Multiplicative Computation in the Vestibulo-Ocular Reflex (VOR)

2007 ◽  
Vol 97 (4) ◽  
pp. 2780-2789 ◽  
Author(s):  
Wu Zhou ◽  
Youguo Xu ◽  
Ivra Simpson ◽  
Yidao Cai
Keyword(s):  
Neural Mechanism ◽  
Eye Position ◽  
Neural Pathways ◽  
Basic Operation ◽  
Gain Modulation ◽  
Ocular Reflex ◽  
Sensorimotor Transformations ◽  
Fixation Distance ◽  
Vestibulo Ocular Reflex ◽  
Behaving Monkeys

Multiplicative computation is a basic operation that is crucial for neural information processing, but examples of multiplication by neural pathways that perform well-defined sensorimotor transformations are scarce. Here in behaving monkeys, we identified a multiplication of vestibular and eye position signals in the vestibulo-ocular reflex (VOR). Monkeys were trained to maintain fixation on visual targets at different horizontal locations and received brief unilateral acoustic clicks (1 ms, rarefaction, 85∼110 db NHL) that were delivered into one of their external ear canals. We found that both the click-evoked horizontal eye movement responses and the click-evoked neuronal responses of the abducens neurons exhibited linear dependencies on horizontal conjugate eye position, indicating that the interaction of vestibular and horizontal conjugate eye position was multiplicative. Latency analysis further indicated that the site of the multiplication was within the direct VOR pathways. Based on these results, we propose a novel neural mechanism that implements the VOR gain modulation by fixation distance and gaze eccentricity. In this mechanism, the vestibular signal from a single labyrinth interacts multiplicatively with the position signals of each eye (Principle of Multiplication). These effects, however, interact additively with the other labyrinth (Principle of Addition). Our analysis suggests that the new mechanism can implement the VOR gain modulation by fixation distance and gaze eccentricity within the direct VOR pathways.

Oculomotor Control of Primary Eye Position Discriminates Between Translation and Tilt

1999 ◽  
Vol 81 (1) ◽  
pp. 394-398 ◽  
Author(s):  
Bernhard J. M. Hess ◽  
Dora E. Angelaki
Keyword(s):  
Dynamic Control ◽  
Linear Acceleration ◽  
Oculomotor System ◽  
Oculomotor Control ◽  
Eye Position ◽  
Axis Orientation ◽  
Fast Phase ◽  
Ocular Reflex ◽  
Vestibulo Ocular Reflex ◽  
Head Rotations

Hess, Bernhard J. M. and Dora E. Angelaki. Oculomotor control of primary eye position discriminates between translation and tilt. J. Neurophysiol. 81: 394–398, 1999. We have previously shown that fast phase axis orientation and primary eye position in rhesus monkeys are dynamically controlled by otolith signals during head rotations that involve a reorientation of the head relative to gravity. Because of the inherent ambiguity associated with primary otolith afferent coding of linear accelerations during head translation and tilts, a similar organization might also underlie the vestibulo-ocular reflex (VOR) during translation. The ability of the oculomotor system to correctly distinguish translational accelerations from gravity in the dynamic control of primary eye position has been investigated here by comparing the eye movements elicited by sinusoidal lateral and fore-aft oscillations (0.5 Hz ± 40 cm, equivalent to ± 0.4 g) with those during yaw rotations (180°/s) about a vertically tilted axis (23.6°). We found a significant modulation of primary eye position as a function of linear acceleration (gravity) during rotation but not during lateral and fore-aft translation. This modulation was enhanced during the initial phase of rotation when there was concomitant semicircular canal input. These findings suggest that control of primary eye position and fast phase axis orientation in the VOR are based on central vestibular mechanisms that discriminate between gravity and translational head acceleration.

Recruitment Order of Cat Abducens Motoneurons and Internuclear Neurons

2003 ◽  
Vol 90 (4) ◽  
pp. 2240-2252 ◽  
Author(s):  
Ángel M. Pastor ◽  
David González-Forero
Keyword(s):  
Rectus Muscle ◽  
Neuronal Firing ◽  
Eye Position ◽  
High Dose ◽  
Recruitment Threshold ◽  
Ocular Reflex ◽  
Lateral Rectus Muscle ◽  
Vestibulo Ocular Reflex ◽  
Recruitment Order ◽  
Eye Velocity

Abducens neurons undergo a dose-dependent synaptic blockade (either disinhibition or complete blockade) when tetanus neurotoxin (TeNT) is injected into the lateral rectus muscle at either a low (0.5) or a high dose (5 ng/kg). We studied the firing pattern and recruitment order in abducens neurons both in control and after TeNT injection. The eye position threshold for recruitment of control abducens neurons was exponentially related to the eye position and velocity sensitivities. We also found a constancy of recruitment threshold for different eye movement modalities (spontaneous, optokinetic, and vestibular). Exponential relationships were found, as well, for eye velocity sensitivity during saccades and for position and velocity sensitivities during the vestibulo-ocular reflex. Likewise, inverse relationships were found between recruitment threshold or position sensitivity with the antidromic latency in control abducens neurons. These relationships, however, did not apply following TeNT treatment. Neuronal firing after TeNT appeared either disinhibited (low dose) or depressed (high dose), but the relationships between neuronal sensitivities and recruitment still applied. However, the pattern of recruitment shifted toward the treated side as more inputs were blocked by the low- and high-dose treatments, respectively. Nonetheless, although the recruitment-to-sensitivity relationships persisted under the TeNT synaptic blockade, we conclude that synaptic inputs are determinant for establishing the recruitment threshold and recruitment spacing of abducens motoneurons and internuclear neurons.

