Positive and negative facial valence perception are modulated differently by eccentricity in the parafovea: Replication from KDEF to NimStim.

While perceiving the emotional state of others may be crucial for our behavior even when this information is present outside of central vision, emotion perception studies typically focus on central visual field. We have recently investigated emotional valence (pleasantness) perception across the parafovea (≤ 4°) and found that for briefly presented (200 ms) emotional face images (from the established KDEF image-set), positive (happy) valence was the least affected by eccentricity (distance from the central visual field) and negative (fearful) valence the most. Furthermore, we found that performance at 2° predicted performance at 4°. Here we tested (n = 37) whether these effects replicate with face stimuli of different identities from a different well-established image-set (NimStim). All our prior findings replicated and eccentricity-based modulation magnitude was smaller with NimStim (~ 16.6% accuracy reduction at 4°) than with KDEF stimuli (~ 27.3% reduction). Our current investigations support our earlier findings that for briefly presented parafoveal stimuli, positive and negative valence perception are differently affected by eccentricity and may be dissociated. Furthermore, our results highlight the importance of investigating emotions beyond central vision and demonstrate commonalities and differences across different image sets in the parafovea, emphasizing the contribution of replication studies to substantiate our knowledge about perceptual mechanisms.

Higher-contrast images are better remembered during naturalistic encoding.

It is unclear whether memory for images of poorer visibility (as low contrast or small size) will be lower due to weak signals elicited in early visual processing stages, or perhaps better since their processing may entail top-down processes (as effort and attention) associated with deeper encoding. We have recently shown that during naturalistic encoding (free viewing without task-related modulations), for image sizes between 3°-24°, bigger images stimulating more visual system processing resources at early processing stages are better remembered. Similar to size, higher contrast leads to higher activity in early visual processing. Therefore, here we hypothesized that during naturalistic encoding, at critical visibility ranges, higher contrast images will lead to higher signal-to-noise ratio and better signal quality flowing downstream and will thus be better remembered. Indeed, we found that during naturalistic encoding higher contrast images were remembered better than lower contrast ones (~ 15% higher accuracy, ~ 1.58 times better) for images at 7.5-60 RMS contrast range. Although image contrast and size modulate early visual processing very differently, our results further substantiate that at poor visibility ranges, during naturalistic non-instructed visual behavior, physical image dimensions (contributing to image visibility) impact image memory.

Parafoveal vision reveals qualitative differences between fusiform face area and parahippocampal place area.

The center-periphery visual field axis guides early visual system organization with enhanced resources devoted to central vision leading to reduced peripheral performance relative to that of central vision (i.e., behavioral eccentricity effect) for many visual functions. The center-periphery organization extends to high-order visual cortex where, for example, the well-studied face-sensitive fusiform face area (FFA) shows sensitivity to central vision and the place-sensitive parahippocampal place area (PPA) shows sensitivity to peripheral vision. As we have recently found that face perception is more sensitive to eccentricity than place perception, here we examined whether these behavioral findings reflect differences in FFA's and PPA's sensitivities to eccentricity. We assumed FFA would show higher sensitivity to eccentricity than PPA would, but that both regions' modulation by eccentricity would be invariant to the viewed category. We parametrically investigated (fMRI, n = 32) how FFA's and PPA's activations are modulated by eccentricity (≤8°) and category (upright/inverted faces/houses) while keeping stimulus size constant. As expected, FFA showed an overall higher sensitivity to eccentricity than PPA. However, both regions' activation modulations by eccentricity were dependent on the viewed category. In FFA, a reduction of activation with growing eccentricity ("BOLD eccentricity effect") was found (with different amplitudes) for all categories. In PPA however, qualitatively different BOLD eccentricity effect modulations were found (e.g., at 8° mild BOLD eccentricity effect for houses but a reverse BOLD eccentricity effect for faces and no modulation for inverted faces). Our results emphasize that peripheral vision investigations are critical to further our understanding of visual processing.

Positive and negative facial valence perception are modulated differently by eccentricity in the parafovea.

