Symmetry Processing in the Macaque Visual Cortex.

Symmetry is a highly salient feature of the natural world that is perceived by many species. In humans, the cerebral areas processing symmetry are now well identified from neuroimaging measurements. Macaque could constitute a good animal model to explore the underlying neural mechanisms, but a previous comparative study concluded that functional magnetic resonance imaging responses to mirror symmetry in this species were weaker than those observed in humans. Here, we re-examined symmetry processing in macaques from a broader perspective, using both rotation and reflection symmetry embedded in regular textures. Highly consistent responses to symmetry were found in a large network of areas (notably in areas V3 and V4), in line with what was reported in humans under identical experimental conditions. Our results suggest that the cortical networks that process symmetry in humans and macaques are potentially more similar than previously reported and point toward macaque as a relevant model for understanding symmetry processing.

Perceived group size is determined by the centroids of the component elements.

To accomplish the deceptively simple task of perceiving the size of objects in the visual scene, the visual system combines information about the retinal size of the object with several other cues, including perceived distance, relative size, and prior knowledge. When local component elements are perceptually grouped to form objects, the task is further complicated because a grouped object does not have a continuous contour from which retinal size can be estimated. Here, we investigate how the visual system solves this problem and makes it possible for observers to judge the size of perceptually grouped objects. We systematically vary the shape and orientation of the component elements in a two-alternative forced-choice task and find that the perceived size of the array of component objects can be almost perfectly predicted from the distance between the centroids of the component elements and the center of the array. This is true whether the global contour forms a circle or a square. When elements were positioned such that the centroids along the global contour were at different distances from the center, perceived size was based on the average distance. These results indicate that perceived size does not depend on the size of individual elements, and that smooth contours formed by the outer edges of the component elements are not used to estimate size. The current study adds to a growing literature highlighting the importance of centroids in visual perception and may have implications for how size is estimated for ensembles of different objects.

Visual and auditory brain areas share a representational structure that supports emotion perception.

Emotionally expressive music and dance occur together across the world. This may be because features shared across the senses are represented the same way even in different sensory brain areas, putting music and movement in directly comparable terms. These shared representations may arise from a general need to identify environmentally relevant combinations of sensory features, particularly those that communicate emotion. To test the hypothesis that visual and auditory brain areas share a representational structure, we created music and animation stimuli with crossmodally matched features expressing a range of emotions. Participants confirmed that each emotion corresponded to a set of features shared across music and movement. A subset of participants viewed both music and animation during brain scanning, revealing that representations in auditory and visual brain areas were similar to one another. This shared representation captured not only simple stimulus features but also combinations of features associated with emotion judgments. The posterior superior temporal cortex represented both music and movement using this same structure, suggesting supramodal abstraction of sensory content. Further exploratory analysis revealed that early visual cortex used this shared representational structure even when stimuli were presented auditorily. We propose that crossmodally shared representations support mutually reinforcing dynamics across auditory and visual brain areas, facilitating crossmodal comparison. These shared representations may help explain why emotions are so readily perceived and why some dynamic emotional expressions can generalize across cultural contexts.

The human visual system preserves the hierarchy of two-dimensional pattern regularity.

Symmetries are present at many scales in natural scenes. Humans and other animals are highly sensitive to visual symmetry, and symmetry contributes to numerous domains of visual perception. The four fundamental symmetries-reflection, rotation, translation and glide reflection-can be combined into exactly 17 distinct regular textures. These wallpaper groups represent the complete set of symmetries in two-dimensional images. The current study seeks to provide a more comprehensive description of responses to symmetry in the human visual system, by collecting both brain imaging (steady-state visual evoked potentials measured using high-density EEG) and behavioural (symmetry detection thresholds) data using the entire set of wallpaper groups. This allows us to probe the hierarchy of complexity among wallpaper groups, in which simpler groups are subgroups of more complex ones. We find that both behaviour and brain activity preserve the hierarchy almost perfectly: subgroups consistently produce lower-amplitude symmetry-specific responses in visual cortex and require longer presentation durations to be reliably detected. These findings expand our understanding of symmetry perception by showing that the human brain encodes symmetries with a high level of precision and detail. This opens new avenues for research on how fine-grained representations of regular textures contribute to natural vision.

