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Grill-Spector, K.

Publications and source records attributed to Grill-Spector, K..

At least 19 recordsLinked to original sources

Multiphasic myelination and dendritic growth modulate qMRI signals in human visual cortex.

How does myelin develop in human visual cortex? By combining immunohistochemistry with in vivo and postmortem magnetic resonance imaging of longitudinal relaxation rate (R1), which increases with myelin content, we find that myelin and R1 increase across development but follow distinct trajectories. Immunohistochemistry reveals two phases of myelination: an infant phase of limited oligodendrogenesis, with myelin restricted to deep cortical layers, followed by widespread myelination across all layers during childhood. Cortical R1 also increases across development and correlates with myelin by childhood. However, in infancy, R1 increases outpace myelin growth and instead tracks dendritic arborization, indicating that the microstructural drivers of R1 change across development. We hypothesize that deep layer myelination in infancy contributes to early visual function whereas later myelination of superficial layers enables prolonged cortical plasticity and learning of complex visual behaviors.

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From adolescence to adulthood: functional fingerprints of high-level visual cortex reveal differential development of visuospatial processing

Reading, social interaction, and navigation rely on visuospatial computations by population receptive fields (pRFs) in category-selective regions of the ventral, lateral, and dorsal streams. However, how visuospatial computations vary across streams and category, or develop during adolescence is unknown. Using functional magnetic resonance imaging (fMRI) and pRF modeling in adolescents and adults, we investigate the development of pRFs and category-selectivity. Adolescents and adults show a consistent functional fingerprint whereby, pRF location, pRF size, and visual field coverage vary by category-selectivity, stream, and hemisphere. While pRF location is largely adult-like by adolescence, pRF size, visual field coverage, and category-selectivity exhibit region-specific increases and decreases from adolescence to adulthood. Together, these findings delineate a timeline of continued functional plasticity during adolescence and provide a multidimensional framework for understanding the organization of high-level visual cortex.

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Hierarchical microstructural tissue growth of the gray and white matter of human visual cortex during the first year of life

Development of gray and white matter tissue microstructure is critical for the emergence of sensory and cognitive functions. However, it is unknown how microstructural tissue properties of the human visual system develop in the first year of human life. Here, we use tissue relaxation rate (R1) obtained using quantitative MRI to measure the longitudinal development of gray and white matter in brain areas spanning three visual processing streams: dorsal, lateral, and ventral, during the first year of life. R1 in gray and white matter of all visual regions in the three processing streams increases postnatally, indicating microstructural tissue growth. R1 increases faster between 0-6 months than 6-12 months, and faster in white matter than gray matter, with white matter R1 surpassing that of gray matter after two months of age. Strikingly, this microstructural growth is hierarchical: across all streams, early visual areas are more mature at birth than higher-level areas but develop more slowly postnatally than higher-level areas. The exception is TO1 (MT) which is similar to V1: it is microstructurally more mature at birth and develops slower than neighboring areas. Overall, our findings provide the first comprehensive measurement of microstructural tissue growth in infancy across three visual processing streams and propose a new hypothesis that functional development of the visual cortex may be coupled with microstructural development and follows a similar hierarchical trajectory.

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Visuospatial computations vary by category and stream and continue to develop in adolescence

Reading, face recognition, and navigation are supported by visuospatial computations in category-selective regions across ventral, lateral, and dorsal visual streams. However, the nature of visuospatial computations across streams and their development in adolescence remain unknown. Using fMRI and population receptive field (pRF) modeling in adolescents and adults, we estimate pRFs in high-level visual cortex and determine their development. Results reveal that pRF location, size, and visual field coverage vary across category, stream, and hemisphere in both adolescents and adults. While pRF location is mature by adolescence, pRF size and visual field coverage continue to develop - increasing in face-selective and decreasing in place-selective regions - alongside similar development of category selectivity. These findings provide a timeline for differential development of visual functions and suggest that visuospatial computations in high-level visual cortex continue to be optimized to accommodate both category and stream demands through adolescence.

