Previously we mapped stereopsis across the visual field and showed that local stereopsis is impaired in the central visual field for individuals with known stereo deficits due to anisometropia or microstrabismus, while peripheral stereopsis was spared. As disparity drives fusional vergence responses, we hypothesized that the residual sensitivity to coarse disparities in the near periphery likely drives fusional vergence eye movements. Furthermore, if stereopsis in the central foveal region is impaired, then the fusional vergence response to a small stimulus confined to the near foveal region will be reduced. We used binocular eye tracking (Eyelink 1000 in the table-mount configuration), to measure the vergence response to a disparity step as the difference in the right and left eye position signals. We measured vergence as a function of stimulus configuration and the size of the disparity step. The disparity step occurred on 3 configurations: a large disc 16°in diameter, a small disc 4° in diameter, and an annulus with outer and inner diameters corresponding to the large and small discs. After the observer aligned nonius lines, a key press initiated the disparity step that lasted 3 seconds. Individuals with anisometropia or microstrabismus (n=3) had low vergence gain for small stimuli, that sometimes increased to near normal levels for larger stimuli, consistent with abnormal stereopsis in the central visual field. Among controls with no history of amblyopia or strabismus (n=8), those with intact local stereopsis across the visual field had vergence gains near 1, for all stimulus sizes (n=4). However, the remaining observers were stereoanamolous in the central visual field, and had abnormal fusional vergence. These abnormalites were either transient (could be made normal with increased effort) or remained persistent. These results suggest that the stereo-deficiency in the central retina is associated with poor fusional drive.

I entered science at a particularly lucky time. By the mid-1960s, women were being encouraged to pursue serious scientific careers. During the 60-year span of my career, women have become equal partners with men in scientific research, particularly in the biological sciences. There also has been abundant funding for research, which allowed me to succeed in a “soft-money” position at Smith-Kettlewell Eye Research Institute, a place that was especially supportive for a woman scientist with children. In this article, I describe the findings that I think represent the most interesting and enduring scientific work from my career.

This article describes human binocular vision. While it is focused primarily on human stereopsis, it also briefly tells about other binocular functions, including binocular summation, rivalry, and vergence, the eye movement that is driven by stereopsis. Stereopsis refers to the depth perception generated by small differences in the locations of visual features in the two retinal images; these differences in retinal location are called disparities. Disparities are detected by special binocularly driven cortical neurons whose properties are outlined here; the article also describes studies that have used fMRI imaging to show that many areas of human cortex respond to depth based on disparity. The development of stereopsis in human infants, as well as clinical abnormalities in stereopsis, is also documented.

This article describes human binocular vision. While it is focused primarily on human stereopsis, it also briefly tells about other binocular functions, including binocular summation, rivalry, and vergence, the eye movement that is driven by stereopsis. Stereopsis refers to the depth perception generated by small differences in the locations of visual features in the two retinal images; these differences in retinal location are called disparities. Disparities are detected by special binocularly driven cortical neurons whose properties are outlined here; the article also describes studies that have used fMRI imaging to show that many areas of human cortex respond to depth based on disparity. The development of stereopsis in human infants, as well as clinical abnormalities in stereopsis, is also documented.

•Amblyopia is a neuro-developmental abnormality associated with deficits in a broad range of low- and high-level visual tasks.•In strabismic amblyopia, fixation is unstable and there is an increased frequency of microsaccades.•There is a close association between eye movements and attention.•We propose a novel hypothesis: that the cost of unstable fixation in amblyopia is a deficit in selective attention.•The increased latency for saccades and manual response time with amblyopic-eye viewing is consistent with this hypothesis.

Observers can identify the disparity sign (crossed or uncrossed) of briefly-presented diplopic targets (<100msec) for disparities ranging up to 14 deg (Blakemore, 1970). However, they cannot localize these targets to a particular depth. At longer durations, the half-images of targets presented with large disparities appear to lie in the fixation plane separated laterally by a distance corresponding to target disparity. Schor, Wood & Ogawa (1983) asked observers to increase target disparity until they achieved this fixation-plane percept, a disparity they called the upper depth limit. McKee, Levi & Bowne (l990) found that disparity discrimination thresholds for disparities at or beyond the upper depth limit were identical to monocular width discrimination thresholds for widths equal to the disparity(‘dichoptic width’) separating the half-images. The disparity value where dichoptic and monocular width thresholds become equivalent provides a rigorous estimate of the upper depth limit -- the point where disparity no longer produces a sense of depth nor affects visual direction. We measured disparity and width discrimination in the lower visual field to determine their equivalence point at three eccentricities (0, 5, 10 deg). The eccentricity function for this upper depth limit is surprisingly shallow, increasing at 10 deg eccentricity by only a factor of 2 from the foveal value of ~1.7 deg. We speculate that the narrow range of disparities that support a depth percept, even at eccentric loci, reflects the limited range of disparities generated by features in the natural world.

