Interocular Velocity Differences Research Articles

The magnitude of monocular light attenuation required to elicit the Pulfrich illusion

In the Pulfrich illusion, the depth of a moving object is misperceived due to induced retinal disparity and/or interocular velocity differences arising from differences in luminance, contrast, or spatial frequency between the two eyes. These effects have been shown to occur both for visual deficits and for optical corrections that introduce significant binocular differences between the retinal images. However, it remains unknown to what extent the illusion might arise given normal variation between the eyes, such as natural interocular variation in pupil diameter (anisocoria). To assess this, we examined the threshold interocular retinal illuminance difference required to experience illusory depth in two random-dot fields moving in opposite directions in 24 normally-sighted observers with dilated pupils. Interocular difference in retinal illuminance was induced by placing neutral density filters of different intensities before the left eye. A minority of subjects (n = 8) did not provide meaningful data on changes in the experience of illusory depth with interocular difference in retinal illuminance and four subjects showed biases >±10% from the 50% point of subjective equality in the psychometric function. For the remaining 12 participants, the retinal illuminance had to differ by approximately 40% for the depth between the planes to become visible at threshold levels. This difference was approximately constant over a range of absolute luminance levels from 10 to 80 cd/m2. Our results suggest that while motion-in-depth illusions due to interocular differences in retinal illuminance may be pronounced in certain ophthalmic diseases or following certain optical interventions, it is unlikely to be manifest as a result of normal interocular variations in retinal illuminance. Further, our results also point towards the existence of substantial individual differences in the experience of what is otherwise thought of as a readily appreciable motion-in-depth illusion.

Head jitter enhances three-dimensional motion perception.

Motion perception is a critical function of the visual system. In a three-dimensional environment, multiple sensory cues carry information about an object's motion trajectory. Previous work has quantified the contribution of binocular motion cues, such as interocular velocity differences and changing disparities over time, as well as monocular motion cues, such as size and density changes. However, even when these cues are presented in concert, observers will systematically misreport the direction of motion-in-depth. Although in the majority of laboratory experiments head position is held fixed using a chin or head rest, an observer's head position is subject to involuntary small movements under real-world viewing conditions. Here, we considered the potential impact of such “head jitter” on motion-in-depth perception. We presented visual stimuli in a head-mounted virtual reality device that facilitated low latency head tracking and asked observers to judge 3D object motion. We found performance improved when we updated the visual display consistent with the small changes in head position. When we disrupted or delayed head movement–contingent updating of the visual display, the proportion of motion-in-depth misreports again increased, reflected in both a reduction in sensitivity and an increase in bias. Our findings identify a critical function of head jitter in visual motion perception, which has been obscured in most (head-fixed and non-head jitter contingent) laboratory experiments.

Decoding Neural Responses to Motion-in-Depth Using EEG.

Two stereoscopic cues that underlie the perception of motion-in-depth (MID) are changes in retinal disparity over time (CD) and interocular velocity differences (IOVD). These cues have independent spatiotemporal sensitivity profiles, depend upon different low-level stimulus properties, and are potentially processed along separate cortical pathways. Here, we ask whether these MID cues code for different motion directions: do they give rise to discriminable patterns of neural signals, and is there evidence for their convergence onto a single “motion-in-depth” pathway? To answer this, we use a decoding algorithm to test whether, and when, patterns of electroencephalogram (EEG) signals measured from across the full scalp, generated in response to CD- and IOVD-isolating stimuli moving toward or away in depth can be distinguished. We find that both MID cue type and 3D-motion direction can be decoded at different points in the EEG timecourse and that direction decoding cannot be accounted for by static disparity information. Remarkably, we find evidence for late processing convergence: IOVD motion direction can be decoded relatively late in the timecourse based on a decoder trained on CD stimuli, and vice versa. We conclude that early CD and IOVD direction decoding performance is dependent upon fundamentally different low-level stimulus features, but that later stages of decoding performance may be driven by a central, shared pathway that is agnostic to these features. Overall, these data are the first to show that neural responses to CD and IOVD cues that move toward and away in depth can be decoded from EEG signals, and that different aspects of MID-cues contribute to decoding performance at different points along the EEG timecourse.