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White matter connections of human ventral temporal cortex are organized by cytoarchitecture, eccentricity, and category-selectivity from birth

Category-selective regions in ventral temporal cortex (VTC) have a consistent anatomical organization, which is hypothesized to be scaffolded by white matter connections. However, it is unknown how white matter connections are organized from birth. Here, we scanned newborn to 6-month-old infants and adults to determine the organization of the white matter connections of VTC. We find that white matter connections are organized by cytoarchitecture, eccentricity, and category from birth. Connectivity profiles of functional regions in the same cytoarchitectonic area are similar from birth and develop in parallel, with decreases in endpoint connectivity to lateral occipital, and parietal, and somatosensory cortex, and increases to lateral prefrontal cortex. Additionally, connections between VTC and early visual cortex are organized topographically by eccentricity bands and predict eccentricity biases in VTC. These data show that there are both innate organizing principles of white matter connections of VTC, and the capacity for white matter connections to change over development.

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A single computational objective drives specialization of streams in visual cortex

Human visual cortex is organized into dorsal, lateral, and ventral streams. A long-standing hypothesis is that the functional organization into streams emerged to support distinct visual behaviors. Here, we compare neural network-based computational models against a massive fMRI dataset to investigate why visual streams emerge. We find that a self-supervised Topographic Deep Artificial Neural Network (TDANN), which encourages nearby units to respond similarly, better captures brain responses, as well as spatial segregation and functional differentiation across streams, than DANN models trained for stream-specific visual behaviors. These findings challenge the prevailing view that streams evolved to separately support different behaviors and suggest instead the possibility that functional organization can arise from a single principle: learning generally useful visual representations subject to local spatial constraints.

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Both mOTS-words and pOTS-words prefer emoji stimuli over text stimuli during a reading task

The visual word form area in the occipitotemporal sulcus (OTS), here referred to as OTS-words, responds more strongly to text than other visual stimuli and is crucial for reading. We hypothesized, that this text preference may be driven by a preference for reading tasks, as in most prior fMRI studies only the text stimuli were readable. Hence, we performed three fMRI experiments (N=15) and systematically varied the participant s task and the stimulus, investigating mOTS-words and pOTS-words subregions. In experiment 1, we contrasted text stimuli with non-readable visual stimuli (faces, limbs, houses, objects). Experiment 2 utilized an fMRI adaptation paradigm, presenting compound words in text or emoji formats. In experiment 3, participants performed a reading or a color task on compound words in text or emoji format. Using experiment 1 data, we identified mOTS-words and pOTS-words by contrasting texts with non-readable stimuli. In experiment 2, pOTS-words, but not mOTS-words, showed fMRI adaptation for compound words in both text and emoji formats. In experiment 3, surprisingly, both subregions showed higher responses to compound words in emoji than text format. Moreover, mOTS-words showed higher responses during the reading than the color task and a task-stimulus interaction. Multivariate analyses revealed that distributed responses in pOTS-words encode the visual stimulus, while responses in mOTS-words encode both stimulus and task. Together, our findings suggest that the function of the OTS-words subregions goes beyond the specific visual processing of text and that these regions are flexibly recruited whenever semantic meaning needs to be assigned to visual input. Significance StatementReading skills are essential in modern society and supported by a brain region in the occipitotemporal sulcus (OTS-words) that is critical for fluent reading. Here we evaluated if responses in OTS-words are driven by the activity of reading or simply by seeing text or other readable symbols (emojis). We found that OTS-words can be divided into two sub-regions which both prefer readable emojis over text, whereas the anterior sub-region also prefers reading over other tasks. These results suggest that OTS-words is flexibly recruited to encode any readable visual stimulus, not just text. By demonstrating OTS-words flexibility, this work reconciles previous contradictory findings on this regions functional properties and inspires future research on OTS-words, including its emergence during literacy acquisition.

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A Unifying Principle for the Functional Organization of Visual Cortex

A key feature of many cortical systems is functional organization: the arrangement of neurons with specific functional properties in characteristic spatial patterns across the cortical surface. However, the principles underlying the emergence and utility of functional organization are poorly understood. Here we develop the Topographic Deep Artificial Neural Network (TDANN), the first unified model to accurately predict the functional organization of multiple cortical areas in the primate visual system. We analyze the key factors responsible for the TDANNs success and find that it strikes a balance between two specific objectives: achieving a task-general sensory representation that is self-supervised, and maximizing the smoothness of responses across the cortical sheet according to a metric that scales relative to cortical surface area. In turn, the representations learned by the TDANN are lower dimensional and more brain-like than those in models that lack a spatial smoothness constraint. Finally, we provide evidence that the TDANNs functional organization balances performance with inter-area connection length, and use the resulting models for a proof-of-principle optimization of cortical prosthetic design. Our results thus offer a unified principle for understanding functional organization and a novel view of the functional role of the visual system in particular.

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When Do Visual Category Representations Emerge in Infants' Brains?

