Torsional dynamics and cross-coupling in the human vestibulo-ocular reflex during active head rotation

2000 ◽  
Vol 10 (2) ◽  
pp. 119-125 ◽  
Author(s):  
H. Misslisch ◽  
D. Tweed
Keyword(s):  
Cross Coupling ◽  
Head Rotation ◽  
Adaptive Networks ◽  
Low Frequencies ◽  
3 Dimensional ◽  
Ocular Reflex ◽  
Eye Rotation ◽  
Eye Motion ◽  
Vestibulo Ocular Reflex ◽  
Save Energy

Six subjects fixated an imagined space-fixed target in darkness, or a visible target against a structured visual background, while rotating their heads actively in yaw, pitch and roll at four different frequencies, from 0.3 to 2.4 Hz. We used search coils to measure the 3-dimensional rotations of the head and eye, and described the relation between them – the input-output function of the rotational vestibulo-ocular reflex (VOR) – using gain matrices. We found consistent cross-coupling in which torsional head rotation evoked horizontal eye rotation. The reason may be that the eyes are above the axis of torsional head rotation, and therefore may translate horizontally during the head motion, so the VOR rotates them horizontally to compensate. Torsional gain was lower than horizontal or vertical, more variable from subject to subject and decreased at low frequencies. One reason for the low gain may be that torsional head rotation produces little retinal slip near the fovea; hence little compensatory eye motion is needed, and so the VOR reduces its torsional gain to save energy or to approximate Listing's law by keeping ocular torsion near zero. In addition, the human VOR has little experience with purely torsional head rotations and so its adaptive networks may be poorly trained for such stimuli. The drop in torsional gain at low frequencies can be explained based on the leak in the neural integrator that helps convert torsional eye-velocity commands into eye-position commands.

Combined Influence of Vergence and Eye Position on Three-Dimensional Vestibulo-Ocular Reflex in the Monkey

2002 ◽  
Vol 88 (5) ◽  
pp. 2368-2376 ◽  
Author(s):  
H. Misslisch ◽  
B.J.M. Hess
Keyword(s):  
Three Dimensional ◽  
Head Rotation ◽  
Eye Position ◽  
Near Vision ◽  
Ocular Reflex ◽  
Rotation Axes ◽  
Eye Rotation ◽  
Visual Background ◽  
Vestibulo Ocular Reflex ◽  
Head Rotations

This study examined two kinematical features of the rotational vestibulo-ocular reflex (VOR) of the monkey in near vision. First, is there an effect of eye position on the axes of eye rotation during yaw, pitch and roll head rotations when the eyes are converged to fixate near targets? Second, do the three-dimensional positions of the left and right eye during yaw and roll head rotations obey the binocular extension of Listing's law (L2), showing eye position planes that rotate temporally by a quarter as far as the angle of horizontal vergence? Animals fixated near visual targets requiring 17 or 8.5° vergence and placed at straight ahead, 20° up, down, left, or right during yaw, pitch, and roll head rotations at 1 Hz. The 17° vergence experiments were performed both with and without a structured visual background, the 8.5° vergence experiments with a visual background only. A 40° horizontal change in eye position never influenced the axis of eye rotation produced by the VOR during pitch head rotation. Eye position did not affect the VOR eye rotation axes, which stayed aligned with the yaw and roll head rotation axes, when torsional gain was high. If torsional gain was low, eccentric eye positions produced yaw and roll VOR eye rotation axes that tilted somewhat in the directions predicted by Listing's law, i.e., with or opposite to gaze during yaw or roll. These findings were seen in both visual conditions and in both vergence experiments. During yaw and roll head rotations with a 40° vertical change in gaze, torsional eye position followed on average the prediction of L2: the left eye showed counterclockwise (ex-) torsion in down gaze and clockwise (in-) torsion in up gaze and vice versa for the right eye. In other words, the left and right eye's position plane rotated temporally by about a quarter of the horizontal vergence angle. Our results indicate that torsional gain is the central mechanism by which the brain adjusts the retinal image stabilizing function of the VOR both in far and near vision and the three dimensional eye positions during yaw and roll head rotations in near vision follow on average the predictions of L2, a kinematic pattern that is maintained by the saccadic/quick phase system.