A motion-in-depth model based on inter-ocular velocity to estimate direction in depth

Perception of motion in depth is one of the most important visual functions for living in the three-dimensional world. Two binocular cues have been investigated for motion in depth: inter-ocular velocity difference (IOVD) and changing disparity (CD). IOVD provides direction information directly by comparing velocity signals from the two retinas. In this study, we propose for the first time a motion-in-depth model of IOVD that predicts motion-in-depth direction. The model is based on a psychophysical assumption that there are four channels tuned to different directions in depth (Journal of Physiology 235 (1973) 17–29). We modeled these channels by combining outputs of low-level motion detectors that are sensitive to left and right retinal stimulation. Using these channels, we constructed a model of motion in depth that successfully predicted a variety of psychophysical results including direction discrimination, perceived direction, spatial frequency tuning, effect of speed on rotation in depth, effect of lateral motion direction, and effect of binocular and temporal correlations.

Relative contributions to vergence eye movements of two binocular cues for motion-in-depth

When we track an object moving in depth, our eyes rotate in opposite directions. This type of “disjunctive” eye movement is called horizontal vergence. The sensory control signals for vergence arise from multiple visual cues, two of which, changing binocular disparity (CD) and inter-ocular velocity differences (IOVD), are specifically binocular. While it is well known that the CD cue triggers horizontal vergence eye movements, the role of the IOVD cue has only recently been explored. To better understand the relative contribution of CD and IOVD cues in driving horizontal vergence, we recorded vergence eye movements from ten observers in response to four types of stimuli that isolated or combined the two cues to motion-in-depth, using stimulus conditions and CD/IOVD stimuli typical of behavioural motion-in-depth experiments. An analysis of the slopes of the vergence traces and the consistency of the directions of vergence and stimulus movements showed that under our conditions IOVD cues provided very little input to vergence mechanisms. The eye movements that did occur coinciding with the presentation of IOVD stimuli were likely not a response to stimulus motion, but a phoria initiated by the absence of a disparity signal.

Encoding- and decision-related brain activity during a motion judgment task

We have previously used steady-state VEPs to show that responses in visual cortex are strongly suppressed when motion stimuli produce inter-ocular velocity differences (Kohler et al., 2018), regardless of whether these differences give rise to movement in depth (MID). Here we used an event-related VEP design to explore how activity evoked by lateral movement and MID unfolds over time. Participants (n=20) viewed stereoscopically presented random-dot patterns in which a central region moved in one of four directions. Dots underwent single-shot apparent motion on every trial: in-phase motion between the two eyes produced lateral movement (left/right), while anti-phase motion gave rise to MID (towards/away). Participants indicated movement direction as quickly and accurately as possible using the keyboard arrow keys. For lateral movement, accuracy was at ceiling and reaction time (RT) was ~800ms, while MID produced lower accuracies (~80%) and longer RTs (~1000ms). We used reliable components analysis to extract maximally correlated signal components from the EEG data (Dmochowski et al., 2012). A medio-frontal component appeared to capture decision-related activity, exhibiting a ramp-like shape that was shallower for MID, consistent with a longer integration period leading to slower RTs. An additional component, centered over occipital cortex, appeared to primarily capture encoding-related activity. Lateral movement and MID produced indistinguishable positive peaks at ~70ms, but diverged at later negative (~180ms) and positive (~350ms) peaks. MID responses were enhanced (more negative) around the negative peak (100–200ms) and suppressed (less positive) leading up to the second positive peak (250–350ms). This late-onset suppression is consistent with the finding that suppression depends on second-order processes, including extraction of relative motion and relative disparity (Kohler et al., 2018). The current results provide a time-resolved electrophysiological analogue to psychophysical data showing that temporal integration underlying decision making is near-perfect for lateral motion, but sub-optimal for MID (Katz et al., 2015).

