical, and horizontal
components of the eye position vector E. From the best fit plane
parameters a, b, and c, primary eye position, P, was
determined as the rotation vector: P = [a,c, –
b]t, where t denotes transpose (Hess and
Angelaki
1997a,1997b,
1999). Note that in upright
the x-component of primary eye position is zero for gaze in reference
direction (i.e., a = 0: the best fit plane passes through the origin
of the coordinate system).
Data collected in tilted head orientations were then expressed relative to
upright primary position (Listing's coordinates) (i.e., relative to an
orthogonal coordinate system whose first axis was aligned with primary gaze
direction). For this, we left-multiplied all eye position vectors,
E, with the inverse of primary eye position:
E' = P–1 o
E = (P–1 +
E +
P–1o
E)/(1 – P–1
E), where "^" denotes the cross product and
"" denotes the scalar product. For pursuit analyses, only
the slow-phase portions where the eye followed the motion of the target were
included. For the saccade/fixation protocols, the whole data set (including
both saccades and fixations) was included in the analyses. Subsequently, eye
positions in each tilted head orientation were fitted separately for pursuit
and saccades/fixations with planar surfaces. The parameter
"a" then described the torsional offset of these best fit
planes, while "b" and "c" described
the temporal and forward-backward tilt of the best fit plane relative to
upright Listing's plane. The "thickness" of the best fit planes
was characterized by the torsional SD of eye positions relative to the plane.
This torsional SD was computed as
 |
and
and collected all saccades such that
15° (for i = 1 to N). Presented data were collected during 20 experimental sessions for each animal. Statistical comparisons were based on analyses of covariance (ANCOVA) with tilt angle as a covariate.
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
|---|
). In
the following we compare the spatial organization of horizontal and vertical
smooth pursuit eye movements with those of saccadic eye movements that have
been obtained in the same animal under identical experimental conditions. For
an easy comparison, all eye movements were expressed in Listing's coordinates
relative to primary position, which was obtained on each experimental day from
visually guided saccadic eye movements in upright orientation (see
METHODS). Figures 1 and 2 illustrate the 3D organization of smooth pursuit eye movements in tilted roll and pitch head orientations, respectively. In both plots, the top traces show torsional, vertical, and horizontal eye position as a function of time during 0.1 Hz pursuit centered at three different directions of gaze. During horizontal pursuit (Figs. 1A and 2A), gaze direction pointed straight ahead, as well as 15° upward and downward. During vertical pursuit (Figs. 1B and 2B), gaze pointed straight ahead, as well as 15° to the left and to the right. Thus each plot in Figs. 1, A and B, and 2, A and B, consisted of nine different traces, corresponding to three gaze directions x three head orientations (upright and left/right side-down or supine/prone). Torsional eye position, although negligible in upright orientation, increased its amplitude in side-down positions (Fig. 1, A and B). Specifically during horizontal smooth pursuit, there was a positive torsional shift in left side-down positions and a negative torsional shift in right side-down positions (Fig. 1A). Similarly, during vertical smooth pursuit, a similar torsional shift was also observed in the respective roll head orientations (Fig. 1B).
The change in the 3D organization of smooth pursuit eye movements in upright versus tilted head orientations became more apparent when the same data were now plotted in spatial coordinates (Fig. 1, C and D). Specifically, Fig. 1C plots eye positions in the sagittal (horizontal-torsional) plane, whereas Fig. 1D plots eye positions in the horizontal (vertical/torsional) plane (see cartoon drawings). For these spatial orientation plots, we have combined data during both horizontal and vertical smooth pursuit eye movements at all different vertical and horizontal eccentricities. All upright smooth pursuit eye positions have been shown in yellow, whereas left and right side-down data have been plotted in blue and green, respectively. To quantify any changes in plane orientation, these 3D eye positions were fitted with planar surfaces (solid lines in Fig. 1, C and D). Although in tilted head orientations eye positions still exhibited a small (<1°) torsional SD relative to the fitted planar surface, a clear change in the orientation of this plane (including both a torsional shift, Fig. 1C, and a temporal rotation; Fig. 1D) was apparent. In fact, these changes in plane orientation were very comparable to those during visually guided saccades/fixations under identical experimental conditions (Fig. 1, C and D, insets on the right).
