Optics and neural adaptation jointly limit human stereovision.

Stereovision is the ability to perceive fine depth variations from small differences in the two eyes' images. Using adaptive optics, we show that even minute optical aberrations that are not clinically correctable, and go unnoticed in everyday vision, can affect stereo acuity. Hence, the human binocular system is capable of using fine details that are not experienced in everyday vision. Interestingly, stereo acuity varied considerably across individuals even when they were provided identical perfect optics. We also found that individuals' stereo acuity is better when viewing with their habitual optics rather than someone else's (better) optics. Together, these findings suggest that the visual system compensates for habitual optical aberrations through neural adaptation and thereby optimizes stereovision uniquely for each individual. Thus, stereovision is limited by small optical aberrations and by neural adaptation to one's own optics.

Procedure for extracting temporal structure embedded within psychophysical data.

The idea that mental events unfold over time with an intrinsically paced regularity has a long history within experimental psychology, and it has gained traction from the actual measurement of brain rhythms evident in EEG signals recorded from the human brain and from direct recordings of action potentials and local field potentials within the nervous systems of nonhumans. The weak link in this idea, however, is the challenge of extracting signatures of this temporal structure from behavioral measures. Because there is nothing in the seamless stream of conscious awareness that belies rhythmic modulations in sensitivity or mental acuity, one must deploy inferential strategies for extracting evidence for the existence of temporal regularities in neural activity. We have devised a parametric procedure for analysis of temporal structure embedded in behaviorally measured data comprising durations. We confirm that this procedure, dubbed PATS, achieves comparable results to those obtained using spectral analysis, and that it outperforms conventional spectral analysis when analyzing human response time data containing just a few hundred data points per condition. PATS offers an efficient, sensitive means for bridging the gap between oscillations identified neurophysiologically and estimates of rhythmicity embedded within durations measured behaviorally.

CFS-crafter: An open-source tool for creating and analyzing images for continuous flash suppression experiments.

Continuous flash suppression (CFS) is a popular masking technique used to manipulate visual awareness. By presenting a rapidly changing stimulus to one eye (the 'mask'), a static image viewed by the other (the 'target') may remain invisible for many seconds. This effectiveness affords a means to assess unconscious visual processing, leading to the widespread use of CFS in several basic and clinical sciences. However, the lack of principled stimulus selection has impeded generalization of conclusions across studies, as the strength of interocular suppression is dependent on the spatiotemporal properties of the CFS mask and target. To address this, we created CFS-crafter, a point-and-click, open-source tool for creating carefully controlled CFS stimuli. The CFS-crafter provides a streamlined workflow to create, modify, and analyze mask and target stimuli, requiring only a rudimentary understanding of image processing that is well supported by help files in the application. Users can create CFS masks ranging from classic Mondrian patterns to those comprising objects or faces, or they can create, upload, and analyze their own images. Mask and target images can be custom-designed using image-processing operations performed in the frequency domain, including phase-scrambling and spatial/temporal/orientation filtering. By providing the means for the customization and analysis of CFS stimuli, the CFS-crafter offers controlled creation, analysis, and cross-study comparison. Thus, the CFS-crafter-with its easy-to-use image processing functionality-should facilitate the creation of visual conditions that allow a principled assessment of hypotheses about visual processing outside of awareness.

Evidence for neural rhythms embedded within binocular rivalry.

Evidence for perceptual periodicity emerges from studies showing periodic fluctuations in visual perception and decision making that are accompanied by neural oscillations in brain activity. We have uncovered signs of periodicity in the time course of binocular rivalry, a widely studied form of multistable perception. This was done by analyzing time series data contained in an unusually large dataset of rivalry state durations associated with states of exclusive monocular dominance and states of mixed perception during transitions between exclusive dominance. Identifiable within the varying durations of dynamic mixed perception are rhythmic clusters of durations whose incidence falls within the frequency band associated with oscillations in neural activity accompanying periodicity in perceptual judgments. Endogenous neural oscillations appear to be especially impactful when perception is unusually confounding.