Understanding whether people around us are in a good, bad or neutral mood can be critical to our behavior, both when looking directly at them or when they are in our peripheral visual field. However, facial expressions of emotions are often investigated at central visual field or at locations right or left of fixation. Here we assumed that perception of facial emotional valence (the emotion's pleasantness) changes with distance from central visual field (eccentricity) and that different emotions may be influenced differently by eccentricity. Participants (n = 58) judged the valence of emotional faces across the parafovea (≤ 4°, positive (happy), negative (fearful), or neutral)) while their eyes were being tracked. As expected, performance decreased with eccentricity. Positive valence perception was least affected by eccentricity (accuracy reduction of 10-19% at 4°) and negative the most (accuracy reduction of 35-38% at 4°), and this was not a result of speed-accuracy trade-off or response biases. Within-valence (but not across-valence) performance was associated across eccentricities suggesting perception of different valences is supported by different mechanisms. While our results may not generalize to all positive and negative emotions, they indicate that beyond-foveal investigations can reveal additional characteristics of the mechanisms that underlie facial expression processing and perception.

Larger images are better remembered during naturalistic encoding.

We are constantly exposed to multiple visual scenes, and while freely viewing them without an intentional effort to memorize or encode them, only some are remembered. It has been suggested that image memory is influenced by multiple factors, such as depth of processing, familiarity, and visual category. However, this is typically investigated when people are instructed to perform a task (e.g., remember or make some judgment about the images), which may modulate processing at multiple levels and thus, may not generalize to naturalistic visual behavior. Visual memory is assumed to rely on high-level visual perception that shows a level of size invariance and therefore is not assumed to be highly dependent on image size. Here, we reasoned that during naturalistic vision, free of task-related modulations, bigger images stimulate more visual system processing resources (from retina to cortex) and would, therefore, be better remembered. In an extensive set of seven experiments, naïve participants (n = 182) were asked to freely view presented images (sized 3° to 24°) without any instructed encoding task. Afterward, they were given a surprise recognition test (midsized images, 50% already seen). Larger images were remembered better than smaller ones across all experiments (∼20% higher accuracy or ∼1.5 times better). Memory was proportional to image size, faces were better remembered, and outdoors the least. Results were robust even when controlling for image set, presentation order, screen resolution, image scaling at test, or the amount of information. While multiple factors affect image memory, our results suggest that low- to high-level processes may all contribute to image memory.

Gait Speed Modulations Are Proportional to Grades of Virtual Visual Slopes-A Virtual Reality Study.

Gait is a complex mechanism relying on integration of several sensory inputs such as vestibular, proprioceptive, and visual cues to maintain stability while walking. Often humans adapt their gait to changes in surface inclinations, and this is typically achieved by modulating walking speed according to the inclination in order to counteract the gravitational forces, either uphill (exertion effect) or downhill (braking effect). The contribution of vision to these speed modulations is not fully understood. Here we assessed gait speed effects by parametrically manipulating the discrepancy between virtual visual inclination and the actual surface inclination (aka visual incongruence). Fifteen healthy participants walked in a large-scale virtual reality (VR) system on a self-paced treadmill synchronized with projected visual scenes. During walking they were randomly exposed to varying degrees of physical-visual incongruence inclinations (e.g., treadmill leveled & visual scene uphill) in a wide range of inclinations (-15° to +15°). We observed an approximately linear relation between the relative change in gait speed and the anticipated gravitational forces associated with the virtual inclinations. Mean relative gait speed increase of ~7%, ~11%, and ~17% were measured for virtual inclinations of +5°, +10°, and +15°, respectively (anticipated decelerating forces were proportional to sin[5°], sin[10°], sin[15°]). The same pattern was seen for downhill virtual inclinations with relative gait speed modulations of ~-10%, ~-16%, and ~-24% for inclinations of -5°, -10°, and -15°, respectively (in anticipation of accelerating forces). Furthermore, we observed that the magnitude of speed modulation following virtual inclination at ±10° was associated with subjective visual verticality misperception. In conclusion, visual cues modulate gait speed when surface inclinations change proportional to the anticipated effect of the gravitational force associated the inclinations. Our results emphasize the contribution of vision to locomotion in a dynamic environment and may enhance personalized rehabilitation strategies for gait speed modulations in neurological patients with gait impairments.

Vision Affects Gait Speed but not Patterns of Muscle Activation During Inclined Walking-A Virtual Reality Study.