Changes in eye position plane orientation, although typically smaller, were
also obtained when the animal was tilted in the pitch plane
(Fig. 2). In this case, rather
than a torsional shift (Fig.
1), there was a small but systematic pitch tilt in the 3D plane of
eye positions during smooth pursuit. This tilt was most apparent in the
sagittal plane view (Fig.
2C). For clarity due to the small effects, responses
obtained in the upright position have not been illustrated in the spatial
plots. These observations for static pitch tilts were similar to those during
saccades and fixations (Fig. 2, C
and D, insets on the right; see also
Haslwanter et al. 1992).
Data from both animals have been summarized in Fig. 3. Because there was no difference in the spatial organization of 3D eye positions during pursuit at 0.1 and 0.5 Hz (R(3,56)= 1.5, P > 0.05), data were combined. The spatial orientation and thickness of the 3D planes as a function of tilt angle were described by four parameters, including the torsional shift, the temporal tilt angle (i.e., yaw-plane rotation), the forward/backward tilt angle (i.e., pitch-plane rotation), and the torsional SD (Fig. 3, A–D). There were no significant differences in the torsional shift, temporal tilt, or forward/backward tilt as a function of tilt angle for smooth pursuit and visually guided saccades (R(3,121) = 0.8, P > 0.05; Fig. 3, compare open with solid circles, respectively). A significant correlation between the torsional shift of the planes and tilt angle was only observed for roll tilts (pursuit: r = 0.95, saccades: r = 0.97; Fig. 3A). The temporal tilt angle of the fitted planes (parameter b; see METHODS) was also found to vary as a function of roll (but not pitch) tilt (pursuit: r = 0.87, saccades: r = 0.73; Fig. 3C). In contrast, the forward/backward tilt of the fitted planes (parameter c; see METHODS) exhibited a systematic dependence on pitch (but not roll) tilt angle (pursuit: r = 0.73, saccades: r = 0.94; Fig. 3D).
|
When considering the whole range of saccadic eye movements recorded, smooth pursuit planes exhibited a smaller torsional SD compared with saccade/fixation data (F(1,123) = 81.6, P < 0.05; Fig. 3B, compare open with solid circles, respectively). This difference was due to the large eccentricities (±35°) used for saccades compared with pursuit (±15°), as this difference was no longer present when displacement planes for saccades/fixations were restricted to a similar oculomotor range (±15° relative to straight ahead; F(1,123) = 2.9, P > 0.05; Fig. 3B, solid triangles).
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
|---|
).
Although clearly present, these effects were rather small, typically
compensating for <10% of the head tilt.
In addition to the torsional shift, there was also a significant change in
the temporal (yaw) tilt of Listing's plane as a function of roll tilt.
Orienting gaze shifts have been studied mostly in the horizontal plane as a
shift in the beating field of vestibular or optokinetic nystagmus
("Schlagfeldverlagerung") in the direction of the ocular quick
phases (man: Jung and Mittermaier
1939; monkey: O-Uchi et al.
1981; Solomon and Cohen
1992a,b;
cat: Chun and Robinson 1978;
Vidal et al. 1982; pigeon:
Gioanni 1988; rat:
Maier and Dieringer 1993).
Whether the small but significant conjugate rotation of Listing's plane toward
the contraversive side, which we observed here in static side-down positions,
can be interpreted in this context is not clear because primary gaze tends to
move away from the direction in which one would fall. Thus the gravity-driven
modulation of Listing's plane in the yaw plane appears not to follow the
principle that subjects tend to orient gaze toward the direction of (loco-)
motion (Chun and Robinson
1978).
In recent years, there is growing evidence that the visuomotor control of
3D eye orientation is implemented downstream of the superior colliculus
(Hepp et al. 1993;
Van Opstal et al. 1991).
Visual and eye movement related signal processing in many cortical areas as
well as in the superior colliculus seem to be organized in retinal coordinates
and 3D eye/head coordination, including torsional eye movements and Donder's
law are implemented downstream of the superior colliculus (Klier et al.
2001,
2003). Burst neurons in the
midbrain have been reported to change their firing rates as a function of
static head position (Scherberger et al.
