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. 2014 May 14;34(20):6721-35.
doi: 10.1523/JNEUROSCI.4802-13.2014.

Thinking outside the box: rectilinear shapes selectively activate scene-selective cortex

Shahin Nasr  1 , Cesar E Echavarria  2 , Roger B H Tootell  3
Affiliations

Thinking outside the box: rectilinear shapes selectively activate scene-selective cortex

Shahin Nasr et al. J Neurosci. .

Abstract

Fifteen years ago, an intriguing area was found in human visual cortex. This area (the parahippocampal place area [PPA]) was initially interpreted as responding selectively to images of places. However, subsequent studies reported that PPA also responds strongly to a much wider range of image categories, including inanimate objects, tools, spatial context, landmarks, objectively large objects, indoor scenes, and/or isolated buildings. Here, we hypothesized that PPA responds selectively to a lower-level stimulus property (rectilinear features), which are common to many of the above higher-order categories. Using a novel wavelet image filter, we first demonstrated that rectangular features are common in these diverse stimulus categories. Then we tested whether PPA is selectively activated by rectangular features in six independent fMRI experiments using progressively simplified stimuli, from complex real-world images, through 3D/2D computer-generated shapes, through simple line stimuli. We found that PPA was consistently activated by rectilinear features, compared with curved and nonrectangular features. This rectilinear preference was (1) comparable in amplitude and selectivity, relative to the preference for category (scenes vs faces), (2) independent of known biases for specific orientations and spatial frequency, and (3) not predictable from V1 activity. Two additional scene-responsive areas were sensitive to a subset of rectilinear features. Thus, rectilinear selectivity may serve as a crucial building block for category-selective responses in PPA and functionally related areas.

Keywords: categorization; fMRI; feature selectivity; parahippocampal place area; wavelet.

