Functional anatomy of predictive vergence and saccade eye movements in humans: A functional MRI investigation

Purpose

The purpose of this study is to investigate the functional neural anatomy that generates vergence eye movement responses from predictive versus random symmetrical vergence step stimuli in humans and compare it to a similar saccadic task via the blood oxygenation level dependent signal from functional MRI.

Methods

Eight healthy subjects participated in fMRI scans obtained from a 3 T Siemens Allegra scanner. Subjects tracked random and predictable vergent steps and then tracked random and predictable saccadic steps each within a block design. A general linear model (GLM) was used to determine significantly (p < 0.001) active regions of interest through a combination of correlation threshold and cluster extent. A paired t-test of the GLM beta weight coefficients was computed to determine significant spatial differences between the saccade and vergence data sets.

Results

Predictive saccadic and vergent eye movements induced many common sites of significant functional cortical activity including: the dorsolateral prefrontal cortex (DLPFC), parietal eye field (PEF), cuneus, precuneus, anterior and posterior cingulate, and the cerebellum. However, differentiation in spatial location was observed within the frontal lobe for the functional activity of the saccadic and vergent network induced while studying prediction. A paired t-test of the beta weights from the individual subjects showed that peak activity induced by predictive versus random vergent eye movements was significantly (t > 2.7, p < 0.03) more anterior within the frontal eye field (FEF) and the supplementary eye field (SEF) when compared to the functional activity from predictive saccadic eye movements.

Conclusion

This research furthers our knowledge of which cortical sites facilitate a subject’s ability to predict within the vergence and saccade networks. Using a predictive versus random visual task, saccadic and vergent eye movements induced activation in many shared cortical sites and also stimulated differentiation in the FEF and SEF.     

Binocular eye movements during accommodative vergence

Binocular eye position was monitored by the photoelectric technique during accommodative vergence. Contrary to previous reports indicating that accommodative vergence was a uniocular phenomenon, without exception, binocular accommodative vergence movements were recorded. The total vergence amplitude in the viewing eye was reduced, on the average, by approximately 88% with respect to the vergence movement measured in the covered eye. Some saccadic eye movements that occurred during vergence movements were likewise reduced in amplitude in the viewing eye by up to 20%. Smooth eye movements were utilized to counteract the vergence movement in the viewing eye. This smooth movement alone, or in conjunction with a late saccade, returned the eye to the target and helped to maintain the retinal image of the target coincident with the foveal center for the duration of the accommodative vergence movement. Thus, there appears to be a fixation-holding mechanism which produced a general attenuation of both vergence and some saccadic movements in the viewing eye. Although this control strategy produced violations of Hering's law with respect to the magnitude of the movements in the eyes but not with respect to the direction of the movement, it was implemented in the interest of retaining the target within the sensitive foveal region.     

Dynamic vergence eye movements in strabismus and amblyopia: asymmetric vergence.

This report investigates line-of-sight asymmetric disparity vergence in patients having either intermittent strabismus, constant strabismus with amblyopia, or amblyopia without strabismus. We find an absence of disparity vergence in all patients with strabismus and in some with amblyopia only. Accommodative vergence and saccades place the dominant eye on the targets moving in depth. These accommodative vergence responses have normal dynamic characteristics, thus indicating a properly functioning vergence motor system. We purpose there is a higher-level central defect in which incoming information of one eye is suppressed, so that the disparity vergence system is rendered inoperable.     

Rapid and slow-velocity vergence eye movements *

Previously we have measured rapid-velocity vergence responses to targets at different distances that provided no disparity or accommodative stimulation. To evaluate the possibility that this rapid-velocity vergence occurs during succades. the latencies or eye movement between two long dim luminous rods were compared under two conditions. Rapid-velocity vergence with an average latency of ≈300ms was elicited when subjects alternately viewed horizontal rods at distances of 38 and 78 cm, and with a vertical separation of 5.2°. Horizontal saccades with a comparable latency were measured when the rods were equidistant and oriented vertically. The correlation between the mean latencies of vergence and saccadic movements was 0.97, sugesting that the two movements occurred together. In a second experiment vegence responses were measured when the subject looked between u bright vertical line on a screen at 76cm and ii second pair of lines (vertically displaced between 0.15 and 3°) with crossed disparity to simulate a target al 38cm. Slow-velocity vergence often occurred alone when the vertical separation between targets was small: rapid-velocity vergence intruded when the separation between the targets was larger. The results can be accounted for if proximity and disparity stimulation act through a single vergence controller, the output of which produces slow- or rapid-velocity vergence depending upon whether the saccadic system is concurrently active.     