Multistable Perception and the Role of the Frontoparietal Cortex in Perceptual Inference.

A given pattern of optical stimulation can arise from countless possible real-world sources, creating a dilemma for vision: What in the world actually gives rise to the current pattern? This dilemma was pointed out centuries ago by the astronomer and mathematician Ibn Al-Haytham and was forcefully restated 150 years ago when von Helmholtz characterized perception as unconscious inference. To buttress his contention, von Helmholtz cited multistable perception: recurring changes in perception despite unchanging sensory input. Recent neuroscientific studies have exploited multistable perception to identify brain areas uniquely activated in association with these perceptual changes, but the specific roles of those activations remain controversial. This article provides an overview of theoretical models of multistable perception, a review of recent neuroimaging and brain stimulation studies focused on mechanisms associated with these perceptual changes, and a synthesis of available evidence within the context of current notions about Bayesian inference that find their historical roots in von Helmholtz's work.

Novel procedure for generating continuous flash suppression: Seurat meets Mondrian.

Continuous flash suppression (CFS) entails presentation of a stationary target to one eye and an animated sequence of arrays of geometric figures, the mask, to the other eye. The prototypical CFS sequence comprises different sized rectangles of various colors, dubbed Mondrians. Presented as a rapid, changing sequence to one eye, Mondrians or other similarly constructed textured arrays can abolish awareness of the target viewed by the other eye for many seconds at a time, producing target suppression durations much longer than those associated with conventional binocular rivalry. We have devised an animation technique that replaces meaningless Mondrian figures with recognizable visual objects and scenes as inducers of CFS, allowing explicit manipulation of the visual semantic content of those masks. By converting each image of these CFS sequences into successively presented objects or scenes each comprised of many small, circular patches of color, we create pointillist CFS sequences closely matched in terms of their spatio-temporal power spectra. Randomly rearranging the positions of the pointillist patches scrambles the images so they are no longer recognizable. CFS sequences comprising a stream of different objects produces more robust interocular suppression than do sequences comprising a stream of different scenes, even when the two categories of CFS are matched in root mean square contrast and spatial frequency content. Factors promoting these differences in CFS potency could range from low-level, image-based features to high-level factors including attention and recognizability. At the same time, object- and scene-based CFS sequences, when themselves suppressed from awareness, do not differ in their durations of suppression, implying that semantic content of those images comprising CFS sequences are not registered during suppression. The pointillist technique itself offers a potentially useful means for examining the impact of high-level image meaning on aspects of visual perception other than interocular suppression.

Probing Electrophysiological Indices of Perceptual Awareness across Unisensory and Multisensory Modalities.

The neural underpinnings of perceptual awareness have been extensively studied using unisensory (e.g., visual alone) stimuli. However, perception is generally multisensory, and it is unclear whether the neural architecture uncovered in these studies directly translates to the multisensory domain. Here, we use EEG to examine brain responses associated with the processing of visual, auditory, and audiovisual stimuli presented near threshold levels of detectability, with the aim of deciphering similarities and differences in the neural signals indexing the transition into perceptual awareness across vision, audition, and combined visual-auditory (multisensory) processing. More specifically, we examine (1) the presence of late evoked potentials (∼>300 msec), (2) the across-trial reproducibility, and (3) the evoked complexity associated with perceived versus nonperceived stimuli. Results reveal that, although perceived stimuli are associated with the presence of late evoked potentials across each of the examined sensory modalities, between-trial variability and EEG complexity differed for unisensory versus multisensory conditions. Whereas across-trial variability and complexity differed for perceived versus nonperceived stimuli in the visual and auditory conditions, this was not the case for the multisensory condition. Taken together, these results suggest that there are fundamental differences in the neural correlates of perceptual awareness for unisensory versus multisensory stimuli. Specifically, the work argues that the presence of late evoked potentials, as opposed to neural reproducibility or complexity, most closely tracks perceptual awareness regardless of the nature of the sensory stimulus. In addition, the current findings suggest a greater similarity between the neural correlates of perceptual awareness of unisensory (visual and auditory) stimuli when compared with multisensory stimuli.

