Gaze Orienting in Dynamic Visual Double Steps

2005 ◽  
Vol 94 (6) ◽  
pp. 4300-4313 ◽  
Author(s):  
Joyce Vliegen ◽  
Tom J. Van Grootel ◽  
A. John Van Opstal

Visual stimuli are initially represented in a retinotopic reference frame. To maintain spatial accuracy of gaze (i.e., eye in space) despite intervening eye and head movements, the visual input could be combined with dynamic feedback about ongoing gaze shifts. Alternatively, target coordinates could be updated in advance by using the preprogrammed gaze-motor command (“predictive remapping”). So far, previous experiments have not dissociated these possibilities. Here we study whether the visuomotor system accounts for saccadic eye–head movements that occur during target presentation. In this case, the system has to deal with fast dynamic changes of the retinal input and with highly variable changes in relative eye and head movements that cannot be preprogrammed by the gaze control system. We performed visual–visual double-step experiments in which a brief (50-ms) stimulus was presented during a saccadic eye–head gaze shift toward a previously flashed visual target. Our results show that gaze shifts remain accurate under these dynamic conditions, even for stimuli presented near saccade onset, and that eyes and head are driven in oculocentric and craniocentric coordinates, respectively. These results cannot be explained by a predictive remapping scheme. We propose that the visuomotor system adequately processes dynamic changes in visual input that result from self-initiated gaze shifts, to construct a stable representation of visual targets in an absolute, supraretinal (e.g., world) reference frame. Predictive remapping may subserve transsaccadic integration, thus enabling perception of a stable visual scene despite eye movements, whereas dynamic feedback ensures accurate actions (e.g., eye–head orienting) to a selected goal.

2008 ◽  
Vol 100 (4) ◽  
pp. 1848-1867 ◽  
Author(s):  
Sigrid M. C. I. van Wetter ◽  
A. John van Opstal

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.


2007 ◽  
Vol 97 (2) ◽  
pp. 1149-1162 ◽  
Author(s):  
Mario Prsa ◽  
Henrietta L. Galiana

Models of combined eye-head gaze shifts all aim to realistically simulate behaviorally observed movement dynamics. One of the most problematic features of such models is their inability to determine when a saccadic gaze shift should be initiated and when it should be ended. This is commonly referred to as the switching mechanism mediated by omni-directional pause neurons (OPNs) in the brain stem. Proposed switching strategies implemented in existing gaze control models all rely on a sensory error between instantaneous gaze position and the spatial target. Accordingly, gaze saccades are initiated after presentation of an eccentric visual target and subsequently terminated when an internal estimate of gaze position becomes nearly equal to that of the target. Based on behavioral observations, we demonstrate that such a switching mechanism is insufficient and is unable to explain certain types of movements. We propose an improved hypothesis for how the OPNs control gaze shifts based on a visual-vestibular interaction of signals known to be carried on anatomical projections to the OPN area. The approach is justified by the analysis of recorded gaze shifts interrupted by a head brake in animal subjects and is demonstrated by implementing the switching mechanism in an anatomically based gaze control model. Simulated performance reveals that a weighted sum of three signals: gaze motor error, head velocity, and eye velocity, hypothesized as inputs to OPNs, successfully reproduces diverse behaviorally observed eye-head movements that no other existing model can account for.


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)


2000 ◽  
Vol 84 (2) ◽  
pp. 1103-1106 ◽  
Author(s):  
Tyson A. Tu ◽  
E. Gregory Keating

The frontal eye field (FEF), an area in the primate frontal lobe, has long been considered important for the production of eye movements. Past studies have evoked saccade-like movements from the FEF using electrical stimulation in animals that were not allowed to move their heads. Using electrical stimulation in two monkeys that were free to move their heads, we have found that the FEF produces gaze shifts that are composed of both eye and head movements. Repeated stimulation at a site evoked gaze shifts of roughly constant amplitude. However, that gaze shift could be accomplished with varied amounts of head and eye movements, depending on their (head and eye) respective starting positions. This evidence suggests that the FEF controls visually orienting movements using both eye and head rotations rather than just shifting the eyes as previously thought.


2011 ◽  
Vol 106 (4) ◽  
pp. 2000-2011 ◽  
Author(s):  
Luis C. Populin ◽  
Abigail Z. Rajala

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.