Asymmetries between achromatic and chromatic extraction of 3D motion signals

Motion in depth (MID) can be cued by high-resolution changes in binocular disparity over time (CD), and low-resolution interocular velocity differences (IOVD). Computational differences between these two mechanisms suggest that they may be implemented in visual pathways with different spatial and temporal resolutions. Here, we used fMRI to examine how achromatic and S-cone signals contribute to human MID perception. Both CD and IOVD stimuli evoked responses in a widespread network that included early visual areas, parts of the dorsal and ventral streams, and motion-selective area hMT+. Crucially, however, we measured an interaction between MID type and chromaticity. fMRI CD responses were largely driven by achromatic stimuli, but IOVD responses were better driven by isoluminant S-cone inputs. In our psychophysical experiments, when S-cone and achromatic stimuli were matched for perceived contrast, participants were equally sensitive to the MID in achromatic and S-cone IOVD stimuli. In comparison, they were relatively insensitive to S-cone CD. These findings provide evidence that MID mechanisms asymmetrically draw on information in precortical pathways. An early opponent motion signal optimally conveyed by the S-cone pathway may provide a substantial contribution to the IOVD mechanism.

Eye-specific pattern-motion signals support the perception of three-dimensional motion.

An object moving through three-dimensional (3D) space typically yields different patterns of velocities in each eye. For an interocular velocity difference cue to be used, some instances of real 3D motion in the environment (e.g., when a moving object is partially occluded) would require an interocular velocity difference computation that operates on motion signals that are not only monocular (or eye specific) but also depend on each eye's two-dimensional (2D) direction being estimated over regions larger than the size of V1 receptive fields (i.e., global pattern motion). We investigated this possibility using 3D motion aftereffects (MAEs) with stimuli comprising many small, drifting Gabor elements. Conventional frontoparallel (2D) MAEs were local—highly sensitive to the test elements being in the same locations as the adaptor (Experiment 1). In contrast, 3D MAEs were robust to the test elements being in different retinal locations than the adaptor, indicating that 3D motion processing involves relatively global spatial pooling of motion signals (Experiment 2). The 3D MAEs were strong even when the local elements were in unmatched locations across the two eyes during adaptation, as well as when the adapting stimulus elements were randomly oriented, and specified global motion via the intersection of constraints (Experiment 3). These results bolster the notion of eye-specific computation of 2D pattern motion (involving global pooling of local, eye-specific motion signals) for the purpose of computing 3D motion, and highlight the idea that classically “late” computations such as pattern motion can be done in a manner that retains information about the eye of origin.

Motion-in-depth perception and prey capture in the praying mantisSphodromantis lineola

Perceiving motion-in-depth is essential to detecting approaching or receding objects, predators and prey. This can be achieved using several cues, including binocular stereoscopic cues such as changing disparity and interocular velocity differences, and monocular cues such as looming. Although these have been studied in detail in humans, only looming responses have been well characterized in insects and we know nothing about the role of stereoscopic cues and how they might interact with looming cues. We used our 3D insect cinema in a series of experiments to investigate the role of the stereoscopic cues mentioned above, as well as looming, in the perception of motion-in-depth during predatory strikes by the praying mantis Sphodromantis lineola Our results show that motion-in-depth does increase the probability of mantis strikes but only for the classic looming stimulus, an expanding luminance edge. Approach indicated by radial motion of a texture or expansion of a motion-defined edge, or by stereoscopic cues, all failed to elicit increased striking. We conclude that mantises use stereopsis to detect depth but not motion-in-depth, which is detected via looming.

Investigating Human Visual Sensitivity to Binocular Motion-in-Depth for Anti- and De-Correlated Random-Dot Stimuli.

