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.

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.

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.

Neuroanatomy predicts individual risk attitudes.

Over the course of the last decade a multitude of studies have investigated the relationship between neural activations and individual human decision-making. Here we asked whether the anatomical features of individual human brains could be used to predict the fundamental preferences of human choosers. To that end, we quantified the risk attitudes of human decision-makers using standard economic tools and quantified the gray matter cortical volume in all brain areas using standard neurobiological tools. Our whole-brain analysis revealed that the gray matter volume of a region in the right posterior parietal cortex was significantly predictive of individual risk attitudes. Participants with higher gray matter volume in this region exhibited less risk aversion. To test the robustness of this finding we examined a second group of participants and used econometric tools to test the ex ante hypothesis that gray matter volume in this area predicts individual risk attitudes. Our finding was confirmed in this second group. Our results, while being silent about causal relationships, identify what might be considered the first stable biomarker for financial risk-attitude. If these results, gathered in a population of midlife northeast American adults, hold in the general population, they will provide constraints on the possible neural mechanisms underlying risk attitudes. The results will also provide a simple measurement of risk attitudes that could be easily extracted from abundance of existing medical brain scans, and could potentially provide a characteristic distribution of these attitudes for policy makers.

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.

The role of human ventral visual cortex in motion perception.

Visual motion perception is fundamental to many aspects of visual perception. Visual motion perception has long been associated with the dorsal (parietal) pathway and the involvement of the ventral 'form' (temporal) visual pathway has not been considered critical for normal motion perception. Here, we evaluated this view by examining whether circumscribed damage to ventral visual cortex impaired motion perception. The perception of motion in basic, non-form tasks (motion coherence and motion detection) and complex structure-from-motion, for a wide range of motion speeds, all centrally displayed, was assessed in five patients with a circumscribed lesion to either the right or left ventral visual pathway. Patients with a right, but not with a left, ventral visual lesion displayed widespread impairments in central motion perception even for non-form motion, for both slow and for fast speeds, and this held true independent of the integrity of areas MT/V5, V3A or parietal regions. In contrast with the traditional view in which only the dorsal visual stream is critical for motion perception, these novel findings implicate a more distributed circuit in which the integrity of the right ventral visual pathway is also necessary even for the perception of non-form motion.

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.

Resting state functional connectivity reflects abnormal task-activated patterns in a developmental object agnosic.

Even in the absence of stimulation or task, the cerebral cortex shows an incessant pattern of ultra slow fluctuations which are coherent across brain regions. In the healthy brain these coherent patterns (also termed resting state functional connectivity) often exhibit spatial similarity to the large scale organization of task-induced functional networks. However, it is not clear to what extent the resting state patterns can also reflect task-induced abnormalities in cortical activations which are often detected in various brain pathologies. Here we examined whether an abnormal visual activation pattern is recapitulated in the resting state functional connectivity. We examined LG, a sighted young adult with developmental object agnosia and no apparent cortical structural abnormality. We have previously reported that upon visual stimulation, LG's intermediate visual areas (V2, V3) are paradoxically deactivated. Here, examining LG's resting state functional connectivity revealed the same pattern of functional abnormality - including a strong atypical decorrelation between areas V2-V3 and the rest of the visual system. Thus, our results suggest that resting-state functional connectivity could provide a powerful tool which could complement task-specific paradigms in detecting task-related abnormalities in cortical activity without resorting to task performance.

Neuroanatomical correlates of visual car expertise.

Expertise in non-visual domains such as musical performance is associated with differences in gray matter volume of particular regions of the human brain. Whether this is also the case for expertise in visual object recognition is unknown. Here we tested whether individual variability in the ability to recognize car models, from novice performance to high level of expertise, is associated with specific structural changes in gray matter volume. We found that inter-individual variability in expertise with cars was significantly and selectively correlated with gray matter volume in prefrontal cortex. Inter-individual differences in the recognition of airplanes, that none of the participants had expertise with, were correlated with structural variability of regions bordering the visual cortex. These results highlight the role of prefrontal regions outside the visual cortex in accessing and processing visual knowledge about objects from the domain of expertise and suggest that expertise in visual object recognition may entail structural changes in regions associated with semantic knowledge.

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.

Top-down engagement modulates the neural expressions of visual expertise.