Closed-loop and open-loop accommodative vergence eye movements

We examined accommodative vergence eye movements under conditions in which feedback about retinal-image slip was and was not present (i.e. closed-loop and open-loop conditions). We found that (a) in both conditions the two eyes started to move at the same time; (b) in the open-loop condition, vergence continued in both eyes; and (c) in the closed-loop condition, vergence continued in the occluded eye only, and the magnitude and velocity exceeded that of the occluded eye in the open-loop condition by a factor of two.     

Latency of saccades, vergence and combined saccade vergence movements in a subject with manifest latent nystagmus

PURPOSE: To study eye movements in 3D space - saccades, vergence and combined eye movements - in a subject with Manifest Latent Nystagmus (MLN). METHODS: A 13-year-old girl diagnosed with MLN participated in this study. Saccades, pure vergence along the median plane and combined saccade-vergence movements were recorded under both binocular and monocular viewing. Horizontal eye movements from both eyes were recorded simultaneously with a photoelectric device (Bouis Oculometer). RESULTS: The recordings of saccades, vergence or both components of combined movements show that such movements have a staircase trajectory. The consequence of this staircase behavior is that the time for approaching the target is prolonged. The latency of all types of eye movements is extended when the subject is viewing binocularly, while latency values are normal when viewing monocularly; the difference between the viewing conditions is significant for vergence. CONCLUSION: The normal latency values under monocular viewing are attributed to facilitation of eye movement initiation by the increased nystagmus.     

Additivity of fuslonal vergence and pursuit eye movements

We measured binocular eye movements photoelectrically while subjects tracked a target moving smoothly along a horizontal path in the fronto-parallel plane, with interpolated step changes in depth. By measuring eye movement speeds when only fusional vergence or only pursuit was required we were able to ascertain how the vergence and pursuit movements combined when called out together. When the two were in opposite directions the net eye movement speed was equal to the difference of the vergence and pursuit components, reflecting perfect additivity. When vergence and pursuit were in the same direction a significant deviation from strict additivity was found, i.e. the combined eye movements were on average 11% slower than expected. We speculate that this attenuation may be peripheral in origin.     

Mechanical interdependence of version and vergence eye movements

In this paper, the authors investigate whether the idea of independent control of version and vergence eye movements is compatible with the mechanics of the eye plant. By computing the change in the axes of action of the eye muscles as a function of ocular vergence, they prove that, regardless of the muscle pulley locations, the required muscle activity for vertical version depends on the initial vergence angle. The binocular extension of Listing’s law (‘L2’) describes how the torsional orientation of the eye depends on both gaze direction and ocular convergence. The authors show that for each vergence angle there is a range of possible muscle pulley locations that would cause independent control of version and vergence to result in L2. They also show that this mechanical explanation of L2 requires that the muscle pulleys move as a function of vergence.     

Mechanical interdependence of version and vergence eye movements

In this paper, the authors investigate whether the idea of independent control of version and vergence eye movements is compatible with the mechanics of the eye plant. By computing the change in the axes of action of the eye muscles as a function of ocular vergence, they prove that, regardless of the muscle pulley locations, the required muscle activity for vertical version depends on the initial vergence angle. The binocular extension of Listing's law ('L2') describes how the torsional orientation of the eye depends on both gaze direction and ocular convergence. The authors show that for each vergence angle there is a range of possible muscle pulley locations that would cause independent control of version and vergence to result in L2. They also show that this mechanical explanation of L2 requires that the muscle pulleys move as a function of vergence.     

Initial control component in disparity vergence eye movements

Recent experimental evidence indicates that a portion of the oculomotor response to disparity stimulation is functionally open-loop; that is, the response occurs without the aid of visual feedback. To investigate the stimulus features that elicit or influence this dynamic movement, convergence responses to a step, a step followed by target disappearance, and a pulse followed by target disappearance were obtained from four subjects using infrared oculography. The target was a thin vertical line (0.25) either 2 or 10 in height. Stimuli having different amplitudes (1. 2, 4 and 8) and disappearance times (50. 100 and 200ms) were selected randomly along with occasional divergent stimuli to minimize prediction and voluntary vergence. Experiments showed that the dynamic characteristics of the initial portion of the response were essentially the same, even when the target disappeared before the movement took place. The magnitude of the initial response depended on the stimulus amplitude, but was not influenced by either stimulus duration or target height. For example, stimulus durations as short as 50 ms elicited responses similar to those caused by standard steps. The initial response was shown to be active over a well-defined time period of about 200 ms. after which the response appears to be mediated by a visually-guided control component. These results support the recently developed dual-mode theory of vergence control in which an initial preprogrammed (open-loop) control component is followed by a feedback (closed-loop) controlled component which reduces any remaining disparity.     