Spatial orientation of the angular vestibulo-ocular reflex

1999 ◽  
Vol 9 (3) ◽  
pp. 163-172
Author(s):  
Bernard Cohen ◽  
Susan Wearne ◽  
Mingjia Dai ◽  
Theodore Raphan
Keyword(s):  
Spatial Orientation ◽  
Optokinetic Nystagmus ◽  
Vestibular Nuclei ◽  
Velocity Storage ◽  
Gravitational Acceleration ◽  
Ocular Reflex ◽  
Eye Rotation ◽  
Slow Velocity ◽  
Vestibulo Ocular Reflex ◽  
Vector Sum

During vestibular nystagmus, optokinetic nystagmus (OKN), and optokinetic afternystagmus (OKAN), the axis of eye rotation tends to align with the vector sum of linear accelerations acting on the head. This includes gravitational acceleration and the linear accelerations generated by translation and centrifugation. We define the summed vector of gravitational and linear accelerations as gravito-inertial acceleration (GIA) and designate the phenomenon of alignment as spatial orientation of the angular vestibuloocular reflex (aVOR). On the basis of studies in the monkey, we postulated that the spatial orientation of the aVOR is dependent on the slow (velocity storage) component of the aVOR, not on the short latency, compensatory aVOR component, which is in head-fixed coordinates. Experiments in which velocity storage was abolished by midline medullary section support this postulate. The velocity storage component of the aVOR is likely to be generated in the vestibular nuclei, and its spatial orientation was shown to be controlled through the nodulus and uvula of the vestibulo-cerebellum. Separate regions of the nodulus/uvula appear to affect the horizontal and vertical/torsional components of the response differently. Velocity storage is weaker in humans than in monkeys, but responds in a similar fashion in both species. We postulate that spatial orientation of the aVOR plays an important role in aligning gaze with the GIA and in maintaining balance during angular locomotion.

Modification of compensatory saccades after aVOR gain recovery

2007 ◽  
Vol 16 (6) ◽  
pp. 285-291
Author(s):  
Michael C. Schubert ◽  
Americo A. Migliaccio ◽  
Charles C. Della Santina
Keyword(s):  
Head Rotation ◽  
Rehabilitation Program ◽  
Inverse Dynamic ◽  
Gaze Stabilization ◽  
Ocular Reflex ◽  
Dynamic Relationship ◽  
Vestibulo Ocular Reflex ◽  
Functional Relevance ◽  
Vestibular Neuronitis ◽  
Eye Velocity

The recruitment of extra-vestibular mechanisms to assist a deficient angular vestibulo-ocular reflex (aVOR) during ipsilesional head rotations is well established and includes saccades of reduced latency that occur in the direction of the lesioned aVOR, termed compensatory saccades (CS). Less well known is the functional relevance of these unique saccades. Here we report a 42 y.o. male diagnosed with right unilateral vestibular hypofunction due to vestibular neuronitis who underwent a vestibular rehabilitation program including gaze stabilization exercises. After three weeks, he had a significant improvement in his ability to see clearly during head rotation. Our data show a reduction in the recruitment and magnitude of CS as well as improved peripheral aVOR gain (eye velocity/head velocity) and retinal eye velocity. Our data suggest an inverse, dynamic relationship between the recruitment of CS and the gain of the aVOR.

Click-evoked vestibulo-ocular reflex

Neurology ◽  
2006 ◽  
Vol 66 (7) ◽  
pp. 1079-1087 ◽  
Author(s):  
S. T. Aw ◽  
M. J. Todd ◽  
G. E. Aw ◽  
J. S. Magnussen ◽  
I. S. Curthoys ◽  
...  
Keyword(s):  
Semicircular Canal ◽  
Rotation Axis ◽  
Head Orientation ◽  
Superior Canal Dehiscence ◽  
Ocular Reflex ◽  
Eye Rotation ◽  
Vestibulo Ocular Reflex ◽  
Low Threshold ◽  
Canal Dehiscence ◽  
Click Polarity