Stereopsis is important for tasks of daily living such as eye-hand coordination. It is best in central vision but is also mediated by the periphery. Previously we have shown that individuals with central-field loss who have residual stereopsis in the periphery perform better at an eye-hand-coordination task when they perform the task binocularly rather than monocularly. Here we seek to determine what sets the limit of stereopsis, defined as the largest disparity that supports the sustained appearance of depth, in the near periphery in healthy individuals. While stereoacuity thresholds increase sharply with eccentricity, Panum's area increases much more slowly. We used a rigorous method to determine the uppermost limit of disparity. At long durations, the two half-images that define a large disparity appear as two isolated targets in the same flat plane; small incremental changes in disparity produce changes in the separation between the half-images, and disparity magnitude can be judged on the basis of separation, like a monocular width judgment. The disparity limit is the point at which the threshold for judging dichoptic separation between the half-images is equal to the monocular width-discrimination threshold. The disparity limit at 10° was a factor of 2-4 times larger than the fovea, regardless of the meridian tested. The increase in the disparity limit with eccentricity was shallow, similar to that of Panum's area. Within this disparity limit, disparity increment thresholds were comparable for foveal and peripheral targets, illustrating the significance and utility of peripheral stereopsis, especially in the absence of foveal stereopsis.

Abnormal early visual development can result in a constellation of neural and visual deficits collectively known as amblyopia. Among the many deficits, a common finding is that both saccadic and manual reaction times to targets presented to the amblyopic eye are substantially delayed when compared to the fellow eye or to normal eyes. Given the well-known deficits in contrast sensitivity in the amblyopic eye, a natural question is whether the prolonged reaction times are simply a consequence of reduced stimulus visibility. To address this question, in Experiment 1 we measure saccadic reaction times (RT) to perifoveal stimuli as a function of effective stimulus contrast (i.e., contrast scaled by the amblyopic eye's contrast threshold). We find that when sensory differences between the eyes are minimized, the asymptotic RTs of our anisometropic amblyopes were similar in the two eyes. However, our results suggest that some strabismic amblyopes have an irreducible delay at the asymptote. That is, even when the sensory differences of the stimulus were accounted for, these observers still had large interocular differences (on average, 77 ms) in saccadic reaction time. In Experiment 2, to assess the role of fixation on saccadic reaction time we compared reaction time with and without a foveal target (the “gap effect”). Our results suggest that, while removing the fixation target does indeed speed up reaction time in the amblyopic eye, the gap effect is similar in the two eyes. Therefore, the gap effect does not eliminate the irreducible delay in the amblyopic eye. Finally, in Experiment 3 we compared the interocular differences in saccadic and manual reaction times in the same observers. This allowed us to determine the relationship between the latencies in the two modalities. We found a strong correlation between the differences in saccadic and manual reaction times; however, the manual RT difference is about half that of saccadic RT, suggesting that there may be two separable effects on saccadic reaction time: (a) a central problem with directing actions to a target, related to disengagement of attention at the fovea, which results in delays in both saccadic and manual reaction times, and (b) a further delay in saccadic reaction times because of the motor refractory period from a previous saccade or microsaccade, made in an attempt to stabilize the amblyopic eye of strabismics.

Amblyopia is a developmental disorder that affects the spatial vision of one or both eyes in the absence of an obvious organic cause; it is associated with a history of abnormal visual experience during childhood. Subtypes have been defined based on the purported etiology, namely, strabismus (misaligned eyes) and/or anisometropia (unequal refractive error). Here we consider the usefulness of these subclassifications.