The accommodative contribution to binocular vergence eye movements

Forced vergence fixation disparity curves were generated for both with and without an accommodative stimulus (accommodative closed and open loop conditions respectively) for fifteen asymptomatic subjects. All subjects exhibited an exophoric shift in fixation disparity for the accommodative open loop condition at the forced convergence side of the curve. No corresponding bias was found at the forced divergence side of the curve. The findings are discussed in terms of the results of previous studies and the existing models of vergence eye movements.     

Inhibition of saccade initiation improves saccade accuracy: The role of local and remote visual distractors in the control of saccadic eye movements

When a distractor appears close to the target location, saccades are less accurate. However, the presence of a further distractor, remote from those stimuli, increases the saccade response latency and improves accuracy. Explanations for this are either that the second, remote distractor impacts directly on target selection processes or that the remote distractor merely impairs the ability to initiate a saccade and changes the time at which unaffected target selection processes are accessed. In order to tease these two explanations apart, here we examine the relationship between latency and accuracy of saccades to a target and close distractor pair while a remote distractor appears at variable distance. Accuracy improvements are found to follow a similar pattern, regardless of the presence of the remote distractor, which suggests that the effect of the remote distractor is not the result of a direct impact on the target selection process. Our findings support the proposal that a remote distractor impairs the ability to initiate a saccade, meaning the competition between target and close distractor is accessed at a later time, thus resulting in more accurate saccades.     

Induced motion in depth and the effects of vergence eye movements

Induced motion is the false impression that physically stationary objects move when in the presence of other objects that really move. In this study, we investigated this motion illusion in the depth dimension. We raised three related questions, as follows: (1) What cues in the stimulus are responsible for this motion illusion in depth? (2) Is the size of this illusion affected by vergence eye movements? And (3) are the effects of eye movements different for motion in depth and for motion in the frontoparallel plane? To answer these questions, we measured the point of subjective stationarity. Observers viewed an inducer target that oscillated in depth and a test target that was located directly above it. The test target moved in phase or out of phase with the inducer, but with a smaller amplitude. Observers had to indicate whether the test target and the inducer target moved in phase or out of phase with one another. They were asked to keep their eyes either on the test target or on the inducer. For motion in depth, created by binocular disparity and retinal size change or by binocular disparity alone, we found that when the eyes followed the inducer, subjective stationarity occurred at approximately 40-45% of the inducer's amplitude. When the eyes were kept fixated on the test target, the bias decreased tenfold to around 4%. When size change was the only cue to motion in depth, there was no illusory motion. When the eyes were kept on an inducer moving in the frontoparallel plane, induced motion was of the same order as for induced motion in depth, namely, approximately 44%. When the induced motion was in the frontoparallel plane, we found that perceived stationarity occurred at approximately 23% of inducer's amplitude when the eyes were kept on the test target.     

The influence of repetitive eye movements on vergence performance

We measured the peak velocity of convergence eye movement responses in four normal subjects before and after a large number of either repetitive vergence or repetitive saccadic eye movements. A 20% decrease in the mean value of peak velocity was observed in vergence responses after 100 repetitive step vergence eye movements. However, 100 cycles of slow sinusoidal vergence tracking did not induce any notable change in vergence dynamics. Five hundred repetitive saccadic eye movements also caused an approximately 20% decrease in peak velocity. The reduction in peak velocity was related to the number of repetitions for both vergence and saccadic fatiguing stimuli. The frequency of occurrence of double-vergences was also used as an index to monitor the influence of repetitive eye movements on convergence performance. Results showed that repetitive step convergence movements could double, or even triple, the frequency of the occurrence of double-vergence responses, while slow sinusoidal vergence tracking or repetitive saccades had no influence on the frequency of response doubles.     

Short term modification of disparity vergence eye movements.

