Eye Movements and Visual-Vestibular Interactions during Linear Head Motion

1992 ◽  
pp. 479-482
Author(s):  
Gary D. Paige ◽  
David L. Tomko
Keyword(s):  
Eye Movements ◽  
Head Motion

Vestibuloocular Reflex Dynamics During High-Frequency and High-Acceleration Rotations of the Head on Body in Rhesus Monkey

2002 ◽  
Vol 88 (1) ◽  
pp. 13-28 ◽  
Author(s):  
Marko Huterer ◽  
Kathleen E. Cullen
Keyword(s):  
Eye Movements ◽  
High Frequency ◽  
The Body ◽  
Whole Body ◽  
Head Motion ◽  
Similar Response ◽  
Vestibuloocular Reflex ◽  
Frequency Range ◽  
Response Dynamics ◽  
Passive Rotation

For frequencies >10 Hz, the vestibuloocular reflex (VOR) has been primarily investigated during passive rotations of the head on the body in humans. These prior studies suggest that eye movements lag head movements, as predicted by a 7-ms delay in the VOR reflex pathways. However, Minor and colleagues recently applied whole-body rotations of frequencies ≤15 Hz in monkeys and found that eye movements were nearly in phase with head motion across all frequencies. The goal of the present study was to determine whether VOR response dynamics actually differ significantly for whole-body versus head-on-body rotations. To address this question, we evaluated the gain and phase of the VOR induced by high-frequency oscillations of the head on the body in monkeys by directly measuring both head and eye movements using the magnetic search coil technique. A torque motor was used to rotate the heads of three Rhesus monkeys over the frequency range 5–25 Hz. Peak head velocity was held constant, first at ±50°/s and then ±100°/s. The VOR was found to be essentially compensatory across all frequencies; gains were near unity (1.1 at 5 Hz vs. 1.2 at 25 Hz), and phase lag increased only slightly with frequency (from 2° at 5 Hz to 11° at 25 Hz, a marked contrast to the 63° lag at 25 Hz predicted by a 7-ms VOR latency). Furthermore, VOR response dynamics were comparable in darkness and when viewing a target and did not vary with peak velocity. Although monkeys offered less resistance to the initial cycles of applied head motion, the gain and phase of the VOR did not vary for early versus late cycles, suggesting that an efference copy of the motor command to the neck musculature did not alter VOR response dynamics. In addition, VOR dynamics were also probed by applying transient head perturbations with much greater accelerations (peak acceleration >15,000°/s2) than have been previously employed. The VOR latency was between 5 and 6 ms, and mean gain was close to unity for two of the three animals tested. A simple linear model well described the VOR responses elicited by sinusoidal and transient head on body rotations. We conclude that the VOR is compensatory over a wide frequency range in monkeys and has similar response dynamics during passive rotation of the head on body as during passive rotation of the whole body in space.

scholarly journals Two distinct types of eye-head coupling in freely moving mice

2020 ◽  
Author(s):  
Arne F. Meyer ◽  
John O’Keefe ◽  
Jasper Poort
Keyword(s):  
Eye Movements ◽  
Ground Plane ◽  
Sensory Information ◽  
Head Tilt ◽  
Head Rotation ◽  
Head Movements ◽  
Head Motion ◽  
List Type ◽  
Visually Guided ◽  
Freely Moving

SummaryAnimals actively interact with their environment to gather sensory information. There is conflicting evidence about how mice use vision to sample their environment. During head restraint, mice make rapid eye movements strongly coupled between the eyes, similar to conjugate saccadic eye movements in humans. However, when mice are free to move their heads, eye movement patterns are more complex and often non-conjugate, with the eyes moving in opposite directions. Here, we combined eye tracking with head motion measurements in freely moving mice and found that both observations can be explained by the existence of two distinct types of coupling between eye and head movements. The first type comprised non-conjugate eye movements which systematically compensated for changes in head tilt to maintain approximately the same visual field relative to the horizontal ground plane. The second type of eye movements were conjugate and coupled to head yaw rotation to produce a “saccade and fixate” gaze pattern. During head initiated saccades, the eyes moved together in the same direction as the head, but during subsequent fixation moved in the opposite direction to the head to compensate for head rotation. This “saccade and fixate” pattern is similar to that seen in humans who use eye movements (with or without head movement) to rapidly shift gaze but in mice relies on combined eye and head movements. Indeed, the two types of eye movements very rarely occurred in the absence of head movements. Even in head-restrained mice, eye movements were invariably associated with attempted head motion. Both types of eye-head coupling were seen in freely moving mice during social interactions and a visually-guided object tracking task. Our results reveal that mice use a combination of head and eye movements to sample their environment and highlight the similarities and differences between eye movements in mice and humans.HighlightsTracking of eyes and head in freely moving mice reveals two types of eye-head couplingEye/head tilt coupling aligns gaze to horizontal planeRotational eye and head coupling produces a “saccade and fixate” gaze pattern with head leading the eyeBoth types of eye-head coupling are maintained during visually-guided behaviorsEye movements in head-restrained mice are related to attempted head movements