A case-control study of visual, auditory and audio-visual sensory interactions in children with autism spectrum disorder.

To assess the relative integrity of early visual and auditory processes in autism spectrum disorder (ASD), we used frequency-tagged visual and auditory stimulation and high-density electroencephalogram recordings of unimodal and dual-modality responses in a case-control design. To test for the specificity of effects on ASD, we recorded from a smaller group of children with attention-deficit hyperactivity disorder (ADHD). Horizontal 3 cycle per degree (cpd) gratings were presented at 5 Hz, and a random stream of /ba/, /da/, /ga/ syllables was presented at 6 Hz. Grating contrast response functions were measured unimodally and in the presence of a 64-dB auditory input. Auditory response functions were measured unimodally and in the presence of a 40% contrast grating. Children with ASD (n = 34) and ADHD (n = 13) showed a common lack of audio-visual interaction compared to typically developing children (n = 40) when measured at the first harmonic of the visual stimulus frequency. Both patient groups also showed depressed first harmonic responses at low contrast, but the ADHD group had consistently higher first-harmonic responses at high contrast. Children with ASD had a preferential loss of second-harmonic (transient) responses. The alteredtransient responses in ASD are likely to arise very early in the visual pathway and could thus have downstream consequences for many other visual mechanisms and processes. The alteration in audio-visual interaction could be a signature of a comorbid phenotype shared by ASD and ADHD, possibly due to alterations in attentional selection systems.

The neural signature of numerosity by separating numerical and continuous magnitude extraction in visual cortex with frequency-tagged EEG.

The ability to handle approximate quantities, or number sense, has been recurrently linked to mathematical skills, although the nature of the mechanism allowing to extract numerical information (i.e., numerosity) from environmental stimuli is still debated. A set of objects is indeed not only characterized by its numerosity but also by other features, such as the summed area occupied by the elements, which often covary with numerosity. These intrinsic relations between numerosity and nonnumerical magnitudes led some authors to argue that numerosity is not independently processed but extracted through a weighting of continuous magnitudes. This view cannot be properly tested through classic behavioral and neuroimaging approaches due to these intrinsic correlations. The current study used a frequency-tagging EEG approach to separately measure responses to numerosity as well as to continuous magnitudes. We recorded occipital responses to numerosity, total area, and convex hull changes but not to density and dot size. We additionally applied a model predicting primary visual cortex responses to the set of stimuli. The model output was closely aligned with our electrophysiological data, since it predicted discrimination only for numerosity, total area, and convex hull. Our findings thus demonstrate that numerosity can be independently processed at an early stage in the visual cortex, even when completely isolated from other magnitude changes. The similar implicit discrimination for numerosity as for some continuous magnitudes, which correspond to basic visual percepts, shows that both can be extracted independently, hence substantiating the nature of numerosity as a primary feature of the visual scene.

EEGSourceSim: A framework for realistic simulation of EEG scalp data using MRI-based forward models and biologically plausible signals and noise.

