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

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)     

Gaze shifts evoked by stimulation of the superior colliculus in the head-free cat conform to the motor map but also depend on stimulus strength and fixation activity

In our previous paper we demonstrated that electrical microstimulation of the fixation area at the rostral pole of the cat superior colliculus (SC) elicits no gaze movement but, rather, transiently suppresses eye-head gaze saccades. In this paper, we investigated the more caudal region of the SC and its interaction with the fixation area. In the alert head-free cat, supra-threshold stimulation in the anterior portion of the SC but outside the fixation area evoked small saccadic shifts of gaze consisting mainly of an eye movement, the head's contribution being small. Stimulating more posteriorly elicited large gaze saccades consisting of an ocular saccade combined with a rapid head movement. At these latter stimulation sites, craniocentric (goal-directed) eye movements were evoked when the cat's head was restrained. The amplitude of eye-head gaze saccades elicited at a particular stimulation site increased with stimulus duration, current strength, and pulse rate, until a constant or unit value was reached. The peak velocity of gaze shifts depended on both pulse rate and current strength. The movement direction was not affected by stimulus parameters. The unit gaze vector evoked, in the head-free condition, by stimulating one collicular site was similar to that coded by efferent neurons recorded at that site, thereby indicating a retinotopically coded gaze error representation on the collicular motor map which is not revealed by stimulating the head-fixed animal. Evoked gaze saccades were found to be influenced by fixation behavior. The amplitude of evoked gaze shifts was reduced if stimulation occurred when the hungry animal fixated a food target. Electrical activation of the collicular fixation area was found to mimic well the effects of natural fixation on evoked gaze shifts. Taken together, our results support the view that the overall distribution and level of collicular activity contributes to the encoding of the metrics of gaze saccades. We suggest that the combined levels of activity at the site being stimulated and at the fixation area influence the amplitude of evoked gaze saccades through competition. When stimulation is at low intensities, fixation-related activity reduces the amplitude of evoked gaze saccades. At high activation levels, the site being stimulated dominates and the gaze vector is specified only by that site's collicular output neurons, from which arises the close correspondence between the unit-evoked gaze saccades and the neurally coded gaze vector at that site.     

Combined eye-head gaze shifts in the primate. III. Contributions to the accuracy of gaze saccades

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)     

Eye, head, and body coordination during large gaze shifts in rhesus monkeys: movement kinematics and the influence of posture

Coordinated movements of the eye, head, and body are used to redirect the axis of gaze between objects of interest. However, previous studies of eye-head gaze shifts in head-unrestrained primates generally assumed the contribution of body movement to be negligible. Here we characterized eye-head-body coordination during horizontal gaze shifts made by trained rhesus monkeys to visual targets while they sat upright in a standard primate chair and assumed a more natural sitting posture in a custom-designed chair. In both postures, gaze shifts were characterized by the sequential onset of eye, head, and body movements, which could be described by predictable relationships. Body motion made a small but significant contribution to gaze shifts that were > or =40 degrees in amplitude. Furthermore, as gaze shift amplitude increased (40-120 degrees ), body contribution and velocity increased systematically. In contrast, peak eye and head velocities plateaued at velocities of approximately 250-300 degrees /s, and the rotation of the eye-in-orbit and head-on-body remained well within the physical limits of ocular and neck motility during large gaze shifts, saturating at approximately 35 and 60 degrees , respectively. Gaze shifts initiated with the eye more contralateral in the orbit were accompanied by smaller body as well as head movement amplitudes and velocities were greater when monkeys were seated in the more natural body posture. Taken together, our findings show that body movement makes a predictable contribution to gaze shifts that is systematically influenced by factors such as orbital position and posture. We conclude that body movements are part of a coordinated series of motor events that are used to voluntarily reorient gaze and that these movements can be significant even in a typical laboratory setting. Our results emphasize the need for caution in the interpretation of data from neurophysiological studies of the control of saccadic eye movements and/or eye-head gaze shifts because single neurons can code motor commands to move the body as well as the head and eyes.     

