Eye-position dependence of torsional velocity during interaural translation, horizontal pursuit, and yaw-axis rotation in humans

The saccadic amplitude of humans and monkeys can be adapted using intrasaccadic target steps in the McLaughlin paradigm. It is generally believed that, as a result of a purely retinal reference frame, after adaptation of a saccade of a certain amplitude and direction, saccades of the same amplitude and direction are all adapted to the same extent, independently from the initial eye position. However, recent studies in humans have put the pure retinal coding in doubt by revealing that the initial eye position has an effect on the transfer of adaptation to saccades of different starting points. Since humans and monkeys show some species differences in adaptation, we tested the eye position dependence in monkeys. Two trained Macaca fascicularis performed reactive rightward saccades from five equally horizontally distributed starting positions. All saccades were made to targets with the same retinotopic motor vector. In each session, the saccades that started at one particular initial eye position, the adaptation position, were adapted to shorter amplitude, and the adaptation of the saccades starting at the other four positions was measured. The results show that saccades that started at the other positions were less adapted than saccades that started at the adaptation position. With increasing distance between the starting position of the test saccade and the adaptation position, the amplitude change of the test saccades decreased with a Gaussian profile. We conclude that gain-decreasing saccadic adaptation in macaques is specific to the initial eye position at which the adaptation has been induced.

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Eye-position dependence of torsional velocity during step-ramp pursuit and transient yaw rotation in humans

Experimental Brain Research ◽

10.1007/s00221-005-0261-1 ◽

2005 ◽

Vol 171 (2) ◽

pp. 225-230 ◽

Cited By ~ 5

Author(s):

Jing Tian ◽

David S. Zee ◽

Mark F. Walker

Keyword(s):

Eye Position ◽

Position Dependence

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Compensatory and Orienting Eye Movements Induced By Off-Vertical Axis Rotation (OVAR) in Monkeys

Journal of Neurophysiology ◽

10.1152/jn.00197.222 ◽

2002 ◽

Vol 88 (5) ◽

pp. 2445-2462 ◽

Cited By ~ 27

Author(s):

Keisuke Kushiro ◽

Mingjia Dai ◽

Mikhail Kunin ◽

Sergei B. Yakushin ◽

Bernard Cohen ◽

...

Keyword(s):

Eye Movements ◽

Vertical Axis ◽

Velocity Storage ◽

Eye Position ◽

Rotational Axis ◽

Vestibuloocular Reflex ◽

Time Constants ◽

Head Velocity ◽

Axis Rotation ◽

Eye Velocity

Nystagmus induced by off-vertical axis rotation (OVAR) about a head yaw axis is composed of a yaw bias velocity and modulations in eye position and velocity as the head changes orientation relative to gravity. The bias velocity is dependent on the tilt of the rotational axis relative to gravity and angular head velocity. For axis tilts <15°, bias velocities increased monotonically with increases in the magnitude of the projected gravity vector onto the horizontal plane of the head. For tilts of 15–90°, bias velocity was independent of tilt angle, increasing linearly as a function of head velocity with gains of 0.7–0.8, up to the saturation level of velocity storage. Asymmetries in OVAR bias velocity and asymmetries in the dominant time constant of the angular vestibuloocular reflex (aVOR) covaried and both were reduced by administration of baclofen, a GABAB agonist. Modulations in pitch and roll eye positions were in phase with nose-down and side-down head positions, respectively. Changes in roll eye position were produced mainly by slow movements, whereas vertical eye position changes were characterized by slow eye movements and saccades. Oscillations in vertical and roll eye velocities led their respective position changes by ≈90°, close to an ideal differentiation, suggesting that these modulations were due to activation of the orienting component of the linear vestibuloocular reflex (lVOR). The beating field of the horizontal nystagmus shifted the eyes 6.3°/ g toward gravity in side down position, similar to the deviations observed during static roll tilt (7.0°/ g). This demonstrates that the eyes also orient to gravity in yaw. Phases of horizontal eye velocity clustered ∼180° relative to the modulation in beating field and were not simply differentiations of changes in eye position. Contributions of orientating and compensatory components of the lVOR to the modulation of eye position and velocity were modeled using three components: a novel direct otolith-oculomotor orientation, orientation-based velocity modulation, and changes in velocity storage time constants with head position re gravity. Time constants were obtained from optokinetic after-nystagmus, a direct representation of velocity storage. When the orienting lVOR was combined with models of the compensatory lVOR and velocity estimator from sequential otolith activation to generate the bias component, the model accurately predicted eye position and velocity in three dimensions. These data support the postulates that OVAR generates compensatory eye velocity through activation of velocity storage and that oscillatory components arise predominantly through lVOR orientation mechanisms.