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Figures

Figure 1.
Figure 1.
Illustration of different Gabors filters used to quantify the strength of the representation of different angles. A, Variations in orientation. B, Variations in spatial scale. C, Gabors used to detect the range of test angles.
Figure 2.
Figure 2.
The value indexing the strength of representation of right angles (a defining feature of rectilinear shapes) was measured in a subset of stimulus sets used in previous studies to localize PPA and other scene-selective areas, based on (A) scenes versus nonscenes (Nasr et al., 2011) and (B) scenes versus faces (Nasr et al., 2011; Nasr and Tootell, 2012a, b). The same measurement was applied to stimuli from additional studies, which evoked higher fMRI activity in PPA, based on a preference for (C) indoor scenes versus outdoor scenes versus faces (Nasr et al., 2011), (D) tools versus other nonface objects versus faces (Chao et al., 1999), and (E) objectively large versus small objects (Konkle and Oliva, 2012). In all these results, stimuli that were reported to evoke a stronger response in PPA also showed a correspondingly higher rectilinearity index. F, Conversely, a stimulus comparison that activated only the anterior tip (but not most) of PPA did not show any significant difference between the index values (Bar and Aminoff, 2003). Error bars indicate 1 SE.
Figure 3.
Figure 3.
Stimuli and results in Experiments 1 and 2. Stimuli were images of “rectilinear” or “round” multiple (A) or single (C) real-world objects, in Experiments 1 and 2, respectively. B, D, Corresponding group-averaged maps, based on random effect analysis, demonstrating that all three scene-selective areas (PPA, TOS, and RSC) responded preferentially to the rectilinear objects. No masking was used in any of the analyses in this study. In the group activity maps, the borders of PPA, TOS, and RSC are indicated using solid, dashed, and dotted lines, respectively, based on an independent set of localizing scans comparing faces versus scenes in the same group of subjects (e.g., Fig. 5). This stimulus contrast did not produce significant selectivity for rectilinear objects within visually stimulated V1 (or other early retinotopic areas), as defined based on retinotopic mapping in the same group of subjects (see Materials and Methods). This V1 border is indicated with dashed white lines (asterisk = foveal representation). Activity is shown in both the inflated (leftmost and rightmost) and flattened (middle) cortical surface formats. Error bars indicate 1 SE. R, Right hemisphere.
Figure 4.
Figure 4.
Localization of the rectilinearity-related activity evoked in response to the contrast of rectilinear versus round multiple real-world objects, for all 15 individual subjects that participated in Experiment 1. A, Ventral (and slightly medial) view of the averaged brain. The yellow rectangle represents the brain region magnified in B. B, Activity resulting from rectilinear versus round stimuli, and the borders of PPA based on the scenes versus faces localizer, for each individual subject (black lines). To facilitate the comparison between subjects, each individual subject's activity was overlaid on the averaged brain. In all panels, the anterior versus posterior axis is oriented upward versus downward, respectively.
Figure 5.
Figure 5.
Localization of the group-averaged rectilinearity-related activity in Experiment 1, relative to the border of PPA defined using the contrast of either scenes versus faces, or scenes versus objects, based on either fixed or random effect analyses. Additional borders of PPA (black lines) were defined based on an independent study (and a nonoverlapping group of subjects and a different scanning site, compared with that used in Experiment 1) using the group-constrained subject specific method (Julian et al., 2012) (see Materials and Methods). The location and surface area of PPA were similar across these conditions. The highest rectilinearity-related activity was located within all four borders of PPA as defined in the current study, and mostly within PPA based on the independent study.
Figure 6.
Figure 6.
Localization of the rectilinearity-related activity evoked in response to images of single real-world rectilinear versus round objects, relative to the borders of PPA (defined based on an independent scenes vs faces contrast) for all 11 individual subjects that participated in Experiment 2. Other details are as in Figure 4.
Figure 7.
Figure 7.
Stimuli and results in Experiment 3. A, Stimuli included arrays of cubes and pyramids (i.e., “rectilinear” shapes; top) compared with arrays of cones and spheres (i.e., “rounded” shapes; bottom). The cones were oriented so that they showed only curved edges and surfaces, excepting the apical singularity. Thus, from this viewpoint, the cones were considered “round” in terms of 2D contours. The four-sided pyramids were considered “rectilinear” because they are essentially cubes seen from an atypical viewpoint. In these stimulus examples, the source location of the virtual illuminant was varied to illustrate the experimental range in shading. However, in the actual experiment, the illuminant source was varied systematically in semirandom order, equivalently for all shape types. B, Group-averaged activity map showed a significant preference for the arrays of rectilinear objects, relative to the round ones, largely limited to PPA and TOS. In this experiment, dorsal RSC also responded selectively to the rectilinear objects. As in Experiment 1, a significant rectilinear activity bias was not found within V1. C, Results of ROI analysis within these three scene-selective areas. Other details are similar to those in Figure 3.
Figure 8.
Figure 8.
Localization of the rectilinearity-related activity evoked in response to computer-generated rectilinear shapes (i.e., cubes and pyramids) versus round shapes (spheres and cones), relative to the borders of PPA (defined based on scenes vs faces contrast), for all 12 individual subjects that participated in Experiment 3. Other details are as in Figure 4.
Figure 9.
Figure 9.
Comparison of fMRI responses with differences in stimulus shape (left) compared with differences in stimulus category (right), in areas PPA (A) and TOS (B). Stimulus shape differences were based on the responses to arrays of 3D spheres versus cubes, used in Experiment 3. Category differences were based on the contrast of faces versus scenes, a robust and common localizer for PPA and TOS (Nasr et al., 2011; Epstein and Kanwisher, 1998; Rajimehr et al., 2011; Nasr and Tootell, 2012a, b). In each panel, white data points indicate the activity for individual subjects measured relative to fixation-only blocks. Group-averaged means are shown in red and green, for cubes versus spheres and faces versus scenes, respectively.