Experimental study and modeling of vestibulo-ocular reflex modulation during large shifts of gaze in humans

Summary An experimental study of head-free and headfixed gaze shifts explores the role of the vestibulo-ocular reflex (VOR) during saccadic and slow phase components of the gaze shifts. A systematic comparison of head-free and head-fixed gaze shifts in humans revealed that while the VOR is switched off as soon as the saccade starts, its function is progressively restored during the terminal phase of the saccade. The duration of this restoration period is fairly constant; therefore, the faster the gaze saccade, the sooner the VOR function starts to be restored. On the basis of these experimental data, a new eye-head coordination model is proposed. This model is an extension of the one proposed by Laurutis and Robinson (1986) where VOR gain is a function of both the dynamic gaze error signal and head velocity. This extension has also been added to another eye-head coordination model (Guitton et al. 1990). Both modified models yield simulation results comparable to experimental data. This study pinpoints the high efficiency of the gaze control system. Indeed, a fixed period of time (40 ms) is needed to restore the inhibited VOR; the gaze control system thus must have a knowledge of its own dynamics in order to be able to anticipate the end of the saccadic movement.     

Head-unrestrained gaze shifts after muscimol injection in the caudal fastigial nucleus of the monkey

The effects of unilateral cFN inactivation on horizontal and vertical gaze shifts generated from a central target toward peripheral ones were tested in two head unrestrained monkeys. After muscimol injection, the eye component was hypermetric during ipsilesional gaze shifts, hypometric during contralesional ones and deviated toward the injected side during vertical gaze shifts. The ipsilesional gaze hypermetria increased with target eccentricity until approximately 24 degrees after which it diminished and became smaller than the hypermetria of the eye component. Contrary to eye saccades, the amplitude and peak velocity of which were enhanced, the amplitude and peak velocity of head movements were reduced during ipsilesional gaze shifts. These changes in head movement were not correlated with those affecting the eye saccades. Head movements were also delayed relative to the onset of eye saccades. The alterations in head movement and the faster eye saccades likely explained the reduced head contribution to the amplitude of ipsilesional gaze shifts. The contralesional gaze hypometria increased with target eccentricity and was associated with uncorrelated reductions in eye and head peak velocities. When compared with control movements of similar amplitude, contralesional eye saccades had lower peak velocity and longer duration. This slowing likely accounted for the increase in head contribution to the amplitude of contralesional gaze shifts. These data suggest different pathways for the fastigial control of eye and head components during gaze shifts. Saccade dysmetria was not compensated by appropriate changes in head contribution, raising the issue of the feedback control of movement accuracy during combined eye-head gaze shifts.     

Three-dimensional eye-head coordination is implemented downstream from the superior colliculus

How the brain transforms two-dimensional visual signals into multi-dimensional motor commands, and subsequently how it constrains the redundant degrees of freedom, are fundamental problems in sensorimotor control. During fixations between gaze shifts, the redundant torsional degree of freedom is determined by various neural constraints. For example, the eye- and head-in-space are constrained by Donders' law, whereas the eye-in-head obeys Listing's law. However, where and how the brain implements these laws is not yet known. In this study, we show that eye and head movements, elicited by unilateral microstimulations of the superior colliculus (SC) in head-free monkeys, obey the same Donders' strategies observed in normal behavior (i.e., Listing's law for final eye positions and the Fick strategy for the head). Moreover, these evoked movements showed a pattern of three-dimensional eye-head coordination, consistent with normal behavior, where the eye is driven purposely out of Listing's plane during the saccade portion of the gaze shift in opposition to a subsequent torsional vestibuloocular reflex slow phase, such that the final net torsion at the end of each head-free gaze shift is zero. The required amount of saccade-related torsion was highly variable, depending on the initial position of the eye and head prior to a gaze shift and the size of the gaze shift, pointing to a neural basis of torsional control. Because these variable, context-appropriate torsional saccades were correctly elicited by fixed SC commands during head-free stimulations, this shows that the SC only encodes the horizontal and vertical components of gaze, leaving the complexity of torsional organization to downstream control systems. Thus we conclude that Listing's and Donders' laws of the eyes and head, and their three-dimensional coordination mechanisms, must be implemented after the SC.     

