Initial Vergence Responses Research Articles

Human vergence eye movements initiated by competing disparities: Evidence for a winner-take-all mechanism

Vergence eye movements were elicited in human subjects at short latencies (∼70 ms) by applying binocular disparities briefly (200 ms) to large grating patterns (46° wide, 35° high). The positions of both eyes were recorded with the electromagnetic search coil technique. Using a dichoptic viewing arrangement (Wheatstone stereoscope), each eye viewed two overlapping 1-D sine waves that had the same orientation but different spatial frequencies. These two sine waves each had a binocular disparity that was 1/4 of its wavelength and the effect of varying their relative contrasts was examined (15 contrast ratios ranging from 0.125 to 8). The first experiment used horizontal gratings and recorded the vertical vergence responses when the two sine waves had spatial frequencies in the ratio 3:5 and vertical disparities of opposite sign. Initial vergence responses showed a highly nonlinear dependence on the contrast ratio. On average, when the contrast of one sine wave exceeded that of the other by a factor of >2.2, the sine wave with the higher contrast dominated responses and the sine wave with the lower contrast had almost no influence: winner-take-all. A second experiment, which used vertical gratings and recorded the horizontal vergence responses when the two sine waves had spatial frequencies in the ratio 3:5 and horizontal disparities of opposite sign, also uncovered nonlinear interactions but these were much more variable from one subject to another and, on average, one sine wave did not achieve complete dominance until its contrast exceeded that of the other by a factor of >4.5. When these two experiments were repeated with grating patterns in which the two sine waves had spatial frequencies in the ratio 3:7 and disparities of the same sign, similar nonlinear interactions were apparent. We attribute the nonlinear dependence on relative contrast to mutual inhibition between the neural elements processing the disparities of the two sine waves. We further suggest that this interaction will help to maintain binocular alignment on the objects in the plane of regard because the retinal images of those objects will tend to be better focused—and hence tend to have higher contrasts—than the images of objects in other depth planes.

Eye-Movement Responses to Disparity Vergence Stimuli with Artificial Monocular Scotomas

The effects of artificial monocular scotomas on eye-movement responses to horizontal disparity vergence stimuli were studied in six subjects with normal binocular vision. Subjects viewed stereoscopic 1.5° horizontal step disparity vergence stimuli through liquid crystal shutter glasses. The central portion of the stimulus presented to the right eye was removed to simulate monocular artificial scotomas of variable diameters (2° to 10°). Eye movements were recorded with a binocular head-mounted eye tracker. Responses included pure vergence, vergence followed by saccades, and pure saccadic eye movements. The rate of responses with saccadic eye movements increased with the diameter of the artificial scotoma (p < 0.0001); there was an increase in the rate of responses starting with saccades (p < 0.0001), as well as an increase in the rate of saccades after initial vergence responses (p < 0.01). The probability of saccades after initial vergence responses was affected by the open-loop gain of the vergence response (p < 0.001). The open-loop gain decreased with increased diameters of the artificial scotomas (p < 0.0001). As the diameter of the artificial scotomas increased, the amplitude of the initial vergence eye-movement responses decreased, and the prevalence of saccadic eye movements and asymmetric vergence increased. The effects of the diameter of artificial monocular scotomas on eye-movement responses in subjects with normal binocular vision are consistent with the effects of diameter of suppression scotomas on eye-movement responses to disparity vergence stimuli in patients with infantile esotropia.

Relation between static and dynamic aspects of vergence, estimated with a subjective test using flashed dichoptic nonius lines.

The psychophysical technique for measuring vergence with dichoptic nonius lines was used to investigate dynamic responses to step vergence stimuli. Liquid crystal shutter glasses were operated with a cathode ray tube monitor to present convergent or divergent step stimuli of 32 min arc at t = 0. The resulting initial vergence response was estimated with nonius lines that appeared for 80 ms at a fixed delay of 400 ms after the vergence step stimulus. The vergence state reached 400 ms after the step depended on the vergence accuracy assumed before the step, i.e. baseline fixation disparity (FD). The following physiologically plausible results were found: (i) the amount of dynamic vergence changes within 400 ms tended to be negatively correlated between the convergent and divergent direction; (ii) subjects with a smaller convergent dynamic change had a steeper proximity-FD curve measured with static fusion targets as a function of viewing distance; (iii) FD was more eso or more exo depending on whether the vergence change was larger in the convergent or divergent direction respectively.

Central and peripheral visual interactions in disparity-induced vergence eye movements: I. Spatial interaction.

To evaluate the interaction between central and peripheral disparities in the initiation of vergence eye movements. Eye movements were recorded in eight normal subjects using an infrared limbus tracker. Three-dimensional visual stimuli were back projected onto a tangent screen by using two liquid crystal display (LCD) projectors through crossed polarizers. The central target was a vertical bar, which always jumped from 2 to 1 m. The peripheral target was a random-dot pattern that jumped from 2 to 0.75, 1, or 1.5 m (near planes), 2 m (no change), or 3 m (far plane) simultaneously with the central target jump. Latency, amplitude at 150 ms, and average amplitude over 1 to 2 seconds after vergence onset; peak velocity; and the main-sequence relationship of the initial vergence response were calculated. How far the central target appeared to jump was scored subjectively. In half of the subjects, there was a clear effect of the peripheral disparity on the dynamics of the vergence response to the central disparity. The amplitude of vergence at 150 ms, as an index of open-loop gain, was significantly greater when the peripheral target moved closer, but steady state amplitude (average during 1-2 seconds) did not change, and the vergence latency was significantly greater when the peripheral target jumped away. There was no obvious relationship between the perceived amount of movement of the central target and the parameters of the dynamic properties of the vergence response. Peripheral disparity can modulate the dynamics of the initial vergence response to a central disparity and is probably independent of the perception of motion in depth.