2001). Recent models of the otolith effects on the static
orientation of the eyes have suggested a direct involvement of the
velocity-to-position neural integrator
(Crawford et al. 1999;
Glasauer et al. 2001). The
present results, showing similar gravity dependence for pursuit and saccades,
are consistent with this notion. Although the neural networks for integration
of eye velocity signals, including the nucleus prepositus hypoglossi, the
interstitial nucleus of Cajal, and the paramedian tract neurons
(Cannon and Robinson 1987;
Crawford 1994;
Crawford et al. 1991;
Fukushima 1991;
Godaux and Cheron 1996;
Kaneko 1997;
Nakamagoe et al. 2000) are
extensively interconnected with the vestibular nuclei (see Buettner-Ennever
1989, 1999 for review), the details of these interactions and computations are
still missing.
The functional significance of this small but systematic shifts and tilts
of Listing's plane as a smooth function of the head roll and pitch angles
remains unknown, although it has been postulated that it merely represents a
vestigial remnant of ocular counterrolling and counterpitching that is large
in lateral-eyed species (Vilis
1993). This hypothesis arises from the fact that ocular
counterrolling is small in humans
(Collewijn et al. 1985; Diamond
and Markham 1981,
1983;
Diamond et al. 1982;
Hannen et al. 1966;
Markham and Diamond 2001;
Miller and Graybiel 1971) but
large in lateral-eyed species (Baarsma and
Collewijn 1975; Barmack and
Pettorossi 1988; Dickman and
Angelaki 1999; Hess and Dieringer
1990,
1991).
The findings reported here that not only saccades but also pursuit eye
movements are modulated by head orientation relative to gravity further raises
the question of why these static otolith-driven orientation reflexes have not
been completely eliminated during evolution, if of no functional role
(Vilis 1993). Notably, during
movement, the systematic shifts and rotations of 3D eye position planes of
visually guided saccades as a function of head orientation in space not only
persist but are also much larger than those observed under static conditions
(Hess and Angelaki 1997b). In
addition, these shifts/rotations of 3D eye position planes were reported to
increase as a function of tilt movement frequency not only during visually
guided saccades but also during smooth pursuit eye movements as well
(Hess and Angelaki 2002). We
have previously proposed that the low gain changes in the 3D organization of
eye positions under static tilt conditions might represent the low-frequency
tail of a functionally relevant vestibular mechanism that subserves
orientation constancy with respect to earth-vertical during motion.
Accordingly, under static tilt conditions, otolith-driven 3D eye position
changes contribute only minimally to the spatial constancy of retinal images,
which is then mainly guaranteed by visually driven mechanisms. In contrast,
during mid- and high-frequency rotations when visually driven mechanisms are
less effective, a vestibularly driven orientation mechanism appears to exist
that maintains the coordinates of Listing's plane largely invariant with
respect to earth-vertical. This hypothesis remains to be tested in future
studies.
|
DISCLOSURES |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
|---|
|
ACKNOWLEDGMENTS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
|---|
|
FOOTNOTES |
|---|
Address for reprint requests: B.J.M. Hess, Dept. of Neurology, Zürich University Hospital, Frauenklinikstrasse 26, CH-8091, Zürich, Switzerland (E-mail: bhess{at}neurol.unizh.ch).
|
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
|---|
Baarsma EA and
Collewijn H. Eye movements due to linear accelerations in the rabbit.
J Physiol 245:
227–247, 1975.
Barmack NH and Pettorossi VE. The otolith origin of the vertical vestibuloocular reflex following bilateral blockage of the vertical semicircular canals in the rabbit. J Neurosci 8: 2827–2835, 1988.[Abstract]
Bockisch CJ and Haslwanter T. Three-dimensional eye position during static roll and pitch in humans. Vision Res 41: 2127–2137, 2001.[Web of Science][Medline]
Büttner-Ennever JA. Neuroanatomy of the Oculomotor System. Rev. Oculomotor Res., Vol. 2, Amsterdam: Elsevier, 1989.
Büttner-Ennever JA. A review of otolith pathways to brainstem and cerebellum. Ann NY Acad Sci 871: 51–64, 1999.[Web of Science][Medline]
Cannon SC and Robinson DA. Loss of the neural integrator of the oculomotor system from brain stem lesion of the monkey. J Neurophysiol 57: 1326–1345, 1987.