scholarly journals Magnetic Resonance Imaging of Human Extraocular Muscles During Static Ocular Counter-Rolling

2005 ◽  
Vol 94 (5) ◽  
pp. 3292-3302 ◽  
Author(s):  
Joseph L. Demer ◽  
Robert A. Clark
Keyword(s):  
Cross Section ◽  
Cross Sections ◽  
Three Dimensions ◽  
Eye Position ◽  
Ocular Torsion ◽  
Resonance Imaging ◽  
Central Target ◽  
Ocular Reflex ◽  
Adult Humans ◽  
Vestibulo Ocular Reflex

The rectus extraocular muscle (EOM) pulleys constrain EOM paths. During visual fixation with head immobile, actively controlled pulleys are known to maintain positions causing EOM pulling directions to change by one-half the change in eye position. This pulley behavior is consistent with Listing's law (LL) of ocular torsion as observed during fixation, saccades, and pursuit. However, pulley behavior during the vestibulo-ocular reflex (VOR) has been unstudied. This experiment studied ocular counter-rolling (OCR), a static torsional VOR that violates LL but can be evoked during MRI. Tri-planar MRI was performed in 10 adult humans during central target fixation while positioned in right and left side down positions known to evoke static OCR. EOM cross-sections and paths were determined from area centroids. Paths were used to locate pulleys in three dimensions. Significant ( P < 0.025) counter-rotational repositioning of the rectus pulley arrays of both orbits was observed in the coronal plane averaging 4.1° (maximum, 8.7°) from right to left side down positions for the inferior, medial, and superior rectus pulleys. There was a trend for the lateral rectus averaging 1.4°. Torsional shift of the rectus pulley array was associated with significant contractile cross-section changes in the superior and inferior oblique muscles. Torsional rectus pulley shift during OCR, which changes pulling directions of the rectus EOMs, correlates with known insertions of the oblique EOM orbital layers on rectus pulleys. The amount of pulley reconfiguration is roughly one-half of published values of ocular torsion during static OCR, an arrangement that would cause rectus pulling directions to change by less than one-half the amount of ocular torsion.

scholarly journals Kinematic Principles of Primate Rotational Vestibulo-Ocular Reflex II. Gravity-Dependent Modulation of Primary Eye Position

1997 ◽  
Vol 78 (4) ◽  
pp. 2203-2216 ◽  
Author(s):  
Bernhard J. M. Hess ◽  
Dora E. Angelaki
Keyword(s):  
Slow Phase ◽  
Head Orientation ◽  
Eye Position ◽  
Single Plane ◽  
Fast Phase ◽  
Ocular Reflex ◽  
Listing's Plane ◽  
Vestibulo Ocular Reflex ◽  
Torsional Component ◽  
Listing’S Plane

Hess, Bernhard J. M. and Dora E. Angelaki. Kinematic principles of primate rotational vestibulo-ocular reflex. II. Gravity-dependent modulation of primary eye position. J. Neurophysiol. 78: 2203–2216, 1997. The kinematic constraints of three-dimensional eye positions were investigated in rhesus monkeys during passive head and body rotations relative to gravity. We studied fast and slow phase components of the vestibulo-ocular reflex (VOR) elicited by constant-velocity yaw rotations and sinusoidal oscillations about an earth-horizontal axis. We found that the spatial orientation of both fast and slow phase eye positions could be described locally by a planar surface with torsional variation of <2.0 ± 0.4° (displacement planes) that systematically rotated and/or shifted relative to Listing's plane. In supine/prone positions, displacement planes pitched forward/backward; in left/right ear-down positions, displacement planes were parallel shifted along the positive/negative torsional axis. Dynamically changing primary eye positions were computed from displacement planes. Torsional and vertical components of primary eye position modulated as a sinusoidal function of head orientation in space. The torsional component was maximal in ear-down positions and approximately zero in supine/prone orientations. The opposite was observed for the vertical component. Modulation of the horizontal component of primary eye position exhibited a more complex dependence. In contrast to the torsional component, which was relatively independent of rotational speed, modulation of the vertical and horizontal components of primary position depended strongly on the speed of head rotation (i.e., on the frequency of oscillation of the gravity vector component): the faster the head rotated relative to gravity, the larger was the modulation. Corresponding results were obtained when a model based on a sinusoidal dependence of instantaneous displacement planes (and primary eye position) on head orientation relative to gravity was fitted to VOR fast phase positions. When VOR fast phase positions were expressed relative to primary eye position estimated from the model fits, they were confined approximately to a single plane with a small torsional standard deviation (∼1.4–2.6°). This reduced torsional variation was in contrast to the large torsional spread (well >10–15°) of fast phase positions when expressed relative to Listing's plane. We conclude that primary eye position depends dynamically on head orientation relative to space rather than being fixed to the head. It defines a gravity-dependent coordinate system relative to which the torsional variability of eye positions is minimized even when the head is moved passively and vestibulo-ocular reflexes are evoked. In this general sense, Listing's law is preserved with respect to an otolith-controlled reference system that is defined dynamically by gravity.