While walking, our locomotion is affected by and adapts to the environment based on vision- and body-based (vestibular and proprioception) cues. When transitioning to downhill walking, we modulate gait by braking to avoid uncontrolled acceleration, and when transitioning to uphill walking, we exert effort to avoid deceleration. In this study, we aimed to measure the influence of visual inputs on this behavior and on muscle activation. Specifically, we aimed to explore whether the gait speed modulations triggered by mere visual cues after transitioning to virtually inclined surface walking are accompanied by changes in muscle activation patterns typical to those triggered by veridical (gravitational) surface inclination transitions. We used an immersive virtual reality system equipped with a self-paced treadmill and projected visual scenes that allowed us to modulate physical-visual inclination congruence parametrically. Gait speed and leg muscle electromyography were measured in 12 healthy young adults. In addition, the magnitude of subjective visual verticality misperception (SVV) was measured by the rod and frame test. During virtual (non-veridical) inclination transitions, vision modulated gait speed by (i) slowing down to counteract the excepted gravitational "boost" in virtual downhill inclinations and (ii) speeding up to counteract the expected gravity resistance in virtual uphill inclinations. These gait speed modulations were reflected in muscle activation intensity changes and associated with SVV misperception. However, temporal patterns of muscle activation were not affected by virtual (visual) inclination transitions. Our results delineate the contribution of vision to locomotion and may lead to enhanced rehabilitation strategies for neurological disorders affecting movement.

Investigating face and house discrimination at foveal to parafoveal locations reveals category-specific characteristics.

Since perceptual and neural face sensitivity is associated with a foveal bias, and neural place sensitivity is associated with a peripheral bias (integration over space), we hypothesized that face perception ability will decline more with eccentricity than place perception ability. We also wanted to examine whether face perception ability would show a left visual field (LeVF) bias due to earlier reports suggesting right hemisphere dominance for faces, or would show an upper or lower visual field bias. Participants performed foveal and parafoveal face and house discrimination tasks for upright or inverted stimuli (≤4°) while their eye movements were monitored. Low-level visual tasks were also measured. The eccentricity-related accuracy reductions were evident for all categories. Through detailed analyses we found (i) a robust face inversion effect across the parafovea, while for houses an opposite effect was found, (ii) higher eccentricity-related sensitivity for face performance than for house performance (via inverted vs. upright within-category eccentricity-driven reductions), (iii) within-category but not across-category performance associations across eccentricities, and (iv) no hemifield biases. Our central to parafoveal investigations suggest that high-level vision processing may be reflected in behavioural performance.

The contribution of facial dynamics to subtle expression recognition in typical viewers and developmental visual agnosia.

Facial expressions are inherently dynamic cues that develop and change over time, unfolding their affective signal. Although facial dynamics are assumed important for emotion recognition, testing often involves intense and stereotypical expressions and little is known about the role of temporal information in the recognition of subtle, non-stereotypical expressions. In Experiment 1 we demonstrate that facial dynamics are critical for recognizing subtle and non-stereotypical facial expressions, but not for recognizing intense and stereotypical displays of emotion. In Experiment 2 we further examined whether the facilitative effect of motion can lead to improved emotion recognition in LG, an individual with developmental visual agnosia and prosopagnosia, who has poor emotion recognition when tested with static facial expressions. LG's emotion recognition improved when subtle, non-stereotypical faces were dynamic rather than static. However, compared to controls, his relative gain from temporal information was diminished. Furthermore, LG's eye-tracking data demonstrated atypical visual scanning of the dynamic faces, consisting of longer fixations and lower fixation rates for the dynamic-subtle facial expressions, comparing to the dynamic-intense facial expressions. We suggest that deciphering subtle dynamic expressions strongly relies on integrating broad facial regions across time, rather than focusing on local emotional cues, skills which are impaired in developmental visual agnosia.

Developmental visual perception deficits with no indications of prosopagnosia in a child with abnormal eye movements.

