"Walking selectivity" in the occipital place area in 8-year-olds, not 5-year-olds.

A recent neuroimaging study in adults found that the occipital place area (OPA)-a cortical region involved in "visually guided navigation" (i.e. moving about the immediately visible environment, avoiding boundaries, and obstacles)-represents visual information about walking, not crawling, suggesting that OPA is late developing, emerging only when children are walking, not beforehand. But when precisely does this "walking selectivity" in OPA emerge-when children first begin to walk in early childhood, or perhaps counterintuitively, much later in childhood, around 8 years of age, when children are adult-like walking? To directly test these two hypotheses, using functional magnetic resonance imaging (fMRI) in two groups of children, 5- and 8-year-olds, we measured the responses in OPA to first-person perspective videos through scenes from a "walking" perspective, as well as three control perspectives ("crawling," "flying," and "scrambled"). We found that the OPA in 8-year-olds-like adults-exhibited walking selectivity (i.e. responding significantly more to the walking videos than to any of the others, and no significant differences across the crawling, flying, and scrambled videos), while the OPA in 5-year-olds exhibited no walking selectively. These findings reveal that OPA undergoes protracted development, with walking selectivity only emerging around 8 years of age.

Visuospatial processing in early brain-based visual impairment is associated with differential recruitment of dorsal and ventral visual streams.

Visuospatial processing impairments are prevalent in individuals with cerebral visual impairment (CVI) and are typically ascribed to "dorsal stream dysfunction" (DSD). However, the contribution of other cortical regions, including early visual cortex (EVC), frontal cortex, or the ventral visual stream, to such impairments remains unknown. Thus, here, we examined fMRI activity in these regions, while individuals with CVI (and neurotypicals) performed a visual search task within a dynamic naturalistic scene. First, behavioral performance was measured with eye tracking. Participants were instructed to search and follow a walking human target. CVI participants took significantly longer to find the target, and their eye gaze patterns were less accurate and less precise. Second, we used the same task in the MRI scanner. Along the dorsal stream, activation was reduced in CVI participants, consistent with the proposed DSD in CVI. Intriguingly, however, visual areas along the ventral stream showed the complete opposite pattern, with greater activation in CVI participants. In contrast, we found no differences in either EVC or frontal cortex between groups. These results suggest that the impaired visuospatial processing abilities in CVI are associated with differential recruitment of the dorsal and ventral visual streams, likely resulting from impaired selective attention.

Dissociable Cognitive Systems for Recognizing Places and Navigating through Them: Developmental and Neuropsychological Evidence.

Recent neural evidence suggests that the human brain contains dissociable systems for "scene categorization" (i.e., recognizing a place as a particular kind of place, for example, a kitchen), including the parahippocampal place area, and "visually guided navigation" (e.g., finding our way through a kitchen, not running into the kitchen walls or banging into the kitchen table), including the occipital place area. However, converging behavioral data - for instance, whether scene categorization and visually guided navigation abilities develop along different timelines and whether there is differential breakdown under neurologic deficit - would provide even stronger support for this two-scene-systems hypothesis. Thus, here we tested scene categorization and visually guided navigation abilities in 131 typically developing children between 4 and 9 years of age, as well as 46 adults with Williams syndrome, a developmental disorder with known impairment on "action" tasks, yet relative sparing on "perception" tasks, in object processing. We found that (1) visually guided navigation is later to develop than scene categorization, and (2) Williams syndrome adults are impaired in visually guided navigation, but not scene categorization, relative to mental age-matched children. Together, these findings provide the first developmental and neuropsychological evidence for dissociable cognitive systems for recognizing places and navigating through them.SIGNIFICANCE STATEMENT Two decades ago, Milner and Goodale showed us that identifying objects and manipulating them involve distinct cognitive and neural systems. Recent neural evidence suggests that the same may be true of our interactions with our environment: identifying places and navigating through them are dissociable systems. Here we provide converging behavioral evidence supporting this two-scene-systems hypothesis - finding both differential development and breakdown of "scene categorization" and "visually guided navigation." This finding suggests that the division of labor between perception and action systems is a general organizing principle for the visual system, not just a principle of the object processing system in particular.

