Binocular Eye Movements Are Adapted to the Natural Environment

Abstract

Humans and many animals make frequent saccades requiring coordinated movements of the eyes. When landing on the new fixation point, the eyes must converge accurately or double images will be perceived. We asked whether the visual system uses statistical regularities in the natural environment to aid eye alignment at the end of saccades. We measured the distribution of naturally occurring disparities in different parts of the visual field. The central tendency of the distributions was crossed (nearer than fixation) in the lower field and uncrossed (farther) in the upper field in male and female participants. It was uncrossed in the left and right fields. We also measured horizontal vergence after completion of vertical, horizontal, and oblique saccades. When the eyes first landed near the eccentric target, vergence was quite consistent with the natural-disparity distribution. For example, when making an upward saccade, the eyes diverged to be aligned with the most probable uncrossed disparity in that part of the visual field. Likewise, when making a downward saccade, the eyes converged to enable alignment with crossed disparity in that part of the field. Our results show that rapid binocular eye movements are adapted to the statistics of the 3D environment, minimizing the need for large corrective vergence movements at the end of saccades. The results are relevant to the debate about whether eye movements are derived from separate saccadic and vergence neural commands that control both eyes or from separate monocular commands that control the eyes independently.

Mice Discriminate Stereoscopic Surfaces Without Fixating in Depth

“…In primates, saccades and slower more careful changes in alignment are triggered by changes in disparity (Rashbass and Westheimer, 1961;Enright, 1984;Cumming and Judge, 1986). Even when presented with ambiguous disparity information, saccades tend to diverge or converge to expected disparities based on natural scene statistics (Gibaldi and Banks, 2019). Disparity-induced vergence is a reflexive behavior in primates making it nearly impossible for a primate to prevent vergence eye movements when nonzero disparity occurs within the fovea (Fig.…”

“…These vergence eye movements dynamically adjust fixation to be at zero disparity. This can be accomplished with saccades that are of different magnitudes between the two eyes (Enright, 1984;Gibaldi and Banks, 2019) or with slower convergent/divergent rotations of the eyes (Rashbass and Westheimer, 1961; Cumming and Judge, 1986). This behavior allows the foveal visual system to process disparities over a narrow range, which corresponds to the distribution of disparity tuning in the primate visual system (Prince et al, 2002a;Samonds et al, 2012;Sprague et al, 2015).…”

“…Primate eyes selectively converge and diverge to stimuli that are closer to or farther from fixation, respectively, to allow finer discrimination of relative depth at each new absolute depth (Rashbass and Westheimer, 1961;Cumming and Judge, 1986). Saccadic eye movements also selectively converge and diverge in a similar manner when moving the eyes to align on targets at different depths (Enright, 1984;Gibaldi and Banks, 2019). Mammals lacking a fovea typically do not exhibit such eye movements and do not fixate on objects (Stahl, 2004) so these eye movements have received little attention in mice.…”

Natural scene statistics predict how humans pool information across space in the estimation of surface tilt

“…In recent years, a series of papers have provided evidence linking certain statistical aspects of natural images and scenes [15,28,[33][34][35][36][37][38] to the design of the human visual system [39][40][41], and to the performance of human observers in perceptual tasks [14,16,37,[42][43][44][45][46][47][48][49]. This broad program of research has, with varying degrees of rigor, invoked natural scene statistics to account for a strikingly diverse set of topics: how the shape of pupils changes across species in different ecological niches [41], where corresponding points are located in the two retinas [39,40], how biases in binocular eye movements manifest [48], how targets are detected in natural images [47], how image contours are perceptually grouped [37,42], how image orientation is estimated [45], how binocular disparity is estimated [44,50,51], how image motion is estimated [46,49,52], how 3D tilt is estimated [16], and now, how cues to 3D tilt are pooled across space. Over this same period, numerous modeling frameworks have emerged that provide theoretical and computational methods for predicting and accounting for these links [50,[53]…”

Optimal Stereoacuity Reveals More Than Critical Time in Patients With Intermittent Exotropia

“…Stereopsis in humans is absent at birth, emerges around 3 months of age and gradually reaches adult levels around 5 years of age (Aslin, 1977;Fox et al, 1980;Birch et al, 1982;Birch et al, 1985;Giaschi et al, 2013). It is common knowledge that binocular vision adapts to natural occurring disparities, for what concerns stereopsis (Sprague et al, 2015;Gibaldi et al, 2017) and binocular coordination (Gibaldi and Banks, 2019). Due to the high level of neural plasticity in early life, abnormal binocular visual experience often can quickly disrupt this developmental process (Wiesel and Hubel, 1963;Birch et al, 1998).…”