Visual categories are associated with eccentricity biases in high-order visual cortex: Faces and reading with foveally-biased regions, while common objects and space with mid- and peripherally-biased regions. As face perception and reading are among the most challenging human visual skills, and are often regarded as the peak achievements of a distributed neural network supporting common objects perception, it is unclear why objects, which also rely on foveal vision to be processed, are associated with mid-peripheral rather than with a foveal bias. Here, we studied BN, a 9 y.o. boy who has normal basic-level vision, abnormal (limited) oculomotor pursuit and saccades, and shows developmental object and contour integration deficits but with no indication of prosopagnosia. Although we cannot infer causation from the data presented here, we suggest that normal pursuit and saccades could be critical for the development of contour integration and object perception. While faces and perhaps reading, when fixated upon, take up a small portion of central visual field and require only small eye movements to be properly processed, common objects typically prevail in mid-peripheral visual field and rely on longer-distance voluntary eye movements as saccades to be brought to fixation. While retinal information feeds into early visual cortex in an eccentricity orderly manner, we hypothesize that propagation of non-foveal information to mid and high-order visual cortex critically relies on circuitry involving eye movements. Limited or atypical eye movements, as in the case of BN, may hinder normal information flow to mid-eccentricity biased high-order visual cortex, adversely affecting its development and consequently inducing visual perceptual deficits predominantly for categories associated with these regions.

Perceptual similarity and the neural correlates of geometrical illusions in human brain structure.

Geometrical visual illusions are an intriguing phenomenon, in which subjective perception consistently misjudges the objective, physical properties of the visual stimulus. Prominent theoretical proposals have been advanced attempting to find common mechanisms across illusions. But empirically testing the similarity between illusions has been notoriously difficult because illusions have very different visual appearances. Here we overcome this difficulty by capitalizing on the variability of the illusory magnitude across participants. Fifty-nine healthy volunteers participated in the study that included measurement of individual illusion magnitude and structural MRI scanning. We tested the Muller-Lyer, Ebbinghaus, Ponzo, and vertical-horizontal geometrical illusions as well as a non-geometrical, contrast illusion. We found some degree of similarity in behavioral judgments of all tested geometrical illusions, but not between geometrical illusions and non-geometrical, contrast illusion. The highest similarity was found between Ebbinghaus and Muller-Lyer geometrical illusions. Furthermore, the magnitude of all geometrical illusions, and particularly the Ebbinghaus and Muller-Lyer illusions, correlated with local gray matter density in the parahippocampal cortex, but not in other brain areas. Our findings suggest that visuospatial integration and scene construction processes might partly mediate individual differences in geometric illusory perception. Overall, these findings contribute to a better understanding of the mechanisms behind geometrical illusions.

Neuroanatomy accounts for age-related changes in risk preferences.

Many decisions involve uncertainty, or 'risk', regarding potential outcomes, and substantial empirical evidence has demonstrated that human aging is associated with diminished tolerance for risky rewards. Grey matter volume in a region of right posterior parietal cortex (rPPC) is predictive of preferences for risky rewards in young adults, with less grey matter volume indicating decreased tolerance for risk. That grey matter loss in parietal regions is a part of healthy aging suggests that diminished rPPC grey matter volume may have a role in modulating risk preferences in older adults. Here we report evidence for this hypothesis and show that age-related declines in rPPC grey matter volume better account for age-related changes in risk preferences than does age per se. These results provide a basis for understanding the neural mechanisms that mediate risky choice and a glimpse into the neurodevelopmental dynamics that impact decision-making in an aging population.

Visual motion serves but is not under the purview of the dorsal pathway.

Visual motion processing is often attributed to the dorsal visual pathway despite visual motion's involvement in almost all visual functions. Furthermore, some visual motion tasks critically depend on the structural integrity of regions outside the dorsal pathway. Here, based on numerous studies, I propose that visual motion signals are swiftly transmitted via multiple non-hierarchical routes to primary motion-dedicated processing regions (MT/V5 and MST) that are not part of the dorsal pathway, and then propagated to a multiplicity of brain areas according to task demands, reaching these regions earlier than the dorsal/ventral hierarchical flow. This not only places MT/V5 at the same or even earlier visual processing stage as that of V1, but can also elucidate many findings with implications to visual awareness. While the integrity of the non-hierarchical motion pathway is necessary for all visual motion perception, it is insufficient on its own, and the transfer of visual motion signals to additional brain areas is crucial to allow the different motion perception tasks (e.g. optic flow, visuo-vestibular balance, movement observation, dynamic form detection and perception, and even reading). I argue that this lateral visual motion pathway can be distinguished from the dorsal pathway not only based on faster response latencies and distinct anatomical connections, but also based on its full field representation. I also distinguish between this primary lateral visual motion pathway sensitive to all motion in the visual field, and a much less investigated optic flow sensitive medial processing pathway (from V1 to V6 and V6A) that appears to be part of the dorsal pathway. Multiple additional predictions are provided that allow testing this proposal and distinguishing between the visual pathways.