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Kinematics of the Rotational Vestibuloocular Reflex: Role of the Cerebellum

Journal of Neurophysiology ◽

10.1152/jn.00215.2007 ◽

2007 ◽

Vol 98 (1) ◽

pp. 295-302 ◽

Cited By ~ 4

Author(s):

Mark F. Walker ◽

Jing Tian ◽

David S. Zee

Keyword(s):

Tilt Angle ◽

Three Dimensional ◽

Head Rotation ◽

Normal Subjects ◽

Eye Position ◽

Vestibuloocular Reflex ◽

Gaze Stabilization ◽

Eye Rotation ◽

Axis Rotation ◽

Head Impulses

We studied the effect of cerebellar lesions on the 3-D control of the rotational vestibuloocular reflex (RVOR) to abrupt yaw-axis head rotation. Using search coils, three-dimensional (3-D) eye movements were recorded from nine patients with cerebellar disease and seven normal subjects during brief chair rotations (200°/s2 to 40°/s) and manual head impulses. We determined the amount of eye-position dependent torsion during yaw-axis rotation by calculating the torsional-horizontal eye-velocity axis for each of three vertical eye positions (0°, ±15°) and performing a linear regression to determine the relationship of the 3-D velocity axis to vertical eye position. The slope of this regression is the tilt angle slope. Overall, cerebellar patients showed a clear increase in the tilt angle slope for both chair rotations and head impulses. For chair rotations, the effect was not seen at the onset of head rotation when both patients and normal subjects had nearly head-fixed responses (no eye-position-dependent torsion). Over time, however, both groups showed an increasing tilt-angle slope but to a much greater degree in cerebellar patients. Two important conclusions emerge from these findings: the axis of eye rotation at the onset of head rotation is set to a value close to head-fixed (i.e., optimal for gaze stabilization during head rotation), independent of the cerebellum and once the head rotation is in progress, the cerebellum plays a crucial role in keeping the axis of eye rotation about halfway between head-fixed and that required for Listing's Law to be obeyed.

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Vertical Eye Position–Dependence of the Human Vestibuloocular Reflex During Passive and Active Yaw Head Rotations

Journal of Neurophysiology ◽

10.1152/jn.1999.81.5.2415 ◽

1999 ◽

Vol 81 (5) ◽

pp. 2415-2428 ◽

Cited By ~ 28

Author(s):

Matthew J. Thurtell ◽

Ross A. Black ◽

G. Michael Halmagyi ◽

Ian S. Curthoys ◽

Swee T. Aw

Keyword(s):

Three Dimensional ◽

Head Position ◽

Eye Position ◽

Vestibuloocular Reflex ◽

Head Velocity ◽

High Acceleration ◽

Position Dependence ◽

Head Impulses ◽

Eye Velocity ◽

Head Rotations

Vertical eye position–dependence of the human vestibuloocular reflex during passive and active yaw head rotations. The effect of vertical eye-in-head position on the compensatory eye rotation response to passive and active high acceleration yaw head rotations was examined in eight normal human subjects. The stimuli consisted of brief, low amplitude (15–25°), high acceleration (4,000–6,000°/s2) yaw head rotations with respect to the trunk (peak velocity was 150–350°/s). Eye and head rotations were recorded in three-dimensional space using the magnetic search coil technique. The input-output kinematics of the three-dimensional vestibuloocular reflex (VOR) were assessed by finding the difference between the inverted eye velocity vector and the head velocity vector (both referenced to a head-fixed coordinate system) as a time series. During passive head impulses, the head and eye velocity axes aligned well with each other for the first 47 ms after the onset of the stimulus, regardless of vertical eye-in-head position. After the initial 47-ms period, the degree of alignment of the eye and head velocity axes was modulated by vertical eye-in-head position. When fixation was on a target 20° up, the eye and head velocity axes remained well aligned with each other. However, when fixation was on targets at 0 and 20° down, the eye velocity axis tilted forward relative to the head velocity axis. During active head impulses, the axis tilt became apparent within 5 ms of the onset of the stimulus. When fixation was on a target at 0°, the velocity axes remained well aligned with each other. When fixation was on a target 20° up, the eye velocity axis tilted backward, when fixation was on a target 20° down, the eye velocity axis tilted forward. The findings show that the VOR compensates very well for head motion in the early part of the response to unpredictable high acceleration stimuli—the eye position– dependence of the VOR does not become apparent until 47 ms after the onset of the stimulus. In contrast, the response to active high acceleration stimuli shows eye position–dependence from within 5 ms of the onset of the stimulus. A model using a VOR-Listing’s law compromise strategy did not accurately predict the patterns observed in the data, raising questions about how the eye position–dependence of the VOR is generated. We suggest, in view of recent findings, that the phenomenon could arise due to the effects of fibromuscular pulleys on the functional pulling directions of the rectus muscles.

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