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

Static Ocular Counterroll Is Implemented Through the 3-D Neural Integrator

2003 ◽  
Vol 90 (4) ◽  
pp. 2777-2784 ◽  
Author(s):  
J. Douglas Crawford ◽  
Douglas B. Tweed ◽  
Tutis Vilis
Keyword(s):  
Equilibrium Position ◽  
Neural Mechanism ◽  
Neural Integrator ◽  
Interstitial Nucleus Of Cajal ◽  
Ocular Reflex ◽  
Ocular Counterroll ◽  
Vestibulo Ocular Reflex ◽  
Input Model ◽  
Head Roll ◽  
Static Head

Static head roll about the naso-occipital axis is known to produce an opposite ocular counterroll with a gain of approximately 10%, but the purpose and neural mechanism of this response remain obscure. In theory counterroll could be maintained either by direct tonic vestibular inputs to motoneurons, or by a neurally integrated pulse, as observed in the saccade generator and vestibulo-ocular reflex. When simulated together with ocular drift related to torsional integrator failure, the direct tonic input model predicted that the pattern of drift would shift torsionally as in ordinary counterroll, but the integrated pulse model predicted that the equilibrium position of torsional drift would be unaffected by head roll. This was tested experimentally by measuring ocular counterroll in 2 monkeys after injection of muscimol into the mesencephalic interstitial nucleus of Cajal. Whereas 90° head roll produced a mean ocular counterroll of 8.5° (±0.7° SE) in control experiments, the torsional equilibrium position observed during integrator failure failed to counterroll, showing a torsional shift of only 0.3° (±0.6° SE). This result contradicted the direct tonic input model, but was consistent with models that implement counterroll by a neurally integrated pulse.

Dynamics of Adaptive Change in Human Vestibulo-Ocular Reflex Direction

1990 ◽  
Vol 1 (1) ◽  
pp. 23-29
Author(s):  
T.T. Khater ◽  
J.F. Baker ◽  
B.W. Peterson
Keyword(s):  
Eye Movements ◽  
Vertical Component ◽  
Onset Time ◽  
Eye Position ◽  
Complete Darkness ◽  
Ocular Reflex ◽  
Before And After ◽  
Adaptation Procedure ◽  
Vestibulo Ocular Reflex ◽  
Horizontal Rotations

Adaptive modification of vestibulo-ocular reflex (VOR) direction was characterized in humans by recording vertical and horizontal VOR eye movements during horizontal rotations in darkness at frequencies of 0.05 to 1 Hz before and after exposure to a VOR direction adaptation procedure. This procedure paired yaw horizontal vestibular rotation at 0.25 Hz with synchronous pitch vertical optokinetic motion. Saccades were removed from eye position records and VOR gain and phase were recorded. With an onset time constant of 36 min, the VOR measured during horizontal rotation in complete darkness acquired a vertical component in phase with the optokinetic stimulus presented during adaptation. The amplitude of this newly acquired vertical VOR component was maximal during rotation at the frequency of adaptation; at other frequencies, the amplitude was lower, but still significant. Unlike VOR direction adaptation in cats, the phase of the adaptive VOR component in humans did not show significant leads or lags at test frequencies below or above the adaptation frequency. These data suggest that, like the cat, the human VOR can be directionally adapted, and the pathways involving the adaptive component of the VOR are frequency specific.

A review of the effects of space flight on the asymmetry of vertical optokinetic and vestibulo-ocular reflexes

2003 ◽  
Vol 13 (4-6) ◽  
pp. 255-263
Author(s):  
Gilles Clément
Keyword(s):  
Phase Velocity ◽  
Optokinetic Nystagmus ◽  
Visual Stimulation ◽  
Head Movements ◽  
Slow Phase ◽  
Eye Position ◽  
Slow Phase Velocity ◽  
Ocular Reflex ◽  
Vestibulo Ocular Reflex ◽  
Eye Velocity

Prolonged microgravity during orbital flight is a unique way to modify the otolith inputs and to determine the extent of their contribution to the vertical vestibulo-ocular reflex (VOR) and optokinetic nystagmus (OKN). This paper reviews the data collected on 10 astronauts during several space missions and focuses on the changes in the up-down asymmetry. Both the OKN elicited by vertical visual stimulation and the active VOR elicited by voluntary pitch head movements showed an asymmetry before flight, with upward slow phase velocity higher than downward slow phase velocity. Early in-flight, this asymmetry was inverted, and a symmetry of both responses was later observed. An upward shift in the vertical mean eye position in both OKN and VOR suggests that these effects may be related to otolith-dependent changes in eye position which, in themselves, affect slow phase eye velocity.

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