Time Course of Vestibuloocular Reflex Suppression During Gaze Shifts

2004 ◽  
Vol 92 (6) ◽  
pp. 3408-3422 ◽  
Author(s):  
Kathleen E. Cullen ◽  
Marko Huterer ◽  
Danielle A. Braidwood ◽  
Pierre A. Sylvestre
Keyword(s):  
Short Duration ◽  
Rhesus Monkeys ◽  
Time Course ◽  
Normal Values ◽  
Behavioral Strategies ◽  
Gaze Shifts ◽  
Absolute Level ◽  
Gaze Shift ◽  
The Gaze ◽  
The Status

Although numerous investigations have probed the status of the vestibuloocular (VOR) during gaze shifts, its exact status remains strangely elusive. The goal of the present study was to precisely evaluate the dynamics of VOR suppression immediately before, throughout, and just after gaze shifts. A torque motor was used to apply rapid (100°/s), short-duration (20–30 ms) horizontal head perturbations in three Rhesus monkeys. The status of the VOR elicited by this transient head perturbation was first compared during 15, 40, and 60° gaze shifts. The level of VOR suppression just after gaze-shift onset (40 ms) increased with gaze-shift amplitude in two monkeys, approaching values of 80 and 35%. In contrast, in the third monkey, the VOR was not significantly attenuated for all gaze-shift amplitudes. The time course of VOR attenuation was then studied in greater detail for all three monkeys by imposing the same short-duration head perturbations 40, 100, and 150 ms after the onset of 60° gaze shifts. Overall we found a consistent trend, in which VOR suppression was maximal early in the gaze shift and progressively recovered to reach normal values near gaze-shift end. However, the high variability across subjects prevented establishing a unifying description of the absolute level and time course of VOR suppression during gaze shifts. We propose that differences in behavioral strategies may account, at least in part, for these differences between subjects.

Combined eye-head gaze shifts in the primate. II. Interactions between saccades and the vestibuloocular reflex

1986 ◽  
Vol 56 (6) ◽  
pp. 1558-1570 ◽  
Author(s):  
R. D. Tomlinson ◽  
P. S. Bahra
Keyword(s):  
Head Movement ◽  
Rhesus Monkeys ◽  
Vertical Component ◽  
Horizontal Component ◽  
Vestibuloocular Reflex ◽  
Water Reward ◽  
Gaze Shifts ◽  
Gaze Shift ◽  
The Gaze ◽  
Eye Velocity

The mechanisms of eye-head coordination were studied in two alert juvenile rhesus monkeys. Animals were trained to follow a target light to obtain a water reward and the combined eye-head gaze shifts in response to target steps with a variably sized horizontal components were studied. During a certain random portion of the gaze shifts, a torque motor was used to perturb the head to investigate the operational state of the vestibuloocular reflex (VOR) during the saccadic gaze shift. The effects of perturbing the head were assessed during five different conditions: horizontal target steps ranging from 10 to 80 degrees in amplitude; oblique target steps where the vertical component was larger than the horizontal component; purely vertical target steps 10-40 degrees in amplitude; both horizontal and oblique target steps delivered while the animals' saccades had been slowed by the use of diazepam; and large spontaneous gaze shifts in response to both sounds and visual stimuli. Comparison of perturbed and unperturbed large-amplitude (greater than 40 degrees) gaze shifts indicate that the VOR is turned off for most of the duration of the movement. Nonetheless, there is an apparent interaction between the saccadic eye movement and the head movement, thus, as the head velocity increases, the eye velocity decreases so that gaze velocity remains nearly constant throughout the gaze shift. Since the VOR is turned off when this interaction occurs, it must represent an interaction between the actual eye and head movement motor programs themselves. Although the results were not quite as clear for small saccades (less than 20 degrees), experiments on animals whose saccades had been slowed either by the use of diazepam or by combining a small horizontal component with a large vertical component indicate that the VOR is left on during these smaller gaze shifts. During quite small gaze shifts (less than 10 degrees), the VOR is clearly functioning; however, as the size of the gaze shift is increased, this becomes less clear, and there appears to be a region where the VOR operates with a gain substantially less than normal before it enters the large gaze shift region where the VOR is turned off entirely.(ABSTRACT TRUNCATED AT 400 WORDS)

