Directional asymmetry during combined saccade-vergence movements

We investigated relationships between saccadic and vergence components of gaze shifts as 10 human subjects switched visual fixation between targets aligned in the midsagittal plane that lay in different vertical directions and at different distances. When fixation was shifted between a higher distant target and a lower near target, peak convergence velocity followed peak vertical saccadic velocity by a median interval of 12 ms. However, when fixation was shifted between a lower distant target and a higher near target, peak convergence velocity followed peak vertical saccadic velocity by a median interval of 76 ms. For the 2 stimulus arrangements, the median intervals by which peak divergence velocity followed the peak vertical saccadic velocity were 4 and 20 ms, respectively. The dissociation interval between the peak velocities of convergence and upward saccades increased with vertical saccade size, required convergence angle, and elevation of the endpoint of the movement. Velocity waveforms of vergence responses were more skewed when peak velocity was closely associated with saccadic peak velocity than when the vergence responses were delayed. Convergence peak velocities did not vary in any consistent pattern, but divergence peak velocities were generally smaller with responses that were delayed. Vergence movements were accompanied by small, high-frequency conjugate oscillations, suggesting that omnipause neurons were inhibited for both types of responses. In conclusion, the present findings indicate that the dynamic properties of horizontal vergence movements depend on the direction and timing of vertical saccades; these findings suggest experimental tests for current models of saccade-vergence interaction.     

Dynamic coding of vertical facilitated vergence by premotor saccadic burst neurons

To redirect our gaze in three-dimensional space we frequently combine saccades and vergence. These eye movements, known as disconjugate saccades, are characterized by eyes rotating by different amounts, with markedly different dynamics, and occur whenever gaze is shifted between near and far objects. How the brain ensures the precise control of binocular positioning remains controversial. It has been proposed that the traditionally assumed "conjugate" saccadic premotor pathway does not encode conjugate commands but rather encodes monocular commands for the right or left eye during saccades. Here, we directly test this proposal by recording from the premotor neurons of the horizontal saccade generator during a dissociation task that required a vergence but no horizontal conjugate saccadic command. Specifically, saccadic burst neurons (SBNs) in the paramedian pontine reticular formation were recorded while rhesus monkeys made vertical saccades made between near and far targets. During this task, we first show that peak vergence velocities were enhanced to saccade-like speeds (e.g., >150 vs. <100 degrees/s during saccade-free movements for comparable changes in vergence angle). We then quantified the discharge dynamics of SBNs during these movements and found that the majority of the neurons preferentially encode the velocity of the ipsilateral eye. Notably, a given neuron typically encoded the movement of the same eye during horizontal saccades that were made in depth. Taken together, our findings demonstrate that the brain stem saccadic burst generator encodes integrated conjugate and vergence commands, thus providing strong evidence for the proposal that the classic saccadic premotor pathway controls gaze in three-dimensional space.     

Dynamics and efficacy of saccade-facilitated vergence eye movements in monkeys.

1. Four macaque monkeys were trained to fixate visual targets. Eye movements were recorded binocularly using the search coil technique. Saccades, vergence movements, and combinations of the two were elicited by training the monkeys to alternate the gaze between real visual targets that differed in viewing distance and eccentricity with respect to the monkeys' heads. 2. When they shifted the gaze between targets that were at different viewing distances, the monkeys made vergence eye movements. For targets placed along the midsagittal plane, the monkeys often made binocularly symmetric vergence movements. The peak speed of symmetric divergence movements increased linearly with vergence amplitude by 5.7 deg/s per degree of vergence. The peak speed of symmetric convergence movements increased linearly with vergence amplitude by 7.9 deg/s per degree of vergence. 3. For gaze shifts between targets placed eccentrically with respect to the midsagittal plane and at different viewing distances, the monkeys made saccades in combination with vergence eye movements. When a saccade occurred during a vergence movement, peak vergence eye speed increased abruptly and reached a peak that was proportional to the speed of the saccade. For four monkeys, peak divergence speed ranged from 242 to 315 deg/s and peak convergence speed ranged from 257 to 340 deg/s for 16-deg vergence and 20-deg saccadic eye movements. 4. For gaze shifts between far targets at the same viewing distance but different eccentricities, saccadic eye movements were transiently disjunctive even though there was no vergence requirement. Initially, the eyes diverged and then converged to restore fixation to the correct depth plane. Divergence was followed by convergence regardless of the direction of the saccade. 5. The presence of transient saccade-related disjunctive eye movements suggested that the abrupt increase in peak vergence speed during combined saccadic and vergence eye movements was produced by the linear addition of a vergence eye movement and the saccade-related transients. Consistent with this hypothesis, the rate of change in peak vergence speed during various-sized saccades between far targets (no vergence required) was similar to the rate of change in peak vergence speed during combined saccadic and vergence movements. However, the peak vergence speeds during the combined movements were higher than predicted by the linear addition hypothesis, suggesting the presence of an additional mechanism. 6. The saccade-related increase in peak vergence speed during combined saccades and vergences led to a significant decrease in the amount of time required to complete vergence movements.(ABSTRACT TRUNCATED AT 400 WORDS)     

