Scaling of the Fore-Aft Vestibulo-Ocular Reflex by Eye Position During Smooth Pursuit

2006 ◽  
Vol 96 (2) ◽  
pp. 936-940 ◽  
Author(s):  
Jennifer A. Semrau ◽  
Min Wei ◽  
Dora Angelaki

An eye position signal scales the amplitude of compensatory eye velocity in the translational vestibulo-ocular reflex (TVOR). To investigate the origin of such a modulatory signal, we studied the kinematics of the fore-aft TVOR as rhesus monkeys pursued a horizontally moving target at velocities between 0.5 and 30°/s. We found that the “V-shaped” curve of the fore-aft TVOR amplitude as a function of eye position was shifted opposite to the direction of pursuit eye movement. As a result, the tip of the V-shaped curve that occurred close to zero eye position during steady-state fixation was shifted to the right during leftward pursuit and to the left during rightward pursuit eye movements. The faster the pursuit velocity the larger the observed shift. These results suggest that the scaling of the TVOR can precede actual eye position changes by several tens of milliseconds, which averaged 169 ± 87 ms in three rhesus monkeys. Thus, central motor commands, rather than low-level efference copy or proprioceptive information, may be the signals scaling TVOR amplitude.

2003 ◽  
Vol 90 (4) ◽  
pp. 2240-2252 ◽  
Author(s):  
Ángel M. Pastor ◽  
David González-Forero

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.


2003 ◽  
Vol 13 (4-6) ◽  
pp. 255-263
Author(s):  
Gilles Clément

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.


1999 ◽  
Vol 81 (1) ◽  
pp. 394-398 ◽  
Author(s):  
Bernhard J. M. Hess ◽  
Dora E. Angelaki

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.


2007 ◽  
Vol 16 (6) ◽  
pp. 285-291
Author(s):  
Michael C. Schubert ◽  
Americo A. Migliaccio ◽  
Charles C. Della Santina

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.


2019 ◽  
Vol 122 (5) ◽  
pp. 1909-1917
Author(s):  
Svenja Gremmler ◽  
Markus Lappe

We investigated whether the proprioceptive eye position signal after the execution of a saccadic eye movement is used to estimate the accuracy of the movement. If so, saccadic adaptation, the mechanism that maintains saccade accuracy, could use this signal in a similar way as it uses visual feedback after the saccade. To manipulate the availability of the proprioceptive eye position signal we utilized the finding that proprioceptive eye position information builds up gradually after a saccade over a time interval comparable to typical saccade latencies. We confined the retention time of gaze at the saccade landing point by asking participants to make fast return saccades to the fixation point that preempt the usability of proprioceptive eye position signals. In five experimental conditions we measured the influence of the visual and proprioceptive feedback, together and separately, on the development of adaptation. We found that the adaptation of the previously shortened saccades in the case of visual feedback being unavailable after the saccade was significantly weaker when the use of proprioceptive eye position information was impaired by fast return saccades. We conclude that adaptation can be driven by proprioceptive eye position feedback. NEW & NOTEWORTHY We show that proprioceptive eye position information is used after a saccade to estimate motor error and adapt saccade control. Previous studies on saccadic adaptation focused on visual feedback about saccade accuracy. A multimodal error signal combining visual and proprioceptive information is likely more robust. Moreover, combining proprioceptive and visual measures of saccade performance can be helpful to keep vision, proprioception, and motor control in alignment and produce a coherent representation of space.


2005 ◽  
Vol 94 (5) ◽  
pp. 3292-3302 ◽  
Author(s):  
Joseph L. Demer ◽  
Robert A. Clark

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.


1997 ◽  
Vol 78 (4) ◽  
pp. 2203-2216 ◽  
Author(s):  
Bernhard J. M. Hess ◽  
Dora E. Angelaki

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.


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

1992 ◽  
Vol 68 (1) ◽  
pp. 244-264 ◽  
Author(s):  
C. A. Scudder ◽  
A. F. Fuchs

1. To describe in detail the secondary neurons of the horizontal vestibuloocular reflex (VOR), we recorded the extracellular activity of neurons in the rostral medial vestibular nucleus of alert, trained rhesus monkeys. On the basis of their activity during horizontal head and eye movements, neurons were divided into several different types. Position-vestibular-pause (PVP) units discharged in relation to head velocity, eye velocity, eye position, and ceased firing during some saccades. Eye and head velocity (EHV) units discharged in relation to eye velocity and head velocity in the same direction so that the two signals partially canceled during the VOR. Two cell types discharged in relation to eye position and velocity but not head velocity; other types discharged in relation to head velocity only. 2. The position in the neural path from the primary vestibular afferents to abducens motoneurons was examined for each type. Direct input from the vestibular nerve was indicated if the cell could be activated by shocks to the nerve at latencies less than or equal to 1.4 ms. A projection to abducens motoneurons was indicated if spike-triggered averaging of lateral rectus electromyographic (EMG) activity yielded responses with a sharp onset at monosynaptic latencies. 3. PVP neurons were the principal interneuron in the VOR “three-neuron arc.” Eighty percent received primary afferent input, and 66% made excitatory connections with contralateral abducens motoneurons. Surprisingly few, approximately 11%, made inhibitory connections with ipsilateral abducens motoneurons. This imbalance in the ipsi- and contralateral projections was confirmed by measuring the EMG activity evoked by electrical microstimulation in regions where PVP neurons were located. 4. EHV neurons whose activity increased during contralaterally directed head or eye movements were also interneurons in the ipsilateral inhibitory pathway. Eighty-nine percent received ipsilateral primary afferent input, and 25% projected to ipsilateral abducens motoneurons. EHV neurons excited during ipsilateral movements received neither direct primary afferent input nor projected to either abducens nucleus. A small proportion of each of two other cell types having sensitivity to contralateral eye position made excitatory connections with contralateral abducens motoneurons. Other types rarely were activated from the eighth nerve or projected to the abducens nucleus. 5. The significance of the connections of VOR interneurons and the signals they convey is discussed for three situations: smooth pursuit of a moving target, suppression of the VOR, and the VOR itself. PVP neurons convey a signal with a ratio of eye position and velocity components that is inappropriate to drive motoneurons during pursuit or the VOR.(ABSTRACT TRUNCATED AT 400 WORDS)


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