BACKGROUND: Electroencephalography (EEG) is widely used to investigate human brain function. Simulation studies are essential for assessing the validity of EEG analysis methods and the interpretability of results. NEW METHOD: Here we present a simulation environment for generating EEG data by embedding biologically plausible signal and noise into MRI-based forward models that incorporate individual-subject variability in structure and function. RESULTS: The package includes pipelines for the evaluation and validation of EEG analysis tools for source estimation, functional connectivity, and spatial filtering. EEG dynamics can be simulated using realistic noise and signal models with user specifiable signal-to-noise ratio (SNR). We also provide a set of quantitative metrics tailored to source estimation, connectivity and spatial filtering applications. COMPARISON WITH EXISTING METHOD(S): We provide a larger set of forward solutions for individual MRI-based head models than has been available previously. These head models are surface-based and include two sets of regions-of-interest (ROIs) that have been brought into registration with the brain of each individual using surface-based alignment - one from a whole brain and the other from a visual cortex atlas. We derive a realistic model of noise by fitting different model components to measured resting state EEG. We also provide a set of quantitative metrics for evaluating source-localization, functional connectivity and spatial filtering methods. CONCLUSIONS: The inclusion of a larger number of individual head-models, combined with surface-atlas based labeling of ROIs and plausible models of signal and noise, allows for simulation of EEG data with greater realism than previous packages.

Image Segmentation Based on Relative Motion and Relative Disparity Cues in Topographically Organized Areas of Human Visual Cortex.

The borders between objects and their backgrounds create discontinuities in image feature maps that can be used to recover object shape. Here we used functional magnetic resonance imaging to identify cortical areas that encode two of the most important image segmentation cues: relative motion and relative disparity. Relative motion and disparity cues were isolated by defining a central 2-degree disk using random-dot kinematograms and stereograms, respectively. For motion, the disk elicited retinotopically organized activations starting in V1 and extending through V2 and V3. In the surrounding region, we observed phase-inverted activations indicative of suppression, extending out to at least 6 degrees of retinal eccentricity. For disparity, disk activations were only found in V3, while suppression was observed in all early visual areas. Outside of early visual cortex, several areas were sensitive to both types of cues, most notably LO1, LO2 and V3B, making them additional candidate areas for motion- and disparity-cue combination. Adding an orthogonal task at fixation did not diminish these effects, and in fact led to small but measurable disk activations in V1 and V2 for disparity. The overall pattern of extra-striate activations is consistent with recent three-stream models of cortical organization.

Neural dynamics underlying coherent motion perception in children and adults.

Motion sensitivity increases during childhood, but little is known about the neural correlates. Most studies investigating children's evoked responses have not dissociated direction-specific and non-direction-specific responses. To isolate direction-specific responses, we presented coherently moving dot stimuli preceded by incoherent motion, to 6- to 7-year-olds (n = 34), 8- to 10-year-olds (n = 34), 10- to 12-year-olds (n = 34) and adults (n = 20). Participants reported the coherent motion direction while high-density EEG was recorded. Using a data-driven approach, we identified two stimulus-locked EEG components with distinct topographies: an early component with an occipital topography likely reflecting sensory encoding and a later, sustained positive component over centro-parietal electrodes that we attribute to decision-related processes. The component waveforms showed clear age-related differences. In the early, occipital component, all groups showed a negativity peaking at ˜300 ms, like the previously reported coherent-motion N2. However, the children, unlike adults, showed an additional positive peak at ˜200 ms, suggesting differential stimulus encoding. The later positivity in the centro-parietal component rose more steeply for adults than for the youngest children, likely reflecting age-related speeding of decision-making. We conclude that children's protracted development of coherent motion sensitivity is associated with maturation of both early sensory and later decision-related processes.

Revisiting the functional significance of binocular cues for perceiving motion-in-depth.

Binocular differencing of spatial cues required for perceiving depth relationships is associated with decreased sensitivity to the corresponding retinal image displacements. However, binocular summation of contrast signals increases sensitivity. Here, we investigated this divergence in sensitivity by making direct neural measurements of responses to suprathreshold motion in human adults and 5-month-old infants using steady-state visually evoked potentials. Interocular differences in retinal image motion generated suppressed response functions and correspondingly elevated perceptual thresholds compared to motion matched between the two eyes. This suppression was of equal strength for horizontal and vertical motion and therefore not specific to the perception of motion-in-depth. Suppression is strongly dependent on the presence of spatial references in the image and highly immature in infants. Suppression appears to be the manifestation of a succession of spatial and interocular opponency operations that occur at an intermediate processing stage either before or in parallel with the extraction of motion-in-depth.