The occipital place area represents visual information about walking, not crawling.

Recent work has shown that the occipital place area (OPA)-a scene-selective region in adult humans-supports "visually guided navigation" (i.e. moving about the local visual environment and avoiding boundaries/obstacles). But what is the precise role of OPA in visually guided navigation? Considering humans move about their local environments beginning with crawling followed by walking, 1 possibility is that OPA is involved in both modes of locomotion. Another possibility is that OPA is specialized for walking only, since walking and crawling are different kinds of locomotion. To test these possibilities, we measured the responses in OPA to first-person perspective videos from both "walking" and "crawling" perspectives as well as for 2 conditions by which humans do not navigate ("flying" and "scrambled"). We found that OPA responded more to walking videos than to any of the others, including crawling, and did not respond more to crawling videos than to flying or scrambled ones. These results (i) reveal that OPA represents visual information only from a walking (not crawling) perspective, (ii) suggest crawling is processed by a different neural system, and (iii) raise questions for how OPA develops; namely, OPA may have never supported crawling, which is consistent with the hypothesis that OPA undergoes protracted development.

A stimulus-driven approach reveals vertical luminance gradient as a stimulus feature that drives human cortical scene selectivity.

Human neuroimaging studies have revealed a dedicated cortical system for visual scene processing. But what is a "scene"? Here, we use a stimulus-driven approach to identify a stimulus feature that selectively drives cortical scene processing. Specifically, using fMRI data from BOLD5000, we examined the images that elicited the greatest response in the cortical scene processing system, and found that there is a common "vertical luminance gradient" (VLG), with the top half of a scene image brighter than the bottom half; moreover, across the entire set of images, VLG systematically increases with the neural response in the scene-selective regions (Study 1). Thus, we hypothesized that VLG is a stimulus feature that selectively engages cortical scene processing, and directly tested the role of VLG in driving cortical scene selectivity using tightly controlled VLG stimuli (Study 2). Consistent with our hypothesis, we found that the scene-selective cortical regions-but not an object-selective region or early visual cortex-responded significantly more to images of VLG over control stimuli with minimal VLG. Interestingly, such selectivity was also found for images with an "inverted" VLG, resembling the luminance gradient in night scenes. Finally, we also tested the behavioral relevance of VLG for visual scene recognition (Study 3); we found that participants even categorized tightly controlled stimuli of both upright and inverted VLG to be a place more than an object, indicating that VLG is also used for behavioral scene recognition. Taken together, these results reveal that VLG is a stimulus feature that selectively engages cortical scene processing, and provide evidence for a recent proposal that visual scenes can be characterized by a set of common and unique visual features.

Rapid topographic reorganization in adult human primary visual cortex (V1) during noninvasive and reversible deprivation.

Can the primary visual cortex (V1), once wired up in development, change in adulthood? Although numerous studies have demonstrated topographic reorganization in adult V1 following the loss of bottom-up input, others have challenged such findings, offering alternative explanations. Here we use a noninvasive and reversible deprivation paradigm and converging neural and behavioral approaches to address these alternatives in the experimental test case of short-term topographic reorganization in adult human V1. Specifically, we patched one eye in typical adults, thereby depriving the cortical representation of the other eye's blind spot (BS), and immediately tested for topographic reorganization using functional magnetic resonance imaging and psychophysics. Strikingly, within just minutes of eye-patching, the BS representation in V1 began responding to stimuli presented outside of the BS, and these same stimuli were perceived as elongated toward the BS. Thus, we provide converging neural and behavioral evidence of rapid topographic reorganization in adult human V1, and the strongest evidence yet that visual deprivation produces bona fide cortical change.

Connectivity at the origins of domain specificity in the cortical face and place networks.

