Shahin Nasr

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.

Thinking Outside the Box: Rectilinear Shapes Selectively Activate Scene-Selective Cortex

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.

A cardinal orientation bias in scene-selective visual cortex

It has long been known that human vision is more sensitive to contours at cardinal (horizontal and vertical) orientations, compared with oblique orientations; this is the “oblique effect.” However, the real-world relevance of the oblique effect is not well understood. Experiments here suggest that this effect is linked to scene perception, via a common bias in the image statistics of scenes. This statistical bias for cardinal orientations is found in many “carpentered environments” such as buildings and indoor scenes, and some natural scenes. In Experiment 1, we confirmed the presence of a perceptual oblique effect in a specific set of scene stimuli. Using those scenes, we found that a well known “scene-selective” visual cortical area (the parahippocampal place area; PPA) showed distinctively higher functional magnetic resonance imaging (fMRI) activity to cardinal versus oblique orientations. This fMRI-based oblique effect was not observed in other cortical areas (including scene-selective areas transverse occipital sulcus and retrosplenial cortex), although all three scene-selective areas showed the expected inversion effect to scenes. Experiments 2 and 3 tested for an analogous selectivity for cardinal orientations using computer-generated arrays of simple squares and line segments, respectively. The results confirmed the preference for cardinal orientations in PPA, thus demonstrating that the oblique effect can also be produced in PPA by simple geometrical images, with statistics similar to those in scenes. Thus, PPA shows distinctive fMRI selectivity for cardinal orientations across a broad range of stimuli, which may reflect a perceptual oblique effect.

Interdigitated Color- and Disparity-Selective Columns within Human Visual Cortical Areas V2 and V3

In nonhuman primates (NHPs), secondary visual cortex (V2) is composed of repeating columnar stripes, which are evident in histological variations of cytochrome oxidase (CO) levels. Distinctive “thin” and “thick” stripes of dark CO staining reportedly respond selectively to stimulus variations in color and binocular disparity, respectively. Here, we first tested whether similar color-selective or disparity-selective stripes exist in human V2. If so, available evidence predicts that such stripes should (1) radiate “outward” from the V1–V2 border, (2) interdigitate, (3) differ from each other in both thickness and length, (4) be spaced ∼3.5–4 mm apart (center-to-center), and, perhaps, (5) have segregated functional connections. Second, we tested whether analogous segregated columns exist in a “next-higher” tier area, V3. To answer these questions, we used high-resolution fMRI (1 × 1 × 1 mm3) at high field (7 T), presenting color-selective or disparity-selective stimuli, plus extensive signal averaging across multiple scan sessions and cortical surface-based analysis. All hypotheses were confirmed. V2 stripes and V3 columns were reliably localized in all subjects. The two stripe/column types were largely interdigitated (e.g., nonoverlapping) in both V2 and V3. Color-selective stripes differed from disparity-selective stripes in both width (thickness) and length. Analysis of resting-state functional connections (eyes closed) showed a stronger correlation between functionally alike (compared with functionally unlike) stripes/columns in V2 and V3. These results revealed a fine-scale segregation of color-selective or disparity-selective streams within human areas V2 and V3. Together with prior evidence from NHPs, this suggests that two parallel processing streams extend from visual subcortical regions through V1, V2, and V3. SIGNIFICANCE STATEMENT In current textbooks and reviews, diagrams of cortical visual processing highlight two distinct neural-processing streams within the first and second cortical areas in monkeys. Two major streams consist of segregated cortical columns that are selectively activated by either color or ocular interactions. Because such cortical columns are so small, they were not revealed previously by conventional imaging techniques in humans. Here we demonstrate that such segregated columnar systems exist in humans. We find that, in humans, color versus binocular disparity columns extend one full area further, into the third visual area. Our approach can be extended to reveal and study additional types of columns in human cortex, perhaps including columns underlying more cognitive functions.

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.

Spatial encoding and underlying circuitry in scene-selective cortex

Three cortical areas (Retro-Splenial Cortex (RSC), Transverse Occipital Sulcus (TOS) and Parahippocampal Place Area (PPA)) respond selectively to scenes. However, their wider role in spatial encoding and their functional connectivity remain unclear. Using fMRI, first we tested the responses of these areas during spatial comparison tasks using dot targets on white noise. Activity increased during task performance in both RSC and TOS, but not in PPA. However, the amplitude of task-driven activity and behavioral measures of task demand were correlated only in RSC. A control experiment showed that none of these areas were activated during a comparable shape comparison task. Secondly, we analyzed functional connectivity of these areas during the resting state. Results revealed a significant connection between RSC and frontal association areas (known to be involved in perceptual decision-making). In contrast, TOS showed functional connections dorsally with the Inferior Parietal Sulcus, and ventrally with the Lateral Occipital Complex--but not with RSC and/or frontal association areas. Moreover, RSC and TOS showed differentiable functional connections with the anterior-medial and posterior-lateral parts of PPA, respectively. These results suggest two parallel pathways for spatial encoding, including RSC and TOS respectively. Only the RSC network was involved in active spatial comparisons.