2010 ◽  
Vol 104 (2) ◽  
pp. 811-828 ◽  
Author(s):  
Bernard P. Bechara ◽  
Neeraj J. Gandhi

High-frequency burst neurons in the pons provide the eye velocity command (equivalently, the primary oculomotor drive) to the abducens nucleus for generation of the horizontal component of both head-restrained (HR) and head-unrestrained (HU) gaze shifts. We sought to characterize how gaze and its eye-in-head component differ when an “identical” oculomotor drive is used to produce HR and HU movements. To address this objective, the activities of pontine burst neurons were recorded during horizontal HR and HU gaze shifts. The burst profile recorded on each HU trial was compared with the burst waveform of every HR trial obtained for the same neuron. The oculomotor drive was assumed to be comparable for the pair yielding the lowest root-mean-squared error. For matched pairs of HR and HU trials, the peak eye-in-head velocity was substantially smaller in the HU condition, and the reduction was usually greater than the peak head velocity of the HU trial. A time-varying attenuation index, defined as the difference in HR and HU eye velocity waveforms divided by head velocity [α = ( Ḣhr − Ėhu)/ Ḣ] was computed. The index was variable at the onset of the gaze shift, but it settled at values several times greater than 1. The index then decreased gradually during the movement and stabilized at 1 around the end of gaze shift. These results imply that substantial attenuation in eye velocity occurs, at least partially, downstream of the burst neurons. We speculate on the potential roles of burst-tonic neurons in the neural integrator and various cell types in the vestibular nuclei in mediating the attenuation in eye velocity in the presence of head movements.


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.


1996 ◽  
Vol 76 (2) ◽  
pp. 927-952 ◽  
Author(s):  
E. G. Freedman ◽  
T. R. Stanford ◽  
D. L. Sparks

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


2009 ◽  
Vol 101 (1) ◽  
pp. 198-206 ◽  
Author(s):  
Aarlenne Z. Khan ◽  
Gunnar Blohm ◽  
Robert M. McPeek ◽  
Philippe Lefèvre

A salient peripheral cue can capture attention, influencing subsequent responses to a target. Attentional cueing effects have been studied for head-restrained saccades; however, under natural conditions, the head contributes to gaze shifts. We asked whether attention influences head movements in combined eye–head gaze shifts and, if so, whether this influence is different for the eye and head components. Subjects made combined eye–head gaze shifts to horizontal visual targets. Prior to target onset, a behaviorally irrelevant cue was flashed at the same (congruent) or opposite (incongruent) location at various stimulus-onset asynchrony (SOA) times. We measured eye and head movements and neck muscle electromyographic signals. Reaction times for the eye and head were highly correlated; both showed significantly shorter latencies (attentional facilitation) for congruent compared with incongruent cues at the two shortest SOAs and the opposite pattern (inhibition of return) at the longer SOAs, consistent with attentional modulation of a common eye–head gaze drive. Interestingly, we also found that the head latency relative to saccade onset was significantly shorter for congruent than that for incongruent cues. This suggests an effect of attention on the head separate from that on the eyes.


1984 ◽  
Vol 52 (6) ◽  
pp. 1030-1050 ◽  
Author(s):  
D. Guitton ◽  
R. M. Douglas ◽  
M. Volle

Gaze is the position of the visual axis in space and is the sum of the eye movement relative to the head plus head movement relative to space. In monkeys, a gaze shift is programmed with a single saccade that will, by itself, take the eye to a target, irrespective of whether the head moves. If the head turns simultaneously, the saccade is correctly reduced in size (to prevent gaze overshoot) by the vestibuloocular reflex (VOR). Cats have an oculomotor range (OMR) of only about +/- 25 degrees, but their field of view extends to about +/- 70 degrees. The use of the monkey's motor strategy to acquire targets lying beyond +/- 25 degrees requires the programming of saccades that cannot be physically made. We have studied, in cats, rapid horizontal gaze shifts to visual targets within and beyond the OMR. Heads were either totally unrestrained or attached to an apparatus that permitted short unexpected perturbations of the head trajectory. Qualitatively, similar rapid gaze shifts of all sizes up to at least 70 degrees could be accomplished with the classic single-eye saccade and a saccade-like head movement. For gaze shifts greater than 30 degrees, this classic pattern frequently was not observed, and gaze shifts were accomplished with a series of rapid eye movements whose time separation decreased, frequently until they blended into each other, as head velocity increased. Between discrete rapid eye movements, gaze continued in constant velocity ramps, controlled by signals added to the VOR-induced compensatory phase that followed a saccade. When the head was braked just prior to its onset in a 10 degrees gaze shift, the eye attained the target. This motor strategy is the same as that reported for monkeys. However, for larger target eccentricities (e.g., 50 degrees), the gaze shift was interrupted by the brake and the average saccade amplitude was 12-15 degrees, well short of the target and the OMR. Gaze shifts were completed by vestibularly driven eye movements when the head was released. Braking the head during either quick phases driven by passive head displacements or visually triggered saccades resulted in an acceleration of the eye, thereby implying interaction between the VOR and these rapid-eye-movement signals. Head movements possessed a characteristic but task-dependent relationship between maximum velocity and amplitude. Head movements terminated with the head on target. The eye saccade usually lagged the head displacement.(ABSTRACT TRUNCATED AT 400 WORDS)


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