Eye-Head Coordination During Head-Unrestrained Gaze Shifts in Rhesus Monkeys

1997 ◽  
Vol 77 (5) ◽  
pp. 2328-2348 ◽  
Author(s):  
Edward G. Freedman ◽  
David L. Sparks
Keyword(s):  
Head Movement ◽  
Rhesus Monkeys ◽  
Initial Position ◽  
Head Movements ◽  
Gaze Shifts ◽  
Unit Recording ◽  
Gaze Shift ◽  
The Gaze ◽  
Two Factors ◽  
Eye Velocity

Freedman, Edward G. and David L. Sparks. Eye-head coordination during head-unrestrained gaze shifts in rhesus monkeys. J. Neurophysiol. 77: 2328–2348, 1997. We analyzed gaze shifts made by trained rhesus monkeys with completely unrestrained heads during performance of a delayed gaze shift task. Subjects made horizontal, vertical, and oblique gaze shifts to visual targets. We found that coordinated eye-head movements are characterized by a set of lawful relationships, and that the initial position of the eyes in the orbits and the direction of the gaze shift are two factors that influence these relationships. Head movements did not contribute to the change in gaze position during small gaze shifts (<20°) directed along the horizontal meridian, when the eyes were initially centered in the orbits. For larger gaze shifts (25–90°), the head contribution to the gaze shift increased linearly with increasing gaze shift amplitude, and eye movement amplitude saturated at an asymptotic amplitude of ∼35°. When the eyes began deviated in the orbits contralateral to the direction of the ensuing gaze shift, the head contributed less and the eyes more to amplitude-matched gaze shifts. The relative timing of eye and head movements was altered by initial eye position; head latency relative to gaze onset increased as the eyes began in more contralateral initial positions. The direction of the gaze shift also affected the relative amplitudes of eye and head movements; as gaze shifts were made in progressively more vertical directions, eye amplitude increased and head contribution declined systematically. Eye velocity was a saturating function of gaze amplitude for movements without a head contribution (gaze amplitude <20°). As head contribution increased with increasing gaze amplitude (20–60°), peak eye velocity declined by >200°/s and head velocity increased by 100°/s. For constant-amplitude eye movements (∼30°), eye velocity declined as the velocity of the concurrent head movement increased. On the basis of these relationships, it is possible to accurately predict gaze amplitude, the amplitudes of the eye and head components of the gaze shift, and gaze, eye, and head velocities, durations and latencies if the two-dimensional displacement of the target and the initial position of the eyes in the orbits are known. These data indicate that signals related to the initial positions of the eyes in the orbits and the direction of the gaze shift influence separate eye and head movement commands. The hypothesis that this divergence of eye and head commands occurs downstream from the superior colliculus is supported by recent electrical stimulation and single-unit recording data.

Perisaccadic Mislocalization of Visual Targets by Head-Free Gaze Shifts: Visual or Motor?

2008 ◽  
Vol 100 (4) ◽  
pp. 1848-1867 ◽  
Author(s):  
Sigrid M. C. I. van Wetter ◽  
A. John van Opstal
Keyword(s):  
Target Location ◽  
Saccadic Eye Movements ◽  
Open Loop ◽  
Spatial Updating ◽  
Gaze Shifts ◽  
Gaze Shift ◽  
The Gaze ◽  
Visual Probe ◽  
Saccade Onset ◽  
Saccade Direction

Such perisaccadic mislocalization is maximal in the direction of the saccade and varies systematically with the target-saccade onset delay. We have recently shown that under head-fixed conditions perisaccadic errors do not follow the quantitative predictions of current visuomotor models that explain these mislocalizations in terms of spatial updating. These models all assume sluggish eye-movement feedback and therefore predict that errors should vary systematically with the amplitude and kinematics of the intervening saccade. Instead, we reported that errors depend only weakly on the saccade amplitude. An alternative explanation for the data is that around the saccade the perceived target location undergoes a uniform transient shift in the saccade direction, but that the oculomotor feedback is, on average, accurate. This “ visual shift” hypothesis predicts that errors will also remain insensitive to kinematic variability within much larger head-free gaze shifts. Here we test this prediction by presenting a brief visual probe near the onset of gaze saccades between 40 and 70° amplitude. According to models with inaccurate gaze-motor feedback, the expected perisaccadic errors for such gaze shifts should be as large as 30° and depend heavily on the kinematics of the gaze shift. In contrast, we found that the actual peak errors were similar to those reported for much smaller saccadic eye movements, i.e., on average about 10°, and that neither gaze-shift amplitude nor kinematics plays a systematic role. Our data further corroborate the visual origin of perisaccadic mislocalization under open-loop conditions and strengthen the idea that efferent feedback signals in the gaze-control system are fast and accurate.