Distinct Representations of Magnitude and Spatial Position within Parietal Cortex during Number-Space Mapping.

Mapping numbers onto space is foundational to mathematical cognition. These cognitive operations are often conceptualized in the context of a "mental number line" and involve multiple brain regions in or near the intraparietal sulcus (IPS) that have been implicated both in numeral and spatial cognition. Here we examine possible differentiation of function within these brain areas in relating numbers to spatial positions. By isolating the planning phase of a number line task and introducing spatiotopic mapping tools from fMRI into mental number line task research, we are able to focus our analysis on the neural activity of areas in anterior IPS (aIPS) previously associated with number processing and on spatiotopically organized areas in and around posterior IPS (pIPS), while participants prepare to place a number on a number line. Our results support the view that the nonpositional magnitude of a numerical symbol is coded in aIPS, whereas the position of a number in space is coded in posterior areas of IPS. By focusing on the planning phase, we are able to isolate activation related to the cognitive, rather than the sensory-motor, aspects of the task. Also, to allow the separation of spatial position from magnitude, we tested both a standard positive number line (0 to 100) and a zero-centered mixed number line (-100 to 100). We found evidence of a functional dissociation between aIPS and pIPS: Activity in aIPS was associated with a landmark distance effect not modulated by spatial position, whereas activity in pIPS revealed a contralateral preference effect.

Dynamics of perceptual decisions about symmetry in visual cortex.

Neuroimaging studies have identified multiple extra-striate visual areas that are sensitive to symmetry in planar images (Kohler et al., 2016; Sasaki et al., 2005). Here, we investigated which of these areas are directly involved in perceptual decisions about symmetry, by recording high-density EEG in participants (n = 25) who made rapid judgments about whether an exemplar image contained rotation symmetry or not. Stimulus-locked sensor-level analysis revealed symmetry-specific activity that increased with increasing order of rotation symmetry. Response-locked analysis identified activity occurring between 600 and 200 ms before the button-press, that was directly related to perceptual decision making. We then used fMRI-informed EEG source imaging to characterize the dynamics of symmetry-specific activity within an extended network of areas in visual cortex. The most consistent cortical source of the stimulus-locked activity was VO1, a topographically organized area in ventral visual cortex, that was highly sensitive to symmetry in a previous study (Kohler et al., 2016). Importantly, VO1 activity also contained a strong decision-related component, suggesting that this area plays a crucial role in perceptual decisions about symmetry. Other candidate areas, such as lateral occipital cortex, had weak stimulus-locked symmetry responses and no evidence of correlation with response timing.

Evidence for long-range spatiotemporal interactions in infant and adult visual cortex.

The development of spatiotemporal interactions giving rise to classical receptive field properties has been well studied in animal models, but little is known about the development of putative nonclassical mechanisms in any species. Here we used visual evoked potentials to study the developmental status of spatiotemporal interactions for stimuli that were biased to engage long-range spatiotemporal integration mechanisms. We compared responses to widely spaced stimuli presented either in temporal succession or at the same time. The former configuration elicits a percept of apparent motion in adults but the latter does not. Component flash responses were summed to make a linear prediction (no spatiotemporal interaction) for comparison with the measured evoked responses to sequential or simultaneous flash conditions. In adults, linear summation of the separate flash responses measured with 40% contrast stimuli predicted sequential flash responses twice as large as those measured, indicating that the response measured under apparent motion conditions is subadditive. Simultaneous-flash responses at the same spatial separation were also subadditive, but substantially less so. The subadditivity in both cases could be modeled as a simple multiplicative gain term across all electrodes and time points. In infants aged 3-8 months, responses to the stimuli used in adults were similar to their linear predictions at 40%, but the responses measured at 80% contrast resembled the subadditive responses of the adults for both sequential and simultaneous flash conditions. We interpret the developmental data as indicating that adult-like long-range spatiotemporal interactions can be demonstrated by 3-8 months, once stimulus contrast is high enough.