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.     

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.     

Effects of voluntary blinks on saccades,vergence eye movements,and saccade-vergence interactions in humans

Blinks are known to change the kinematic properties of horizontal saccades, probably by influencing the saccadic premotor circuit. The neuronal basis of this effect could be explained by changes in the activity of omnipause neurons in the nucleus raphe interpositus or in the saccade-related burst neurons of the superior colliculus. Omnipause neurons cease discharge during both saccades and vergence movements. Because eyelid blinks can influence both sets of neurons, we hypothesized that blinks would influence the kinematic parameters of saccades in all directions, vergence, and saccade-vergence interactions. To test this hypothesis, we investigated binocular eye and lid movements in five normal healthy subjects with the magnetic search coil technique. The subjects performed conjugate horizontal and vertical saccades from gaze straight ahead to targets at 20 degrees up, down, right, or left while either attempting not to blink or voluntarily blinking. While following the same blink instruction, subjects made horizontal vergence eye movements of 7 degrees and combined saccade-vergence movements with a version amplitude of 20 degrees. The movements were performed back and forth from two targets simultaneously presented nearby (38 cm) and more distant (145 cm). Small vertical saccades accompanied most vergence movements. These results show that blinks change the kinematics (saccade duration, peak velocity, peak acceleration, peak deceleration) of not only horizontal but also of vertical saccades, of horizontal vergence eye movements, and of combined saccade-vergence eye movements. Peak velocity, acceleration, and deceleration of eye movements were decreased on the average by 30%, and their duration increased by 43% on the average when they were accompanied by blinks. The blink effect was time dependent with respect to saccade and vergence onset: the greatest effect occurred 100 ms prior to saccade onset, whereas there was no effect when the blink started after saccade onset. The effects of blinks on saccades and vergence, which are tightly coupled to latency, support the hypothesis that blinks cause profound spatiotemporal perturbations of the eye movements by interfering with the normal saccade/vergence premotor circuits. However, the measured effect may to a certain degree but not exclusively be explained by mechanical interference.     

Discharge of saccade-related superior colliculus neurons during saccades accompanied by vergence

It has long been believed that the superior colliculus (SC) is involved in the production of saccades but plays no role in the generation of vergence eye movements. However, results from several recent studies suggest that it may be worthwhile to examine the role of the SC in saccade-vergence interactions. Specifically, the available literature suggests two questions: do saccade-related neurons in SC have three-dimensional movement fields and is the slowing of saccades by vergence attributable, in part, to changes in the level of activity in SC? Single-unit data were recorded from 51 saccade-related neurons in rhesus monkey SC during saccades without vergence, saccades accompanied by convergence, and saccades accompanied by divergence. Most cells (78% for convergence, 86% for divergence) showed a significant reduction in peak spike density when the saccade was accompanied by vergence. A minority of cells (16% for convergence, 2% for divergence) increased their firing rate for saccades accompanied by vergence. Three cells were found that discharged in association with saccades, vergence, and the combination of the two. There were no cells that exhibited the pattern of discharge that would be expected of a cell tuned for saccades with divergence. Thus the present results do not support the hypothesis that saccade-related SC neurons are, as a rule, tuned in three dimensions. Small, but significant, differences in firing rate were often found for saccades without vergence at near and far distances. Approximately half of the cells showed a significant relationship between spike activity and saccade velocity, but the correlations tended to be very weak. This suggests that the decreased neuronal activity of SC neurons has only a limited effect on saccade velocity. For some cells, the movement field shifted for saccades with vergence. These shifts were highly variable from one cell to another.     