Chun KS and Robinson DA. A model of quick phase generation in the vestibulo-ocular reflex. Biol Cybern 28: 209–221, 1978.[Web of Science][Medline]
Collewijn H, Van Der Steen J, Ferman L, and Jansen TC. Human ocular counterroll: assessment of static and dynamic properties from electromagnetic scleral coil recordings. Exp Brain Res 59: 185–196, 1985.[Web of Science][Medline]
Crawford JD. The oculomotor neural integrator uses a behavior-related coordinate system. J Neurosci 14: 6911–6923, 1994.[Abstract]
Crawford JD,
Cadera W, and Vilis T. Generation of torsional and vertical eye position
signals by the interstitial nucleus of Cajal. Science
252: 1551–1553,
1991.
Crawford JD,
Ceylan MZ, Klier EM, and Guitton D. Three-dimensional eye-head
coordination during gaze saccades in the primate. J
Neurophysiol 81:
1760–1782, 1999.
Crawford JD and
Vilis T. Axes of eye rotation and Listing's law during rotations of the
head. J Neurophysiol 65:
407–423, 1991.
Diamond SG and Markham CH. Binocular counterrolling in humans with unilateral labyrinthectomy and in normal controls. Ann NY Acad Sci 374: 69–79, 1981.[Web of Science][Medline]
Diamond SG and Markham CH. Ocular counterrolling during constant velocity roll in patients with brainstem compression. Adv Otorhinolaryngol 30: 183–186, 1983.[Medline]
Diamond SG, Markham CH, and Furuya N. Binocular counterrolling during sustained body tilt in normal humans and in a patient with unilateral vestibular nerve section. Ann Otol Rhinol Laryngol 91: 225–229, 1982.[Web of Science][Medline]
Dickman JD and Angelaki DE. Three-dimensional organization of vestibular related eye movements to off-vertical axis rotation and linear translation in pigeons. Exp Brain Res 129: 391–400, 1999.[Web of Science][Medline]
Ferman L, Collewijn H, and Van Den Berg AV. A direct test of Listing's Law. I. Human ocular torsion measured in static tertiary positions. Vision Res 27: 929–938, 1987.[Web of Science][Medline]
Fukushima K. The interstitial nucleus of Cajal in the midbrain reticular formation and vertical eye movement. Neurosci Res 10: 159–187, 1991.[Web of Science][Medline]
Furman JM and Schor RH. Orientation of Listing's plane during static tilt in young and older human subjects. Vision Res 43: 67–76, 2003.[Web of Science][Medline]
Glasauer S,
Dieterich M, and Brandt T. Central positional nystagmus simulated by a
mathematical ocular motor model of otolith-dependent modification of Listing's
plane. J Neurophysiol 86:
1546–1554, 2001.
Gioanni H. Stabilizing gaze reflexes in the pigeon (Columba livia). I. Horizontal and vertical optokinetic eye (OKN) and head (OCR) reflexes. Exp Brain Res 69: 567–582, 1988.[Web of Science][Medline]
Godaux E and
Cheron G. The hypothesis of the uniqueness of the oculomotor neural
integrator: direct experimental evidence in the cat. J
Physiol 492:
517–527, 1996.
Hannen RA, Kabrisky M, Replogle CR, Hartzler VL, and Roccaforte PA. Experimental determination of a portion of the human vestibular system response through measurement of eyeball counterroll. IEEE Trans Biomed Eng 13: 65–70, 1966.[Medline]
Haslwanter T, Straumann D, Hepp K, Hess BJM, and Henn V. Smooth pursuit eye movements obey Listing's Law in the monkey. Exp Brain Res 87: 470–472, 1991.[Web of Science][Medline]
Haslwanter T, Straumann D, Hess BJM, and Henn V. Static roll and pitch in the monkey: shift and rotation of Listing's plane. Vision Res 23: 1341–1348, 1992.
Haustein W. Considerations on Listing's law and the primary position by means of a matrix description of eye position control. Biol Cybern 60: 411–420, 1989.[Web of Science][Medline]
Helmholtz von H. Handbuch der Physiologischen Optik. Hamburg: Voss, 1867.