Neural basis for motor learning in the vestibuloocular reflex of primates. I. Changes in the responses of brain stem neurons

1994 ◽  
Vol 72 (2) ◽  
pp. 928-953 ◽  
Author(s):  
S. G. Lisberger ◽  
T. A. Pavelko ◽  
D. M. Broussard
Keyword(s):  
Eye Movements ◽  
Motor Learning ◽  
Firing Rate ◽  
Brain Stem ◽  
Head Rotation ◽  
Head Motion ◽  
Vestibuloocular Reflex ◽  
Neural Basis ◽  
Ventral Paraflocculus ◽  
The Brain

1. We recorded from neurons in the brain stem of monkeys before and after they had worn magnifying or miniaturizing spectacles to cause changes in the gain of the vestibuloocular reflex (VOR). The gain of the VOR was estimated as eye speed divided by head speed during passive horizontal head rotation in darkness. Electrical stimulation in the cerebellum was used to identify neurons that receive inhibition at monosynaptic latencies from the flocculus and ventral paraflocculus (flocculus target neurons or FTNs). Cells were studied during smooth pursuit eye movements with the head stationary, fixation of different positions, cancellation of the VOR, and the VOR evoked by rapid changes in head velocity. 2. FTNs were divided into two populations according to their responses during pursuit with the head stationary. The two groups showed increased firing during smooth eye motion toward the side of recording (Eye-ipsiversive or E-i) or away from the side of recording (Eye-contraversive or E-c). A higher percentage of FTNs showed increased firing rate for contraversive pursuit when the gain of the VOR was high (> or = 1.6) than when the gain of the VOR was low (< or = 0.4). 3. Changes in the gain of the VOR had a striking effect on the responses during the VOR for the FTNs that were E-c during pursuit with the head stationary. Firing rate increased during contraversive VOR eye movements when the gain of the VOR was high or normal and decreased during contraversive VOR eye movements when the gain of the VOR was low. Changes in the gain of the VOR caused smaller changes in the responses during the VOR of FTNs that were E-i during pursuit with the head stationary. We argue that motor learning in the VOR is the result of changes in the responses of individual FTNs. 4. The responses of E-i and E-c FTNS during cancellation of the VOR depended on the gain of the VOR. Responses tended to be in phase with contraversive head motion when the gain of the VOR was low and in phase with ipsiversive head motion when the gain of the VOR was high. Comparison of the effect of motor learning on the responses of FTNs during cancellation of the VOR with the results of similar experiments on horizontal-gaze velocity Purkinje cells in the flocculus and ventral paraflocculus suggests that the brain stem vestibular inputs to FTNs are one site of motor learning in the VOR.(ABSTRACT TRUNCATED AT 400 WORDS)

Anticipatory VOR Suppression Induced by Visual and Nonvisual Stimuli in Humans

2004 ◽  
Vol 92 (3) ◽  
pp. 1501-1511 ◽  
Author(s):  
G. R. Barnes ◽  
G. D. Paige
Keyword(s):  
Eye Movements ◽  
Eye Movement ◽  
Visual Target ◽  
Head Motion ◽  
Vestibuloocular Reflex ◽  
Fixed Target ◽  
Target Movement ◽  
Anticipatory Eye Movements ◽  
Predictive Behavior ◽  
Anticipatory Smooth Eye Movements