Dynamics of disparity vergence eye movements can be modified by adaptive stimuli that generate large transient disparities. These modifications were observed for convergence as well as divergence eye movements. After modification, the peak velocities of the step responses for convergence and divergence were substantially higher than in normal baseline responses, a change observed in all four subjects studied. The change in peak velocity of a step response occurred very rapidly after presentation of the adaptive stimuli. Main sequence plots showed that first-order dynamic characteristics increased for post-adaptive responses with respect to normal step responses. Hence, response modification could be quantified as a change in gain accompanied with an increase in the effective response time constant. The adaptive responses to convergent and divergent 'disappearing' step stimuli revealed that the adaptation process modifies the high-velocity component of both disparity convergence and divergence eye movements. Moreover, a gain change in this component alone could account for both the gain and the time constant modifications seen in the overall response. A process of recovery or de-adaptation was also observed for both convergence and divergence eye movements. This observed short-term modification demonstrates a unique control mechanism for vergence eye movements that is effective in either direction.     

Interaction between saccade and tracking vergence

Additivity of saccade and tracking vergence was examined. Binocular eye movements were measured photoelectrically while subjects tracked a target moving smoothly on a radial line with an interpolated step change to a new radial line. Examining the abrupt portions of the two eyes' movements, we found the durations were almost the same for the two eyes, but that there were reliable differences in the magnitudes which were too large to be understood by an additivity hypothesis.     

The relationship between fusional vergence eye movements and fixation disparity

The fusional vergence system is under the control of a fast neural integrator which aligns the eyes and a slow neural integrator which maintains binocular alignment. These controllers are distinguished by their decay time constants and their stimuli. Previous studies indicate that the fast fusional vergence controller responds to retinal image disparity and the slow fusional vergence controller responds to the output of the fast neural integrator. Slow fusional vergence as evidenced by adaptation of the phoria is unaffected by accommodative vergence when disparity vergence is open loop. Under closed loop conditions both accommodation and disparity induced vergence influence slow fusional vergence. These results indicate that the slow vergence controller is located before the site of interaction between convergence and accommodation. Fixation disparity is described as a steady-state error of the neural integrator controlling fast fusional vergence and its amplitude is shown to be inversely related to adaptation of the phoria to prism.     

On Pulfrich-illusion eye movements and accommodation vergence during visual pursuit

When the Pulfrich illusion is perceived with stationary fixation, and visual pursuit of the pendulum is then initiated, rapid vergence changes occur which correspond to the illusory elliptical path. During steady-state visual tracking of the illusion, however, the eyes move along a planar path without systematic changes in vergence. These latter pursuit movements with monocular filter involve large fixation disparities relative to unobstructed vision (0.5 degree to 1 degree divergence); hence, it is proposed that the planar tracking path probably results from strong dominance of the oculomotor system by stimuli from the unobstructed eye. During visual tracking with monocular filter and a target moving along a nonillusory elliptical path in depth, appropriate changes in vergence occur, but comparable vergence changes also arise when the target is fully hidden from one eye. This response apparently represents a superposition of accommodation vergence upon smooth pursuit movements; similar responses also occur during monocular tracking of a target moving around a circular path in depth.     

Short-term predictive changes in the dynamics of disparity vergence eye movements

Repetitive stimulation of the disparity vergence system to large convergent step stimuli has been shown to increase the dynamics of subsequent responses to smaller step stimuli. Here we show that decreases in the dynamics of both disparity convergence and divergence eye movements can be induced using a frequently occurring small amplitude conditioning stimulus to modify responses to a larger, occasionally presented test stimulus. In one experiment, a simple conditioning stimulus consisting of repetitive 1 degrees step stimuli was used to modify the dynamic vergence response to an occasional 4 degrees step test stimulus. An experimental trial consisted of three phases: baseline, conditioning, and recovery. The baseline and recovery phases used only the 4 degrees test stimuli. The dynamic characteristics of the responses to test stimuli were quantified by measuring the magnitude of the peak velocity. A statistically significant change was observed between the dynamics of conditioned responses compared to baseline and recovery responses indicting modification by the conditioning stimuli. During recovery, the response dynamics returned to levels near baseline levels showing that the decrease in response dynamics was caused by the conditioning stimulus, not fatigue. Another experiment showed that the response dynamics to large stimuli could be decreased whereas the dynamics of small stimuli could be increased by the same intermediate conditioning stimulus. Other experiments suggest that the modifications are due to a predictive mechanism. The results indicate that the dynamics of disparity vergence eye movements are malleable and depend to some extent on the amplitude of preceding stimuli.