Eye position and target amplitude effects on human visual saccadic latencies

Gaze shifts vary in the extent of eye and head contribution; a large amplitude and/or an eccentric ocular orbital starting position alter the participation of head movement in the shift. The interval between eye onset and head onset determines compensatory counterrolling before and after the shift and the extent of vestibular ocular reflex reduction during the shift. The latency of eye saccades in the head-fixed condition was measured with respect to target amplitude and orbital position in order to establish base-line operations of these two variables as they apply to the headfree condition. Eye movements were measured during single-step saccades in nine young adult humans. The target step, hereafter called a jump, started from three possible fixation lights; e.g., rightward saccades started from the midline (0°) or from -20 or -40° left of the midline, with a maximum amplitude of 80°. The latency of saccades starting from the primary position increased with jump amplitude (amplitude-latency relation). When the eye started eccentrically, the latency was decreased (orbital position-latency relation), with the largest jump amplitudes most affected. These changes can be related to active eye-head coordination. Thus, with a leftward maximal orbital eccentricity, compensatory eye rotation would be impossible with a rightward head movement; however, incorporating the orbital position-latency relation, the forward ocular saccade is expedited by 90 ms. Conversely, with a primary starting position, the ocular component of an 80° gaze saccade could be slowed 125 ms by incorporating the amplitude-latency relation, thus facilitating a head contribution to the gaze shift. The orbital position and amplitude-latency relations were prominent in those subjects with habitually large head contributions to the gaze shift and minimal in individuals with typically small head contributions.     

Conjugate and vergence oscillations during saccades and gaze shifts: implications for integrated control of binocular movement.

Saccades made between targets at optical infinity require both eyes to rotate by the same angle. Nevertheless, these saccades are consistently accompanied by transient vergence eye movements. Here we have investigated whether the dynamics of these vergence movements depend on the trajectory of the coincident conjugate movement, and whether moving the head during eye-head gaze shifts modifies vergence dynamics. In agreement with previous reports, saccades with more symmetric (i.e., "bell-shaped") conjugate velocity profiles were accompanied by stereotyped biphasic vergence transients (i.e., a divergence phase immediately followed by a convergence phase). However, we found that saccades with more asymmetric, oscillatory-like dynamics (characterized by a typical conjugate reacceleration of the eyes following the initial peak velocity) were systematically accompanied by more complex vergence movements that also exhibited oscillatory-like dynamics. These findings could be extended to conditions where the head was free to move: comparable conjugate and vergence oscillations were observed during head-restrained saccades and combined eye-head gaze shifts. The duration of the vergence oscillation increased with gaze shift amplitude, such that as many as four vergence phases (divergence-convergence-divergence-convergence) were recorded during 55 degrees gaze shifts (approximately 240 ms). To quantify these observations, we first determined whether conjugate and vergence peak velocities were systematically correlated. Conjugate peak velocity was linearly related to the peak velocity of the initial divergence phase for saccades and gaze shifts of all amplitudes, regardless of their dynamics. However, for more asymmetric saccades and gaze shifts, the subsequent convergence and divergence peak velocities were not correlated with either the initial peak conjugate velocity or the peak velocity of the conjugate reacceleration. Next, we determined that the duration of the different conjugate and vergence oscillation phases remained relatively constant across all saccades and gaze shifts, and that the conjugate and vergence profiles oscillated together at approximately 7.5-10 Hz. Using computer simulations, we show that a classic feed-forward model is unable to reproduce vergence oscillations based solely on peripheral mechanisms. Furthermore, we demonstrate that small modifications to the gain and delay of a simple feedback model for saccade generation can generate conjugate oscillations, and propose that such changes reflect the influence of lowered alertness on the tecto-reticular pathways. We conclude that peripheral mechanisms can only account for the initial divergence that accompanies all saccades, and that the conjugate and vergence oscillations observed during asymmetric movements arise centrally from an integrative binocular controller.     

