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

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.

2006 ◽  
Vol 95 (4) ◽  
pp. 2530-2540 ◽  
Author(s):  
Hui Meng ◽  
Dora E. Angelaki

To stabilize objects of interest on the fovea during translation, vestibular-driven compensatory eye movements [translational vestibulo-ocular reflex (TVOR)] must scale with both target distance and eccentricity. To identify the neural correlates of these properties, we recorded from different groups of eye movement–sensitive neurons in the prepositus hypoglossi and vestibular nuclei of macaque monkeys during lateral and fore-aft displacements. All neuron types exhibited some increase in modulation amplitude as a function of target distance during high-frequency (4 Hz) lateral motion in darkness, with slopes that were correlated with the cell's pursuit gain, but not eye position sensitivity. Vergence angle dependence was largest for burst-tonic (BT) and contralateral eye-head (EH) neurons and smallest for ipsilateral EH and position-vestibular-pause (PVP) cells. On the other hand, the EH and PVP neurons with ipsilateral eye movement preferences exhibited the largest vergence-independent responses, which would be inappropriate to drive the TVOR. In addition to target distance, the TVOR also scales with target eccentricity, as evidenced during fore-aft motion, where eye velocity amplitude exhibits a “V-shaped ” dependence and phase shifts 180° for right versus left eye positions. Both the modulation amplitude and phase of BT and contralateral EH cells scaled with eye position, similar to the evoked eye movements during fore-aft motion. In contrast, the response modulation of ipsilateral EH and PVP cells during fore-aft motion was characterized by neither the V-shaped scaling nor the phase reversal. These results show that distinct premotor cell types carry neural signals that are appropriately scaled by vergence angle and eye position to generate the geometrically appropriate compensatory eye movements in the translational vestibulo-ocular reflex.


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

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.


1994 ◽  
Vol 72 (3) ◽  
pp. 1443-1447 ◽  
Author(s):  
D. E. Angelaki ◽  
B. J. Hess

1. The vestibulo-ocular reflex (VOR) was investigated in rhesus monkeys before and after surgical ablation of the cerebellar nodulus and ventral uvula. The lesion resulted in an alteration of the torsional VOR: compensatory eye movements were poor in the low frequency range and the time constant was reduced to values comparable to those of primary semicircular canal afferents. In addition, animals permanently lost their ability to generate torsional optokinetic nystagmus (OKN). 2. The effects of the lesion on the torsional VOR differed from those observed in the horizontal and vertical vestibulo-ocular systems. While the vertical VOR and OKN were unaltered, the horizontal VOR and OKN were characterized by increased time constants and smaller phase leads during low frequency head oscillations. 3. These results suggest that the cerebellar nodulus and/or ventral uvula exert a distinct and specific dynamic control on the torsional vestibulo-ocular and optokinetic reflexes. Such specific effects on the torsional system could reflect a functional segregation of the vestibulo-cerebellum in terms of the controls of torsional versus horizontal and vertical slow phase eye movements.


1991 ◽  
Vol 1 (3) ◽  
pp. 223-239
Author(s):  
G. Cheron

This study was intended to test the adaptive plasticity of the vestibulo-ocular reflex before and after either a midsagittal or parasagittal incision in the brainstem. Eye movements were measured with the electromagnetic search coil technique during the vestibulo-ocular reflex (VORD) in the dark, the optokinetic reflex (OKN), and the visuo-vestibular adaptive training procedure. Two types of visual-vestibular combined stimulation were applied by means of low frequency stimuli (0.05 to 0.10 Hz). In order to increase or decrease the VORD gain, the optokinetic drum was oscillated either 180∘ out-of-phase or in-phase with the vestibular stimulus turntable. This “training” procedure was applied for 4 hours. Initial measurements of the VORD were normal with a mean gain value of 0.92 ± 0.08. After 4 hours of “training” with the out-of-phase condition (180∘), VORD gain reached mean values of 1.33 ± 0.11 (n = 6 cats). In the in-phase combination, the mean VORD gain decreased from 1.0 to 0.63 ± 0.02 (n = 2 cats). No significant change of VORD phase was found in any of the cats. Midsagittal or parasagittal pontomedullary brainstem incisions were performed in 4 cats. Recovery of the VOR was tested on the 2nd, 7th, and 30th day after operation. After the 30th day, recovery of the VORD gain stabilized at about 66% of the initial preoperative value. At this stage of the recovery, the optokinetic response (OKN) of the midsagittal-Iesioned cats was practically normal: in the parasagittal-Jesioned cats, the postoperative OKN responses were asymmetric. After stabilization of recovery, lesioned cats were trained with the same adaptation procedure. Although the direct effect of the visuo-vestibular combined stimulation during the training was still operative in all lesioned cats, the adaptive plasticity was completely abolished by the lesions. These results suggest that the commissural brainstem network may play a crucial role in the acquisition of the forced VOR adaptation.