We investigated how the fusional range scales with eccentricity. Specifically, we measured the fusional range in the fovea and at 10 degrees below fixation. The limits of Panum's area are usually measured by increasing the disparity until the target appears "fuzzy". This is a poor method for the periphery as targets often appear fuzzy, even when presented with zero disparity. Here, we used a more rigorous method to determine the uppermost limit of fusion. At long durations, the two half-images that define a large disparity appear as two isolated targets in the same flat plane; small incremental changes in disparity produce changes in the separation between the half-images and disparity magnitude can be judged on the basis of separation, just like a monocular width judgment. The fusion limit is the point at which the threshold for judging dichoptic separation between the half-images is equal to the width threshold for monocular targets with the same separation. The targets were two patches of dynamic random dots. For dichoptic viewing, the reference target was presented in the fixation plane while the test target had a standing pedestal disparity. Participants made incremental judgments of disparity around this pedestal. For monocular presentation, two patches were shown to one eye and participants judged the width between the targets. Thresholds for incremental disparity and width discrimination were plotted as a function of the pedestal disparity or width. For both fovea and periphery, dichoptic thresholds initially increased with pedestal and then decreased until they matched the monocular thresholds. The fusional range at 10 degrees was a factor of 2-4 times larger than the fovea - smaller than eccentricity scaling for cortical magnification (5-6) or for hyperacuity (10 – 15). Our estimate is consistent with Ogle's (1954)'s estimate of fusion at 10 deg along the horizontal meridian. Meeting abstract presented at VSS 2017

We measured saccadic latencies in a large sample (total n = 459) of individuals with amblyopia or risk factors for amblyopia, e.g., strabismus or anisometropia, and normal control subjects. We presented an easily visible target randomly to the left or right, 3.5° from fixation. The interocular difference in saccadic latency is highly correlated with the interocular difference in LogMAR (Snellen) acuity—as the acuity difference increases, so does the latency difference. Strabismic and strabismic-anisometropic amblyopes have, on average, a larger difference between their eyes in LogMAR acuity than anisometropic amblyopes and thus their interocular latency difference is, on average, significantly larger than anisometropic amblyopes. Despite its relation to LogMAR acuity, the longer latency in strabismic amblyopes cannot be attributed either to poor resolution or to reduced contrast sensitivity, because their interocular differences in grating acuity and in contrast sensitivity are roughly the same as for anisometropic amblyopes. The correlation between LogMAR acuity and saccadic latency arises because of the confluence of two separable effects in the strabismic amblyopic eye—poor letter recognition impairs LogMAR acuity while an intrinsic sluggishness delays reaction time. We speculate that the frequent microsaccades and the accompanying attentional shifts, made while strabismic amblyopes struggle to maintain fixation with their amblyopic eyes, result in all types of reactions being irreducibly delayed.

Macular degeneration (MD) results in vision loss in and around the fovea. When both eyes are affected, and there is binocular central field loss, individuals often adopt a peripheral preferred retinal locus (PRL) at the margin of the scotoma, with the scotoma above it and relatively intact visual field below this gaze position. We have shown previously that individuals with MD can benefit from stereopsis when roughly corresponding areas in the two eyes are used to view a target in depth (Verghese et al, 2014 ARVO). Depth perception can also be useful for navigation to avoid falling. For example, a curb with a drop of 15 cm subtends a disparity of 3 to 8 arcmin at a distance of 1 to 2 m, assuming an eye height of 150 cm and interpupillary distance of 6 cm. To determine whether intact peripheral retina has the disparity sensitivity to support such discrimination, we mapped stereoacuity thresholds across the lower visual field (horizontal, vertical and diagonal meridians) in three normally sighted participants. Consistent with previous studies (Fendick & Westheimer, 1983), our results show that stereoacuity declines as a function of eccentricity, roughly doubling every 3 degrees. Importantly, we find that stereoacuity in the lower visual field is 4 arcmin or better for eccentricities up to 14 degrees, which is near the limit of observed PRL distance from the old fovea in individuals with macular degeneration. This suggests that individuals with intact peripheral retina up to about 14 degrees eccentricity in the lower visual field have the potential to detect a curb drop off and avoid falling. Meeting abstract presented at VSS 2016