It is well established that the adult brain contains a mosaic of domain-specific networks. But how do these domain-specific networks develop? Here we tested the hypothesis that the brain comes prewired with connections that precede the development of domain-specific function. Using resting-state fMRI in the youngest sample of newborn humans tested to date, we indeed found that cortical networks that will later develop strong face selectivity (including the "proto" occipital face area and fusiform face area) and scene selectivity (including the "proto" parahippocampal place area and retrosplenial complex) by adulthood, already show domain-specific patterns of functional connectivity as early as 27 d of age (beginning as early as 6 d of age). Furthermore, we asked how these networks are functionally connected to early visual cortex and found that the proto face network shows biased functional connectivity with foveal V1, while the proto scene network shows biased functional connectivity with peripheral V1. Given that faces are almost always experienced at the fovea, while scenes always extend across the entire periphery, these differential inputs may serve to facilitate domain-specific processing in each network after that function develops, or even guide the development of domain-specific function in each network in the first place. Taken together, these findings reveal domain-specific and eccentricity-biased connectivity in the earliest days of life, placing new constraints on our understanding of the origins of domain-specific cortical networks.

Distinct representations of spatial and categorical relationships across human scene-selective cortex.

We represent the locations of places (e.g., the coffee shop on 10th Street vs. the coffee shop on Peachtree Street) so that we can use them as landmarks to orient ourselves while navigating large-scale environments. While several neuroimaging studies have argued that the parahippocampal place area (PPA) represents such navigationally relevant information, evidence from other studies suggests otherwise, leaving this issue unresolved. Here we hypothesize that the PPA is, in fact, not well suited to recognize specific landmarks in the environment (e.g., the coffee shop on 10th Street), but rather is involved in recognizing the general category membership of places (e.g., a coffee shop, regardless of its location). Using fMRI multivoxel pattern analysis, we directly test this hypothesis. If the PPA represents landmark information, then it must be able to discriminate between 2 places of the same category, but in different locations. Instead, if the PPA represents general category information (as hypothesized here), then it will not represent the location of a particular place, but only the category of the place. As predicted, we found that the PPA represents 2 buildings from the same category, but in different locations, as more similar than 2 buildings from different categories, but in the same location. In contrast, another scene-selective region of cortex, the retrosplenial complex (RSC), showed the exact opposite pattern of results. Such a double dissociation suggests distinct neural systems involved in categorizing and navigating our environment, including the PPA and RSC, respectively.

Concavity as a diagnostic feature of visual scenes.

Despite over two decades of research on the neural mechanisms underlying human visual scene, or place, processing, it remains unknown what exactly a "scene" is. Intuitively, we are always inside a scene, while interacting with the outside of objects. Hence, we hypothesize that one diagnostic feature of a scene may be concavity, portraying "inside", and predict that if concavity is a scene-diagnostic feature, then: 1) images that depict concavity, even non-scene images (e.g., the "inside" of an object - or concave object), will be behaviorally categorized as scenes more often than those that depict convexity, and 2) the cortical scene-processing system will respond more to concave images than to convex images. As predicted, participants categorized concave objects as scenes more often than convex objects, and, using functional magnetic resonance imaging (fMRI), two scene-selective cortical regions (the parahippocampal place area, PPA, and the occipital place area, OPA) responded significantly more to concave than convex objects. Surprisingly, we found no behavioral or neural differences between images of concave versus convex buildings. However, in a follow-up experiment, using tightly-controlled images, we unmasked a selective sensitivity to concavity over convexity of scene boundaries (i.e., walls) in PPA and OPA. Furthermore, we found that even highly impoverished line drawings of concave shapes are behaviorally categorized as scenes more often than convex shapes. Together, these results provide converging behavioral and neural evidence that concavity is a diagnostic feature of visual scenes.

The Uncanny Valley Phenomenon and the Temporal Dynamics of Face Animacy Perception.

Human replicas highly resembling people tend to elicit eerie sensations-a phenomenon known as the uncanny valley. To test whether this effect is attributable to people's ascription of mind to (i.e., mind perception hypothesis) or subtraction of mind from androids (i.e., dehumanization hypothesis), in Study 1, we examined the effect of face exposure time on the perceived animacy of human, android, and mechanical-looking robot faces. In Study 2, in addition to exposure time, we also manipulated the spatial frequency of faces, by preserving either their fine (high spatial frequency) or coarse (low spatial frequency) information, to examine its effect on faces' perceived animacy and uncanniness. We found that perceived animacy decreased as a function of exposure time only in android but not in human or mechanical-looking robot faces (Study 1). In addition, the manipulation of spatial frequency eliminated the decrease in android faces' perceived animacy and reduced their perceived uncanniness (Study 2). These findings link perceived uncanniness in androids to the temporal dynamics of face animacy perception. We discuss these findings in relation to the dehumanization hypothesis and alternative hypotheses of the uncanny valley phenomenon.

