Curvature processing in human visual cortical areas

Abstract

Curvature is one of many visual features shown to be important for visual perception. We recently showed that curvilinear features provide sufficient information for categorizing animate vs. inanimate objects, while rectilinear features do not (Zachariou et al., 2018). Results from our fMRI study in rhesus monkeys (Yue et al., 2014) have shed light on some of the neural substrates underlying curvature processing by revealing a network of visual cortical patches with a curvature response preference. However, it is unknown whether a similar network exists in human visual cortex. Thus, the current study was designed to investigate cortical areas with a preference for curvature in the human brain using fMRI at 7T. Consistent with our monkey fMRI results, we found a network of curvature preferring cortical patches-some of which overlapped well-known face-selective areas. Moreover, principal component analysis (PCA) using all visually-responsive voxels indicated that curvilinear features of visual stimuli were associated with specific retinotopic regions in visual cortex. Regions associated with positive curvilinear PC values encompassed the central visual field representation of early visual areas and the lateral surface of temporal cortex, while those associated with negative curvilinear PC values encompassed the peripheral visual field representation of early visual areas and the medial surface of temporal cortex. Thus, we found that broad areas of curvature preference, which encompassed face-selective areas, were bound by central visual field representations. Our results support the hypothesis that curvilinearity preference interacts with central-peripheral processing biases as primary features underlying the organization of temporal cortex topography in the adult human brain.

Trial registration: ClinicalTrials.gov NCT00001360.

Keywords: Curvature patches; FFA; MT; OFA; PPA; aIT.

Conflict of interest statement

Declaration of Competing Interest The authors declare no competing financial interests.

Copyright © 2020. Published by Elsevier Inc.

Figures

Fig. 1.

Examples of stimuli: (a) round vs. rectilinear shapes; (b) computer-generated 3D spheres vs. pyramid arrays; (c) faces vs. scenes; (d) objects vs. scrambled objects.

Fig. 2.

Calculating predicted BOLD responses with a linear combination of simple curvilinear features. (Left) Low, middle, and high curvilinear values for each image were first generated by averaging the values of the two lowest and highest curvilinear degrees and leaving the middle value intact. Three curvilinear values (low, middle, and high) per condition (represented by underscores) were then calculated by averaging the three curvilinear values of the images in each condition. Seven conditions (e.g. excluding faces) were selected and each condition’s BOLD response was regressed with its respective curvilinear values. (Right) The matrix of regression coefficients from the seven conditions and the curvilinear values of the left-out condition (e.g. faces) were used to predict the BOLD response to that condition. This process was repeated to get a predicted BOLD response for each condition. x: indicates values left out of regression.

Fig. 3.

A cortical map of regions with strong curvature response preference in a single example subject. The map was produced by contrasting the fMRI responses to curvilinear (round shapes and computer-generated 3D sphere array) > rectilinear (rectilinear shapes and computer-generated 3D pyramid array) stimuli. The yellow/red activation indicates the curvature response preference; blue/cyan activation indicates the rectilinear response preference. Three of the five curvature-preferring patches were located in dorsal and ventral V3, and V4 in both hemispheres, which we termed as V3dCP, V3vCP, and V4CP. Black outlines indicate boundaries of the occipital curvature patch (OCP), located in the lateral occipitotemporal cortex, and white outlines indicate boundaries of the fusiform curvature patch (FCP), located in the fusiform gyrus. The orientation of the brains are indicated in white letters (A = anterior; P = posterior; M = medial; L = lateral).

Fig. 4.

Group-averaged cortical map of curvature-preferring regions projected onto the freesurfer averaged inflated brain (top) and a flattened brain (bottom). The map was generated by contrasting fMRI responses to curvilinear (round shapes and computer-generated 3D sphere array) > rectilinear (rectilinear shapes and computer-generated 3D pyramid array) stimuli, the same contrast as in Fig. 3. Red/yellow activation indicates curvature response preference, and blue/cyan activation indicates rectilinear response preference. The dotted white lines shown on the flattened brain (bottom) indicate the retinotopic boundaries between early visual areas identified by the retinotopic mapping runs. Black lines indicate the boundary of OCP and solid white lines indicate the boundary of FCP. The blue outline shows the boundary of the occipital face area (OFA) and green lines show the boundaries of the fusiform face area (FFA) and anterior temporal face area (ATFA). The right OCP completely overlapped the right OFA and bilateral FCP partially overlapped FFA in both hemispheres (see Section 3.3 for quantification). Scene-selective areas were defined by fMRI responses to scenes > curvilinear and rectilinear stimuli. Yellow lines indicate the boundary of the parahippocampal place area (PPA) and dotted yellow lines outline retrosplenial cortex. The rectilinear-preferring patch overlapped PPA bilaterally (see Section 3.3 for quantification). The corrected statistical threshold was FDR

Fig. 5.