Saccade-vergence interactions in humans.

1. We recorded eye movements in four normal human subjects during refixations between targets calling for various combinations of saccades and vergence. We confirmed and extended prior observations of 1) transient changes in horizontal ocular alignment during both pure horizontal saccades (relative divergence followed by relative convergence) and pure vertical saccades (usually divergence for upward and convergence for downward saccades); 2) occasional, high-frequency (20-25 Hz), conjugate oscillations along the axis orthogonal to the main saccade; and 3) the speeding up of horizontal vergence by both horizontal and vertical saccades. 2. To interpret these findings, we developed a hypothesis for the generation of vergence to step changes in target depth, both with and without associated saccades. The essential features of this hypothesis are 1) the transient changes in horizontal ocular alignment during pure horizontal saccades reflect asymmetries in the mechanical properties of the lateral and medial rectus muscles causing adduction to lag abduction; 2) pure vergence movements in response to step changes in target depth are generated by a neural network that uses a desired change in vergence position as its input command and instantaneous vergence motor error (the difference between the desired change and the actual change in vergence) to drive vergence premoter neurons; and 3) the facilitation of horizontal vergence by saccades arises from nonlinear interactions in central premotor circuits. 3. The hypothetical network for generating pure vergence to step changes in target depth is analogous in structure to the local feedback model for the generation of saccades and has the same conceptual appeal. With the assumption of a single nonlinearity describing the relationship between a vergence motor error signal and the output of the neurons that generate promoter vergence velocity commands, this model generates pure vergence movements with peak velocity-amplitude relationships and trajectories that closely match those of experimental data. 4. Several types of models are proposed for the central, nonlinear interaction that occurs when saccades and vergence are combined. Common to all models is the idea that omnidirectional pause neurons (OPN), which are thought to gate activity for saccade burst neurons, also gate activity for saccade-related vergence. In one model we hypothesize the existence of a separate class of saccade-related vergence burst neurons, which generate premotor horizontal vergence commands but only during saccades. In a second model we hypothesize separate right eye and left eye saccadic burst neurons that receive not only conjugate, but also equal but oppositely directed vergence error signals.(ABSTRACT TRUNCATED AT 400 WORDS)     

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

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)     

Interactions between gaze-evoked blinks and gaze shifts in monkeys

Rapid eyelid closure, or a blink, often accompanies head-restrained and head-unrestrained gaze shifts. This study examines the interactions between such gaze-evoked blinks and gaze shifts in monkeys. Blink probability increases with gaze amplitude and at a faster rate for head-unrestrained movements. Across animals, blink likelihood is inversely correlated with the average gaze velocity of large-amplitude control movements. Gaze-evoked blinks induce robust perturbations in eye velocity. Peak and average velocities are reduced, duration is increased, but accuracy is preserved. The temporal features of the perturbation depend on factors such as the time of blink relative to gaze onset, inherent velocity kinematics of control movements, and perhaps initial eye-in-head position. Although variable across animals, the initial effect is a reduction in eye velocity, followed by a reacceleration that yields two or more peaks in its waveform. Interestingly, head velocity is not attenuated; instead, it peaks slightly later and with a larger magnitude. Gaze latency is slightly reduced on trials with gaze-evoked blinks, although the effect was more variable during head-unrestrained movements; no reduction in head latency is observed. Preliminary data also demonstrate a similar perturbation of gaze-evoked blinks during vertical saccades. The results are compared with previously reported effects of reflexive blinks (evoked by air-puff delivered to one eye or supraorbital nerve stimulation) and discussed in terms of effects of blinks on saccadic suppression, neural correlates of the altered eye velocity signals, and implications on the hypothesis that the attenuation in eye velocity is produced by a head movement command.     