Role of superior colliculus in adaptive eye-head coordination during gaze shifts

The goal of this study was to determine which aspects of adaptive eye-head coordination are implemented upstream or downstream from the motor output layers of the superior colliculus (SC). Two monkeys were trained to perform head-free gaze shifts while looking through a 10 degrees aperture in opaque, head-fixed goggles. This training produced context-dependent alterations in eye-head coordination, including a coordinated pattern of saccade-vestibuloocular reflex (VOR) eye movements that caused eye position to converge toward the aperture, and an increased contribution of head movement to the gaze shift. One would expect the adaptations that were implemented downstream from the SC to be preserved in gaze shifts evoked by SC stimulation. To test this, we analyzed gaze shifts evoked from 19 SC sites in monkey 1 and 38 sites in monkey 2, both with and without goggles. We found no evidence that the goggle paradigm altered the basic gaze position-dependent spatial coding of the evoked movements (i.e., gaze was still coded in an eye-centered frame). However, several aspects of the context-dependent coordination strategy were preserved during stimulation, including the adaptive convergence of final eye position toward the goggles aperture, and the position-dependent patterns of eye and head movement required to achieve this. For example, when initial eye position was offset from the learned aperture location at the time of stimulation, a coordinated saccade-VOR eye movement drove it back to the original aperture, and the head compensated to preserve gaze kinematics. Some adapted amplitude-velocity relationships in eye, gaze, and head movement also may have been preserved. In contrast, context-dependent changes in overall eye and head contribution to gaze amplitude were not preserved during SC stimulation. We conclude that 1) the motor output command from the SC to the brain stem can be adapted to produce different position-dependent coordination strategies for different behavioral contexts, particularly for eye-in-head position, but 2) these brain stem coordination mechanisms implement only the default (normal) level of head amplitude contribution to the gaze shift. We propose that a parallel cortical drive, absent during SC stimulation, is required to adjust the overall head contribution for different behavioral contexts.     

Human eye-head coordination in two dimensions under different sensorimotor conditions

 The coordination between eye and head movements during a rapid orienting gaze shift has been investigated mainly when subjects made horizontal movements towards visual targets with the eyes starting at the centre of the orbit. Under these conditions, it is difficult to identify the signals driving the two motor systems, because their initial motor errors are identical and equal to the coordinates of the sensory stimulus (i.e. retinal error). In this paper, we investigate head-free gaze saccades of human subjects towards visual as well as auditory stimuli presented in the two-dimensional frontal plane, under both aligned and unaligned initial fixation conditions. Although the basic patterns for eye and head movements were qualitatively comparable for both stimulus modalities, systematic differences were also obtained under aligned conditions, suggesting a task-dependent movement strategy. Auditory-evoked gaze shifts were endowed with smaller eye-head latency differences, consistently larger head movements and smaller concomitant ocular saccades than visually triggered movements. By testing gaze control for eccentric initial eye positions, we found that the head displacement vector was best related to the initial head motor-error (target-re-head), rather than to the initial gaze error (target-re-eye), regardless of target modality. These findings suggest an independent control of the eye and head motor systems by commands in different frames of reference. However, we also observed a systematic influence of the oculomotor response on the properties of the evoked head movements, indicating a subtle coupling between the two systems. The results are discussed in view of current eye-head coordination models. Received: 24 April 1996 / Accepted: 25 October 1996     

Head movements evoked by electrical stimulation in the frontal eye field of the monkey: evidence for independent eye and head control