Hepp K, Van
Opstal AJ, Straumann D, Hess BJM, and Henn V. Monkey superior colliculus
represents rapid eye movements in a two-dimensional motor map. J
Neurophysiol 69:
965–979, 1993.
Hess BJM. Dual search coil for measuring 3-dimensional eye movements in experimental animals. Vision Res 30: 597–602, 1990.[Web of Science][Medline]
Hess BJM and
Angelaki DE. Kinematic principles of primate rotational vestibulo-ocular
reflex I. Spatial organization of fast phase velocity axes. J
Neurophysiol 78:
2193–2202, 1997a.
Hess BJM and
Angelaki DE. Kinematic principles of primate rotational vestibulo-ocular
reflex. I. Gravity-dependent modulation of primary eye position. J
Neurophysiol 78:
2203–2216, 1997b.
Hess BJM and
Angelaki DE. Oculomotor control of primary eye position discriminates
between translation and tilt. J Neurophysiol
81: 394–398,
1999.
Hess BJM and Angelaki DE. Gravity modifies 3D coordinates of visually guided saccades and smooth pursuit eye movements. Soc Neurosci Abstr 2002.
Hess BJM and Dieringer N. Spatial organization of the maculoocular reflexes in the rat: responses during off-vertical axis rotation. Eur J Neurosci 2: 909–919, 1990.[Web of Science][Medline]
Hess BJM and
Dieringer N. Spatial organization of linear vestibuloocular reflexes of
the rat: responses during horizontal and vertical linear acceleration.
J Neurophysiol 66:
1805–1818, 1991.
Hess BJM, Van Opstal AJ, Straumann D, and Hepp K. Calibration of three-dimensional eye position using search coil signals in the rhesus monkey. Vision Res 32: 1647–1654, 1992.[Web of Science][Medline]
Jung R and Mittermaier R. Zur objektiven Registrierung und Analyse verschiedener Nystagmusformen: vestibulärer, optokinetischer und spontaner Nystagmus in ihren Wechselbeziehungen. Arch Ohren Nasen Kehlkopfheilkd 146: 410–439, 1939.
Kaneko CR.
Eye movement deficits after ibotenic acid lesions of the nucleus prepositus
hypoglossi in monkeys. I. Saccades and fixation. J
Neurophysiol 78:
1753–1768, 1997.
Klier EM, Wang H, and Crawford JD. The superior colliculus encodes gaze commands in retinal coordinates. Nat Neurosci 4: 627–632, 2001.[Web of Science][Medline]
Klier EM, Wang
H, and Crawford JD. Three-dimensional eye-head coordination is implemented
downstream from the superior colliculus. J
Neurophysiol, 89:
2839–2853, 2003.
Maier RK and Dieringer N. The role of compensatory eye and head movements in the rat for image stabilization and gaze orientation. Exp Brain Res 96: 54–64, 1993.[Web of Science][Medline]
Markham CH and Diamond SG. Ocular counterrolling differs in dynamic and static stimulation. Acta Otolaryngol Suppl 545: 97–100, 2001.[Medline]
Miller EF 2nd
and Graybiel AM. Effect of gravitoinertial force on ocular counterrolling.
J Appl Physiol 31:
697–700, 1971.
Misslich H,
Tweed D, and Hess BJM. Stereopsis outweighs gravity in the control of the
eyes. J Neurosci 21:
RC126, 2001.
Nakamagoe K,
Iwamoto Y, and Yoshida K. Evidence for brainstem structures participating
in oculomotor integration. Science
288: 857–859,
2000.
O-Uchi T, Igarashi M, and Kubo T. Effect of frontal-eye-field lesion on eye-head coordination in squirrel monkeys. Ann NY Acad Sci 374: 656–673, 1981.[Web of Science][Medline]
Pettorossi VE, Errico P, and Ferraresi A. Difference in quick phases induced by horizontal and vertical vestibular stimulations. J Vestib Res 7: 89–99, 1997a.[Web of Science][Medline]
Pettorossi VE, Manni E, Errico P, Ferraresi A, and Bortolami R. Otolithic and extraocular muscle proprioceptive influences on the spatial organization of the vestibulo- and cervico-ocular quick phases. Acta Otolaryngol 117: 139–142, 1997b.[Medline]
Scherberger H,
Cabungcal J-H, Hepp K, Suzuki Y, Straumann D, and Henn V. Ocular
counterroll modulates the preferred direction of saccade-related pontine burst
neurons in the monkey. J Neurophysiol
86: 935–949,
2001.