Short-latency disparity-vergence eye movements in humans: sensitivity to simulated orthogonal tropias

Small disparity stimuli applied to large random-dot patterns elicit machine-like vergence eye movements at short latency. We have examined the sensitivity of these eye movements to simulated orthogonal tropias in three normal subjects by recording (1) the effects of vertical disparities on the initial horizontal vergence responses elicited by 2° crossed and uncrossed (horizontal) disparity stimuli, and (2) the effects of horizontal disparities on the initial vertical vergence responses elicited by 1.2° left-hyper and 0.8° right-hyper (vertical) disparity stimuli. Initial vergence responses were strongest when the orthogonal disparity was close to zero, and decreased to zero as the orthogonal disparity increased to 3°–5°, i.e., there was only a limited tolerance for orthogonal disparity. Tuning curves describing the dependence of the initial change in the vergence angle on the orthogonal disparity were well fit by a Gaussian function. An additional subject, who had an esotropia of ∼10° in our experimental setup, showed almost no horizontal vergence responses but did show vertical vergence responses to vertical disparity stimuli at short latency (albeit slightly longer than normal) despite the fact that her esotropia resulted in uncrossed disparities that would have totally disabled the vertical vergence mechanism of a normal subject, cf., anomalous retinal correspondence.

Population coding in cortical area MST.

Disparity steps applied to large patterns elicit vergence eye movements at ultrashort latencies. Disparity tuning curves, describing the dependence of the amplitude of the initial vergence responses on the amplitude of the disparity steps, resemble the derivative of a gaussian and indicate that appropriate servo-like behavior occurs only with small disparity steps (<1 degree). Lesion data from monkeys suggest that these vergence responses are mediated, at least in part, by neurons in the medial superior temporal area of the cerebral cortex, and we here review a recent study of the associated single unit activity in that area. Few medial superior temporal neurons have disparity tuning curves whose shapes resemble the tuning curve for vergence. Yet, when the disparity tuning curves for all of the disparity-sensitive cells recorded from a given monkey are summed together, they match the tuning curves for the vergence responses of that monkey very closely, even reproducing that animal's idiosyncracies. When all of the spike trains elicited by a given disparity step are summed together to give an average discharge profile for the whole population of recorded cells, many are noisy, but others that are less so match the temporal profile of the motor response, vergence velocity, quite well. We conclude that the discharges of the disparity-sensitive cells in the medial superior temporal area each represent only a very limited aspect of the sensory stimulus (and/or associated motor response?), but when pooled together, they provide a complete description of the vergence velocity motor response: population coding.

Single-unit activity in cortical area MST associated with disparity-vergence eye movements: evidence for population coding.

Single-unit discharges were recorded in the medial superior temporal area (MST) of five behaving monkeys. Brief (230-ms) horizontal disparity steps were applied to large correlated or anticorrelated random-dot patterns (in which the dots had the same or opposite contrast, respectively, at the two eyes), eliciting vergence eye movements at short latencies [65.8 +/- 4.5 (SD) ms]. Disparity tuning curves, describing the dependence of the initial vergence responses (measured over the period 50-110 ms after the step) on the magnitude of the steps, resembled the derivative of a Gaussian, the curves obtained with correlated and anticorrelated patterns having opposite sign. Cells with disparity-related activity were isolated using correlated stimuli, and disparity tuning curves describing the dependence of these initial neuronal responses (measured over the period of 40-100 ms) on the magnitude of the disparity step were constructed (n = 102 cells). Using objective criteria and the fuzzy c-means clustering algorithm, disparity tuning curves were sorted into four groups based on their shapes. A post hoc comparison indicated that these four groups had features in common with four of the classes of disparity-selective neurons in striate cortex, but three of the four groups appeared to be part of a continuum. Most of the data were obtained from two monkeys, and when the disparity tuning curves of all the individual neurons recorded from either monkey were summed together, they fitted the disparity tuning curve for that same animal's vergence responses remarkably well (r(2): 0.93, 0.98). Fifty-six of the neurons recorded from these two monkeys were also tested with anticorrelated patterns, and all showed significant modulation of their activity (P < 0.005, 1-way ANOVA). Further, when all of the disparity tuning curves obtained with these patterns from either monkey were summed together, they too fitted the disparity tuning curve for that same animal's vergence responses very well (r(2): 0.95, 0.96). Indeed, the summed activity even reproduced idiosyncratic differences in the vergence responses of the two monkeys. Based on these and other observations on the temporal coding of events, we hypothesize that the magnitude, direction, and time course of the initial vergence velocity responses associated with disparity steps applied to large patterns are all encoded in the summed activity of the disparity-sensitive cells in MST. Latency data suggest that this activity in MST occurs early enough to play an active role in the generation of vergence eye movements at short latencies.

The area of spatial integration for initial horizontal disparity vergence.

We investigated over what central area disparity in a random dot stereogram is integrated to stimulate an initial vergence response. Vergence was measured subjectively, with a forced choice dichoptic nonius vernier task following a brief (230 msec) stimulus presentation. Stimuli were random-dot stereograms showing a central circular disc of 12.5 min arc crossed retinal disparity in front of, and occluding, a same density fixation plane surround. The size of the disc was varied. All ten observers responded to the brief stimulus. Initial vergence increased with increasing disc diameter and, for nine out of ten subjects, reached a maximum with the disc ca 6 deg, suggesting this is the extent of the spatial integration region. Below 6 deg diameter, surround and target disparities were averaged together. Initial horizontal vergence responds automatically to a cyclopean target presented in the centre of gaze by pooling disparities within a limited but surprisingly large area.