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     

The brain stem saccadic burst generator encodes gaze in three-dimensional space

When we look between objects located at different depths the horizontal movement of each eye is different from that of the other, yet temporally synchronized. Traditionally, a vergence-specific neuronal subsystem, independent from other oculomotor subsystems, has been thought to generate all eye movements in depth. However, recent studies have challenged this view by unmasking interactions between vergence and saccadic eye movements during disconjugate saccades. Here, we combined experimental and modeling approaches to address whether the premotor command to generate disconjugate saccades originates exclusively in "vergence centers." We found that the brain stem burst generator, which is commonly assumed to drive only the conjugate component of eye movements, carries substantial vergence-related information during disconjugate saccades. Notably, facilitated vergence velocities during disconjugate saccades were synchronized with the burst onset of excitatory and inhibitory brain stem saccadic burst neurons (SBNs). Furthermore, the time-varying discharge properties of the majority of SBNs (>70%) preferentially encoded the dynamics of an individual eye during disconjugate saccades. When these experimental results were implemented into a computer-based simulation, to further evaluate the contribution of the saccadic burst generator in generating disconjugate saccades, we found that it carries all the vergence drive that is necessary to shape the activity of the abducens motoneurons to which it projects. Taken together, our results provide evidence that the premotor commands from the brain stem saccadic circuitry, to the target motoneurons, are sufficient to ensure the accurate control shifts of gaze in three dimensions.     

Pontine omnipause activity during conjugate and disconjugate eye movements in macaques

Previous reports have shown that saccades executed during vergence eye movements are often slower and longer than conjugate saccades. Lesions in the nucleus raphe interpositus, where pontine omnipause neurons (OPNs) are located, were also shown to result in slower and longer saccades. If vergence transiently suppresses the activity of the OPNs just before a saccade, then reduced presaccadic activity might mimic the behavioral effects of a lesion. To test this hypothesis, 64 OPNs were recorded from 7 alert rhesus monkeys during smooth vergence and saccades with and without vergence. The firing rate of many OPNs was modulated by static vergence angle but not by version and showed transient changes during slow vergence without saccades. This modulation was smooth, and not the abrupt pause seen for saccades, indicating that OPNs do not act as gates for vergence commands. We confirmed that saccades made during both convergence and divergence are significantly slower and longer than conjugate saccades. OPNs paused for all saccades, and the pause lead (interval between pause onset and saccadic onset) was significantly longer for saccades with convergence, in agreement with our hypothesis. Contrary to our hypothesis, pause lead was not longer for saccades with divergence, even though these saccades were slowed as much as those occurring during convergence. Furthermore, there was no significant correlation, on a trial-by-trial basis, between pause lead and saccadic slowing. These results suggest that it is unlikely that presaccadic slowing of OPNs is responsible for the slower saccades seen during vergence movements.     

Dynamics of abducens nucleus neuron discharges during disjunctive saccades

In this report, we provide the first characterization of abducens nucleus neuron (ABN) discharge dynamics during horizontal disjunctive saccades. These movements function to rapidly transfer the visual axes between targets located at different eccentricities and depths. Our primary objective was to determine whether the signals carried by ABNs during these movements are appropriate to drive the motion of the eye to which they project. We also asked whether ABNs encode eye movements similarly during disjunctive saccades and disjunctive fixation. To address the first objective we 1) assessed whether we could predict the discharge dynamics of individual neurons during disjunctive saccades based on their discharge properties during conjugate saccades and 2) directly estimated the sensitivity of individual neurons to either the ipsilateral/contralateral eye or the conjugate/vergence position and velocity using bootstrap statistics. Our main finding was that during disjunctive saccades in the direction ipsilateral to the recording site (ON-direction), the majority of ABNs preferentially encoded the velocity and the position of the ipsilateral eye. The remaining neurons predominantly encoded the conjugate motion of the eyes (i.e., were equally sensitive to the motion of both eyes). Generally, ipsilateral/contralateral eye based models better described neuronal discharges than conjugate/vergence based models, yet both model structures yielded similar conclusions. Moreover, the preferred eye of individual neurons based on their position and velocity sensitivities were generally well matched. We also found that for saccades in the OFF-direction, the pausing behavior of ABNs was similar during conjugate and disjunctive saccades, with the exception that for movements of small amplitudes, more ABNs paused during conjugate saccades. Finally, we found that putative motoneurons and internuclear neurons encoded ON- and OFF-direction disjunctive saccades in a similar manner. To address our second objective, we compared the discharge properties of individual ABNs during disjunctive saccades and disjunctive fixation. Good coherence was observed between the preferred eye of individual ABNs during the two behaviors. Taken together, our results indicate that although individual ABNs can encode the motion of both eyes to various degrees, the population drive of ABNs accounts for most of the movement of the ipsilateral eye during disjunctive saccades and disjunctive fixation.     