When the head is free to move, electrical stimulation in the frontal eye field (FEF) evokes eye and head movements. However, it is unclear whether FEF stimulation-evoked head movements contribute to shifting the line of sight, like visually guided coordinated eye-head gaze shifts. Here we investigated this issue by systematically varying initial eye (IEP) and head (IHP) positions at stimulation onset. Despite the large variability of IEP and IHP and the extent of stimulation-evoked gaze amplitudes, gaze displacement was entirely accounted for by eye (re head) displacement. Overall, the majority (3/4) of stimulation-evoked gaze shifts consisted of eye-alone movements, in which head movements were below the detection threshold. When head movements did occur, they often started late (re gaze shift onset) and coincided with rapid eye deceleration, resulting in little change in the ensuing gaze amplitudes. These head movements often reached their peak velocities over 100 ms after the end of gaze shifts, indicating that the head velocity profile was temporally dissociated from the gaze drive. Interestingly, head movements were sometimes evoked by FEF stimulation in the absence of gaze shifts, particularly when IEP was deviated contralaterally (re the stimulated side) at stimulation onset. Furthermore, head movements evoked by FEF stimulation resembled a subset of head movements occurring during visually guided gaze shifts. These unique head movements minimized the eye deviation from the center of the orbit and contributed little to gaze shifts. The results suggest that head motor control may be independent from eye control in the FEF.     

Eye-head coordination and the variation of eye-movement accuracy with orbital eccentricity

Different humans vary widely in the tendency to move the head during saccadic shifts in gaze. The reasons for this variation are unknown. Because combined eye-head movements are associated with a recentering of the eyes in the orbits, humans who are "head movers" tend to maintain the eyes within a narrower range than do non-head movers. We explored the possibility that variations in the ability to control eye movements at eccentric positions lead to variations in customary ocular motor range and, by extension, explain the variations in head-movement tendencies. We studied ten normal adults. In each, we measured the full-scale ocular motor range and customary ocular motor range (the eccentricity range within which the eye was found at the conclusion of eye- or eye-head saccades). We also determined the eye-only range, the orbital range within which the probability of a head movement accompanying a gaze shift was low. Customary, eye-only, and full-scale ranges spanned (mean +/-SD) 41.1+/-16.9 degrees, 30.2+/-18.8 degrees, and 92.8+/- 9.1 degrees, respectively. We then assessed variations in kinematics of several ocular motor behaviors as functions of eye eccentricity. The stable fixation range, defined by the range over which drift velocities were below 1 degree/s, spanned 81.1+/-11.2 degrees in the light and 69.5+/-21.5 degrees in the dark. The range over which the gains of the vestibulo-ocular reflex in the light and smooth pursuit approached their values at zero eccentricity spanned 66.3+/-7.1 degrees and 69.0+/-10.0 degrees, respectively. Small centrifugal saccades (5-10 degrees) tended to become either slowed or hypometric with increasing eccentricity. Sensitive to both slowing and hypometria, the ratio of peak gaze velocity to target shift amplitude was flat over a range spanning 65.7+/-14.9 degrees. Finally, the ranges over which the initial saccade placed the fovea upon the target averaged 35.5+/-10.7 degrees for eye-only saccades and 36.6+/-15.0 degrees for eye-head saccades. With the exception of the range of stable fixation in the light, the kinematic ranges were either unrelated or inconsistently related to full-scale range, indicating that the deterioration of eye movements with increasing ocular eccentricity is not a simple consequence of the eyes encountering the limits of their excursion. None of the kinematic ranges correlated positively with customary or eye-only range. Thus, while head movements may be orchestrated so as to maintain the eyes within a desired range, that range (and thus head movement tendencies) is not predicated upon the range of ocular eccentricity over which eye movements are accurately controlled.     

Gaze control in humans: eye-head coordination during orienting movements to targets within and beyond the oculomotor range

