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.

"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.

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.

Deficits in Face Recognition and Consequent Quality-of-Life Factors in Individuals with Cerebral Visual Impairment.

Individuals with cerebral visual impairment (CVI) frequently report challenges with face recognition, and subsequent difficulties with social interactions. However, there is limited empirical evidence supporting poor face recognition in individuals with CVI and the potential impact on social-emotional quality-of-life factors. Moreover, it is unclear whether any difficulties with face recognition represent a broader ventral stream dysfunction. In this web-based study, data from a face recognition task, a glass pattern detection task, and the Strengths and Difficulties Questionnaire (SDQ) were analyzed from 16 participants with CVI and 25 controls. In addition, participants completed a subset of questions from the CVI Inventory to provide a self-report of potential areas of visual perception that participants found challenging. The results demonstrate a significant impairment in the performance of a face recognition task in participants with CVI compared to controls, which was not observed for the glass pattern task. Specifically, we observed a significant increase in threshold, reduction in the proportion correct, and an increase in response time for the faces, but not for the glass pattern task. Participants with CVI also reported a significant increase in sub-scores of the SDQ for emotional problems and internalizing scores after adjusting for the potential confounding effects of age. Finally, individuals with CVI also reported a greater number of difficulties on items from the CVI Inventory, specifically the five questions and those related to face and object recognition. Together, these results indicate that individuals with CVI may demonstrate significant difficulties with face recognition, which may be linked to quality-of-life factors. This evidence suggests that targeted evaluations of face recognition are warranted in all individuals with CVI, regardless of their age.

The development of human cortical scene processing.

Decades of research have uncovered the neural basis of place (or "scene") processing in adulthood, revealing a set of three regions that respond selectively to visual scene information, each hypothesized to support distinct functions within scene processing (e.g., recognizing a particular kind of place versus navigating through it). Despite this considerable progress, surprisingly little is known about how these cortical regions develop. Here we review the limited evidence to date, highlighting the first few studies exploring the origins of cortical scene processing in infancy, and the several studies addressing when the scene regions reach full maturity, unfortunately with inconsistent findings. This inconsistency likely stems from common pitfalls in pediatric functional magnetic resonance imaging, and accordingly, we discuss how these pitfalls may be avoided. Furthermore, we point out that almost all studies to date have focused only on general scene selectivity and argue that greater insight could be gleaned by instead exploring the more distinct functions of each region, as well as their connectivity. Finally, with this last point in mind, we offer a novel hypothesis that scene regions supporting navigation (including the occipital place area and retrosplenial complex) mature later than those supporting scene categorization (including the parahippocampal place area).

Through a Dog's Eyes: fMRI Decoding of Naturalistic Videos from the Dog Cortex.

Recent advancements using machine learning and functional magnetic resonance imaging (fMRI) to decode visual stimuli from the human and nonhuman cortex have resulted in new insights into the nature of perception. However, this approach has yet to be applied substantially to animals other than primates, raising questions about the nature of such representations across the animal kingdom. Here, we used awake fMRI in two domestic dogs and two humans, obtained while each watched specially created dog-appropriate naturalistic videos. We then trained a neural net (Ivis) to classify the video content from a total of 90 min of recorded brain activity from each. We tested both an object-based classifier, attempting to discriminate categories such as dog, human, and car, and an action-based classifier, attempting to discriminate categories such as eating, sniffing, and talking. Compared to the two human subjects, for whom both types of classifier performed well above chance, only action-based classifiers were successful in decoding video content from the dogs. These results demonstrate the first known application of machine learning to decode naturalistic videos from the brain of a carnivore and suggest that the dog's-eye view of the world may be quite different from our own.

Using Live and Video Stimuli to Localize Face and Object Processing Regions of the Canine Brain.

Previous research to localize face areas in dogs' brains has generally relied on static images or videos. However, most dogs do not naturally engage with two-dimensional images, raising the question of whether dogs perceive such images as representations of real faces and objects. To measure the equivalency of live and two-dimensional stimuli in the dog's brain, during functional magnetic resonance imaging (fMRI) we presented dogs and humans with live-action stimuli (actors and objects) as well as videos of the same actors and objects. The dogs (n = 7) and humans (n = 5) were presented with 20 s blocks of faces and objects in random order. In dogs, we found significant areas of increased activation in the putative dog face area, and in humans, we found significant areas of increased activation in the fusiform face area to both live and video stimuli. In both dogs and humans, we found areas of significant activation in the posterior superior temporal sulcus (ectosylvian fissure in dogs) and the lateral occipital complex (entolateral gyrus in dogs) to both live and video stimuli. Of these regions of interest, only the area along the ectosylvian fissure in dogs showed significantly more activation to live faces than to video faces, whereas, in humans, both the fusiform face area and posterior superior temporal sulcus responded significantly more to live conditions than video conditions. However, using the video conditions alone, we were able to localize all regions of interest in both dogs and humans. Therefore, videos can be used to localize these regions of interest, though live conditions may be more salient.

Skeletal representations of shape in the human visual cortex.