Background: An enlarged, low-threshold click-evoked vestibulo-ocular reflex (VOR) can be averaged from the vertical electro-oculogram in a superior canal dehiscence (SCD), a temporal bone defect between the superior semicircular canal and middle cranial fossa.Objective: To determine the origin and quantitative stimulus–response properties of the click-evoked VOR.Methods: Three-dimensional, binocular eye movements evoked by air-conducted 100-microsecond clicks (110 dB normal hearing level, 145 dB sound pressure level, 2 Hz) were measured with dual-search coils in 11 healthy subjects and 19 patients with SCD confirmed by CT imaging. Thresholds were established by decrementing loudness from 110 dB to 70 dB in 10-dB steps. Eye rotation axis of click-evoked VOR computed by vector analysis was referenced to known semicircular canal planes. Response characteristics were investigated with regard to enhancement using trains of three to seven clicks with 1-millisecond interclick intervals, visual fixation, head orientation, click polarity, and stimulation frequency (2 to 15 Hz).Results: In subjects and SCD patients, click-evoked VOR comprised upward, contraversive-torsional eye rotations with onset latency of approximately 9 milliseconds. Its eye rotation axis aligned with the superior canal axis, suggesting activation of superior canal receptors. In subjects, the amplitude was less than 0.01°, and the magnitude was less than 3°/second; in SCD, the amplitude was up to 60 times larger at 0.66°, and its magnitude was between 5 and 92°/second, with a threshold 10 to 40 dB below normal (110 dB). The click-evoked VOR magnitude was enhanced approximately 2.5 times with trains of five clicks but was unaffected by head orientation, visual fixation, click polarity, and stimulation frequency up to 10 Hz; it was also present on the surface electro-oculogram.Conclusion: In superior canal dehiscence, clicks evoked a high-magnitude, low-threshold, 9-millisecond-latency vestibulo-ocular reflex that aligns with the superior canal, suggesting superior canal receptor hypersensitivity to sound.

Vergence-mediated changes in the axis of eye rotation during the human vestibulo-ocular reflex can occur independent of eye position

2003 ◽  
Vol 151 (2) ◽  
pp. 238-248 ◽  
Author(s):  
Americo A. Migliaccio ◽  
Phillip D. Cremer ◽  
Swee T. Aw ◽  
G. Michael Halmagyi ◽  
Ian S. Curthoys ◽  
...  
Keyword(s):  
Eye Position ◽  
Ocular Reflex ◽  
Eye Rotation ◽  
Vestibulo Ocular Reflex

scholarly journals Simultaneous and opposing horizontal VOR adaptation in humans suggests functionally independent neural circuits

2018 ◽  
Vol 120 (4) ◽  
pp. 1496-1504 ◽  
Author(s):  
Yoav Gimmon ◽  
Americo A. Migliaccio ◽  
Christopher J. Todd ◽  
William V. C. Figtree ◽  
Michael C. Schubert
Keyword(s):  
Head Rotation ◽  
Learning Context ◽  
Training Conditions ◽  
Nonlinear Properties ◽  
Ocular Reflex ◽  
Stable Vision ◽  
Vestibulo Ocular Reflex ◽  
Vor Adaptation ◽  
Vor Training ◽  
The Right

The healthy vestibulo-ocular reflex (VOR) ensures that images remain on the fovea of the retina during head rotation to maintain stable vision. VOR behavior can be measured as a summation of linear and nonlinear properties although it is unknown whether asymmetric VOR adaptation can be performed synchronously in humans. The purpose of the present study is twofold. First, examine whether the right and left VOR gains can be synchronously adapted in opposing directions. Second, to investigate whether the adaptation context transfers between both sides. Three separate VOR adaptation sessions were randomized such that the VOR was adapted Up-bilaterally, Down-bilaterally, or Mixed (one side up, opposite side down). Ten healthy subjects completed the study. Subjects were tested while seated upright, 1 meter in front of a wall in complete dark. Each subject made active (self-generated) head impulse rotations for 15 min while viewing a gradually increasing amount of retinal slip. VOR training demand changed by 10% every 90 s. The VOR changed significantly for all training conditions. No significant differences in the magnitude of VOR gain changes between training conditions were found. The human VOR can be simultaneously driven in opposite directions. The similar magnitude of VOR gain changes across training conditions suggests functionally independent VOR circuits for each side of head rotation that mediate simultaneous and opposing VOR adaptations. NEW & NOTEWORTHY Our results indicate that humans have the adaptive capacity for concurrent and opposing directions of vestibulo-ocular reflex (VOR) motor learning. Context specificity of VOR adaptation is dependent on the error signal being unilateral or bilateral, which we illustrate via a lack of VOR gain transfer using unique adaptive demands.

scholarly journals Enhancement of the Vestibulo-Ocular Reflex by Prior Eye Movements