Organizing the continuous stream of visual input into categories like places or faces is important for everyday function and social interactions. However, it is unknown when neural representations of these and other visual categories emerge. Here we used steady state evoked potential electroencephalography to measure cortical responses in infants at 3-4 months, 4-6 months, 6-8 months, and 12-15 months, when they viewed controlled, gray-level images of faces, limbs, corridors, characters, and cars. We found that distinct responses to these categories emerge at different ages. Reliable brain responses to faces emerge first, at 4-6 months, followed by limbs and places around 6-8 months. Between 6-15 months response patterns become more distinct, such that a classifier can decode what an infant is looking at from their brain responses. These findings have important implications for assessing typical and atypical cortical development as they not only suggest that category representations are learned, but also that representations of categories that may have innate substrates emerge at different times during infancy.

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Characterizing spatiotemporal population receptive fields in human visual cortex with fMRI

The use of fMRI and computational modeling has advanced understanding of spatial characteristics of population receptive fields (pRFs) in human visual cortex. However, we know relatively little about the spatiotemporal characteristics of pRFs because neurons temporal properties are one to two orders of magnitude faster than fMRI BOLD responses. Here, we developed an image-computable framework to estimate spatiotemporal pRFs from fMRI data. First, we developed a simulation software that predicts fMRI responses to a time varying visual input given a spatiotemporal pRF model and solves the model parameters. The simulator revealed that ground-truth spatiotemporal parameters can be accurately recovered at the millisecond resolution from synthesized fMRI responses. Then, using fMRI and a novel stimulus paradigm, we mapped spatiotemporal pRFs in individual voxels across human visual cortex in 10 participants. We find that a compressive spatiotemporal (CST) pRF model better explains fMRI responses than a conventional spatial pRF model across visual areas spanning the dorsal, lateral, and ventral streams. Further, we find three organizational principles of spatiotemporal pRFs: (i) from early to later areas within a visual stream, spatial and temporal integration windows of pRFs progressively increase in size and show greater compressive nonlinearities, (ii) later visual areas show diverging spatial and temporal integration windows across streams, and (iii) within early visual areas (V1-V3), both spatial and temporal integration windows systematically increase with eccentricity. Together, this computational framework and empirical results open exciting new possibilities for modeling and measuring fine-grained spatiotemporal dynamics of neural responses in the human brain using fMRI. Significance StatementWe developed a computational framework for estimating spatiotemporal receptive fields of neural populations using fMRI. This framework pushes the boundary of fMRI measurements, enabling quantitative evaluation of neural spatial and temporal processing windows at the resolution of visual degrees and milliseconds, which was thought to be unattainable with fMRI. We not only replicate well-established visual field and pRF size maps, but also estimates of temporal summation windows from electrophysiology. Notably, we find that spatial and temporal windows as well as compressive nonlinearities progressively increase from early to later visual areas in multiple visual processing streams. Together, this framework opens exciting new possibilities for modeling and measuring fine-grained spatiotemporal dynamics of neural responses in the human brain using fMRI.

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Human white matter myelination rate slows down at birth

The formation of myelin, the fatty sheath that insulates nerve fibers, is critical for healthy brain function. A fundamental open question is what is the impact of being born on myelin growth. To address this question, we evaluated a large (n=300) cross-sectional sample of newborns from the Developing Human Connectome Project (dHCP). First, we developed new software for the automated identification of 20 white matter bundles in individuals that is well-suited for large samples. Next, we fit linear models that quantify T1w/T2w, a myelin-sensitive imaging contrast, increases along bundles. We found faster growth of T1w/T2w along the lengths of all bundles before birth than right after birth. Further, in a separate longitudinal sample of preterm infants (N=34), we found lower T1w/T2w at term-equivalent age than in full-term peers. By applying the linear models fit on the cross-section sample to the longitudinal sample of preterm infants, we find that their delay in T1w/T2w growth is well explained by the amount of time preterm infants spend developing in utero and ex utero. These results suggest that being born slows the rate of myelin growths. This reduction in the rate of myelin growth at birth, in turn, explains lower myelin content in individuals born preterm, and could account for long-term cognitive, neurological, and developmental consequences of preterm birth. We hypothesize that closely matching the environment of infants born preterm to what they would have experienced in the womb may reduce delays in myelin growth and hence improve developmental outcomes.