We compared the predictive behavior of smooth pursuit (SP) and suppression of the vestibuloocular reflex (VOR) in humans by examining anticipatory smooth eye movements, a phenomenon that arises after repeated presentations of sudden target movement preceded by an auditory warning cue. We investigated whether anticipatory smooth eye movements also occur prior to cued head motion, particularly when subjects expect interaction between the VOR and either real or imagined head-fixed targets. Subjects were presented with horizontal motion stimuli consisting of a visual target alone (SP), head motion in darkness (VOR), or head motion in the presence of a real or imagined head-fixed target (HFT and IHFT, respectively). Stimulus sequences were delivered as single cycles of a velocity sinusoid (frequency: 0.5 or 1.0 Hz) that were either cued (a sound cue 400 ms earlier) or noncued. For SP, anticipatory smooth eye movements developed over repeated trials in the cued, but not the noncued, condition. In the VOR condition, no such anticipatory eye movements were observed even when cued. In contrast, anticipatory responses were observed under cued, but not noncued, HFT and IHFT conditions, as for SP. Anticipatory HFT responses increased in proportion to the velocity of preceding stimuli. In general, anticipatory gaze responses were similar in cued SP, HFT, and IHFT conditions and were appropriate for expected target motion in space. Anticipatory responses may represent the output of a central mechanism for smooth-eye-movement generation that operates during predictive SP as well as VOR modulations that are linked with SP even in the absence of real visual targets.

Gaze strategies during linear motion in head-free humans

1994 ◽  
Vol 72 (5) ◽  
pp. 2451-2466 ◽  
Author(s):  
L. Borel ◽  
B. Le Goff ◽  
O. Charade ◽  
A. Berthoz
Keyword(s):  
Eye Movements ◽  
Human Subjects ◽  
Linear Acceleration ◽  
Slow Phase ◽  
Head Motion ◽  
Functional Coupling ◽  
Linear Motion ◽  
Experimental Conditions ◽  
Coordination Strategies ◽  
Phase Direction

1. Eye-head coordination strategies during horizontal displacements along the y (interaural) axis were investigated in human subjects seated on a sled (linear accelerator device) and tested in head-free conditions. They were instructed to stabilize their gaze, while in motion, on an earth-fixed memorized target and then, after cart immobilization, to look again at the real target. The last part of the test required a corrective saccade, which enabled us to evaluate the error of the subject's displacement estimation. Eye and head compensatory reflexes were tested within the 0.001–0.2 g acceleration range with a sinusoidal motion amplitude of 0.8 m peak to peak. 2. Fixation stabilization on a memorized target was achieved by different eye-head coordination strategies. According to the relative contribution of eye and head motion, a continuum among individual strategies was observed, covering a range of head contributions varying from 0 to almost 100%. All these strategies were well adapted because they contributed to the counteraction of the displacement and led to an optimal gaze accuracy. 3. The use of various gaze strategies during linear motion to achieve the same movement differed according to the subject, but also depended upon motion kinematics. As a rule, head contribution increased as the magnitude of linear acceleration was enhanced. 4. Different eye-head coordination strategies implicated either a linear vestibulo-ocular reflex (LVOR) or ocular responses composed of a combination of antagonistic angular and linear vestibulo-ocular reflexes (AVOR-LVOR). The slow phase direction of these two oculomotor responses for fixation stabilization on the target were compensatory and anticompensatory, respectively. 5. One of the major points of this study was the contribution of the saccadic system to gaze strategies, even in our experimental conditions where the head was free to move. We concluded that vestibular-saccadic cooperation appears to be a common feature in the elaboration of adequate fixation stabilization in daily life situations. 6. The functional coupling of these various subsystems involved in fixation stabilization depended on the range of motion: while the acceleration increased, the saccadic eye movements were replaced by vestibulo-ocular responses whose slow phase direction was opposite that of head motion and, therefore, directed away from the target. 7. Fast components of the nystagmic pattern of eye movements were able to improve gaze position accuracy, bringing the eyes toward the memorized target.(ABSTRACT TRUNCATED AT 400 WORDS)

Cognitive engagement in emotional text reading: concurrent recordings of eye movements and head motion

2019 ◽  
Vol 33 (7) ◽  
pp. 1448-1460 ◽  
Author(s):  
Ugo Ballenghein ◽  
Olga Megalakaki ◽  
Thierry Baccino
Keyword(s):  
Eye Movements ◽  
Cognitive Engagement ◽  
Head Motion ◽  
Text Reading

Eye movement responses to linear head motion in the squirrel monkey. I. Basic characteristics

