Representation of Maximally Regular Textures in Human Visual Cortex

• Published in: The Journal of neuroscience Vol. 36; no. 3; pp. 714 - 729
• Main Authors: Kohler, Peter J, Clarke, Alasdair, Yakovleva, Alexandra, Liu, Yanxi, Norcia, Anthony M
• Format: Journal Article
• Language: English
• Published: United States Society for Neuroscience 20.01.2016
• Subjects: Adolescent; Adult; Brain Mapping - methods; Female; Humans; Magnetic Resonance Imaging - methods; Male; Middle Aged; Pattern Recognition, Visual - physiology; Photic Stimulation - methods; Visual Cortex - physiology; Visual Pathways - physiology; Visual Perception - physiology; Young Adult; ventral stream; mid-level vision; hierarchical processing; symmetry; texture; perceptual organization
• ISSN: 0270-6474; 1529-2401
• DOI: 10.1523/jneurosci.2962-15.2016

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.