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Ayzenberg, V.

Publications and source records attributed to Ayzenberg, V..

9 recordsLinked to original sources

Functional organization of the human visual system at birth and across late gestation

Understanding how the brains functional architecture emerges prior to substantial postnatal visual experience is crucial for determining what initial capabilities infants possess and how they learn from their environment. Using resting-state fMRI from 584 neonates in the Developing Human Connectome Project, we provide the first comprehensive systems-level characterization of human visual cortex within hours of birth and across the third trimester of gestation. We discover that newborns possess a sophisticated visual architecture already functionally organized into three distinct pathways (ventral, lateral, and dorsal), each exhibiting posterior-to-anterior hierarchical structure and adult-like topographic organization. This tripartite visual organization differs from the bipartite organization observed in macaques, suggesting this architecture emerges through intrinsic developmental mechanisms rather than being a product of extensive postnatal experience and environmental adaptation. Moreover, pathway segregation, hierarchical ordering, and connectivity maturity all strengthen progressively with gestational age, revealing that visual cortical organization emerges through an active developmental program that unfolds across late gestation. Yet, despite this large-scale structure, individual pathways follow strikingly different maturation trajectories: dorsal areas exhibit a near-adult-like functional organization, even at the earliest gestational timepoints tested, whereas ventral areas remain immature and poised for experience-dependent refinement. These findings reframe our understanding of early visual development by revealing that complex functional networks emerge before substantial visual experience, yet are differentially prepared for plasticity, providing crucial insights into how evolution has optimized the brain for rapid learning while maintaining the flexibility needed for adaptation to diverse environments.

neuroscience↗

Fast and robust visual object recognition in young children

By adulthood, humans rapidly identify objects from sparse visual displays and across significant disruptions to their appearance. What are the minimal conditions needed to achieve robust recognition abilities and when might these abilities develop? To test this question, we investigated the upper-limits of childrens object recognition abilities. We found that children as young as 3-years-of-age successfully identified objects at speeds of 100 ms (both forward and backward masked) under sparse and disrupted viewing conditions. By contrast, a range computational models implemented with biologically plausible properties or optimized for visual recognition did not reach child-level performance. Models only matched children if they were trained with more data than children are capable of experiencing. These findings highlight the robustness of the human visual system in the absence of extensive experience and identify important developmental constraints for building biologically plausible machines.

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An intrinsic hierarchical, retinotopic organization of pulvinar connectivity in the human neonate

Thalamic connectivity is crucial for the development of the neocortex. The pulvinar nuclei are thought to be particularly important for visual development due to their involvement in various functions that emerge early in infancy. The development of these connections constrains the role the pulvinar plays in infant visual processing and the maturation of associated cortical networks. However, the extent to which pulvino-cortical pathways found in adults are established at birth remains largely unknown, limiting our understanding of how these thalamic connections may support infant vision. To address this gap, we examined the organization of pulvino-cortical connections in human neonates using probabilistic tractography analyses on diffusion imaging data. Our findings revealed the presence of white matter pathways between the pulvinar and each individual visual area at birth. These pathways exhibited specificity in their connectivity within the pulvinar, reflecting both intraareal retinotopic organization and the hierarchical organization across ventral, lateral, and dorsal visual cortical pathways. These connections could enable detailed processing of information across sensory space and communication along distinct processing pathways. Comparative analyses revealed that the large-scale organization of pulvino-cortical connectivity in neonates mirrored that of adults. However, connectivity with ventral visual cortex was less adult-like than the other cortical pathways, aligning with prior findings of protracted development associated with the visual recognition pathway. These results deepen our understanding of the developmental trajectory of thalamocortical connections and provide a framework for how subcortical structures may support early perceptual abilities and scaffold the development of cortex.

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Visual looming is a primitive for human emotion

Looming objects afford threat of collision across the animal kingdom. Defensive responses to looming and neural computations for looming detection are strikingly conserved across species. In mammals, information about rapidly approaching threats is conveyed from the retina to the midbrain superior colliculus, where variables that indicate the position and velocity of approach are computed to enable defensive behavior. Although neuroscientific theories posit that midbrain representations contribute to emotion through connectivity with distributed brain systems, it remains unknown whether a computational system for looming detection can predict both defensive behavior and phenomenal experience in humans. Here, we show that a shallow convolutional neural network based on the Drosophila visual system predicts defensive blinking to looming objects in infants and superior colliculus responses to optical expansion in adults. Further, the responses of the convolutional network to a broad array of naturalistic video clips predict self-reported emotion largely on the basis of subjective arousal. Our findings illustrate how motor and experiential components of human emotion relate to species-general systems for survival in unpredictable environments.