Motion-Induced Position Shifts Activate Early Visual Cortex.

The ability to correctly determine the position of objects in space is a fundamental task of the visual system. The perceived position of briefly presented static objects can be influenced by nearby moving contours, as demonstrated by various illusions collectively known as motion-induced position shifts. Here we use a stimulus that produces a particularly strong effect of motion on perceived position. We test whether several regions-of-interest (ROIs), at different stages of visual processing, encode the perceived rather than retinotopically veridical position. Specifically, we collect functional MRI data while participants experience motion-induced position shifts and use a multivariate pattern analysis approach to compare the activation patterns evoked by illusory position shifts with those evoked by matched physical shifts. We find that the illusory perceived position is represented at the earliest stages of the visual processing stream, including primary visual cortex. Surprisingly, we found no evidence of percept-based encoding of position in visual areas beyond area V3. This result suggests that while it is likely that higher-level visual areas are involved in position encoding, early visual cortex also plays an important role.

Representation of Maximally Regular Textures in Human Visual Cortex.

Naturalistic textures with an intermediate degree of statistical regularity can capture key structural features of natural images (Freeman and Simoncelli, 2011). V2 and later visual areas are sensitive to these features, while primary visual cortex is not (Freeman et al., 2013). Here we expand on this work by investigating a class of textures that have maximal formal regularity, the 17 crystallographic wallpaper groups (Fedorov, 1891). We used texture stimuli from four of the groups that differ in the maximum order of rotation symmetry they contain, and measured neural responses in human participants using functional MRI and high-density EEG. We found that cortical area V3 has a parametric representation of the rotation symmetries in the textures that is not present in either V1 or V2, the first discovery of a stimulus property that differentiates processing in V3 from that of lower-level areas. Parametric responses were also seen in higher-order ventral stream areas V4, VO1, and lateral occipital complex (LOC), but not in dorsal stream areas. The parametric response pattern was replicated in the EEG data, and source localization indicated that responses in V3 and V4 lead responses in LOC, which is consistent with a feedforward mechanism. Finally, we presented our stimuli to four well developed feedforward models and found that none of them were able to account for our results. Our results highlight structural regularity as an important stimulus dimension for distinguishing the early stages of visual processing, and suggest a previously unrecognized role for V3 in the visual form-processing hierarchy. Significance statement: Hierarchical processing is a fundamental organizing principle in visual neuroscience, with each successive processing stage being sensitive to increasingly complex stimulus properties. Here, we probe the encoding hierarchy in human visual cortex using a class of visual textures--wallpaper patterns--that are maximally regular. Through a combination of fMRI and EEG source imaging, we find specific responses to texture regularity that depend parametrically on the maximum order of rotation symmetry in the textures. These parametric responses are seen in several areas of the ventral visual processing stream, as well as in area V3, but not in V1 or V2. This is the first demonstration of a stimulus property that differentiates processing in V3 from that of lower-level visual areas.

Extrastriate Visual Areas Integrate Form Features over Space and Time to Construct Representations of Stationary and Rigidly Rotating Objects.