Goal-directed arm movements change eye-head coordination

We compared the head movements accompanying gaze shifts while our subjects executed different manual operations, requiring gaze shifts of about 30°. The different tasks yielded different latencies between gaze shifts and hand movements, and different maximum velocities of the hand. These changes in eye-hand coordination had a clear effect on eye-head coordination: the latencies and maximum velocities of head and hand were correlated. The same correlation between movements of the head and hand was also found within a task. Therefore, the changes in eye-head coordination are not caused by changes in the strategy of the subjects. We conclude that head movements and saccades during gaze shifts are not based on the same command: head movements depend both on the actual saccade and on possible future gaze shifts.     

Electrical stimulation of the supplementary eye fields in the head-free macaque evokes kinematically normal gaze shifts

The supplementary eye fields (SEFs), located on the dorsomedial surface of the frontal cortex, are involved in high-level aspects of saccade generation. Some reports suggest that the same area could also be involved in the generation of motor commands for the head. If so, it is important to establish whether this structure encodes eye and head commands separately or gaze commands that give rise to coordinated eye-head movements. Here we systematically stimulated (50 microA, 300 Hz, 200 ms) the SEF of two head-free (head unrestrained) macaques while recording three-dimensional eye and head rotations. A total of 55 sites were found to consistently elicit saccade-like gaze movements, always in the contralateral direction with variable vertical components, and ranging in average amplitude from 5 to 60 degrees. These movements were always a combination of eye-in-head saccades and head-in-space movements. We then performed a comparison between these movements and natural gaze shifts. The kinematics of the elicited movements (i.e., their temporal structure, their velocity-amplitude relationships, and the relative contributions of the eye and the head as a function of movement amplitude) were indistinguishable from those of natural gaze shifts. Additionally, they obeyed the same three-dimensional constraints as natural gaze shifts (i.e., eye-in-head movements obeyed Listing's law, whereas head- and eye-in-space movements obeyed Donders' law). In summary, gaze movements evoked by stimulating the SEF were indistinguishable from natural coordinated eye-head gaze shifts. Based on this we conclude that the SEF explicitly encodes gaze and that the kinematics aspects of eye-head coordination are implicitly specified by mechanisms downstream from the SEF.     

Tests of two hypotheses to account for different-sized saccades during disjunctive gaze shifts

Rapid shifts of the point of visual fixation between objects that lie in different directions and at different depths require disjunctive eye movements. We tested whether the saccadic component of such movements is equal for both eyes (Hering’s law) or is unequal. We compared the saccadic pulses of abducting and adducting movements when horizontal gaze was shifted from a distant to a near target aligned on the visual axis of one eye (Müller paradigm) in ten normal subjects. We similarly compared horizontal saccades made between two distant targets lying in the same field of movement as during the Müller paradigm tests, and between targets lying symmetrically on either side of the midline, at near side of the midline, at near or far. We measured the ratio of the amplitude of the movements of each eye in corresponding directions due to the saccadic component, as well as corresponding ratios of peak velocity and peak acceleration. In response to a Müller test paradigm requiring about 17° of vergence, the change in position of the unaligned eye was typically twice the size of the corresponding movement of the aligned eye. The ratio of peak velocities for the unaligned/aligned eyes was about 1.5, which was greater than for saccades made between distant targets. The ratio of peak acceleration for unaligned/aligned eyes was about 1.0 during shifts from near to far and about 1.3 for shifts from far to near, these values being similar to corresponding ratios for saccades between distant targets. These measurements of peak acceleration indicate that the saccadic pulses sent to each eye during the Müller paradigm are more equal than would be deduced by comparing the changes in eye position. We retested five subjects to compare directly the peak acceleration of saccades made during the Müller paradigm with similar-sized ”conjugate” saccades made between targets at optical infinity. Saccades made during the Müller paradigm were significant slower (P<0.005) than similar-sized conjugate saccades; this indicated that the different-sized movements during Müller paradigm are not simply due differences in saccadic pulse size but are also influenced by the concurrent vergence movement. A model for saccade-vergence interactions, which incorporates equal saccadic pulses for each eye, and differing contributions from convergence and divergence, accounts for many of these findings. Received: 31 December 1998 / Accepted: 14 July 1999     

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.     

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.     

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.