2000 ◽  
Vol 10 (2) ◽  
pp. 75-86 ◽  
Author(s):  
Jacob J. Bloomberg ◽  
Lauren A. Merkle ◽  
Susan R. Barry ◽  
William P. Huebner ◽  
Helen S. Cohen ◽  
...  

The goal of the present study was to determine if adaptive modulation of vestibulo-ocular reflex (VOR) function is associated with commensurate alterations in manual target localization. To measure the effects of adapted VOR on manual responses we developed the Vestibular-Contingent Pointing Test (VCP). In the VCP test, subjects pointed to a remembered target following passive whole body rotation in the dark. In the first experiment, subjects performed VCP before and after wearing 0.5X minifying lenses that adaptively attenuate horizontal VOR gain. Results showed that adaptive reduction in horizontal VOR gain was accompanied by a commensurate change in VCP performance. In the second experiment, bilaterally labyrinthine deficient (LD) subjects were tested to confirm that vestibular cues were central to the spatial coding of both eye and hand movements during VCP. LD subjects performed significantly worse than normal subjects. These results demonstrate that adaptive change in VOR can lead to alterations in manual target localization.


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.


1991 ◽  
Vol 1 (2) ◽  
pp. 161-170
Author(s):  
Jean-Louis Vercher ◽  
Gabriel M. Gauthier

To maintain clear vision, the images on the retina must remain reasonably stable. Head movements are generally dealt with successfully by counter-rotation of the eyes induced by the combined actions of the vestibulo-ocular reflex (VOR) and the optokinetic reflex. A problem of importance relates to the value of the so-called intrinsic gain of the VOR (VORG) in man, and how this gain is modulated to provide appropriate eye movements. We have studied these problems in two situations: 1. fixation of a stationary object of the visual space while the head moves; 2. fixation of an object moving with the head. These two situations were compared to a basic condition in which no visual target was allowed in order to induce “pure” VOR. Eye movements were recorded in seated subjects during stationary sinusoidal and transient rotations around the vertical axis. Subjects were in total darkness (DARK condition) and involved in mental arithmetic. Alternatively, they were provided with a small foveal target, either fixed with respect to earth (earth-fixed target: EFT condition), or moving with them (chair-fixed-target: CFT condition). The stationary rotation experiment was used as baseline for the ensuing experiment and yielded control data in agreement with the literature. In all 3 visual conditions, typical responses to transient rotations were rigorously identical during the first 200 ms. They showed, sequentially, a 16-ms delay of the eye behind the head and a rapid increase in eye velocity during 75 to 80 ms, after which the average VORG was 0.9 ± 0.15. During the following 50 to 100 ms, the gain remained around 0.9 in all three conditions. Beyond 200 ms, the VORG remained around 0.9 in DARK and increased slowly towards 1 or decreased towards zero in the EFT and CFT conditions, respectively. The time-course of the later events suggests that visual tracking mechanisms came into play to reduce retinal slip through smooth pursuit, and position error through saccades. Our data also show that in total darkness VORG is set to 0.9 in man. Lower values reported in the literature essentially reflect predictive properties of the vestibulo-ocular mechanism, particularly evident when the input signal is a sinewave.


1966 ◽  
Vol 44 (2) ◽  
pp. 263-274
Author(s):  
G. A. HORRIDGE

1. A crab in an otherwise dark room will stabilize its eye position by reference to a single small light, so long as the illumination at the eye exceeds about 0.0003 lux. 2. The eye movements follow the movements of the light. 3. Responses to a light moving in a horizontal plane resemble those to a striped drum, but at lower percentage following. 4. Apparent motion is an effective stimulus; with intermittent light the response is reduced. If there is a period of complete darkness after the first light the subsequent movement, when the second light comes on, is slower for longer dark periods. 5. The crab learns, after some repetitions, to discriminate between a continuous light and an intermittent one, as shown by its eventually stabilizing them at different points on its retina.


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