Motion-in-depth can be detected by using two different types of binocular cues: change of disparity (CD) and inter-ocular velocity differences (IOVD). To investigate the underlying detection mechanisms, stimuli can be constructed that isolate these cues or contain both (FULL cue). Two different methods to isolate the IOVD cue can be employed: anti-correlated (aIOVD) and de-correlated (dIOVD) motion signals. While both types of stimuli have been used in studies investigating the perception of motion-in-depth, for the first time, we explore whether both stimuli isolate the same mechanism and how they differ in their relative efficacy. Here, we set out to directly compare aIOVD and dIOVD sensitivity by measuring motion coherence thresholds. In accordance with previous results by Czuba et al. (2010), we found that motion coherence thresholds were similar for aIOVD and FULL cue stimuli for most participants. Thresholds for dIOVD stimuli, however, differed consistently from thresholds for the two other cues, suggesting that aIOVD and dIOVD stimuli could be driving different visual mechanisms.

Sensitivity to Velocity- and Disparity-Based Cues to Motion-In-Depth With and Without Spared Stereopsis in Binocular Visual Impairment.

Two binocular sources of information serve motion-in-depth (MID) perception: changes in disparity over time (CD), and interocular velocity differences (IOVD). While CD requires the computation of small spatial disparities, IOVD could be computed from a much lower-resolution signal. IOVD signals therefore might still be available under conditions of binocular vision impairment (BVI) with limited or no stereopsis, for example, amblyopia. Sensitivity to CD and IOVD was measured in adults who had undergone therapy to correct optical misalignment or amblyopia in childhood (n = 16), as well as normal vision controls with good stereoacuity (n = 8). Observers discriminated the interval containing a smoothly oscillating MID "test" stimulus from a "control" stimulus in a two-interval forced choice paradigm. Of the BVI observers with no static stereoacuity (n = 9), one displayed evidence for sensitivity to IOVD only, while there was otherwise no sensitivity for either CD or IOVD in the group. Generally, BVI observers with measurable stereoacuity (n = 7) displayed a pattern resembling the control group: showing a similar sensitivity for both cues. A neutral density filter placed in front of the fixing eye in a subset of BVI observers did not improve performance. In one BVI observer there was preserved sensitivity to IOVD but not CD, though overall only those BVI observers with at least gross stereopsis were able to detect disparity- or velocity-based cues to MID. The results imply that these logically distinct information sources are somehow coupled, and in some cases BVI observers with no stereopsis may still retain sensitivity to IOVD.

Relationship between vection and motion perception in depth.

This study examined the effects of cues to motion in depth - namely, stereoscopic (i.e., changing-disparity cues and interocular velocity differences) and changing-size cues on forward and backward vection. We conducted four experiments in which participants viewed expanding or contracting optical flows with the addition of either or both cues. In Experiment 1, participants reported vection by pressing a button whenever they felt it. After each trial, they also rated the magnitude of the vection (from 0 to 100). In Experiments 2 and 3, the participants rated the perceived velocity and motion-in-depth impression of the flows relative to standard stimuli, respectively. In Experiment 4, the participants rated the perceived depth and distance of the display. We observed enhancements in vection, motion-in-depth impression, and perceived depth and distance when either or both types of cues indicated motion-in-depth, as compared to those when the cues did not (Experiments 1, 3, and 4). The perceived velocity changed with cue conditions only for the high velocity condition (Experiment 2). Correlational analyses showed that the vection can be best explained by the motion-in-depth impression. This was partially supported by the multiple regression analyses. These results indicate that the enhancement of vection caused by cues is related to the impression of motion-in-depth rather than the perceived velocity and perceived three-dimensionality.