Comparison of group-averaged cortical maps of regions with significant curvature response preference across stimulus type (conditions 1 and 2 vs. conditions 3 and 4). Group-averaged maps were projected onto the FreeSurfer averaged flattened brain. The map on the top was generated using the fMRI activity contrast of round > rectilinear real-world objects. The map on the bottom was generated using the fMRI activity contrast of computer-generated 3D sphere array > computer-generated 3D pyramid array. Yellow/red activation indicates the curvature response preference; blue/cyan indicates the rectilinear response preference. Black outlines indicate the boundaries of the curvature-preferring patches. As expected, because the image size of the computer-generated stimuli was larger than that of the real-world objects, we observed more early visual areas activated by the computer-generated stimuli (top) than real-world objects (bottom). However, all curvature-preferring regions observed in the combined map (Fig. 4) are present in the separated maps, indicating the consistency of curvature preference regions across stimulus type. The corrected statistical threshold was FDR

Fig. 6.

Correlation of fMRI activity with curvilinear values in curvature-preferring patches was significant in left V3dCP (r = 0.763, p = 0.028), left V3vCP (r = 0.729, p = 0.040), and left V4CP (r = 0.866, p = 0.005), but not in right V3dCP/ V3vCP, V4CP (data not shown), or bilateral higher level curvature patches (OCP, FCP, see Fig. S2). All error bars represent the S.E.M. Significant correlations observed for left V3dCP, left V3vCP, and left V4CP suggest that these responses in curvature-preferring patches relate to simple curvilinear information. We did not observe significant correlations between the rectilinear values of the stimuli and fMRI responses in any of the curvature patches (Fig. S3).

Fig. 7.

Correlation of the predicted fMRI response from the linear combination of curvature values with fMRI activity in OCP and FCP. The correlation is significant in left and in right OCP (left OCP, r = 0.885, p = 0.002; right OCP, r = 0.702; p = 0.029), but not in left and right FCP (left FCP, r = 0.444, p = 0.129; right FCP, r = 0.342, p = 0.214), suggesting that OCP plays a role in processing complex curvilinear information derived from simple curvilinear information (such as curved lines).

Fig. 8.

Group PCA map. (top) Inflated view of the ventral surface. Areas outlined in black on the inflated brain indicate the location of the mid-fusiform sulcus. Visual areas in red/yellow were associated with positive values of the second principal component (PC2) while those in blue/cyan were associated with negative PC2 values. (bottom) Flattened view of the ventral surface. The visual cortex associated with the positive PC2 values included OCP (black outline), FCP (white outline), OFA (blue outline), FFA (green outline); the visual cortex associated with the negative PC2 values encompassed PPA (yellow outline) and rectilinear-preferring areas (not outlined, see Fig. 4). The absolute values of PC2 are not meaningful, because the data were normalized in the PCA analysis. Given that the loading of PC2 correlated significantly with the curvilinear values of visual stimuli across conditions (Fig. S5: r = 0.85, p = 0.007; permutation test: see Methods), the areas in red/yellow might be involved in processing curvilinear features and those in blue/cyan might be implicated in processing rectilinear features. The dashed white line indicates the central-peripheral boundary in our stimuli defined by contrasting the fMRI response to computer-generated 3D spheres and pyramid arrays (20 × 15˚) vs. faces and objects (8.4 × 10.0˚). Local orientations of the brain axes on the flattened brain are indicated in white letters (D = dorsal; V = ventral; P = posterior; A = anterior).

Fig. 9.

Individual subject PCA maps. Each subject’s data (N = 15) were projected onto their native flattened surface. Relatively consistent across all subjects, the visual cortex associated with positive PC2 values was confined within the central visual field in the early visual areas, and then extended continuously to the anterior temporal lobe through lateral occipitotemporal areas. Regions of visual cortex associated with negative PC2 values extended from peripheral visual field representations in early visual areas to the medial surface of the occipitotemporal cortex and then to the collateral sulcus (CoS) and parahippocampal gyrus. The dashed white line indicates the anatomical border between the fusiform gyrus and the collateral sulcus. Local orientation of the brain axes on the flattened brain are indicated in white letter (D = dorsal; V = ventral; P = posterior; A = anterior).