Slow and steady, not fast and furious: Slow temporal modulation strengthens continuous flash suppression.

Continuous flash suppression (CFS) involves the presentation of a rapidly changing Mondrian sequence to one eye and a static target in the other eye. Targets presented in this manner remain suppressed for several seconds at a time, and this has seen the prevalent use of CFS in studies of unconscious visual processes. However, the mechanisms behind CFS remain unclear, complicating its use and the comprehension of results obtained with the paradigm. For example, some studies report observations indicative of faster, visual masking processes whereas others suggest slower, rivalry processes. To reconcile this discrepancy, this study investigates the effect of temporal frequency content and Mondrian pattern structure on CFS suppression. Our results show predominant influences of spatial edges and low temporal-frequency content, which are similar to binocular rivalry, affording a parsimonious alternative in unifying the two paradigms.

Melodic sound enhances visual awareness of congruent musical notes, but only if you can read music.

Predictive influences of auditory information on resolution of visual competition were investigated using music, whose visual symbolic notation is familiar only to those with musical training. Results from two experiments using different experimental paradigms revealed that melodic congruence between what is seen and what is heard impacts perceptual dynamics during binocular rivalry. This bisensory interaction was observed only when the musical score was perceptually dominant, not when it was suppressed from awareness, and it was observed only in people who could read music. Results from two ancillary experiments showed that this effect of congruence cannot be explained by differential patterns of eye movements or by differential response sluggishness associated with congruent score/melody combinations. Taken together, these results demonstrate robust audiovisual interaction based on high-level, symbolic representations and its predictive influence on perceptual dynamics during binocular rivalry.

The Occipital Face Area Is Causally Involved in Facial Viewpoint Perception.

Humans reliably recognize faces across a range of viewpoints, but the neural substrates supporting this ability remain unclear. Recent work suggests that neural selectivity to mirror-symmetric viewpoints of faces, found across a large network of visual areas, may constitute a key computational step in achieving full viewpoint invariance. In this study, we used repetitive transcranial magnetic stimulation (rTMS) to test the hypothesis that the occipital face area (OFA), putatively a key node in the face network, plays a causal role in face viewpoint symmetry perception. Each participant underwent both offline rTMS to the right OFA and sham stimulation, preceding blocks of behavioral trials. After each stimulation period, the participant performed one of two behavioral tasks involving presentation of faces in the peripheral visual field: (1) judging the viewpoint symmetry; or (2) judging the angular rotation. rTMS applied to the right OFA significantly impaired performance in both tasks when stimuli were presented in the contralateral, left visual field. Interestingly, however, rTMS had a differential effect on the two tasks performed ipsilaterally. Although viewpoint symmetry judgments were significantly disrupted, we observed no effect on the angle judgment task. This interaction, caused by ipsilateral rTMS, provides support for models emphasizing the role of interhemispheric crosstalk in the formation of viewpoint-invariant face perception. SIGNIFICANCE STATEMENT: Faces are among the most salient objects we encounter during our everyday activities. Moreover, we are remarkably adept at identifying people at a glance, despite the diversity of viewpoints during our social encounters. Here, we investigate the cortical mechanisms underlying this ability by focusing on effects of viewpoint symmetry, i.e., the invariance of neural responses to mirror-symmetric facial viewpoints. We did this by temporarily disrupting neural processing in the occipital face area (OFA) using transcranial magnetic stimulation. Our results demonstrate that the OFA causally contributes to judgments facial viewpoints and suggest that effects of viewpoint symmetry, previously observed using fMRI, arise from an interhemispheric integration of visual information even when only one hemisphere receives direct visual stimulation.

A monocular contribution to stimulus rivalry.

