Combined eye-head gaze shifts in the primate. I. Metrics

1986 ◽  
Vol 56 (6) ◽  
pp. 1542-1557 ◽  
Author(s):  
R. D. Tomlinson ◽  
P. S. Bahra

Gaze (eye-in-space) velocity-duration and velocity-amplitude curves were prepared for head-fixed and head-free gaze shifts in the rhesus monkey with an emphasis on large amplitudes. These plots revealed the presence of two distinct gaze reorientation mechanisms, one used when the gaze shift was small (less than 20 degrees) and the other utilized for large coordinated gaze shifts when the head was free. When head-free and head-fixed saccadic gaze shifts were compared in the same animal, no differences in the metrics were found for amplitudes less than 20 degrees. However, for large gaze shifts where contribution of the head to the change in gaze angle was considerable, head-free saccades were found to exhibit lower peak gaze velocities and greater durations than those recorded with the head-fixed paradigm. In order to differentiate between the eye saccades and combined saccadic eye-head gaze shifts, the latter have been termed gaze saccades. Change in head position and change in eye position were both measured during the actual gaze shift and were plotted against the gaze-shift amplitude to determine whether the head movement contributed significantly to the change in gaze angle. The results indicate that below 20 degrees the gaze shift is accomplished almost exclusively with the eyes and the head moves very little; however, for larger saccades, the head contributes approximately 80% of the total change in gaze angle with the eyes contributing only approximately 20%. Large saccadic eye-head gaze shifts do not exhibit 'bell-shaped' velocity profiles as do smaller head-fixed saccades; instead, gaze accelerates to reach a peak velocity after approximately 30-40 ms. This velocity is then maintained for the duration of the gaze shift. Close scrutiny of the fine structure of the velocity profiles of the eye, head, and gaze channels indicates that during gaze saccades, the eye and head movement motor programs interact to maintain gaze velocity nearly constant, unaffected by changes in head velocity. Previous authors had stated that when velocity-duration plots are obtained for oblique saccades of constant amplitude, the resulting points could be fitted with a hyperbolic function. These results were confirmed for head-free gaze saccades and extended to larger amplitudes. When an oblique saccade is made, the smaller component is stretched in duration to match the duration of the larger component. However, as the gaze shift becomes large (greater than 40 degrees), the relationship becomes more complex.(ABSTRACT TRUNCATED AT 400 WORDS)

1990 ◽  
Vol 64 (6) ◽  
pp. 1873-1891 ◽  
Author(s):  
R. D. Tomlinson

1. The behavior of the combined eye-head gaze saccade mechanism was investigated in the rhesus monkey under both normal circumstances and in the presence of perturbations delivered to the head by a torque motor. Animals were trained to follow a target light that stepped at regular intervals through an angle of 68 degrees (+/- 34 degrees with respect to the midsagittal plane). Thus all primary saccades were center crossing. On randomly occurring trials the torque motor was pulsed so as to perturb the trajectory of the head, thus allowing us to assess both the functional state of the vestibuloocular reflex (VOR) and the effects of such perturbations on gaze saccade accuracy (gaze is defined as the sum of eye-in-head plus head-in-space, and a gaze saccade as a combined eye-head saccadic gaze shift). 2. Gaze shifts can be divided into two discrete sections: the portion during which the gaze angle is changing (the saccadic portion), and the portion during which the gaze is stationary but the head continues to move (the terminal head-movement portion). For the system to accurately acquire eccentric targets, at least two criteria must be met: 1) the saccadic portion must be accurate, and 2) the compensatory eye movement that occurs during the terminal head-movement portion must be equal and opposite to the head movement, thereby maintaining gaze stability. Perturbations delivered during the terminal head-movement portion of the gaze shift indicated that VOR was functioning normally, and thus we concluded that the compensatory eye movements that accompany head movements were vestibular in origin. 3. As reported previously, during the saccadic portion of large-amplitude gaze saccades, the VOR ceases to function. In spite of this observation, the accuracy of the gaze saccade is not affected by perturbations delivered to the head. Gaze accuracy is maintained both by changing the duration of the saccadic portion and by altering the head trajectory. 4. Because rhesus monkeys often make very rapid head movements (1,200 degrees/s), we wished to discover the velocity range over which the monkey VOR might be expected to operate. Accordingly, in a second series of experiments, VOR function was assessed during passive whole-body rotations with the head fixed. By the use of spring-assisted manual rotations, peak velocities up to 850 degrees/s were achieved. When VOR gain was measured during such rotations, it was found to be equal to 0.9 up to the maximum velocities used.(ABSTRACT TRUNCATED AT 400 WORDS)