Figure 10.
Figure 10.
Stimuli and results for Experiment 4. A, Examples of the complete stimuli: arrays of filled overlapping squares presented at either cardinal (left) or oblique (middle) orientations, and an otherwise identical array of circles (right). The group-averaged activity maps (B) showed a stronger response to arrays of squares (averaged over both orientations) compared with circles in PPA and TOS, but not in RSC. In addition, low-amplitude, patchy activity was also found in V1, but that activity was confined to the retinotopic representation at and beyond the peripheral borders of the stimuli (i.e., that activity was not driven by the experimental stimulus contrast). Dashed white lines indicate the borders of stimulus-activated V1 defined using a separate set of retinotopic scans for the same group of subjects (asterisk = foveal representation). Consistent with these results, an ROI analysis (C) showed stronger activity in PPA and TOS in response to squares compared with circles, even when the squares were presented at oblique orientations. Other details are as in Figure 3.
Figure 11.
Figure 11.
Stimuli and results in Experiment 5A. A, Stimulus examples. In the actual experiment, each stimulus array included 40 shapes, instead of the single shapes shown here. Group-averaged activity maps (B) showed a stronger response evoked by arrays of squares compared with circles, largely confined within PPA and TOS, but not within RSC or V1. C, Corresponding ROI analysis. In PPA (bottom left), squares evoked a stronger response compared with other shapes. The TOS response profile (bottom right) was similar but less differentiated across the simplest polygons. Details are otherwise as in Figure 3.
Figure 12.
Figure 12.
Activity maps for the contrast of squares versus triangles (A) and squares versus hexagons (B) in Experiment 5. In both cases, we found a higher response to squares in PPA, tending toward the posterior part of that area. Because the results did not show any difference between the PPA response across the two different matching criteria (i.e., equated for shape vs angle number), in B, the activity maps were averaged over the two matching conditions to increase the overall signal-to-noise ratio.
Figure 13.
Figure 13.
Response comparison for stimulus pairs that were equated for the number of angles (Experiment 5B) instead of the number of shapes (Experiment 5A). Data were generated as a control manipulation, acquired in intermixed blocks in Experiment 5. A, When equated for the number of angles, the group-averaged activity maps showed a stronger response to the array of squares, compared with circles, that was located mainly within PPA and TOS (but not within RSC or V1), similar to the results in Figure 11. These results were also evident in the ROI analysis (B): in both PPA (bottom left) and TOS (bottom right), squares evoked a stronger response compared with circles, regardless of the two criteria by which the stimuli were equated. Dashed line indicates number of shapes; solid line indicates number of angles. Furthermore, comparison of the responses to these two stimuli showed that PPA responses remained statistically equal regardless of this stimulus variation, whereas TOS showed a relatively higher response to those stimuli equated for the number of objects. Other details are as in Figure 3.
Figure 14.
Figure 14.
Stimuli and results for Experiment 6. A, Stimulus shapes. In the actual experiments, each stimulus array contained 120 angles or semicircles, rather than the four shown here. In group-averaged activity maps, arrays of both 90° (B) and 180° (C) angles evoked a stronger response compared with semicircles in PPA and TOS. Analogous biases were not found in RSC or early retinotopic areas (e.g., V1, dashed white lines). The ROI analysis (D) confirmed these results, showing further that PPA (bottom left) had a bimodal response profile (a preference for both 90° and 180° angles). However, the TOS response (bottom right) to 180° angles was significantly smaller than its response to 90° angles. Other details are as in Figure 3.
Figure 15.
Figure 15.
Possible generation of rectilinear selectivity in PPA, based on inputs from a retinotopic and orientation-selective map of early visual cortex. This schematic is based on published maps from orientation-selective subregions in primate cortical areas V1 and V2. It not yet known whether PPA receives direct input from either of these areas, but slight modifications of this model could accommodate the interposition of additional cortical areas or processing stages between early visual areas (e.g., V1/V2) and PPA. Left, Map of preferred orientation (small white bars) and receptive field (retinotopic) location, in an early visual cortical area. Top versus bottom receptive field positions are indicated in red through black. Analogous left-versus-right visual field locations are indicated in blue through black. Right, In subsequent area(s) (e.g., PPA), a template-based sensitivity to right angles and lines can be generated by simply combining single-orientation information from the appropriate visual field position.
Figure 16.
Figure 16.
Detailed topography of activity in PPA in response to the rectilinear versus round shapes, across all six experiments. We found a general anterior-to-posterior shift in the center of activity, consistent with covariations in stimulus complexity. Our most complex stimuli (Experiments 1–4; multiple/single real-world objects, 3D shapes, and overlapping luminance-varying 2D shapes, respectively) produced activity that extended throughout much or all of localizer-defined PPA, thus centered (cyan circles) toward the middle of PPA. In contrast, our simplest stimuli (Experiments 5 and 6, based on line configurations) produced activity that was centered toward the posterior border of PPA. To emphasize the center of activity, here all activity maps were based on fixed rather than random effects, and thresholds were normalized across experiments. For comparison, the center of activity for the localizer itself (scenes vs faces) is indicated with a black asterisk in each panel; it did not shift significantly across the different experiments. In all panels, the PPA borders (black lines) indicate the area borders for the tested groups of subjects, based on independent stimuli and scans (e.g., Fig. 5).
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