Xiaomin Yue

Scene-Selective Cortical Regions in Human and Nonhuman Primates

fMRI studies have revealed three scene-selective regions in human visual cortex [the parahippocampal place area (PPA), transverse occipital sulcus (TOS), and retrosplenial cortex (RSC)], which have been linked to higher-order functions such as navigation, scene perception/recognition, and contextual association. Here, we document corresponding (presumptively homologous) scene-selective regions in the awake macaque monkey, based on direct comparison to human maps, using identical stimuli and largely overlapping fMRI procedures. In humans, our results showed that the three scene-selective regions are centered near—but distinct from—the gyri/sulci for which they were originally named. In addition, all these regions are located within or adjacent to known retinotopic areas. Human RSC and PPA are located adjacent to the peripheral representation of primary and secondary visual cortex, respectively. Human TOS is located immediately anterior/ventral to retinotopic area V3A, within retinotopic regions LO-1, V3B, and/or V7. Mirroring the arrangement of human regions fusiform face area (FFA) and PPA (which are adjacent to each other in cortex), the presumptive monkey homolog of human PPA is located adjacent to the monkey homolog of human FFA, near the posterior superior temporal sulcus. Monkey TOS includes the region predicted from the human maps (macaque V4d), extending into retinotopically defined V3A. A possible monkey homolog of human RSC lies in the medial bank, near peripheral V1. Overall, our findings suggest a homologous neural architecture for scene-selective regions in visual cortex of humans and nonhuman primates, analogous to the face-selective regions demonstrated earlier in these two species.

Lower-Level Stimulus Features Strongly Influence Responses in the Fusiform Face Area

An intriguing region of human visual cortex (the fusiform face area; FFA) responds selectively to faces as a general higher-order stimulus category. However, the potential role of lower-order stimulus properties in FFA remains incompletely understood. To clarify those lower-level influences, we measured FFA responses to independent variation in 4 lower-level stimulus dimensions using standardized face stimuli and functional Magnetic Resonance Imaging (fMRI). These dimensions were size, position, contrast, and rotation in depth (viewpoint). We found that FFA responses were strongly influenced by variations in each of these image dimensions; that is, FFA responses were not “invariant” to any of them. Moreover, all FFA response functions were highly correlated with V1 responses (r = 0.95–0.99). As in V1, FFA responses could be accurately modeled as a combination of responses to 1) local contrast plus 2) the cortical magnification factor. In some measurements (e.g., face size or a combinations of multiple cues), the lower-level variations dominated the range of FFA responses. Manipulation of lower-level stimulus parameters could even change the category preference of FFA from “face selective” to “object selective.” Altogether, these results emphasize that a significant portion of the FFA response reflects lower-level visual responses.

What makes faces special

What may be special about faces, compared to non-face objects, is that their neural representation may be fundamentally spatial, e.g., Gabor-like. Subjects matched a sequence of two filtered images, each containing every other combination of spatial frequency and orientation, of faces or non-face 3D blobs, judging whether the person or blob was the same or different. On a match trial, the images were either identical or complementary (containing the remaining spatial frequency and orientation content). Relative to an identical pair of images, a complementary pair of faces, but not blobs, reduced matching accuracy and released fMRI adaptation in the fusiform face area.

The neural basis of scene preferences.

What is the neural correlate of preference that governs our spontaneous selection of visual information? With a rapid, event-related functional magnetic resonance imaging design, we showed that the viewing of highly preferred compared to less preferred scenes (as assessed by participant ratings) was associated with greater blood-oxygen level dependent responses in the right parahippocampal cortex but not in the lateral occipital complex, ruling out feed forward and attentional effects. Highly preferred images also produced greater activation in the ventral striatum, suggesting that perceptual preference might engage the conventional reward system. These results are consistent with the hypothesis that high activity in the parahippocampal cortex, an area with a high density of cortical μ-opioid receptors, may be experienced as cognitively pleasurable.

Adaptation in the fusiform face area (FFA): Image or person?

Viewing a sequence of faces of two different people results in a greater Blood Oxygenation Level Dependent (BOLD) response in FFA compared to a sequence of identical faces. Changes in identity, however, necessarily involve changes in the image. Is the release from adaptation a result of a change in face identity, per se, or could it be an effect that would arise from any change in the image of a face? Subjects viewed a sequence of two faces that could be of the same or different person, and in the same or different orientation in depth. Critically, the physical similarity of view changes of the same person was scaled, by Gabor-jet differences, to be equivalent to that produced by an identity change. Both person and orientation changes produced equivalent releases from adaptation in FFA (relative to identical faces) suggesting that FFA is sensitive to the physical similarity of faces rather than to the individuals depicted in the images.

The deleterious effect of contrast reversal on recognition is unique to faces, not objects

Faces reversed in contrast cannot be readily recognized, an effect absent in object recognition. Why? Four factors: expertise, reflectance (pigmentation), high similarity, and the need to discriminate metrically varying smooth surfaces have been offered as explanations. Observers achieved expertise on discriminating smoothly shaped, pigmented, non-face blobs with positive contrast, where distractor similarity matched that of a set of faces in shape and reflectance. On a match-to-sample task, reversal of contrast between sample and matching images had no effect when matching such blobs, but markedly degraded performance when matching faces suggesting that this effect is unique to faces.