1995 ◽  
Vol 73 (4) ◽  
pp. 1632-1652 ◽  
Author(s):  
J. O. Phillips ◽  
L. Ling ◽  
A. F. Fuchs ◽  
C. Siebold ◽  
J. J. Plorde

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)


1998 ◽  
Vol 79 (6) ◽  
pp. 3060-3076 ◽  
Author(s):  
Martin Paré ◽  
Daniel Guitton

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.


2007 ◽  
Vol 98 (1) ◽  
pp. 360-373 ◽  
Author(s):  
Neeraj J. Gandhi ◽  
David L. Sparks

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.


1999 ◽  
Vol 81 (3) ◽  
pp. 1284-1295 ◽  
Author(s):  
James O. Phillips ◽  
Leo Ling ◽  
Albert F. Fuchs

Action of the brain stem saccade generator during horizontal gaze shifts. I. Discharge patterns of omnidirectional pause neurons. Omnidirectional pause neurons (OPNs) pause for the duration of a saccade in all directions because they are part of the neural mechanism that controls saccade duration. In the natural situation, however, large saccades are accompanied by head movements to produce rapid gaze shifts. To determine whether OPNs are part of the mechanism that controls the whole gaze shift rather than the eye saccade alone, we monitored the activity of 44 OPNs that paused for rightward and leftward gaze shifts but otherwise discharged at relatively constant average rates. Pause duration was well correlated with the duration of either eye or gaze movement but poorly correlated with the duration of head movement. The time of pause onset was aligned tightly with the onset of either eye or gaze movement but only loosely aligned with the onset of head movement. These data suggest that the OPN pause does not encode the duration of head movement. Further, the end of the OPN pause was often better aligned with the end of the eye movement than with the end of the gaze movement for individual gaze shifts. For most gaze shifts, the eye component ended with an immediate counterrotation owing to the vestibuloocular reflex (VOR), and gaze ended at variable times thereafter. In those gaze shifts where eye counterrotation was delayed, the end of the pause also was delayed. Taken together, these data suggest that the end of the pause influences the onset of eye counterrotation, not the end of the gaze shift. We suggest that OPN neurons act to control only that portion of the gaze movement that is commanded by the eye burst generator. This command is expressed by driving the saccadic eye movement directly and also by suppressing VOR eye counterrotation. Because gaze end is less well correlated with pause end and often occurs well after counterrotation onset, we conclude that elements of the burst generator typically are not active till gaze end, and that gaze end is determined by another mechanism independent of the OPNs.


2010 ◽  
Vol 103 (4) ◽  
pp. 2158-2173 ◽  
Author(s):  
Albert F. Fuchs ◽  
Sandra Brettler ◽  
Leo Ling

This study examines how signals generated in the oculomotor cerebellum could be involved in the control of gaze shifts, which rapidly redirect the eyes from one object to another. Neurons in the caudal fastigial nucleus (cFN), the output of the oculomotor cerebellum, discharged when monkeys made horizontal head-unrestrained gaze shifts, composed of an eye saccade and a head movement. Eighty-seven percent of our neurons discharged a burst of spikes for both ipsiversive and contraversive gaze shifts. In both directions, burst end was much better timed with gaze end than was burst start with gaze start, was well correlated with eye end, and was poorly correlated with head end or the time of peak head velocity. Moreover, bursts accompanied all head-unrestrained gaze shifts whether the head moved or not. Therefore we conclude that the cFN is not part of the pathway that controls head movement. For contraversive gaze shifts, the early part of the burst was correlated with gaze acceleration. Thereafter, the burst of the neuronal population continued throughout the prolonged deceleration of large gaze shifts. For a majority of neurons, gaze duration was correlated with burst duration; for some, gaze amplitude was less well correlated with the number of spikes. Therefore we suggest that the population burst provides an acceleration boost for high acceleration (smaller) contraversive gaze shifts and helps maintain the drive required to extend the deceleration of large contraversive gaze shifts. In contrast, the ipsiversive population burst, which is less well correlated with gaze metrics but whose peak rate occurs before gaze end, seems responsible primarily for terminating the gaze shift.