A Possible Link between Supra-Second Open-Ended Timing Sensitivity and Obsessive-Compulsive Tendencies.

One of the main characteristics of obsessive-compulsive disorder (OCD) is the persistent feeling of uncertainty, affecting many domains of actions and feelings. It was recently hypothesized that OCD uncertainty is related to attenuated access to internal states. As supra-second timing is associated with bodily and interoceptive awareness, we examined whether supra-second timing would be associated with OC tendencies. We measured supra-second (~9 s) and sub-second (~450 ms) timing along with control non-temporal perceptual tasks in a group of 60 university students. Supra-second timing was measured either with fixed criterion tasks requiring to temporally discriminate between two predefined fixed interval durations (9 vs. 9.9 s), or with an open-ended task requiring to discriminate between 9 s and longer intervals which were of varying durations that were not a priori known to the participants. The open-ended task employed an adaptive Bayesian procedure that efficiently estimated the duration difference required to discriminate 9 s from longer intervals. We also assessed symptoms of OCD, depression, and anxiety. Open-ended supra-second temporal sensitivity was correlated with OC tendencies, as predicted (even after controlling for depression and anxiety), whereas the other tasks were not. Higher OC tendencies were associated with lower timing sensitivity to 9 s intervals such that participants with higher OC tendency scores required longer interval differences to discriminate 9 s from longer intervals. While these results need to be substantiated in future research, they suggest that open-ended timing tasks, as those encountered in real-life (e.g., estimating how long it would take to complete a task), might be adversely affected in OCD.

Functional dissociation between action and perception of object shape in developmental visual object agnosia.

According to the two visual systems model, the cortical visual system is segregated into a ventral pathway mediating object recognition, and a dorsal pathway mediating visuomotor control. In the present study we examined whether the visual control of action could develop normally even when visual perceptual abilities are compromised from early childhood onward. Using his fingers, LG, an individual with a rare developmental visual object agnosia, manually estimated (perceptual condition) the width of blocks that varied in width and length (but not in overall size), or simply picked them up across their width (grasping condition). LG's perceptual sensitivity to target width was profoundly impaired in the manual estimation task compared to matched controls. In contrast, the sensitivity to object shape during grasping, as measured by maximum grip aperture (MGA), the time to reach the MGA, the reaction time and the total movement time were all normal in LG. Further analysis, however, revealed that LG's sensitivity to object shape during grasping emerged at a later time stage during the movement compared to controls. Taken together, these results demonstrate a dissociation between action and perception of object shape, and also point to a distinction between different stages of the grasping movement, namely planning versus online control. Moreover, the present study implies that visuomotor abilities can develop normally even when perceptual abilities developed in a profoundly impaired fashion.

Which visual functions depend on intermediate visual regions? Insights from a case of developmental visual form agnosia.

A key question in visual neuroscience is the causal link between specific brain areas and perceptual functions; which regions are necessary for which visual functions? While the contribution of primary visual cortex and high-level visual regions to visual perception has been extensively investigated, the contribution of intermediate visual areas (e.g. V2/V3) to visual processes remains unclear. Here I review more than 20 visual functions (early, mid, and high-level) of LG, a developmental visual agnosic and prosopagnosic young adult, whose intermediate visual regions function in a significantly abnormal fashion as revealed through extensive fMRI and ERP investigations. While expectedly, some of LG's visual functions are significantly impaired, some of his visual functions are surprisingly normal (e.g. stereopsis, color, reading, biological motion). During the period of eight-year testing described here, LG trained on a perceptual learning paradigm that was successful in improving some but not all of his visual functions. Following LG's visual performance and taking into account additional findings in the field, I propose a framework for how different visual areas contribute to different visual functions, with an emphasis on intermediate visual regions. Thus, although rewiring and plasticity in the brain can occur during development to overcome and compensate for hindering developmental factors, LG's case seems to indicate that some visual functions are much less dependent on strict hierarchical flow than others, and can develop normally in spite of abnormal mid-level visual areas, thereby probably less dependent on intermediate visual regions.