Neural Correlates of Personal Space Intrusion

A parietal-frontal network in primates is thought to support many behaviors occurring in the space around the body, including interpersonal interactions and maintenance of a particular “comfort zone” or distance from other people (“personal space”). To better understand this network in humans, we used functional MRI to measure the responses to moving objects (faces, cars, simple spheres) and the functional connectivity of two regions in this network, the dorsal intraparietal sulcus (DIPS) and the ventral premotor cortex (PMv). We found that both areas responded more strongly to faces that were moving toward (vs away from) subjects, but did not show this bias in response to comparable motion in control stimuli (cars or spheres). Moreover, these two regions were functionally interconnected. Tests of activity-behavior associations revealed that the strength of DIPS-PMv connectivity was correlated with the preferred distance that subjects chose to stand from an unfamiliar person (personal space size). In addition, the magnitude of DIPS and PMv responses was correlated with the preferred level of social activity. Together, these findings suggest that this parietal-frontal network plays a role in everyday interactions with others.

Curvature-processing network in macaque visual cortex

Significance The brain processes visual stimuli along different feature dimensions, including edge orientation, visual motion, and color. To expedite visual processing, cells that process a common visual dimension are often anatomically grouped in cortical columns, patches, and/or areas. Here, we tested the hypothesis that (i) image curvature is one of these fundamental visual dimensions and, as such, (ii) curvature-selective cells are grouped together in discrete cortical areas. Using neuroimaging techniques, we confirmed this hypothesis and localized the curvature-processing sites in extrastriate visual cortex. These sites lay along a common cortical strip, spanning lower- to higher-level processing stages. Furthermore, the curvature-processing sites are adjacent to the well-known face-processing cortical areas, suggesting a possible functional link between them. Our visual environment abounds with curved features. Thus, the goal of understanding visual processing should include the processing of curved features. Using functional magnetic resonance imaging in behaving monkeys, we demonstrated a network of cortical areas selective for the processing of curved features. This network includes three distinct hierarchically organized regions within the ventral visual pathway: a posterior curvature-biased patch (PCP) located in the near-foveal representation of dorsal V4, a middle curvature-biased patch (MCP) located on the ventral lip of the posterior superior temporal sulcus (STS) in area TEO, and an anterior curvature-biased patch (ACP) located just below the STS in anterior area TE. Our results further indicate that the processing of curvature becomes increasingly complex from PCP to ACP. The proximity of the curvature-processing network to the well-known face-processing network suggests a possible functional link between them.

Predicting the psychophysical similarity of faces and non-face complex shapes by image-based measures

Shape representation is accomplished by a series of cortical stages in which cells in the first stage (V1) have local receptive fields tuned to contrast at a particular scale and orientation, each well modeled as a Gabor filter. In succeeding stages, the representation becomes largely invariant to Gabor coding (Kobatake & Tanaka, 1994). Because of the non-Gabor tuning in these later stages, which must be engaged for a behavioral response (Tong, 2003; Tong et al., 1998), a V1-based measure of shape similarity based on Gabor filtering would not be expected to be highly correlated with human performance when discriminating complex shapes (faces and teeth-like blobs) that differ metrically on a two-choice, match-to-sample task. Here we show that human performance is highly correlated with Gabor-based image measures (Gabor simple and complex cells), with values often in the mid 0.90s, even without discounting the variability in the speed and accuracy of performance not associated with the similarity of the distractors. This high correlation is generally maintained through the stages of HMAX, a model that builds upon the Gabor metric and develops units for complex features and larger receptive fields. This is the first report of the psychophysical similarity of complex shapes being predictable from a biologically motivated, physical measure of similarity. As accurate as these measures were for accounting for metric variation, a simple demonstration showed that all were insensitive to viewpoint invariant (nonaccidental) differences in shape.

Representation of Shape in Individuals From a Culture With Minimal Exposure to Regular, Simple Artifacts: Sensitivity to Nonaccidental Versus Metric Properties

Many of the phenomena underlying shape recognition can be derived from the greater sensitivity to nonaccidental properties of an image (e.g., whether a contour is straight or curved), which are invariant to orientation in depth, than to the metric properties of an image (e.g., a contours degree of curvature), which can vary with orientation. What enables this sensitivity? One explanation is that it derives from peoples immersion in a manufactured world in which simple, regular shapes distinguished by nonaccidental properties abound (e.g., a can, a brick), and toddlers are encouraged to play with toy shape sorters. This report provides evidence against this explanation. The Himba, a seminomadic people living in a remote region of northwestern Namibia where there is little exposure to regular, simple artifacts, were virtually identical to Western observers in their greater sensitivity to nonaccidental properties than to metric properties of simple shapes.