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 STATEMENTHierarchical 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.

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.

Significance: We do not know how the human brain mediates complex and creative behaviors such as artistic, scientific, and mathematical thought. Scholars theorize that these abilities require conscious experience as realized in a widespread neural network, or “mental workspace,” that represents and manipulates images, symbols, and other mental constructs across a variety of domains. Evidence for such a complex, interconnected network has been difficult to produce with current techniques that mainly study brain activity in isolation and are insensitive to distributed informational processes. The present work takes advantage of emerging techniques in network and information analysis to provide empirical support for such a widespread and interconnected information processing network in the brain that supports the manipulation of visual imagery.

Associations between auditory pitch and visual elevation are widespread in many languages, and behavioral associations have been extensively documented between height and pitch among speakers of those languages. However, it remains unclear whether perceptual correspondences between auditory pitch and visual elevation inform these linguistic associations, or merely reflect them. We probed this cross-modal mapping in members of a remote Kreung hill tribe in northeastern Cambodia who do not use spatial language to describe pitch. Participants viewed shapes rising or falling in space while hearing sounds either rising or falling in pitch, and reported on the auditory change. Associations between pitch and vertical position in the Kreung were similar to those demonstrated in populations where pitch is described in terms of spatial height. These results suggest that associations between visual elevation and auditory pitch can arise independently of language. Thus, widespread linguistic associations between pitch and elevation may reflect universally predisposed perceptual correspondences.