Comparison of horizontal vergence responses to changing disparity and inter-ocular velocity differences

Comparison of horizontal vergence responses to changing disparity and inter-ocular velocity differences

Interocular contrast difference drives illusory 3D percept

Any processing delay between the two eyes can result in illusory 3D percepts for moving objects because of either changes in the pure disparities over time for disparity sensors or by changes to sensors that encode motion/disparity conjointly. This is demonstrated by viewing a fronto-parallel pendulum through a neutral density (ND) filter placed over one eye, resulting in the illusory 3D percept of the pendulum following an elliptical orbit in depth, the so-called Pulfrich phenomenon. Here we use a paradigm where a cylinder rotating in depth, defined by moving Gabor patches is presented at different interocular phases, generating strong to ambiguous depth percepts. This paradigm allows one to manipulate independently the contrast and the luminance of the patches to determine their influence on perceived motion-in-depth. Thus we show psychophysically that an interocular contrast difference can itself result in a similar illusory 3D percept of motion-in-depth. We argue that contrast, like luminance (ND filter) can modify the dynamics of visual neurons resulting in an interocular processing delay or an interocular velocity difference.

Impaired Velocity Processing Reveals an Agnosia for Motion in Depth

Many individuals with normal visual acuity are unable to discriminate the direction of 3-D motion in a portion of their visual field, a deficit previously referred to as a stereomotion scotoma. The origin of this visual deficit has remained unclear. We hypothesized that the impairment is due to a failure in the processing of one of the two binocular cues to motion in depth: changes in binocular disparity over time or interocular velocity differences. We isolated the contributions of these two cues and found that sensitivity to interocular velocity differences, but not changes in binocular disparity, varied systematically with observers’ ability to judge motion direction. We therefore conclude that the inability to interpret motion in depth is due to a failure in the neural mechanisms that combine velocity signals from the two eyes. Given these results, we argue that the deficit should be considered a prevalent but previously unrecognized agnosia specific to the perception of visual motion.

Human short-latency ocular vergence responses produced by interocular velocity differences.

We studied human short-latency vergence eye movements to a novel stimulus that produces interocular velocity differences without a changing disparity signal. Sinusoidal luminance gratings moved in opposite directions (left vs. right; up vs. down) in the two eyes. The grating seen by each eye underwent ¼-wavelength shifts with each image update. This arrangement eliminated changing disparity cues, since the phase difference between the eyes alternated between 0° and 180°. We nevertheless observed robust short-latency vergence responses (VRs), whose sign was consistent with the interocular velocity differences (IOVDs), indicating that the IOVD cue in isolation can evoke short-latency VRs. The IOVD cue was effective only when the images seen by the two eyes overlapped in space. We observed equally robust VRs for opposite horizontal motions (left in one eye, right in the other) and opposite vertical motions (up in one eye, down in the other). Whereas the former are naturally generated by objects moving in depth, the latter are not part of our normal experience. To our knowledge, this is the first demonstration of a behavioral consequence of vertical IOVD. This may reflect the fact that some neurons in area MT are sensitive to these motion signals (Czuba, Huk, Cormack, & Kohn, 2014). VRs were the strongest for spatial frequencies in the range of 0.35–1 c/°, much higher than the optimal spatial frequencies for evoking ocular-following responses observed during frontoparallel motion. This suggests that the two motion signals are detected by different neuronal populations. We also produced IOVD using moving uncorrelated one-dimensional white-noise stimuli. In this case the most effective stimuli have low speed, as predicted if the drive originates in neurons tuned to high spatial frequencies (Sheliga, Quaia, FitzGibbon, & Cumming, 2016).

Optimal Combination of the Binocular Cues to 3D Motion.