Despite normal motor control, saccadic latencies are delayed in the non-preferred eye of patients with amblyopia (≈25-100ms1,2). This delay extends to manual reaction time when responding to targets with the amblyopic eye (≈50-100ms1,3,4). Previous researchers have shown a positive correlation between the delay and the magnitude of visual acuity impairment in the amblyopic eye5. This delay may be due to a difference in effective stimulus strength of the targets, since reaction times to weak stimuli are prolonged, decreasing as stimulus strength increases, until reaching a plateau6. Here, we measure saccadic and manual reaction times of normal and amblyopic subjects to the abrupt appearance of a Gabor patch at 5 degrees to the left or right of fixation, while varying the contrast of the patch. Even after adjusting for differences in effective stimulus strength, we find significant delays in both saccadic and manual response times when viewing with the amblyopic eye. We speculate that this irreducible delay may be a consequence of impaired ability to rapidly direct spatial attention with the amblyopic eye. 1 Mackensen, G. (1958). Reaktionszeitmessungen bei Amblyopia. Graefes Arch Ophthalmol 159:636 – 642. 2 Ciuffreda, K.J., Kenyon R.V. Stark L. (1978). Increased saccadic latencies in amblyopic eyes. Invest Ophthalmol Vis Sci 17: 697-702. 3 Von Noorden, G.K. (1961). Reaction time in normal and amblyopic eyes. Arch Ophthalmol 66:695-699. 4 Levi, D.M., Harwerth, R.S., and Manny, R.E. (1979). Suprathreshold spatial frequency detection and binocular interaction in strabismic and anisometropic amblyopia. Invest Ophthalmol Vis Sci 18:714-725. 5 Hamasaki, D.I. and Flynn, J.T. (1981). Amblyopic eyes have longer reaction times. Invest Ophthalmol Vis Sci 21:846-853. 6 Pieron, H. (1952). The Sensations: Their Functions, Processes and Mechanisms. London: Frederick Muller Ltd. Meeting abstract presented at VSS 2015

The perception of motion-in-depth is important for avoiding collisions and for the control of vergence eye-movements and other motor actions. Previous psychophysical studies have suggested that sensitivity to motion-in-depth has a lower temporal processing limit than the perception of lateral motion. The present study used functional MRI-informed EEG source-imaging to study the spatiotemporal properties of the responses to lateral motion and motion-in-depth in human visual cortex. Lateral motion and motion-in-depth displays comprised stimuli whose only difference was interocular phase: monocular oscillatory motion was either in-phase in the two eyes (lateral motion) or in antiphase (motion-in-depth). Spectral analysis was used to break the steady-state visually evoked potentials responses down into even and odd harmonic components within five functionally defined regions of interest: V1, V4, lateral occipital complex, V3A, and hMT+. We also characterized the responses within two anatomically defined regions: the inferior and superior parietal cortex. Even harmonic components dominated the evoked responses and were a factor of approximately two larger for lateral motion than motion-in-depth. These responses were slower for motion-in-depth and were largely independent of absolute disparity. In each of our regions of interest, responses at odd-harmonics were relatively small, but were larger for motion-in-depth than lateral motion, especially in parietal cortex, and depended on absolute disparity. Taken together, our results suggest a plausible neural basis for reduced psychophysical sensitivity to rapid motion-in-depth.

The natural world provides a rich and varied array of depth information – numerous cues that are commonly divided into monocular (2D) and binocular categories. Our experience with two-dimensional representations of depth in paintings, movies and computer simulations is so compelling that it is often thought that the information supplied by the primary binocular cue, namely stereopsis, is superfluous. Stereopsis, however, provides the most precise data about the location and extent of objects along the line of sight (z-axis). Most of the monocular cues to depth, such as perspective, relative size and texture, depend on changes in angular subtense associated with increasing distance. The minimal detectable change (1 – 2%) in angular subtense requires a change in distance that is generally substantially larger than the change in distance associated with the smallest detectable difference in disparity, at least at moderate distances (<15 meters). Although this conclusion is based on geometry, I will present experimental evidence showing that binocular depth thresholds measured with real objects in a cluttered environment are as much as 10 times better than monocular thresholds. The precision of stereopsis is also important in guiding hand movements, particularly grasp. Thus, the 2 – 3% of the population that are stereo-blind due to crossed eyes (strabismus) in childhood suffer a significant disadvantage in both depth judgments and eye-hand coordination. Recent studies (Ding & Levi, 2011) have shown that with practice some adult strabismics can recover some degree of stereopsis, raising the hope that better therapies in strabismic children can restore this important dimension.