Gaze, the direction of the visual axis in space, is the sum of the eye position relative to the head (E) plus head position relative to space (H). In the old explanation, which we call the oculocentric motor strategy, of how a rapid orienting gaze shift is controlled, it is assumed that 1) a saccadic eye movement is programmed with an amplitude equal to the target's offset angle, 2) this eye movement is programmed without reference to whether a head movement is planned, 3) if the head turns simultaneously the saccade is reduced in size by an amount equal to the head's contribution, and 4) the saccade is attenuated by the vestibuloocular reflex (VOR) slow phase. Humans have an oculomotor range (OMR) of about +/- 55 degrees. The use of the oculocentric motor strategy to acquire targets lying beyond the OMR requires programming saccades that cannot be made physically. We have studied in normal human subjects rapid horizontal gaze shifts to visible and remembered targets situated within and beyond the OMR at offsets ranging from 30 to 160 degrees. Heads were attached to an apparatus that permitted short unexpected perturbations of the head trajectory. The acceleration and deceleration phases of the head perturbation could be timed to occur at different points in the eye movement. 4. Single-step rapid gaze shifts of all sizes up to at least 160 degrees (the limit studied) could be accomplished with the classic single-eye saccade and an accompanying saccadelike head movement. In gaze shifts less than approximately 45 degrees, when head motion was prevented totally by the brake, the eye attained the target. For larger target eccentricities the gaze shift was interrupted by the brake and the average eye saccade amplitude was approximately 45 degrees, well short of the OMR. Thus saccadic eye movement amplitude was neurally, not mechanically, limited. When the head's motion was not perturbed by the brake, the eye saccade amplitude was a function of head velocity: for a given target offset, the faster the head the smaller the saccade. For gaze shifts to targets beyond the OMR and when head velocity was low, the eye frequently attained the 45 degrees position limit and remained there, immobile, until gaze attained the target.(ABSTRACT TRUNCATED AT 400 WORDS)     

Visual-vestibular interaction hypothesis for the control of orienting gaze shifts by brain stem omnipause neurons

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.     

Contribution of head movement to gaze command coding in monkey frontal cortex and superior colliculus

Most of what we know about the neural control of gaze comes from experiments in head-fixed animals, but several "head-free" studies have suggested that fixing the head dramatically alters the apparent gaze command. We directly investigated this issue by quantitatively comparing head-fixed and head-free gaze trajectories evoked by electrically stimulating 52 sites in the superior colliculus (SC) of two monkeys and 23 sites in the supplementary eye fields (SEF) of two other monkeys. We found that head movements made a significant contribution to gaze shifts evoked from both neural structures. In the majority of the stimulated sites, average gaze amplitude was significantly larger and individual gaze trajectories were significantly less convergent in space with the head free to move. Our results are consistent with the hypothesis that head-fixed stimulation only reveals the oculomotor component of the gaze shift, not the true, planned goal of the movement. One implication of this finding is that when comparing stimulation data against popular gaze control models, freeing the head shifts the apparent coding of gaze away from a "spatial code" toward a simpler visual model in the SC and toward an eye-centered or fixed-vector model representation in the SEF.     

Control of orienting gaze shifts by the tectoreticulospinal system in the head-free cat. III. Spatiotemporal characteristics of phasic motor discharges.

1. In this paper we describe the movement-related discharges of tectoreticular and tectoreticulospinal neurons [together called TR (S) Ns] that were recorded in the superior colliculus (SC) of alert cats trained to generate orienting movements in various behavioral situations; the cats' heads were either completely unrestrained (head free) or immobilized (head fixed). TR (S) Ns are organized into a retinotopically coded motor map. These cells can be divided into two groups, fixation TR (S) Ns [f TR (S) Ns] and orientation TR (S) Ns [oTR(S)Ns], depending on whether they are located, respectively, within or outside the zero (or area centralis) representation of the motor map in the rostral SC. 2. oTR(S)Ns discharged phasic motor bursts immediately before the onset of gaze shifts in both the head-free and head-fixed conditions. Ninety-five percent of the oTR(S)Ns tested (62/65) increased their rate of discharge before a visually triggered gaze shift, the amplitude and direction of which matched the cell's preferred movement vector. For movements along the optimal direction, each cell produced a burst discharge for gaze shifts of all amplitudes equal to or greater than the optimum. Hence, oTR(S)Ns had no distal limit to their movement fields. The timing of the burst relative to the onset of the gaze shift, however, depended on gaze shift amplitude: each TR(S)N reached its peak discharge when the instantaneous position of the visual axis relative to the target (i.e., instantaneous gaze motor error) matched the cell's optimal vector, regardless of the overall amplitude of the movement. 3. The intensity of the movement-related burst discharge depended on the behavioral context. For the same vector, the movement-related increase in firing was greatest for visually triggered movements and less pronounced when the cat oriented to a predicted target, a condition in which only 76% of the cells tested (35/46) increased their discharge rate. The weakest movement-related discharges were associated with spontaneous gaze shifts. 4. For some oTR(S)Ns, the average firing frequency in the movement-related burst was correlated to the peak velocity of the movement trajectory in both head-fixed and head-free conditions. Typically, when the head was unrestrained, the correlation to peak gaze velocity was better than that to either peak eye or head velocity alone. 5. Gaze shifts triggered by a high-frequency train of collicular microstimulation had greater peak velocities than comparable amplitude movements elicited by a low-frequency train of stimulation.(ABSTRACT TRUNCATED AT 400 WORDS)     