Perceptual expertise is traditionally associated with enhanced brain activity in response to objects of expertise in category-selective visual cortex, primarily face-selective regions. We reevaluated this view by investigating whether the brain activity associated with expertise in object recognition is limited to category-selective cortex and specifically whether the extent of expertise-related activity manifests automatically or whether it can be top-down modulated. We conducted 2 functional magnetic resonance imaging studies comparing changes in hemodynamic activity associated with car expertise in a conventional 1-back task (Experiment 1) and when the task relevance of cars was explicitly manipulated (Experiment 2). Whole-brain analysis unveiled extensive expertise-related activity throughout the visual cortex, starting as early as V1 and extending into nonvisual areas. However, when the cars were task irrelevant, the expertise-related activity drastically diminished, indeed, becoming similar to the activity elicited by cars in novices. We suggest that expertise entails voluntary top-down engagement of multiple neural networks in addition to stimulus-driven activation associated with perceptual mechanisms.

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.

Perceptual shape sensitivity to upright and inverted faces is reflected in neuronal adaptation.

Using an fMR-adaptation paradigm for different face morphing levels we have recently demonstrated a narrow neuronal tuning to faces even at the sub-exemplar level which was tightly related to perceptual discrimination (Gilaie-Dotan and Malach, 2007). However, it is unclear whether this relationship is unique to faces or is a general property of object representations including unfamiliar objects, and whether the adaptation tuning is due to physical changes in the stimulus or to changes in perceptual discrimination. Here we compared the same face-morph paradigm for upright and inverted faces, thus modulating familiarity and perceptual discrimination effects while equating all low-level features. We found, as expected, a perceptual "inversion effect", i.e. a significant reduction in inverted face discrimination. Importantly, the fMR-adaptation tuning in the fusiform face area (FFA) changed in accordance with the different perceptual sensitivity both for upright and inverted faces. Additional object selective regions displayed differential tuning widths to the two categories. Our results are compatible with a model by which the ability of human observers to discriminate objects depends on the shape tuning properties of individual neurons.

Investigating object representations during change detection in human extrastriate cortex.

Detecting a change in a visual stimulus is particularly difficult when it is accompanied by a visual disruption such as a saccade or flicker. In order to say whether a stimulus has changed across such a disruption, some neural trace must persist. Here we investigated whether two different regions of the human extrastriate visual cortex contain neuronal populations encoding such a trace. Participants viewed a stimulus that included various objects and a short blank period (flicker) made it difficult to distinguish whether an object in the stimulus had changed or not. By applying transcranial magnetic stimulation (TMS) during the visual disruption we show that the lateral occipital (LO) cortex, but not the occipital face area, contains a sustained representation of a visual stimulus. TMS over LO improved the sensitivity and response bias for detecting changes by selectively reducing false alarms. We suggest that TMS enhanced the initial object representation and thus boosted neural events associated with object repetition. Our findings show that neuronal signals in the human LO cortex carry a sustained neural trace that is necessary for detecting the repetition of a stimulus.

Seeing with profoundly deactivated mid-level visual areas: non-hierarchical functioning in the human visual cortex.

A fundamental concept in visual processing is that activity in high-order object-category distinctive regions (e.g., lateral occipital complex, fusiform face area, middle temporal+) is dependent on bottom-up flow of activity in earlier retinotopic areas (V2, V3, V4) whose main input originates from primary visual cortex (V1). Thus, activity in down stream areas should reflect lower-level inputs. Here we qualify this notion reporting case LG, a rare case of developmental object agnosia and prosopagnosia. In this person, V1 was robustly activated by visual stimuli, yet intermediate areas (V2-V4) were strongly deactivated. Despite this intermediate deactivation, activity in down stream visual areas remained robust, showing selectivity for houses and places, while selectivity for faces and objects was impaired. The extent of impairment evident in functional magnetic resonance imaging and electroencephalography activations was somewhat larger in the left hemisphere. This pattern of brain activity, coupled with fairly adequate everyday visual performance is compatible with models emphasizing the role of nonlinear local "amplification" of neuronal inputs in eliciting activity in ventral and dorsal visual pathways as well as perceptual experience in the human brain. Thus, while the proper functioning of intermediate areas appears essential for specialization in the cortex, daily visual behavior and reading are maintained even with deactivated intermediate visual areas.

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.