1991 ◽  
Vol 65 (5) ◽  
pp. 1170-1182 ◽  
Author(s):  
G. D. Paige ◽  
D. L. Tomko
Keyword(s):  
Eye Movements ◽  
Companion Paper ◽  
Head Motion ◽  
Head Orientation ◽  
Otolith Organs ◽  
Response Characteristics ◽  
Systematic Effects ◽  
Gravitoinertial Force ◽  
Static Head ◽  
Head Translation

1. The purpose of this study was to quantify the response characteristics of eye movements produced by linear head oscillations in the dark (the linear vestibuloocular reflex, or LVOR). Horizontal, vertical, and torsional eye movements were measured in adult squirrel monkeys by the use of a dual scleral search-coil technique during linear oscillations (0.5, 1.5, and 5.0 Hz, 0.36 g peak acceleration) along the animals' interaural (IA), dorsoventral (DV), and nasooccipital (NO) axes. 2. Two LVOR responses, horizontal eye movements during IA-axis translation and vertical eye movements during DV-axis motion, were in a compensatory direction for head translation. Response amplitudes increased as frequency increased, whereas phase typically showed a lead. 3. Two other LVORs, torsional responses during IA-axis translation (all frequencies) and vertical responses during NO-axis oscillations (0.5 Hz), behaved differently. These two LVORs cannot be functionally compensatory for head translation because they degrade fixation on targets, and therefore image stability, by rotating the eyes off target (NO-vertical) or torting the eyes relative to the visual world (IA-torsional). Responses to NO-axis motion at frequencies greater than 0.5 Hz depended on initial eye position and fixation distance and are described in the companion paper. 4. The effect of head orientation on the LVOR was assessed by testing four head positions in 90 degrees steps around the axis of head motion for each of the three axes of translation. This was done, first, to determine whether the LVORs are responses to the "swinging vector" of gravitoinertial force during linear head motion or to head translation; and second, to quantify potential effects of static head (otolith) orientation on the LVORs. Results showed no systematic effects of head orientation on LVOR responses in the frequency bandwidth studied. This indicates that the LVORs are dependent on the direction of linear motion relative to the head (and otolith organs) but not on the swinging vector of gravitoinertial force, and that the LVORs are uninfluenced by static orientation of the head and reloading of the otoliths.

Different responses to small visual errors during initiation and maintenance of smooth-pursuit eye movements in monkeys

1987 ◽  
Vol 58 (6) ◽  
pp. 1351-1369 ◽  
Author(s):  
E. J. Morris ◽  
S. G. Lisberger
Keyword(s):  
Eye Movements ◽  
Head Motion ◽  
Vestibuloocular Reflex ◽  
Smooth Pursuit Eye Movements ◽  
Retinal Position ◽  
Pursuit Eye Movements ◽  
Position Errors ◽  
Steady Fixation ◽  
Pursuit System ◽  
Eye Velocity

1. We have investigated the role of retinal and extraretinal signals in the initiation and maintenance of smooth-pursuit eye movements in trained rhesus monkeys. Visual targets were presented in open-loop conditions by using electronic feedback of eye position to form the command for target position. This allowed us to present stimuli that were stabilized with respect to the moving eye or to provide small, precisely controlled retinal position or velocity errors. 2. Pursuit was maintained with only small decreases in eye velocity if retinal errors were eliminated by stabilizing the tracking target in front of the fovea during pursuit at 15 degrees/s. This argues that the pursuit system employs “velocity memory” to maintain pursuit. We suggest that velocity memory is effected by an extraretinal signal derived from positive feedback of eye-velocity commands. 3. Small retinal position errors caused smooth eye accelerations if imposed during pursuit, but were ineffective for initiating the transition from steady fixation to pursuit. Small retinal velocity errors were effective both for initiating pursuit from steady fixation and for altering eye velocity during pursuit. 4. Retinal position errors were effective at changing smooth eye velocity in a variety of conditions that required prior activation of the pursuit system. These include pursuit with or without a stationary background, pursuit with a background that was stabilized with respect to the eye, pursuit with combined eye and head motion (cancellation of the vestibuloocular reflex), and use of pursuit to suppress optokinetic nystagmus. Position errors were ineffective during fixation of stationary targets, even if head motion was provided to evoke the smooth eye velocity of the vestibuloocular reflex. 5. We conclude that retinal position errors are effective only after the pursuit system has been activated. It follows that pursuit initiation involves an active transition from steady fixation and that this transition is normally triggered by retinal velocity errors but not by retinal position errors.

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