Solomon D and
Cohen B. Stabilization of gaze during circular locomotion in light. I.
Compensatory head and eye nystagmus in the running monkey. J
Neurophysiol 67:
1146–1157, 1992a.
Solomon D and
Cohen B. Stabilization of gaze during circular locomotion in darkness. II.
Contribution of velocity storage to compensatory eye and head nystagmus in the
running monkey. J Neurophysiol
67: 1158–1170,
1992b.
Suzuki Y, Kase
M, Kato H, and Fukushima K. Stability of ocular counter-rolling and
Listing's plane during static roll-tilts. Invest Ophthalmol Vis
Sci 38:
2103–2111, 1997.
Tweed D, Fetter M, Andreadaki S, Koenig E, and Dichgans J. Three-dimensional properties of human pursuit eye movements. Vision Res 32: 1225–1238, 1992.[Web of Science][Medline]
Tweed D and
Vilis T. Implications of rotational kinematics for the oculomotor system
in three dimensions. J Neurophysiol
58: 832–849,
1987.
Van Opstal AJ,
Hepp K, Hess BJM, Straumann D, and Henn V. Two-rather than
three-dimensional representation of saccades in monkey superior colliculus.
Science 252:
1313–1315, 1991.
Vidal PP, Roucoux A, and Berthoz A. Horizontal eye position-related activity in neck muscles of the alert cat. Exp Brain Res 46: 448–453, 1982.[Web of Science][Medline]
Vilis T. Interactions between the angular and translational components of the vestibulo-ocular reflex. In: The Vestibulo-Ocular Reflex and Vertigo, edited by Sharpe JA and Barber HO. New York: Raven Press, Ltd., 1993.
This article has been cited by other articles:
|
|
 |
|
  B. T. Crane, J.-R. Tian, and J. L. Demer Shifts in Listing's Plane Produced by Vertical Axis Rotation: Sustained Ocular Torsion Due to Semicircular Canal Stimulation Invest. Ophthalmol. Vis. Sci., May 1, 2007; 48(5): 2076 - 2083. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. T. Crane, J. Tian, and J. L. Demer Temporal Dynamics of Ocular Position Dependence of the Initial Human Vestibulo-ocular Reflex. Invest. Ophthalmol. Vis. Sci., April 1, 2006; 47(4): 1426 - 1438. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Palla, C. J. Bockisch, O. Bergamin, and D. Straumann Dissociated Hysteresis of Static Ocular Counterroll in Humans J Neurophysiol, April 1, 2006; 95(4): 2222 - 2232. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. A. Clark and J. L. Demer Magnetic Resonance Imaging of the Effects of Horizontal Rectus Extraocular Muscle Surgery on Pulley and Globe Positions and Stability Invest. Ophthalmol. Vis. Sci., January 1, 2006; 47(1): 188 - 194. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. L. Demer and R. A. Clark Magnetic Resonance Imaging of Human Extraocular Muscles During Static Ocular Counter-Rolling J Neurophysiol, November 1, 2005; 94(5): 3292 - 3302. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. Kono, V. Poukens, and J. L. Demer Superior Oblique Muscle Layers in Monkeys and Humans Invest. Ophthalmol. Vis. Sci., August 1, 2005; 46(8): 2790 - 2799. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. T. Crane, J. Tian, and J. L. Demer Kinematics of Vertical Saccades during the Yaw Vestibulo-ocular Reflex in Humans Invest. Ophthalmol. Vis. Sci., August 1, 2005; 46(8): 2800 - 2809. [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]
|
|
|
|
|
|
J. L. Demer Pivotal Role of Orbital Connective Tissues in Binocular Alignment and Strabismus The Friedenwald Lecture Invest. Ophthalmol. Vis. Sci., March 1, 2004; 45(3): 729 - 738. [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| Visit Other APS Journals Online |