When corresponding areas of the two eyes view dissimilar images, stable perception gives way to visual competition wherein perceptual awareness alternates between those images. Moreover, a given image can remain visually dominant for several seconds at a time even when the competing images are swapped between the eyes multiple times each second. This perceptual stability across eye swaps has led to the widespread belief that this unique form of visual competition, dubbed stimulus rivalry, is governed by eye-independent neural processes at a purely binocular stage of cortical processing. We tested this idea by investigating the influence of stimulus rivalry on the buildup of the threshold elevation aftereffect, a form of contrast adaptation thought to transpire at early cortical stages that include eye-specific neural activity. Weaker threshold elevation aftereffects were observed when the adapting image was engaged in stimulus rivalry than when it was not, indicating diminished buildup of adaptation during stimulus-rivalry suppression. We then confirmed that this reduction occurred, in part, at eye-specific neural stages by showing that suppression of an image at a given moment specifically diminished adaptation associated with the eye viewing the image at that moment. Considered together, these results imply that eye-specific neural events at early cortical processing stages contribute to stimulus rivalry. We have developed a computational model of stimulus rivalry that successfully implements this idea.

The time course of binocular rivalry during the phases of the menstrual cycle.

Binocular rivalry occurs when markedly different inputs to the two eyes initiate alternations in perceptual dominance between the two eyes' views. A link between individual differences in perceptual dynamics of rivalry and concentrations of GABA, a prominent inhibitory neurotransmitter in the brain, has highlighted binocular rivalry as a potential tool to investigate inhibitory processes in the brain. The present experiment investigated whether previously reported fluctuations of GABA concentrations in a healthy menstrual cycle (Epperson et al., 2002) also are associated with measurable changes in rivalry dynamics within individuals. We obtained longitudinal measures of alternation rate, dominance, and mixture durations in 300 rivalry tracking blocks measured over 5 weeks from healthy female participants who monitored the start of the follicular and luteal phases of their cycle. Although we demonstrate robust and stable individual differences in rivalry dynamics, across analytic approaches and dependent measures, we found no significant change or even trends across menstrual phases in the temporal dynamics of dominance percepts. We found only sparse between-phase differences in skew and kurtosis on mixture percepts when data were pooled across sessions and blocks. These results suggest a complex dynamic between hormonal steroids, binocular rivalry, and GABAeric signaling in the brain and thus implicate the need to consider a systemic perspective when linking GABA with perceptual alternations in binocular rivalry.

Dissociation between neural signatures of stimulus and choice in population activity of human V1 during perceptual decision-making.

Primary visual cortex (V1) forms the initial cortical representation of objects and events in our visual environment, and it distributes information about that representation to higher cortical areas within the visual hierarchy. Decades of work have established tight linkages between neural activity occurring in V1 and features comprising the retinal image, but it remains debatable how that activity relates to perceptual decisions. An actively debated question is the extent to which V1 responses determine, on a trial-by-trial basis, perceptual choices made by observers. By inspecting the population activity of V1 from human observers engaged in a difficult visual discrimination task, we tested one essential prediction of the deterministic view: choice-related activity, if it exists in V1, and stimulus-related activity should occur in the same neural ensemble of neurons at the same time. Our findings do not support this prediction: while cortical activity signifying the variability in choice behavior was indeed found in V1, that activity was dissociated from activity representing stimulus differences relevant to the task, being advanced in time and carried by a different neural ensemble. The spatiotemporal dynamics of population responses suggest that short-term priors, perhaps formed in higher cortical areas involved in perceptual inference, act to modulate V1 activity prior to stimulus onset without modifying subsequent activity that actually represents stimulus features within V1.

Long-range traveling waves of activity triggered by local dichoptic stimulation in V1 of behaving monkeys.