Rapid horizontal gaze movement in the monkey

1995 ◽  
Vol 73 (4) ◽  
pp. 1632-1652 ◽  
Author(s):  
J. O. Phillips ◽  
L. Ling ◽  
A. F. Fuchs ◽  
C. Siebold ◽  
J. J. Plorde
Keyword(s):  
Eye Movement ◽  
Head Movement ◽  
Vertical Axis ◽  
Head Position ◽  
Head Movements ◽  
Gaze Shifts ◽  
Gaze Shift ◽  
The Gaze ◽  
Small Correction ◽  
Horizontal Gaze

1. We studied horizontal eye and head movements in three monkeys that were trained to direct their gaze (eye position in space) toward jumping targets while their heads were both fixed and free to rotate about a vertical axis. We considered all gaze movements that traveled > or = 80% of the distance to the new visual target. 2. The relative contributions and metrics of eye and head movements to the gaze shift varied considerably from animal to animal and even within animals. Head movements could be initiated early or late and could be large or small. The eye movements of some monkeys showed a consistent decrease in velocity as the head accelerated, whereas others did not. Although all gaze shifts were hypometric, they were more hypometric in some monkeys than in others. Nevertheless, certain features of the gaze shift were identifiable in all monkeys. To identify those we analyzed gaze, eye in head position, and head position, and their velocities at three points in time during the gaze shift: 1) when the eye had completed its initial rotation toward the target, 2) when the initial gaze shift had landed, and 3) when the head movement was finished. 3. For small gaze shifts (< 20 degrees) the initial gaze movement consisted entirely of an eye movement because the head did not move. As gaze shifts became larger, the eye movement contribution saturated at approximately 30 degrees and the head movement contributed increasingly to the initial gaze movement. For the largest gaze shifts, the eye usually began counterrolling or remained stable in the orbit before gaze landed. During the interval between eye and gaze end, the head alone carried gaze to completion. Finally, when the head movement landed, it was almost aimed at the target and the eye had returned to within 10 +/- 7 degrees, mean +/- SD, of straight ahead. Between the end of the gaze shift and the end of the head movement, gaze remained stable in space or a small correction saccade occurred. 4. Gaze movements < 20 degrees landed accurately on target whether the head was fixed or free. For larger target movements, both head-free and head-fixed gaze shifts became increasingly hypometric. Head-free gaze shifts were more accurate, on average, but also more variable. This suggests that gaze is controlled in a different way with the head free. For target amplitudes < 60 degrees, head position was hypometric but the error was rather constant at approximately 10 degrees.(ABSTRACT TRUNCATED AT 400 WORDS)

Sound-Localization Performance in the Cat: The Effect of Restraining the Head

2005 ◽  
Vol 93 (3) ◽  
pp. 1223-1234 ◽  
Author(s):  
Daniel J. Tollin ◽  
Luis C. Populin ◽  
Jordan M. Moore ◽  
Janet L. Ruhland ◽  
Tom C. T. Yin
Keyword(s):  
Short Duration ◽  
Saccadic Eye Movements ◽  
Head Movements ◽  
Gaze Shifts ◽  
Localization Accuracy ◽  
Head Restraint ◽  
The Gaze ◽  
Long Duration ◽  
Localization Performance ◽  
Visual Targets