Vestibuloocular reflex inhibition and gaze saccade control characteristics during eye-head orientation in humans

1. In natural conditions, gaze (i.e., eye + head) orientation is a complex behavior involving simultaneously the eye and head motor systems. Thus one of the key problems of gaze control is whether or not the vestibuloocular reflex (VOR) elicited by head rotation and saccadic eye movement linearly add. 2. Kinematics of human gaze saccades within the oculomotor range (OMR) were quantified under different conditions of head motion. Saccades were visually triggered while the head was fixed or passively moving at a constant velocity (200 deg/s) either in the same direction as, or opposite to, the saccade. Active eye-head coordination was also studied in a session in which subjects were trained to actively rotate their head at a nearly constant velocity during the saccade and, in another session, during natural gaze responses. 3. When the head was passively rotated toward the visual target, both maximum and mean gaze velocities increased with respect to control responses with the head fixed; these effects increased with gaze saccade amplitude. In addition, saccade duration was reduced so that corresponding gaze accuracy, although poorer than for control responses, was not dramatically affected by head motion. 4. The same effects on gaze velocity were present during active head motion when a constant head velocity was maintained throughout saccade duration, and gaze saccades were as accurate as with the head fixed. 5. During natural gaze responses, an increased gaze velocity and a decreased saccade duration with respect to control responses became significant only for gaze displacement larger than 30 degrees, due to the negligible contribution of head motion for smaller responses. 6. When the head was passively rotated in the opposite direction to target step, gaze saccades were slower than those obtained with the head fixed; but their average accuracy was still maintained. 7. These results confirm a VOR inhibition during saccadic eye movements within the OMR. This inhibition, present in all 16 subjects studied, ranged from 40 to 96% (for a 40 degree target step) between subjects and increased almost linearly with target step amplitude. Furthermore, the systematic difference between instantaneous VOR gain estimated at the time of maximum gaze velocity and mean VOR gain estimated over the whole saccadic duration indicates a decay of VOR inhibition during the ongoing saccade. 8. A simplified model is proposed with a varying VOR inhibition during the saccade. It suggests that VOR inhibition is not directly controlled by the saccadic pulse generator.(ABSTRACT TRUNCATED AT 400 WORDS)     

Dissociation of eye and head components of gaze shifts by stimulation of the omnipause neuron region

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.     

Comparing extraocular motoneuron discharges during head-restrained saccades and head-unrestrained gaze shifts

Burst neurons (BNs) in the paramedian pontine reticular formation provide the primary input to the extraocular motoneurons (MNs) during head-restrained saccades and combined eye-head gaze shifts. Prior studies have shown that BNs carry eye movement-related signals during saccades and carry head as well as eye movement-related signals during gaze shifts. Therefore MNs receive signals related to head motion during gaze shifts, yet they solely drive eye motion. Here we addressed whether the relationship between MN firing rates and eye movements is influenced by the additional premotor signals present during gaze shifts. Neurons in the abducens nucleus of monkeys were first studied during saccades made with the head stationary. We then recorded from the same neurons during voluntary combined eye-head gaze shifts. We conclude that the activity of MNs, in contrast to that of BNs, is related to eye motion by the same dynamic relationship during head-restrained saccades and head-unrestrained gaze shifts. In addition, we show that a standard metric-based analysis [i.e., counting the number of spikes (NOS) in a burst] yields misleading results when applied to the same data set. We argue that this latter approach fails because it does not properly consider the system's dynamics or the strong interactions between eye and head motion.