Dissociable Neural Systems for Recognizing Places and Navigating through Them.

When entering an environment, we can use the present visual information from the scene to either recognize the kind of place it is (e.g., a kitchen or a bedroom) or navigate through it. Here we directly test the hypothesis that these two processes, what we call "scene categorization" and "visually-guided navigation", are supported by dissociable neural systems. Specifically, we manipulated task demands by asking human participants (male and female) to perform a scene categorization, visually-guided navigation, and baseline task on images of scenes, and measured both the average univariate responses and multivariate spatial pattern of responses within two scene-selective cortical regions, the parahippocampal place area (PPA) and occipital place area (OPA), hypothesized to be separably involved in scene categorization and visually-guided navigation, respectively. As predicted, in the univariate analysis, PPA responded significantly more during the categorization task than during both the navigation and baseline tasks, whereas OPA showed the complete opposite pattern. Similarly, in the multivariate analysis, a linear support vector machine achieved above-chance classification for the categorization task, but not the navigation task in PPA. By contrast, above-chance classification was achieved for both the navigation and categorization tasks in OPA. However, above-chance classification for both tasks was also found in early visual cortex and hence not specific to OPA, suggesting that the spatial patterns of responses in OPA are merely inherited from early vision, and thus may be epiphenomenal to behavior. Together, these results are evidence for dissociable neural systems involved in recognizing places and navigating through them.SIGNIFICANCE STATEMENT It has been nearly three decades since Goodale and Milner demonstrated that recognizing objects and manipulating them involve distinct neural processes. Today we show the same is true of our interactions with our environment: recognizing places and navigating through them are neurally dissociable. More specifically, we found that a scene-selective region, the parahippocampal place area, is active when participants are asked to categorize a scene, but not when asked to imagine navigating through it, whereas another scene-selective region, the occipital place area, shows the exact opposite pattern. This double dissociation is evidence for dissociable neural systems within scene processing, similar to the bifurcation of object processing described by Goodale and Milner (1992).

A face is more than just the eyes, nose, and mouth: fMRI evidence that face-selective cortex represents external features.

What is a face? Intuition, along with abundant behavioral and neural evidence, indicates that internal features (e.g., eyes, nose, mouth) are critical for face recognition, yet some behavioral and neural findings suggest that external features (e.g., hair, head outline, neck and shoulders) may likewise be processed as a face. Here we directly test this hypothesis by investigating how external (and internal) features are represented in the brain. Using fMRI, we found highly selective responses to external features (relative to objects and scenes) within the face processing system in particular, rivaling that observed for internal features. We then further asked how external and internal features are represented in regions of the cortical face processing system, and found a similar division of labor for both kinds of features, with the occipital face area and posterior superior temporal sulcus representing the parts of both internal and external features, and the fusiform face area representing the coherent arrangement of both internal and external features. Taken together, these results provide strong neural evidence that a "face" is composed of both internal and external features.

Representational similarity precedes category selectivity in the developing ventral visual pathway.

Many studies have investigated the development of face-, scene-, and body-selective regions in the ventral visual pathway. This work has primarily focused on comparing the size and univariate selectivity of these neural regions in children versus adults. In contrast, very few studies have investigated the developmental trajectory of more distributed activation patterns within and across neural regions. Here, we scanned both children (ages 5-7) and adults to test the hypothesis that distributed representational patterns arise before category selectivity (for faces, bodies, or scenes) in the ventral pathway. Consistent with this hypothesis, we found mature representational patterns in several ventral pathway regions (e.g., FFA, PPA, etc.), even in children who showed no hint of univariate selectivity. These results suggest that representational patterns emerge first in each region, perhaps forming a scaffold upon which univariate category selectivity can subsequently develop. More generally, our findings demonstrate an important dissociation between category selectivity and distributed response patterns, and raise questions about the relative roles of each in development and adult cognition.

Dissociable spatial memory systems revealed by typical and atypical human development.