In oculomotor research, there are two common methods by which the apparent location of visual and/or auditory targets are measured, saccadic eye movements with the head restrained and gaze shifts (combined saccades and head movements) with the head unrestrained. Because cats have a small oculomotor range (approximately ±25°), head movements are necessary when orienting to targets at the extremes of or outside this range. Here we tested the hypothesis that the accuracy of localizing auditory and visual targets using more ethologically natural head-unrestrained gaze shifts would be superior to head-restrained eye saccades. The effect of stimulus duration on localization accuracy was also investigated. Three cats were trained using operant conditioning with their heads initially restrained to indicate the location of auditory and visual targets via eye position. Long-duration visual targets were localized accurately with little error, but the locations of short-duration visual and both long- and short-duration auditory targets were markedly underestimated. With the head unrestrained, localization accuracy improved substantially for all stimuli and all durations. While the improvement for long-duration stimuli with the head unrestrained might be expected given that dynamic sensory cues were available during the gaze shifts and the lack of a memory component, surprisingly, the improvement was greatest for the auditory and visual stimuli with the shortest durations, where the stimuli were extinguished prior to the onset of the eye or head movement. The underestimation of auditory targets with the head restrained is explained in terms of the unnatural sensorimotor conditions that likely result during head restraint.

scholarly journals Target modality determines eye-head coordination in nonhuman primates: implications for gaze control

2011 ◽  
Vol 106 (4) ◽  
pp. 2000-2011 ◽  
Author(s):  
Luis C. Populin ◽  
Abigail Z. Rajala
Keyword(s):  
Nonhuman Primates ◽  
Saccadic Eye Movements ◽  
Head Movements ◽  
Gaze Shifts ◽  
Gaze Shift ◽  
The Gaze ◽  
Midbrain Structure ◽  
The Subject ◽  
Visual Targets ◽  
Time Of Presentation

We have studied eye-head coordination in nonhuman primates with acoustic targets after finding that they are unable to make accurate saccadic eye movements to targets of this type with the head restrained. Three male macaque monkeys with experience in localizing sounds for rewards by pointing their gaze to the perceived location of sources served as subjects. Visual targets were used as controls. The experimental sessions were configured to minimize the chances that the subject would be able to predict the modality of the target as well as its location and time of presentation. The data show that eye and head movements are coordinated differently to generate gaze shifts to acoustic targets. Chiefly, the head invariably started to move before the eye and contributed more to the gaze shift. These differences were more striking for gaze shifts of <20–25° in amplitude, to which the head contributes very little or not at all when the target is visual. Thus acoustic and visual targets trigger gaze shifts with different eye-head coordination. This, coupled to the fact that anatomic evidence involves the superior colliculus as the link between auditory spatial processing and the motor system, suggests that separate signals are likely generated within this midbrain structure.

Brain Stem Omnipause Neurons and the Control of CombinedEye-Head Gaze Saccades in the Alert Cat

1998 ◽  
Vol 79 (6) ◽  
pp. 3060-3076 ◽  
Author(s):  
Martin Paré ◽  
Daniel Guitton
Keyword(s):  
Gaze Control ◽  
Error Signal ◽  
Gaze Shifts ◽  
Gaze Shift ◽  
The Gaze ◽  
Alert Cat ◽  
Motor Error ◽  
Omnipause Neurons ◽  
Gaze Saccades ◽  
Stimulation Of