1999 ◽  
Vol 81 (6) ◽  
pp. 2884-2892 ◽  
Author(s):  
Vallabh E. Das ◽  
Louis F. Dell’Osso ◽  
R. John Leigh
Keyword(s):  
Eye Movements ◽  
Smooth Pursuit ◽  
Initial Perturbation ◽  
Head Rotation ◽  
Gaze Shift ◽  
Stationary Target ◽  
Ocular Reflex ◽  
Vestibulo Ocular Reflex ◽  
Head Rotations ◽  
Horizontal Head

Enhancement of the vestibulo-ocular reflex by prior eye movements. We investigated the effect of visually mediated eye movements made before velocity-step horizontal head rotations in eleven normal human subjects. When subjects viewed a stationary target before and during head rotation, gaze velocity was initially perturbed by ∼20% of head velocity; gaze velocity subsequently declined to zero within ∼300 ms of the stimulus onset. We used a curve-fitting procedure to estimate the dynamic course of the gain throughout the compensatory response to head rotation. This analysis indicated that the median initial gain of compensatory eye movements (mainly because of the vestibulo-ocular reflex, VOR) was 0.8 and subsequently increased to 1.0 after a median interval of 320 ms. When subjects attempted to fixate the remembered location of the target in darkness, the initial perturbation of gaze was similar to during fixation of a visible target (median initial VOR gain 0.8); however, the period during which the gain increased toward 1.0 was >10 times longer than that during visual fixation. When subjects performed horizontal smooth-pursuit eye movements that ended (i.e., 0 gaze velocity) just before the head rotation, the gaze velocity perturbation at the onset of head rotation was absent or small. The initial gain of the VOR had been significantly increased by the prior pursuit movements for all subjects ( P < 0.05; mean increase of 11%). In four subjects, we determined that horizontal saccades and smooth tracking of a head-fixed target (VOR cancellation with eye stationary in the orbit) also increased the initial VOR gain (by a mean of 13%) during subsequent head rotations. However, after vertical saccades or smooth pursuit, the initial gaze perturbation caused by a horizontal head rotation was similar to that which occurred after fixation of a stationary target. We conclude that the initial gain of the VOR during a sudden horizontal head rotation is increased by prior horizontal, but not vertical, visually mediated gaze shifts. We postulate that this “priming” effect of a prior gaze shift on the gain of the VOR occurs at the level of the velocity inputs to the neural integrator subserving horizontal eye movements, where gaze-shifting commands and vestibular signals converge.

scholarly journals Eye and head movements and vestibulo-ocular reflex in the context of indirect, referent control of motor actions

2020 ◽  
Vol 124 (1) ◽  
pp. 115-133 ◽  
Author(s):  
Anatol G. Feldman ◽  
Lei Zhang
Keyword(s):  
Empirical Studies ◽  
Head Rotation ◽  
Physical Principle ◽  
Task Demands ◽  
Head Movements ◽  
Ocular Reflex ◽  
Motor Outcome ◽  
Vestibulo Ocular Reflex ◽  
Motor Actions ◽  
The Brain

Conventional explanations of the vestibulo-ocular reflex (VOR) and eye and head movements are revisited by considering two alternative frameworks addressing the question of how the brain controls motor actions. Traditionally, biomechanical and/or computational frameworks reflect the views of several prominent scholars of the past, including Helmholtz and von Holst, who assumed that the brain directly specifies the desired motor outcome and uses efference copy to influence perception. However, empirical studies resulting in the theory of referent control of action and perception (an extension of the equilibrium-point hypothesis) revealed that direct specification of motor outcome is inconsistent with nonlinear properties of motoneurons and with the physical principle that the brain can control motor actions only indirectly, by changing or maintaining the values of neurophysiological parameters that influence, but can remain independent of, biomechanical variables. Some parameters are used to shift the origin (referent) points of spatial frames of reference (FRs) or system of coordinates in which motor actions emerge without being predetermined. Parameters are adjusted until the emergent motor actions meet the task demands. Several physiological parameters and spatial FRs have been identified, supporting the notion of indirect, referent control of movements. Instead of integration of velocity-dependent signals, position-dimensional referent signals underlying head motion can likely be transmitted to motoneurons of extraocular muscles. This would produce compensatory eye movement preventing shifts in gaze during head rotation, even after bilateral destruction of the labyrinths. The referent control framework symbolizes a shift in the paradigm for the understanding of VOR and eye and head movement production.

Sign in / Sign up

Export Citation Format

Share Document