Rodent lesion studies have revealed the existence of two causally dissociable spatial memory systems, localized to the hippocampus and striatum that are preferentially sensitive to environmental boundaries and landmark objects, respectively. Here we test whether these two memory systems are causally dissociable in humans by examining boundary- and landmark-based memory in typical and atypical development. Adults with Williams syndrome (WS)-a developmental disorder with known hippocampal abnormalities-and typical children and adults, performed a navigation task that involved learning locations relative to a boundary or a landmark object. We found that boundary-based memory was severely impaired in WS compared to typically-developing mental-age matched (MA) children and chronological-age matched (CA) adults, whereas landmark-based memory was similar in all groups. Furthermore, landmark-based memory matured earlier in typical development than boundary-based memory, consistent with the idea that the WS cognitive phenotype arises from developmental arrest of late maturing cognitive systems. Together, these findings provide causal and developmental evidence for dissociable spatial memory systems in humans.

Places in the Brain: Bridging Layout and Object Geometry in Scene-Selective Cortex.

Diverse animal species primarily rely on sense (left-right) and egocentric distance (proximal-distal) when navigating the environment. Recent neuroimaging studies with human adults show that this information is represented in 2 scene-selective cortical regions-the occipital place area (OPA) and retrosplenial complex (RSC)-but not in a third scene-selective region-the parahippocampal place area (PPA). What geometric properties, then, does the PPA represent, and what is its role in scene processing? Here we hypothesize that the PPA represents relative length and angle, the geometric properties classically associated with object recognition, but only in the context of large extended surfaces that compose the layout of a scene. Using functional magnetic resonance imaging adaptation, we found that the PPA is indeed sensitive to relative length and angle changes in pictures of scenes, but not pictures of objects that reliably elicited responses to the same geometric changes in object-selective cortical regions. Moreover, we found that the OPA is also sensitive to such changes, while the RSC is tolerant to such changes. Thus, the geometric information typically associated with object recognition is also used during some aspects of scene processing. These findings provide evidence that scene-selective cortex differentially represents the geometric properties guiding navigation versus scene categorization.

Memorability: A stimulus-driven perceptual neural signature distinctive from memory.

A long-standing question in neuroscience is how perceptual processes select stimuli for encoding and later retrieval by memory processes. Using a functional magnetic resonance imaging study with human participants, we report the discovery of a global, stimulus-driven processing stream that we call memorability. Memorability automatically tags the statistical distinctiveness of stimuli for later encoding, and shows separate neural signatures from both low-level perception (memorability shows no signal in early visual cortex) and classical subsequent memory based on individual memory. Memorability and individual subsequent memory show dissociable neural substrates: first, memorability effects consistently emerge in the medial temporal lobe (MTL), whereas individual subsequent memory effects emerge in the prefrontal cortex (PFC). Second, memorability effects remain consistent even in the absence of memory (i.e., for forgotten images). Third, the MTL shows higher correlations with memorability-based patterns, while the PFC shows higher correlations with individual memory voxels patterns. Taken together, these results support a reformulated framework of the interplay between perception and memory, with the MTL determining stimulus statistics and distinctiveness to support later memory encoding, and the PFC comparing stimuli to specific individual memories. As stimulus memorability is a confound present in many previous memory studies, these findings should stimulate a revisitation of the neural streams dedicated to perception and memory.

The occipital place area represents the local elements of scenes.

Neuroimaging studies have identified three scene-selective regions in human cortex: parahippocampal place area (PPA), retrosplenial complex (RSC), and occipital place area (OPA). However, precisely what scene information each region represents is not clear, especially for the least studied, more posterior OPA. Here we hypothesized that OPA represents local elements of scenes within two independent, yet complementary scene descriptors: spatial boundary (i.e., the layout of external surfaces) and scene content (e.g., internal objects). If OPA processes the local elements of spatial boundary information, then it should respond to these local elements (e.g., walls) themselves, regardless of their spatial arrangement. Indeed, we found that OPA, but not PPA or RSC, responded similarly to images of intact rooms and these same rooms in which the surfaces were fractured and rearranged, disrupting the spatial boundary. Next, if OPA represents the local elements of scene content information, then it should respond more when more such local elements (e.g., furniture) are present. Indeed, we found that OPA, but not PPA or RSC, responded more to multiple than single pieces of furniture. Taken together, these findings reveal that OPA analyzes local scene elements - both in spatial boundary and scene content representation - while PPA and RSC represent global scene properties.