Paré, Martin and Daniel Guitton. Brain stem omnipause neurons and the control of combined eye-head gaze saccades in the alert cat. J. Neurophysiol. 79: 3060–3076, 1998. When the head is unrestrained, rapid displacements of the visual axis—gaze shifts (eye-re-space)—are made by coordinated movements of the eyes (eye-re-head) and head (head-re-space). To address the problem of the neural control of gaze shifts, we studied and contrasted the discharges of omnipause neurons (OPNs) during a variety of combined eye-head gaze shifts and head-fixed eye saccades executed by alert cats. OPNs discharged tonically during intersaccadic intervals and at a reduced level during slow perisaccadic gaze movements sometimes accompanying saccades. Their activity ceased for the duration of the saccadic gaze shifts the animal executed, either by head-fixed eye saccades alone or by combined eye-head movements. This was true for all types of gaze shifts studied: active movements to visual targets; passive movements induced by whole-body rotation or by head rotation about stationary body; and electrically evoked movements by stimulation of the caudal part of the superior colliculus (SC), a central structure for gaze control. For combined eye-head gaze shifts, the OPN pause was therefore not correlated to the eye-in-head trajectory. For instance, in active gaze movements, the end of the pause was better correlated with the gaze end than with either the eye saccade end or the time of eye counterrotation. The hypothesis that cat OPNs participate in controlling gaze shifts is supported by these results, and also by the observation that the movements of both the eyes and the head were transiently interrupted by stimulation of OPNs during gaze shifts. However, we found that the OPN pause could be dissociated from the gaze-motor-error signal producing the gaze shift. First, OPNs resumed discharging when perturbation of head motion briefly interrupted a gaze shift before its intended amplitude was attained. Second, stimulation of caudal SC sites in head-free cat elicited large head-free gaze shifts consistent with the creation of a large gaze-motor-error signal. However, stimulation of the same sites in head-fixed cat produced small “goal-directed” eye saccades, and OPNs paused only for the duration of the latter; neither a pause nor an eye movement occurred when the same stimulation was applied with the eyes at the goal location. We conclude that OPNs can be controlled by neither a simple eye control system nor an absolute gaze control system. Our data cannot be accounted for by existing models describing the control of combined eye-head gaze shifts and therefore put new constraints on future models, which will have to incorporate all the various signals that act synergistically to control gaze shifts.

scholarly journals Dissociation of Eye and Head Components of Gaze Shifts by Stimulation of the Omnipause Neuron Region

2007 ◽  
Vol 98 (1) ◽  
pp. 360-373 ◽  
Author(s):  
Neeraj J. Gandhi ◽  
David L. Sparks
Keyword(s):  
Head Movement ◽  
Displacement Vector ◽  
Movement Control ◽  
Head Movements ◽  
Gaze Shifts ◽  
Gaze Shift ◽  
The Gaze ◽  
Movement Component ◽  
Neck Motoneurons ◽  
Stimulation Of

Natural movements often include actions integrated across multiple effectors. Coordinated eye-head movements are driven by a command to shift the line of sight by a desired displacement vector. Yet because extraocular and neck motoneurons are separate entities, the gaze shift command must be separated into independent signals for eye and head movement control. We report that this separation occurs, at least partially, at or before the level of pontine omnipause neurons (OPNs). Stimulation of the OPNs prior to and during gaze shifts temporally decoupled the eye and head components by inhibiting gaze and eye saccades. In contrast, head movements were consistently initiated before gaze onset, and ongoing head movements continued along their trajectories, albeit with some characteristic modulations. After stimulation offset, a gaze shift composed of an eye saccade, and a reaccelerated head movement was produced to preserve gaze accuracy. We conclude that signals subject to OPN inhibition produce the eye-movement component of a coordinated eye-head gaze shift and are not the only signals involved in the generation of the head component of the gaze shift.

Combined eye-head gaze shifts produced by electrical stimulation of the superior colliculus in rhesus monkeys

1996 ◽  
Vol 76 (2) ◽  
pp. 927-952 ◽  
Author(s):  
E. G. Freedman ◽  
T. R. Stanford ◽  
D. L. Sparks
Keyword(s):  
Rhesus Monkeys ◽  
Stimulation Frequency ◽  
Head Movements ◽  
Visually Guided ◽  
Maximal Amplitude ◽  
Gaze Shifts ◽  
Gaze Shift ◽  
Site Specific ◽  
Stimulation Parameters ◽  
Frequency Of Stimulation