Shape perception is crucial for object recognition. However, it remains unknown exactly how shape information is represented and used by the visual system. Here, we tested the hypothesis that the visual system represents object shape via a skeletal structure. Using functional magnetic resonance imaging (fMRI) and representational similarity analysis (RSA), we found that a model of skeletal similarity explained significant unique variance in the response profiles of V3 and LO. Moreover, the skeletal model remained predictive in these regions even when controlling for other models of visual similarity that approximate low-to high-level visual features (i.e., Gabor-jet, GIST, HMAX, and AlexNet), and across different surface forms, a manipulation that altered object contours while preserving the underlying skeleton. Together, these findings shed light on shape processing in human vision, as well as the computational properties of V3 and LO. We discuss how these regions may support two putative roles of shape skeletons: namely, perceptual organization and object recognition.

Three cortical scene systems and their development.

Since the discovery of three scene-selective regions in the human brain, a central assumption has been that all three regions directly support navigation. We propose instead that cortical scene processing regions support three distinct computational goals (and one not for navigation at all): (i) The parahippocampal place area supports scene categorization, which involves recognizing the kind of place we are in; (ii) the occipital place area supports visually guided navigation, which involves finding our way through the immediately visible environment, avoiding boundaries and obstacles; and (iii) the retrosplenial complex supports map-based navigation, which involves finding our way from a specific place to some distant, out-of-sight place. We further hypothesize that these systems develop along different timelines, with both navigation systems developing slower than the scene categorization system.

Two scene navigation systems dissociated by deliberate versus automatic processing.

Successfully navigating the world requires avoiding boundaries and obstacles in one's immediately-visible environment, as well as finding one's way to distant places in the broader environment. Recent neuroimaging studies suggest that these two navigational processes involve distinct cortical scene processing systems, with the occipital place area (OPA) supporting navigation through the local visual environment, and the retrosplenial complex (RSC) supporting navigation through the broader spatial environment. Here we hypothesized that these systems are distinguished not only by the scene information they represent (i.e., the local visual versus broader spatial environment), but also based on the automaticity of the process they involve, with navigation through the broader environment (including RSC) operating deliberately, and navigation through the local visual environment (including OPA) operating automatically. We tested this hypothesis using fMRI and a maze-navigation paradigm, where participants navigated two maze structures (complex or simple, testing representation of the broader spatial environment) under two conditions (active or passive, testing deliberate versus automatic processing). Consistent with the hypothesis that RSC supports deliberate navigation through the broader environment, RSC responded significantly more to complex than simple mazes during active, but not passive navigation. By contrast, consistent with the hypothesis that OPA supports automatic navigation through the local visual environment, OPA responded strongly even during passive navigation, and did not differentiate between active versus passive conditions. Taken together, these findings suggest the novel hypothesis that navigation through the broader spatial environment is deliberate, whereas navigation through the local visual environment is automatic, shedding new light on the dissociable functions of these systems.

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.

Maternal Childhood Adversity Associates With Frontoamygdala Connectivity in Neonates.

BACKGROUND: It is well established that exposure to adversity, especially during sensitive periods of development such as childhood, has both behavioral (e.g., increasing one's risk for psychiatric illnesses) and neurobiological consequences. But could these effects of early-life exposure to adversity also be transmitted across generations? We directly address this question, investigating the associations between maternal exposure to adversity during her own childhood and neural connectivity in her neonate. METHODS: Mothers from a sample of Black mother-neonate dyads (n = 48)-a group that is disproportionately affected by early-life adversity-completed questionnaires assessing their current distress (i.e., a composite measure of anxiety, depression, and perceived stress) during the first and third trimesters of pregnancy and retrospectively reported on their own childhood experiences of abuse and neglect. At 1 month postpartum, neonatal offspring of these women underwent a resting-state functional magnetic resonance imaging scan during natural sleep. RESULTS: Greater maternal exposure to emotional neglect during her own childhood correlated with stronger functional connectivity of two different frontoamygdala circuits in these neonates, as early as 1 month after birth. This effect was specific to early experiences of emotional neglect and was not explained by maternal exposure to other forms of childhood maltreatment or by maternal distress during pregnancy. CONCLUSIONS: These results provide novel evidence that the absence of emotional support early in a mother's life, years before conception, are associated with neural changes-namely, in functional connectivity between the amygdala and medial prefrontal regions-in her offspring shortly after birth.

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.

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.

Late Development of Navigationally Relevant Motion Processing in the Occipital Place Area.

Human adults flawlessly and effortlessly navigate boundaries and obstacles in the immediately visible environment, a process we refer to as "visually guided navigation." Neuroimaging work in adults suggests this ability involves the occipital place area (OPA) [1, 2]-a scene-selective region in the dorsal stream that selectively represents information necessary for visually guided navigation [3-9]. Despite progress in understanding the neural basis of visually guided navigation, however, little is known about how this system develops. Is navigationally relevant information processing present in the first few years of life? Or does this information processing only develop after many years of experience? Although a handful of studies have found selective responses to scenes (relative to objects) in OPA in childhood [10-13], no study has explored how more specific navigationally relevant information processing emerges in this region. Here, we do just that by measuring OPA responses to first-person perspective motion information-a proxy for the visual experience of actually navigating the immediate environment-using fMRI in 5- and 8-year-old children. We found that, although OPA already responded more to scenes than objects by age 5, responses to first-person perspective motion were not yet detectable at this same age and rather only emerged by age 8. This protracted development was specific to first-person perspective motion through scenes, not motion on faces or objects, and was not found in other scene-selective regions (the parahippocampal place area or retrosplenial complex) or a motion-selective region (MT). These findings therefore suggest that navigationally relevant information processing in OPA undergoes prolonged development across childhood.

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.

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.