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Differential functional reorganization of ventral and dorsal visual pathways following childhood hemispherectomy

Hemispherectomy is a surgical procedure in which an entire hemisphere of a patients brain is resected or functionally disconnected to manage seizures in individuals with drug-resistant epilepsy. Despite the extensive loss of input from both ventral and dorsal visual pathways of one hemisphere, pediatric patients who have undergone hemispherectomy show a remarkably high degree of perceptual function across many domains. In the current study, we sought to understand the extent to which functions of the ventral and dorsal visual pathways reorganize to the contralateral hemisphere following childhood hemispherectomy. To this end, we collected fMRI data from an equal number of left and right hemispherectomy patients who completed tasks that typically elicit lateralized responses from the ventral or the dorsal pathway, namely, word (left ventral), face (right ventral), tool (left dorsal), and global form (right dorsal) perception. Overall, there was greater evidence of functional reorganization in the ventral pathway than in the dorsal pathway. Importantly, because ventral and dorsal reorganization was tested in the very same patients, these results cannot be explained by idiosyncratic factors such as disease etiology, age at the time of surgery, or age at testing. These findings suggest that because the dorsal pathway may mature earlier, it may have a shorter developmental window of plasticity than the ventral pathway and, hence, be less malleable.

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Temporal asymmetries and interactions between dorsal and ventral visual pathways during object recognition

Despite their anatomical and functional distinctions, there is growing evidence that the dorsal and ventral visual pathways interact to support object recognition. However, the exact nature of these interactions remains poorly understood. Is the presence of identity-relevant object information in the dorsal pathway simply a byproduct of ventral input? Or, might the dorsal pathway be a source of input to the ventral pathway for object recognition? In the current study, we used high-density EEG - a technique with high temporal precision and spatial resolution sufficient to distinguish parietal and temporal lobes - to characterize the dynamics of dorsal and ventral pathways during object viewing. Using multivariate analyses, we found that category decoding in the dorsal pathway preceded that in the ventral pathway. Importantly, the dorsal pathway predicted the multivariate responses of the ventral pathway in a time-dependent manner, rather than the other way around. Together, these findings suggest that the dorsal pathway is a critical source of input to the ventral pathway for object recognition.

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The dorsal visual pathway represents object-centered spatial relations for object recognition

Although there is mounting evidence that input from the dorsal visual pathway is crucial for object processes in the ventral pathway, the specific functional contributions of dorsal cortex to these processes remain poorly understood. Here, we hypothesized that dorsal cortex computes the spatial relations among an objects parts - a processes crucial for forming global shape percepts - and transmits this information to the ventral pathway to support object categorization. Using fMRI with human participants (females and males), we discovered regions in the intraparietal sulcus (IPS) that were selectively involved in computing object-centered part relations. These regions exhibited task-dependent functional and effective connectivity with ventral cortex, and were distinct from other dorsal regions, such as those representing allocentric relations, 3D shape, and tools. In a subsequent experiment, we found that the multivariate response of posterior IPS, defined on the basis of part-relations, could be used to decode object category at levels comparable to ventral object regions. Moreover, mediation and multivariate effective connectivity analyses further suggested that IPS may account for representations of part relations in the ventral pathway. Together, our results highlight specific contributions of the dorsal visual pathway to object recognition. We suggest that dorsal cortex is a crucial source of input to the ventral pathway and may support the ability to categorize objects on the basis of global shape. Significance StatementHumans categorize novel objects rapidly and effortlessly. Such categorization is achieved by representing an objects global shape structure, that is, the relations among object parts. Yet, despite their importance, it is unclear how part relations are represented neurally. Here, we hypothesized that object-centered part relations may be computed by the dorsal visual pathway, which is typically implicated in visuospatial processing. Using fMRI, we identified regions selective for the part relations in dorsal cortex. We found that these regions can support object categorization, and even mediate representations of part relations in the ventral pathway, the region typically thought to support object categorization. Together, these findings shed light on the broader network of brain regions that support object categorization.

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A dual role for shape skeletons in human vision: perceptual organization and object recognition

Shape perception is crucial for object recognition. However, it remains unknown exactly how shape information is represented, and, consequently, used by the visual system. Here, we hypothesized that the visual system represents "shape skeletons" to both (1) perceptually organize contours and component parts into a shape percept, and (2) compare shapes to recognize objects. 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, regions known to be involved in perceptual organization and object recognition, respectively. 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 the functional roles of shape skeletons in human vision, as well as the computational properties of V3 and LO.

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Skeletal descriptions of shape provide unique and privileged perceptual information for object recognition

With seemingly little effort, humans can both identify an object across large changes in orientation and extend category membership to novel exemplars. Although researchers argue that object shape is crucial in these cases, there are open questions as to how shape is represented for object recognition. Here we tested whether the human visual system incorporates a three-dimensional skeletal descriptor of shape to determine an objects identity. Skeletal models not only provide a compact description of an objects global shape structure, but also provide a quantitative metric by which to compare the visual similarity between shapes. Our results showed that a model of skeletal similarity explained the greatest amount of variance in participants object dissimilarity judgments when compared with other computational models of visual similarity (Experiment 1). Moreover, parametric changes to an objects skeleton led to proportional changes in perceived similarity, even when controlling for another model of structure (Experiment 2). Importantly, participants preferentially categorized objects by their skeletons across changes to local shape contours and non-accidental properties (Experiment 3). Our findings highlight the importance of skeletal structure in vision, not only as a shape descriptor, but also as a diagnostic cue of object identity.

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