1. We electrically stimulated the intermediate and deep layers of the superior colliculus (SC) in two rhesus macaques free to move their heads both vertically and horizontally (head unrestrained). Stimulation of the primate SC can elicit high-velocity, combined, eye-head gaze shifts that are similar to visually guided gaze shifts of comparable amplitude and direction. The amplitude of gaze shifts produced by collicular stimulation depends on the site of stimulation and on the parameters of stimulation (frequency, current, and duration of the stimulation train). 2. The maximal amplitude gaze shifts, produced by electrical stimulation at 56 sites in the SC of two rhesus monkeys, ranged in amplitude from approximately 7 to approximately 80 deg. Because the head was unrestrained, stimulation-induced gaze shifts often included movements of the head. Head movements produced at the 56 stimulation sites ranged in amplitude from 0 to approximately 70 deg. 3. The relationships between peak velocity and amplitude and between duration and amplitude of stimulation-induced head movements and gaze shifts were comparable with the relationships observed during visually guided gaze shifts. The relative contributions of the eyes and head to visually guided and stimulation-induced gaze shifts were also similar. 4. As was true for visually guided gaze shifts, the head contribution to stimulation-induced gaze shifts depended on the position of the eyes relative to the head at the onset of stimulation. When the eyes were deviated in the direction of the ensuing gaze shift, the head contribution increased and the latency to head movement onset was decreased. 5. We systematically altered the duration of stimulation trains (10-400 ms) while stimulation frequency and current remained constant. Increases in stimulation duration systematically increased the amplitude of the evoked gaze shift until a site specific maximal amplitude was reached. Further increases in stimulation duration did not increase gaze amplitude. There was a high correlation between the end of the stimulation train and the end of the evoked gaze shift for movements smaller than the site-specific maximal amplitude. 6. Unlike the effects of stimulation duration on gaze amplitude, the amplitude and duration of evoked head movements did not saturate for the range of durations tested (10-400 ms), but continued to increase linearly with increases in stimulation duration. 7. The frequency of stimulation was systematically varied (range: 63-1,000 Hz) while other stimulation parameters remained constant. The velocity of evoked gaze shifts was related to the frequency of stimulation; higher stimulation frequencies resulted in higher peak velocities. The maximal, site-specific amplitude was independent of stimulation frequency. 8. When stimulating a single collicular site using identical stimulation parameters, the amplitude and direction of stimulation-induced gaze shifts, initiated from different initial positions, were relatively constant. In contrast, the amplitude and direction of the eye component of these fixed vector gaze shifts depended upon the initial position of the eyes in the orbits; the endpoints of the eye movements converged on an orbital region, or "goal," that depended on the site of collicular stimulation. 9. When identical stimulation parameters were used and when the eyes were centered initially in the orbits, the gaze shifts produced by caudal collicular stimulation when the head was restrained were typically smaller than those evoked from the same site when the head was unrestrained. This attenuation occurred because stimulation drove the eyes to approximately the same orbital position when the head was restrained or unrestrained. Thus movements produced when the head was restrained were reduced in amplitude by approximately the amount that the head would have contributed if free to move. 10. When the head was restrained, only the eye component of the intended gaze shift

Persistence of the dark-background-contingent gaze upshift during visual fixations of rhesus monkeys

2014 ◽  
Vol 112 (8) ◽  
pp. 1999-2005 ◽  
Author(s):  
Oleg Spivak ◽  
Peter Thier ◽  
Shabtai Barash
Keyword(s):  
Rhesus Monkeys ◽  
Time Course ◽  
Target Location ◽  
Target Object ◽  
Visual Fixation ◽  
Gaze Shift ◽  
Dark Background ◽  
Visual Fixations ◽  
Fixation Interval ◽  
Correction Saccades

During visual fixations, the eyes are directed so that the image of the target (object of interest) falls on the fovea. An exception to this rule was described in macaque monkeys (though not in humans): dark background induces a gaze shift upwards, sometimes large enough to shift the target's image off the fovea. In this article we address an aspect not previously rigorously studied, the time course of the upshift. The time course is critical for determining whether the upshift is indeed an attribute of visual fixation or, alternatively, of saccades that precede the fixation. These alternatives lead to contrasting predictions regarding the time course of the upshift (durable if the upshift is an attribute of fixation, transient if caused by saccades). We studied visual fixations with dark and bright background in three monkeys. We confined ourselves to a single upshift-inducing session in each monkey so as not to study changes in the upshift caused by training. Already at their first sessions, all monkeys showed clear upshift. During the first 0.5 s after the eye reached the vicinity of the target, the upshift was on average larger, but also more variable, than later in the trial; this initial high value 1) strongly depended on target location and was maximal at locations high on the screen, and 2) appears to reflect mostly the intervals between the primary and correction saccades. Subsequently, the upshift stabilized and remained constant, well above zero, throughout the 2-s fixation interval. Thus there is a persistent background-contingent upshift genuinely of visual fixation.

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