The occipital place area is causally and selectively involved in scene perception.

Functional magnetic resonance imaging has revealed a set of regions selectively engaged in visual scene processing: the parahippocampal place area (PPA), the retrosplenial complex (RSC), and a region around the transverse occipital sulcus (previously known as "TOS"), here renamed the "occipital place area" (OPA). Are these regions not only preferentially activated by, but also causally involved in scene perception? Although past neuropsychological data imply a causal role in scene processing for PPA and RSC, no such evidence exists for OPA. Thus, to test the causal role of OPA in human adults, we delivered transcranial magnetic stimulation (TMS) to the right OPA (rOPA) or the nearby face-selective right occipital face area (rOFA) while participants performed fine-grained perceptual discrimination tasks on scenes or faces. TMS over rOPA impaired discrimination of scenes but not faces, while TMS over rOFA impaired discrimination of faces but not scenes. In a second experiment, we delivered TMS to rOPA, or the object-selective right lateral occipital complex (rLOC), while participants performed categorization tasks involving scenes and objects. TMS over rOPA impaired categorization accuracy of scenes but not objects, while TMS over rLOC impaired categorization accuracy of objects but not scenes. These findings provide the first evidence that OPA is causally involved in scene processing, and further show that this causal role is selective for scene perception. Our findings illuminate the functional architecture of the scene perception system, and also argue against the "distributed coding" view in which each category-selective region participates in the representation of all objects.

Domain-specific development of face memory but not face perception.

How does the remarkable human ability for face recognition arise over development? Competing theories have proposed either late maturity (beyond 10 years) or early maturity (before 5 years), but have not distinguished between perceptual and memory aspects of face recognition. Here, we demonstrate a perception-memory dissociation. We compare rate of development for (adult, human) faces versus other social stimuli (bodies), other discrete objects (cars), and other categories processed in discrete brain regions (scenes, bodies), from 5 years to adulthood. For perceptual discrimination, performance improved with age at the same rate for faces and all other categories, indicating no domain-specific development. In contrast, face memory increased more strongly than non-face memory, indicating domain-specific development. The results imply that each theory is partly true: the late maturity theory holds for face memory, and the early maturity theory for face perception.

Reorganization of visual processing in age-related macular degeneration depends on foveal loss.

PURPOSE: When individuals with central vision loss due to macular degeneration (MD) view stimuli in the periphery, most of them activate the region of retinotopic cortex normally activated only by foveal stimuli-a process often referred to as reorganization. Why do some show this reorganization of visual processing whereas others do not? We reported previously that six individuals with complete bilateral loss of central vision showed such reorganization, whereas two with bilateral central vision loss but with foveal sparing did not, and we hypothesized that the effect occurs only after complete bilateral loss of foveal vision. Here, we conduct a stronger test of the dependence of reorganization of visual processing in MD on complete loss of foveal function, by bringing back one (called MD6) of the two participants who previously did not show reorganization and who showed foveal sparing. MD6 has now lost all foveal function, and we predicted that if large-scale reorganization of visual processing in MD individuals depends on complete loss of foveal input, then we will now see such reorganization in this individual. METHODS: MD6 and two normally sighted control subjects were scanned. Stimuli were gray-scale photographs of objects presented at either the fovea or a peripheral retinal location (i.e., the MD participant's preferred retinal locus or the control participants' matched peripheral location). RESULTS: In MD6, visual stimulation at the preferred retinal locus significantly activated not only the expected "peripheral" retinotopic cortex but also the deprived "foveal" cortex. Crucially, MD6 exhibited no such large-scale reorganization 5 years earlier when she had some foveal sparing. By contrast, in the control participants, stimulation at the matched peripheral location produced significant activation in peripheral retinotopic cortex only. CONCLUSIONS: We conclude that complete loss of foveal function may be a necessary condition for large-scale reorganization of visual processing in individuals with MD.