Perception necessarily entails combining separate sensory estimates into a single coherent whole. The perception of three-dimensional (3D) motion, for instance, can rely on two binocular cues: one related to the change in binocular disparity over time (CD) and the other related to interocular velocity differences (IOVD). Although previous work has shown that neither cue is strictly necessary for the perception of 3D motion, observers are able to judge 3D motion in displays in which one or the other cue has been eliminated, it is unclear whether or how the two cues are combined in situations in which both are present. We tested the visual performance of a sample of 81 individuals (Mage = 20.34, 49 females) in four main conditions that measured, respectively, static stereoacuity, CD, IOVD, and combined CD+IOVD sensitivity. We show that the sensitivity to the two binocular cues to 3D motion varies substantially across observers (CD: Md' = 1.01, SDd' = 1.1; IOVD: Md' = 1.16, SDd' = 1.03). Furthermore, sensitivity to the two cues was independent across observers (r[48] = 0.12, P = 0.42). Importantly, however, observed CD+IOVD performance was well-predicted based on the assumption that each observer combines the two cues in a statistically optimal fashion (r[79] = 0.75, P < 0.001). Our findings provide an explanation for the previously puzzling variability found in 3D perception across observers and laboratories, with some results suggesting that motion-in-depth percepts are largely determined by changes in binocular disparity, whereas others indicate that interocular velocity differences are key. Our results underline the existence of two complementary binocular mechanisms underlying 3D motion perception, with observers relying on these two mechanisms to different extents depending on their individual sensitivity.

Binocular Perception of 2D Lateral Motion and Guidance of Coordinated Motor Behavior.

Zannoli, Cass, Alais, and Mamassian (2012) found greater audiovisual lag between a tone and disparity-defined stimuli moving laterally (90-170 ms) than for disparity-defined stimuli moving in depth or luminance-defined stimuli moving laterally or in depth (50-60 ms). We tested if this increased lag presents an impediment to visually guided coordination with laterally moving objects. Participants used a joystick to move a virtual object in several constant relative phases with a laterally oscillating stimulus. Both the participant-controlled object and the target object were presented using a disparity-defined display that yielded information through changes in disparity over time (CDOT) or using a luminance-defined display that additionally provided information through monocular motion and interocular velocity differences (IOVD). Performance was comparable for both disparity-defined and luminance-defined displays in all relative phases. This suggests that, despite lag, perception of lateral motion through CDOT is generally sufficient to guide coordinated motor behavior.

Neural representation of motion-in-depth in area MT.

Neural processing of 2D visual motion has been studied extensively, but relatively little is known about how visual cortical neurons represent visual motion trajectories that include a component toward or away from the observer (motion in depth). Psychophysical studies have demonstrated that humans perceive motion in depth based on both changes in binocular disparity over time (CD cue) and interocular velocity differences (IOVD cue). However, evidence for neurons that represent motion in depth has been limited, especially in primates, and it is unknown whether such neurons make use of CD or IOVD cues. We show that approximately one-half of neurons in macaque area MT are selective for the direction of motion in depth, and that this selectivity is driven primarily by IOVD cues, with a small contribution from the CD cue. Our results establish that area MT, a central hub of the primate visual motion processing system, contains a 3D representation of visual motion.

Aftereffect of motion-in-depth based on binocular cues: Effects of adaptation duration, interocular correlation, and temporal correlation.

There are at least two possible binocular cues to motion-in-depth, namely disparity change over time and interocular velocity differences. There has been significant controversy about their relative contributions to the perception of motion-in-depth. In the present study, we used the technique of selective adaptation to address this question. In Experiment 1, we found that adaptation to motion-in-depth depicted by temporally correlated random-dot stereograms, which contained coherent interocular velocity difference, produced motion aftereffect in the depth direction irrespective of the adaptors' interocular correlation for any adaptation duration tested. This suggests that coherent changing disparity does not contribute to motion-in-depth adaptation. Because the aftereffect duration did not saturate in the tested range of adaptation duration, it is unlikely that the lack of the effect of changing disparity was due to a ceiling effect. In Experiment 2, we used a novel adaptor that contained a unidirectional coherent interocular velocity difference signal and a bidirectional changing disparity signal that should not induce a motion aftereffect in depth. Following the adaptation, motion aftereffect in depth occurred in the opposite direction to the adaptor's motion-in-depth based on interocular velocity difference. Experiment 3 demonstrated that these results generalized in 12 untrained subjects. These experiments suggest that the contribution of interocular velocity difference to the perception of motion-in-depth is substantial, while that of changing disparity is very limited (if any), at least at the stages of direction-selective mechanisms subject to an aftereffect phenomenon.