1986 ◽  
Vol 56 (6) ◽  
pp. 1558-1570 ◽  
Author(s):  
R. D. Tomlinson ◽  
P. S. Bahra

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)


1997 ◽  
Vol 77 (5) ◽  
pp. 2328-2348 ◽  
Author(s):  
Edward G. Freedman ◽  
David L. Sparks

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.


1997 ◽  
Vol 78 (5) ◽  
pp. 2817-2821 ◽  
Author(s):  
James O. Phillips ◽  
Albert F. Fuchs ◽  
Leo Ling ◽  
Yoshiki Iwamoto ◽  
Scott Votaw

Phillips, James O., Albert F. Fuchs, Leo Ling, Yoshiki Iwamoto, and Scott Votaw. Gain adaptation of eye and head movement components of simian gaze shifts. J. Neurophysiol. 78: 2817–2821, 1997. To investigate the site of gaze adaptation in primates, we reduced the gain of large head-restrained gaze shifts made to 50° target steps by jumping the target 40% backwards during a targeting saccade and then tested gain transfer to the eye- and head-movement components of head-unrestrained gaze shifts. After several hundred backstep trials, saccadic gain decreased by at least 10% in 8 of 13 experiments, which were then selected for further study. The minimum saccadic gain decrease in these eight experiments was 12.8% (mean = 18.4%). Head-unrestrained gaze shifts to ordinary 50° target steps experienced a gain reduction of at least 9.3% (mean = 14.9%), a mean gain transfer of 81%. Both the eye and head components of the gaze shift also decreased. However, average head movement gain decreased much more (22.1%) than eye movement gain (9.2%). Also, peak head velocity generally decreased significantly (20%), but peak eye velocity either increased or remained constant (average increase of 5.6%). However, the adapted peak eye and head velocities were appropriate for the adapted, smaller gaze amplitudes. Similar dissociations in eye and head metrics occurred when head-unrestrained gaze shifts were adapted directly ( n = 2). These results indicated that head-restrained saccadic gain adaptation did not produce adaptation of eye movement alone. Nor did it produce a proportional gain change in both eye and head movement. Rather, normal eye and head amplitude and velocity relations for a given gaze amplitude were preserved. Such a result could be explained most easily if head-restrained adaptation were realized before the eye and head commands had been individualized. Therefore, gaze adaptation is most likely to occur upstream of the creation of separate eye and head movement commands.


1999 ◽  
Vol 82 (3) ◽  
pp. 1390-1405 ◽  
Author(s):  
Brian D. Corneil ◽  
Christine A. Hing ◽  
Dorothy V. Bautista ◽  
Douglas P. Munoz

This study examines two current ideas regarding the control of eye-head gaze shifts. The first idea stems from recent studies involving electrical stimulation in the primate superior colliculus that suggest that a residual feedback of gaze displacement persists for ∼100 ms after completion of a gaze shift. In light of this hypothesis, we examined the accuracy of gaze shifts generated very soon after the end of a preceding gaze shift. Human subjects were presented with a visual or auditory target along with an accompanying stimulus of the other modality. The accompanying stimulus appeared either at the same place as the target or at the diametrically opposite position, in which case it was termed a distractor. Subjects often made an incorrect gaze shift (IGS) in the direction of the distractor, followed by a recorrect gaze shift (RGS) in the direction of the target. We found that RGSs were accurately driven to the target, even when they followed IGSs by <5 ms, regardless of the size of the IGS. The second idea is that a gaze shift cannot be cancelled in midflight. The end point of IGSs frequently fell short of the distractor. The dynamics of these movements, and of the head movement components during the IGSs in particular, suggests that these hypometric IGSs were planned for a much larger excursion but were truncated and superceded by the reversing RGSs. These results emphasize that the gaze shifting system can change the desired goal of a gaze shift in midflight and that the superceding movement is accurate regardless of the metrics or timing of the preceding movement.


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