FMRI analysis of contrast polarity in face-selective cortex in humans and monkeys

Recognition is strongly impaired when the normal contrast polarity of faces is reversed. For instance, otherwise-familiar faces become very difficult to recognize when viewed as photographic negatives. Here, we used fMRI to demonstrate related properties in visual cortex: 1) fMRI responses in the human Fusiform Face Area (FFA) decreased strongly (26%) to contrast-reversed faces across a wide range of contrast levels (5.3-100% RMS contrast), in all subjects tested. In a whole brain analysis, this contrast polarity bias was largely confined to the Fusiform Face Area (FFA; p<0.0001), with possible involvement of a left occipital face-selective region. 2) It is known that reversing facial contrast affects three image properties in parallel (absorbance, shading, and specular reflection). Here, comparison of FFA responses to those in V1 suggests that the contrast polarity bias is produced in FFA only when all three component properties were reversed simultaneously, which suggests a prominent non-linearity in FFA processing. 3) Across a wide range (180°) of illumination source angles, 3D face shapes without texture produced response constancy in FFA, without a contrast polarity bias. 4) Consistent with psychophysics, analogous fMRI biases for normal contrast polarity were not produced by non-face objects, with image statistics similar to the face stimuli. 5) Using fMRI, we also demonstrated a contrast polarity bias in awake behaving macaque monkeys, in the cortical region considered homologous to human FFA. Thus common cortical mechanisms may underlie facial contrast processing across ~25 million years of primate evolution.

A parametric study of fear generalization to faces and non-face objects: relationship to discrimination thresholds

Fear generalization is the production of fear responses to a stimulus that is similar—but not identical—to a threatening stimulus. Although prior studies have found that fear generalization magnitudes are qualitatively related to the degree of perceptual similarity to the threatening stimulus, the precise relationship between these two functions has not been measured systematically. Also, it remains unknown whether fear generalization mechanisms differ for social and non-social information. To examine these questions, we measured perceptual discrimination and fear generalization in the same subjects, using images of human faces and non-face control stimuli (“blobs”) that were perceptually matched to the faces. First, each subject’s ability to discriminate between pairs of faces or blobs was measured. Each subject then underwent a Pavlovian fear conditioning procedure, in which each of the paired conditioned stimuli (CS) were either followed (CS+) or not followed (CS−) by a shock. Skin conductance responses (SCRs) were also measured. Subjects were then presented with the CS+, CS− and five levels of a CS+-to-CS− morph continuum between the paired stimuli, which were identified based on individual discrimination thresholds. Finally, subjects rated the likelihood that each stimulus had been followed by a shock. Subjects showed both autonomic (SCR-based) and conscious (ratings-based) fear responses to morphs that they could not discriminate from the CS+ (generalization). For both faces and non-face objects, fear generalization was not found above discrimination thresholds. However, subjects exhibited greater fear generalization in the shock likelihood ratings compared to the SCRs, particularly for faces. These findings reveal that autonomic threat detection mechanisms in humans are highly sensitive to small perceptual differences between stimuli. Also, the conscious evaluation of threat shows broader generalization than autonomic responses, biased towards labeling a stimulus as threatening.

Columnar Segregation of Magnocellular and Parvocellular Streams in Human Extrastriate Cortex

Magnocellular versus parvocellular (M-P) streams are fundamental to the organization of macaque visual cortex. Segregated, paired M-P streams extend from retina through LGN into V1. The M stream extends further into area V5/MT, and parts of V2. However, elsewhere in visual cortex, it remains unclear whether M-P-derived information (1) becomes intermixed or (2) remains segregated in M-P-dominated columns and neurons. Here we tested whether M-P streams exist in extrastriate cortical columns, in 8 human subjects (4 female). We acquired high-resolution fMRI at high field (7T), testing for M- and P-influenced columns within each of four cortical areas (V2, V3, V3A, and V4), based on known functional distinctions in M-P streams in macaque: (1) color versus luminance, (2) binocular disparity, (3) luminance contrast sensitivity, (4) peak spatial frequency, and (5) color/spatial interactions. Additional measurements of resting state activity (eyes closed) tested for segregated functional connections between these columns. We found M- and P-like functions and connections within and between segregated cortical columns in V2, V3, and (in most experiments) area V4. Area V3A was dominated by the M stream, without significant influence from the P stream. These results suggest that M-P streams exist, and extend through, specific columns in early/middle stages of human extrastriate cortex. SIGNIFICANCE STATEMENT The magnocellular and parvocellular (M-P) streams are fundamental components of primate visual cortical organization. These streams segregate both anatomical and functional properties in parallel, from retina through primary visual cortex. However, in most higher-order cortical sites, it is unknown whether such M-P streams exist and/or what form those streams would take. Moreover, it is unknown whether M-P streams exist in human cortex. Here, fMRI evidence measured at high field (7T) and high resolution revealed segregated M-P streams in four areas of human extrastriate cortex. These results suggest that M-P information is processed in segregated parallel channels throughout much of human visual cortex; the M-P streams are more than a convenient sorting property in earlier stages of the visual system.

Differential impact of attention on the early and late categorization related human brain potentials.

Previous human studies have shown that object-selective attention enhances neural activities evoked in response to target stimuli. However, it is not clear whether the magnitude of activity enhancement is constant or varies according to the level of stimulus visibility. To examine the effect of attentional modulation on different event-related potentials (ERPs) and the relationship between attentional modulation and level of stimulus visibility, subjects were instructed to perform face detection and leaf detection tasks in separate blocks while the level of stimulus visibility varied randomly from trial to trial. As a result of object-selective attention, N170 and P400 ERP components were both modulated in response to the task target category compared to when the same category was used as distracter. We found that the magnitude of modulation of the N170 component was independent of the stimulus visibility level, while the P400 ERP component showed increased enhancement as the level of stimulus visibility increased. These findings demonstrate that attention impacts the neural populations, indexed by early (N170) and late (P400) evoked potentials, differentially and that attentional modulation becomes increasingly dependent on the level of stimulus visibility through the course of brain activities.