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.

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.

scholarly journals Functional diversity of motoneurons in the oculomotor system

2019 ◽  
Vol 116 (9) ◽  
pp. 3837-3846 ◽  
Author(s):  
Rosendo G. Hernández ◽  
Paula M. Calvo ◽  
Roland Blumer ◽  
Rosa R. de la Cruz ◽  
Angel M. Pastor
Keyword(s):  
Eye Movements ◽  
Muscle Tension ◽  
Muscle Fibers ◽  
Oculomotor System ◽  
Eye Position ◽  
Abducens Nucleus ◽  
Ocular Reflex ◽  
Morphological Studies ◽  
Vestibulo Ocular Reflex ◽  
Slow Eye Movements

Extraocular muscles contain two types of muscle fibers according to their innervation pattern: singly innervated muscle fibers (SIFs), similar to most skeletal muscle fibers, and multiply innervated muscle fibers (MIFs). Morphological studies have revealed that SIF and MIF motoneurons are segregated anatomically and receive different proportions of certain afferents, suggesting that while SIF motoneurons would participate in the whole repertoire of eye movements, MIF motoneurons would contribute only to slow eye movements and fixations. We have tested that proposal by performing single-unit recordings, in alert behaving cats, of electrophysiologically identified MIF and SIF motoneurons in the abducens nucleus. Our results show that both types of motoneuron discharge in relation to eye position and velocity, displaying a tonic–phasic firing pattern for different types of eye movement (saccades, vestibulo-ocular reflex, vergence) and gaze-holding. However, MIF motoneurons presented an overall reduced firing rate compared with SIF motoneurons, and had significantly lower recruitment threshold and also lower eye position and velocity sensitivities. Accordingly, MIF motoneurons could control mainly gaze in the off-direction, when less force is needed, whereas SIF motoneurons would contribute to increase muscle tension progressively toward the on-direction as more force is required. Anatomically, MIF and SIF motoneurons distributed intermingled within the abducens nucleus, with MIF motoneurons being smaller and having a lesser somatic synaptic coverage. Our data demonstrate the functional participation of both MIF and SIF motoneurons in fixations and slow and phasic eye movements, although their discharge properties indicate a functional segregation.

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.

scholarly journals New advances regarding adaptation of the vestibulo-ocular reflex

2019 ◽  
Vol 122 (2) ◽  
pp. 644-658 ◽  
Author(s):  
Michael C. Schubert ◽  
Americo A. Migliaccio
Keyword(s):  
Training Session ◽  
Whole Body ◽  
Velocity Error ◽  
Ocular Reflex ◽  
Vestibulo Ocular Reflex ◽  
Vor Adaptation ◽  
Effects Of Aging ◽  
Repeated Training ◽  
Head Rotations ◽  
Efferent Vestibular System

This is a review summarizing the development of vestibulo-ocular reflex (VOR) adaptation behavior with relevance to rehabilitation over the last 10 years and examines VOR adaptation using head-on-body rotations, specifically the influence of training target contrast, position and velocity error signal, active vs. passive head rotations, and sinusoidal vs. head impulse rotations. This review discusses optimization of the single VOR adaptation training session, consolidation between repeated training sessions, and dynamic incremental VOR adaptation. Also considered are the effects of aging and the roles of the efferent vestibular system, cerebellum, and otoliths on angular VOR adaptation. Finally, this review examines VOR adaptation findings in studies using whole body rotations.

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.

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 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.

Recovery of vestibulo-ocular reflex-function in subjects with an acute unilateral peripheral vestibular deficit

1999 ◽  
Vol 9 (2) ◽  
pp. 135-144 ◽  
Author(s):  
J.H.J. Allum ◽  
T. Ledin
Keyword(s):  
Low Frequency ◽  
Vestibular Function ◽  
Vertical Axis ◽  
Whole Body ◽  
Horizontal Semicircular Canal ◽  
Ocular Reflex ◽  
Vestibulo Ocular Reflex ◽  
Central Compensation ◽  
Head Rotations ◽  
Vestibular Deficit

The centrally controlled compensation for a reduced horizontal vestibulo-ocular reflex (VOR) gain caused by a unilateral afferent deficit is usually studied following a selective surgical procedure which completely lesions the vestibular nerve or blocks the horizontal semicircular canal. The more common, unilateral, vestibular deficit encountered clinically, is a partial loss of peripheral vestibular function, following which peripheral recovery and/or central compensation may occur. We investigated changes of the VOR gain in response to a sudden, idiopathic, unilateral vestibular deficit in 64 subjects by examining the responses to low-frequency, whole-body, rotations about an earth vertical axis with different accelerations (5, 20 and 40 deg / sec 2 ) during in- and out-patient visits separated by 4 months in an attempt to identify changes brought about by peripheral recovery and by central compensation processes. Peripheral function was assumed to be measured by the response to caloric irrigation. It improved some 30% between the two visits. VOR responses for rotations towards the deficit side also improved between the two visits. Most improvement occurred for 20 deg / sec 2 accelerations. However, the correlation coefficient between rotation and caloric responses was always less than 0.6. Unlike caloric responses which improved over time, responses for rotations to the intact side did not change between the visits. For this reason, the majority of observed VOR rotation responses were nearly symmetrical at the time of the second visit, despite being below normal levels. These findings suggest that both peripheral recovery and central compensation processes help restore symmetrical VOR function for head rotations after a partial unilateral vestibular deficit. However the improvement of VOR response symmetry, particularly to slow ( < 40 deg / sec 2 ) accelerations, is largely independent of the recovery of peripheral sensitivity.

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