Traveling waves of cortical activity, in which local stimulation triggers lateral spread of activity to distal locations, have been hypothesized to play an important role in cortical function. However, there is conflicting physiological evidence for the existence of spreading traveling waves of neural activity triggered locally. Dichoptic stimulation, in which the two eyes view dissimilar monocular patterns, can lead to dynamic wave-like fluctuations in visual perception and therefore, provides a promising means for identifying and studying cortical traveling waves. Here, we used voltage-sensitive dye imaging to test for the existence of traveling waves of activity in the primary visual cortex of awake, fixating monkeys viewing dichoptic stimuli. We find clear traveling waves that are initiated by brief, localized contrast increments in one of the monocular patterns and then, propagate at speeds of ∼ 30 mm/s. These results demonstrate that under an appropriate visual context, circuitry in visual cortex in alert animals is capable of supporting long-range traveling waves triggered by local stimulation.

A new technique for generating disordered point-light animations for the study of biological motion perception.

Studies of biological motion perception often use stimuli depicting human actions portrayed via point-light (PL) displays. Typically, counterpart, or control, stimuli for PL biological motion are created by spatially scrambling motion trajectories of individual PL dots. Depending on the purpose of the study, however, this procedure may be inappropriate as a foil for genuine PL animations, because spatial scrambling not only disrupts coherent motion activity but also eliminates pair-wise motion relationships among dots and, unless corrected, alters the spatial spread of PL dot motions. We introduce a new technique for producing perturbed PL animations, called pair-wise shuffled motion, that preserves the elementary features of biological motion in spatial and motion energy domains and only disrupts the specific sense of global, coherent perception of biological motion. First we describe the procedure for creating pair-wise shuffled motion sequences. Next we compare unperturbed PL animations to pair-wise shuffled motion, to spatially scrambled motion, and to spatially constrained scrambled motion in terms of spatial distributions of the dots, spatiotemporal amplitude spectra derived from Fourier analysis of those sequences, and space-time motion energy associated with those perturbed animations. We then show that the results from those analyses generalize to a large family of PL animations, including the widely used PL walker. Finally we present results from a two-interval forced-choice biological-motion discrimination experiment comparing the robustness of scrambled and pair-wise shuffled motions as foil stimuli. Results from these comparisons suggest that pair-wise shuffled motion offers advantages as a foil stimulus compared to foils using the conventional scrambling technique. Pair-wise shuffled motion provides an additional, effective control display for evaluating PL biological motion perception in future psychophysical, computational, and imaging studies that focus on mechanisms of processing spatiotemporal information signifying biological motion within PL displays.

Chronic and acute biases in perceptual stabilization.

When perceptually ambiguous stimuli are presented intermittently, the percept on one presentation tends to be the same as that on the previous presentation. The role of short-term, acute biases in the production of this perceptual stability is relatively well understood. In addition, however, long-lasting, chronic bias may also contribute to stability. In this paper we develop indices for both biases and for stability, and show that stability can be expressed as a sum of contributions from the two types of bias. We then apply this analytical procedure to binocular rivalry, showing that adjustment of the monocular contrasts can alter the relative contributions of the two biases. Stability is mainly determined by chronic bias when the contrasts are equal, but acute bias dominates stability when right-eye contrast is set lower than left-eye contrast. Finally, we show that the right-eye bias persists in continuous binocular rivalry. Our findings reveal a previously unappreciated contribution of chronic bias to stable perception.

Kinesthesis can make an invisible hand visible.

Self-generated body movements have reliable visual consequences. This predictive association between vision and action likely underlies modulatory effects of action on visual processing. However, it is unknown whether actions can have generative effects on visual perception. We asked whether, in total darkness, self-generated body movements are sufficient to evoke normally concomitant visual perceptions. Using a deceptive experimental design, we discovered that waving one's own hand in front of one's covered eyes can cause visual sensations of motion. Conjecturing that these visual sensations arise from multisensory connectivity, we showed that grapheme-color synesthetes experience substantially stronger kinesthesis-induced visual sensations than nonsynesthetes do. Finally, we found that the perceived vividness of kinesthesis-induced visual sensations predicted participants' ability to smoothly track self-generated hand movements with their eyes in darkness, which indicates that these sensations function like typical retinally driven visual sensations. Evidently, even in the complete absence of external visual input, the brain predicts visual consequences of actions.

A new 'CFS tracking' paradigm reveals uniform suppression depth regardless of target complexity or salience.