Ventral aspect of the visual form pathway is not critical for the perception of biological motion.

Identifying the movements of those around us is fundamental for many daily activities, such as recognizing actions, detecting predators, and interacting with others socially. A key question concerns the neurobiological substrates underlying biological motion perception. Although the ventral "form" visual cortex is standardly activated by biologically moving stimuli, whether these activations are functionally critical for biological motion perception or are epiphenomenal remains unknown. To address this question, we examined whether focal damage to regions of the ventral visual cortex, resulting in significant deficits in form perception, adversely affects biological motion perception. Six patients with damage to the ventral cortex were tested with sensitive point-light display paradigms. All patients were able to recognize unmasked point-light displays and their perceptual thresholds were not significantly different from those of three different control groups, one of which comprised brain-damaged patients with spared ventral cortex (n > 50). Importantly, these six patients performed significantly better than patients with damage to regions critical for biological motion perception. To assess the necessary contribution of different regions in the ventral pathway to biological motion perception, we complement the behavioral findings with a fine-grained comparison between the lesion location and extent, and the cortical regions standardly implicated in biological motion processing. This analysis revealed that the ventral aspects of the form pathway (e.g., fusiform regions, ventral extrastriate body area) are not critical for biological motion perception. We hypothesize that the role of these ventral regions is to provide enhanced multiview/posture representations of the moving person rather than to represent biological motion perception per se.

Training-induced recovery of low-level vision followed by mid-level perceptual improvements in developmental object and face agnosia.

Long-term deprivation of normal visual inputs can cause perceptual impairments at various levels of visual function, from basic visual acuity deficits, through mid-level deficits such as contour integration and motion coherence, to high-level face and object agnosia. Yet it is unclear whether training during adulthood, at a post-developmental stage of the adult visual system, can overcome such developmental impairments. Here, we visually trained LG, a developmental object and face agnosic individual. Prior to training, at the age of 20, LG's basic and mid-level visual functions such as visual acuity, crowding effects, and contour integration were underdeveloped relative to normal adult vision, corresponding to or poorer than those of 5-6 year olds (Gilaie-Dotan, Perry, Bonneh, Malach & Bentin, 2009). Intensive visual training, based on lateral interactions, was applied for a period of 9 months. LG's directly trained but also untrained visual functions such as visual acuity, crowding, binocular stereopsis and also mid-level contour integration improved significantly and reached near-age-level performance, with long-term (over 4 years) persistence. Moreover, mid-level functions that were tested post-training were found to be normal in LG. Some possible subtle improvement was observed in LG's higher-order visual functions such as object recognition and part integration, while LG's face perception skills have not improved thus far. These results suggest that corrective training at a post-developmental stage, even in the adult visual system, can prove effective, and its enduring effects are the basis for a revival of a developmental cascade that can lead to reduced perceptual impairments.

Training improves visual processing speed and generalizes to untrained functions.

Studies show that manipulating certain training features in perceptual learning determines the specificity of the improvement. The improvement in abnormal visual processing following training and its generalization to visual acuity, as measured on static clinical charts, can be explained by improved sensitivity or processing speed. Crowding, the inability to recognize objects in a clutter, fundamentally limits conscious visual perception. Although it was largely considered absent in the fovea, earlier studies report foveal crowding upon very brief exposures or following spatial manipulations. Here we used GlassesOff's application for iDevices to train foveal vision of young participants. The training was performed at reading distance based on contrast detection tasks under different spatial and temporal constraints using Gabor patches aimed at testing improvement of processing speed. We found several significant improvements in spatio-temporal visual functions including near and also non-trained far distances. A remarkable transfer to visual acuity measured under crowded conditions resulted in reduced processing time of 81 ms, in order to achieve 6/6 acuity. Despite a subtle change in contrast sensitivity, a robust increase in processing speed was found. Thus, enhanced processing speed may lead to overcoming foveal crowding and might be the enabling factor for generalization to other visual functions.