When an object moves behind a bush, for example, its visible fragments are revealed at different times and locations across the visual field. Nonetheless, a whole moving object is perceived. Unlike traditional modal and amodal completion mechanisms known to support spatial form integration when all parts of a stimulus are simultaneously visible, relatively little is known about the neural substrates of the spatiotemporal form integration (STFI) processes involved in generating coherent object representations from a succession visible fragments. We used fMRI to identify brain regions involved in two mechanisms supporting the representation of stationary and rigidly rotating objects whose form features are shown in succession: STFI and position updating. STFI allows past and present form cues to be integrated over space and time into a coherent object even when the object is not visible in any given frame. STFI can occur whether or not the object is moving. Position updating allows us to perceive a moving object, whether rigidly rotating or translating, even when its form features are revealed at different times and locations in space. Our results suggest that STFI is mediated by visual regions beyond V1 and V2. Moreover, although widespread cortical activation has been observed for other motion percepts derived solely from form-based analyses [Tse, P. U. Neural correlates of transformational apparent motion. Neuroimage, 31, 766-773, 2006; Krekelberg, B., Vatakis, A., & Kourtzi, Z. Implied motion from form in the human visual cortex. Journal of Neurophysiology, 94, 4373-4386, 2005], increased responses for the position updating that lead to rigidly rotating object representations were only observed in visual areas KO and possibly hMT+, indicating that this is a distinct and highly specialized type of processing.

Motion-induced position shifts are influenced by global motion, but dominated by component motion.

Object motion and position have long been thought to involve largely independent visual computations. However, the motion-induced position shift (Eagleman & Sejnowski, 2007) shows that the perceived position of a briefly presented static object can be influenced by nearby moving contours. Here we combine a particularly strong example of this illusion with a bistable global motion stimulus to compare the relative effects of global and component motion on the shift in perceived position. We used a horizontally oscillating diamond (Lorenceau & Shiffrar, 1992) that produces two possible global directions (left and right when fully visible versus up and down when vertices are occluded by vertical bars) as well as the oblique component motion orthogonal to each contour. To measure the motion-induced shift we flashed a test dot on the contour as the diamond reversed direction (Cavanagh & Anstis, 2013). Although the global motion had a highly significant influence on the direction and size of the motion-induced position shift, the perceived displacement of the probe was closer to the direction of the component motion. These findings show that while global motion can clearly influence position shifts, it is the component motion that dominates in setting the position shift. This is true even though the perceived motion is in the global direction and the component motion is not consciously experienced. This suggests that perceived position is influenced by motion signals that arise earlier in time or earlier in processing compared to the stage at which the conscious experience of motion is determined.

The artist emerges: visual art learning alters neural structure and function.

How does the brain mediate visual artistic creativity? Here we studied behavioral and neural changes in drawing and painting students compared to students who did not study art. We investigated three aspects of cognition vital to many visual artists: creative cognition, perception, and perception-to-action. We found that the art students became more creative via the reorganization of prefrontal white matter but did not find any significant changes in perceptual ability or related neural activity in the art students relative to the control group. Moreover, the art students improved in their ability to sketch human figures from observation, and multivariate patterns of cortical and cerebellar activity evoked by this drawing task became increasingly separable between art and non-art students. Our findings suggest that the emergence of visual artistic skills is supported by plasticity in neural pathways that enable creative cognition and mediate perceptuomotor integration.

Unconscious neural processing differs with method used to render stimuli invisible.

Visual stimuli can be kept from awareness using various methods. The extent of processing that a given stimulus receives in the absence of awareness is typically used to make claims about the role of consciousness more generally. The neural processing elicited by a stimulus, however, may also depend on the method used to keep it from awareness, and not only on whether the stimulus reaches awareness. Here we report that the method used to render an image invisible has a dramatic effect on how category information about the unseen stimulus is encoded across the human brain. We collected fMRI data while subjects viewed images of faces and tools, that were rendered invisible using either continuous flash suppression (CFS) or chromatic flicker fusion (CFF). In a third condition, we presented the same images under normal fully visible viewing conditions. We found that category information about visible images could be extracted from patterns of fMRI responses throughout areas of neocortex known to be involved in face or tool processing. However, category information about stimuli kept from awareness using CFS could be recovered exclusively within occipital cortex, whereas information about stimuli kept from awareness using CFF was also decodable within temporal and frontal regions. We conclude that unconsciously presented objects are processed differently depending on how they are rendered subjectively invisible. Caution should therefore be used in making generalizations on the basis of any one method about the neural basis of consciousness or the extent of information processing without consciousness.