When the eyes view separate and incompatible images, the brain suppresses one image and promotes the other into visual awareness. Periods of interocular suppression can be prolonged during continuous flash suppression (CFS) - when one eye views a static 'target' while the other views a complex dynamic stimulus. Measuring the time needed for a suppressed image to break CFS (bCFS) has been widely used to investigate unconscious processing, and the results have generated controversy regarding the scope of visual processing without awareness. Here, we address this controversy with a new 'CFS tracking' paradigm (tCFS) in which the suppressed monocular target steadily increases in contrast until breaking into awareness (as in bCFS) after which it decreases until it again disappears (reCFS), with this cycle continuing for many reversals. Unlike bCFS, tCFS provides a measure of suppression depth by quantifying the difference between breakthrough and suppression thresholds. tCFS confirms that (i) breakthrough thresholds indeed differ across target types (e.g. faces vs gratings, as bCFS has shown) - but (ii) suppression depth does not vary across target types. Once the breakthrough contrast is reached for a given stimulus, all stimuli require a strikingly uniform reduction in contrast to reach the corresponding suppression threshold. This uniform suppression depth points to a single mechanism of CFS suppression, one that likely occurs early in visual processing because suppression depth was not modulated by target salience or complexity. More fundamentally, it shows that variations in bCFS thresholds alone are insufficient for inferring whether the barrier to achieving awareness exerted by interocular suppression is weaker for some categories of visual stimuli compared to others.

Audiovisual interactions outside of visual awareness during motion adaptation.

Motion aftereffects (MAEs), illusory motion experienced in a direction opposed to real motion experienced during prior adaptation, have been used to assess audiovisual interactions. In a previous study from our laboratory, we demonstrated that a congruent direction of auditory motion presented concurrently with visual motion during adaptation strengthened the consequent visual MAE, compared to when auditory motion was incongruent in direction. Those judgments of MAE strength, however, could have been influenced by expectations or response bias from mere knowledge of the state of audiovisual congruity during adaptation. To prevent such knowledge, we now employed continuous flash suppression to render visual motion perceptually invisible during adaptation, ensuring that observers were completely unaware of visual adapting motion and only aware of the motion direction of the sound they were hearing. We found a small but statistically significant congruence effect of sound on adaptation strength produced by invisible adaptation motion. After considering alternative explanations for this finding, we conclude that auditory motion can impact the strength of visual processing produced by translational visual motion even when that motion transpires outside of awareness.

Binocular rivalry under naturalistic geometry: Evidence from worlds simulated in virtual reality.

Binocular rivalry is a fascinating, widely studied visual phenomenon in which perception alternates between two competing images. This experience, however, is generally restricted to laboratory settings where two irreconcilable images are presented separately to the two eyes, an implausible geometry where two objects occupy the same physical location. Such laboratory experiences are in stark contrast to everyday visual behavior, where rivalry is almost never encountered, casting doubt on whether rivalry is relevant to our understanding of everyday binocular vision. To investigate the external validity of binocular rivalry, we manipulated the geometric plausibility of rival images using a naturalistic, cue-rich, 3D-corridor model created in virtual reality. Rival stimuli were presented in geometrically implausible, semi-plausible, or plausible layouts. Participants tracked rivalry fluctuations in each of these three layouts and for both static and moving rival stimuli. Results revealed significant and canonical binocular rivalry alternations regardless of geometrical plausibility and stimulus type. Rivalry occurred for layouts that mirrored the unnatural geometry used in laboratory studies and for layouts that mimicked real-world occlusion geometry. In a complementary 3D modeling analysis, we show that interocular conflict caused by geometrically plausible occlusion is a common outcome in a visual scene containing multiple objects. Together, our findings demonstrate that binocular rivalry can reliably occur for both geometrically implausible interocular conflicts and conflicts caused by a common form of naturalistic occlusion. Thus, key features of binocular rivalry are not simply laboratory artifacts but generalize to conditions that match the geometry of everyday binocular vision.