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Longitudinal development of category representations in ventral temporal cortex predicts word and face recognition

Regions in ventral temporal cortex (VTC) that are involved in visual recognition of categories like words and faces, undergo differential development during childhood. However, categories are also represented in distributed responses across VTC. How do distributed category representations develop and relate to behavioral changes in recognition? Here, we used fMRI to longitudinally measure the development of distributed responses across VTC to 10 categories in school-age children over several years. Our results reveal both strengthening and weakening of category representations with age, which was mainly driven by changes across category-selective voxels. Representations became particularly more distinct for words in the left hemisphere and for faces bilaterally. Critically, distinctiveness for words and faces across category-selective voxels in left and right lateral VTC, respectively, predicted individual childrens word and face recognition performance. These results suggest that the development of distributed VTC representations has behavioral ramifications and advance our understanding of prolonged cortical development during childhood.

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Comparing visual cortex of children and adults reveals a late-stage change in the architecture of V1

Adult visual performance differs with angular location -it is better for stimuli along the horizontal than vertical, and lower than upper vertical meridian of the visual field. These perceptual asymmetries are paralleled by asymmetries in cortical surface area in primary visual cortex (V1). Children, unlike adults, have similar visual performance at the lower and upper vertical meridian. Do children have similar V1 surface area representing the upper and lower vertical meridian? Using MRI, we measure the surface area of retinotopic maps (V1-V3) in children and adults. Many features of the maps are similar between groups, including greater V1 surface area for the horizontal than vertical meridian. However, unlike adults, children have a similar amount of V1 surface area representing the lower and upper vertical meridian. These data reveal a late-stage change in V1 organization that may relate to the emergence of the visual performance asymmetry along the vertical meridian by adulthood.

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White matter connections of high-level visual areas predict cytoarchitecture better than category-selectivity

Ventral temporal cortex (VTC) consists of high-level visual regions that are arranged in consistent anatomical locations across individuals. This consistency has led to several hypotheses about the factors that constrain the functional organization of VTC. A prevailing theory is that white matter connections influence the organization of VTC, however, the nature of this constraint is unclear. Here, we test two hypotheses: (1) white matter tracts are specific for each category or (2) white matter tracts are specific to cytoarchitectonic areas of VTC. To test these hypotheses, we used diffusion magnetic resonance imaging (dMRI) to identify white matter tracts and functional magnetic resonance imaging (fMRI) to identify category-selective regions in VTC in children and adults. We find that in childhood, white matter connections are linked to cytoarchitecture rather than category-selectivity. In adulthood, however, white matter connections are linked to both cytoarchitecture and category-selectivity. These results suggest a rethinking of the view that category-selective regions in VTC have category-specific white matter connections early in development. Instead, these findings suggest that the neural hardware underlying the processing of categorical stimuli may be more domain-general than previously thought, particularly in childhood.

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Attention enhances category representations across the brain with strengthened residual correlations to ventral temporal cortex

How does attention enhance neural representations of goal-relevant stimuli while suppressing representations of ignored stimuli across regions of the brain? While prior studies have shown that attention enhances visual responses, we lack a cohesive understanding of how selective attention modulates visual representations across the brain. Here, we used functional magnetic resonance imaging (fMRI) while participants performed a selective attention task on superimposed stimuli from multiple categories and used a data-driven approach to test how attention affects both decodability of category information and residual correlations (after regressing out stimulus-driven variance) with category-selective regions of ventral temporal cortex (VTC). Our data reveal three main findings. First, when two objects are simultaneously viewed, the category of the attended object can be decoded more readily than the category of the ignored object, with the greatest attentional enhancements observed in occipital and temporal lobes. Second, after accounting for the response to the stimulus, the correlation in the residual brain activity between a cortical region and a category-selective region of VTC was elevated when that regions preferred category was attended vs. ignored, and more so in the right occipital, parietal, and frontal cortices. Third, we found that the stronger the residual correlations between a given region of cortex and VTC, the better visual category information could be decoded from that region. These findings suggest that heightened residual correlations by selective attention may reflect the sharing of information between sensory regions and higher-order cortical regions to provide attentional enhancement of goal-relevant information.

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Myelin contributes to microstructural growth in human sensory cortex during early infancy.

Development of cortical tissue during infancy is critical for the emergence of typical brain functions in cortex. However, how cortical microstructure develops during infancy remains unknown. We measured the longitudinal development of cortex from newborns to six-months-old infants using multimodal quantitative imaging of cortical microstructure. Here we show that infants cortex undergoes profound microstructural tissue growth during the first six months of human life. Comparison of postnatal to prenatal transcriptomic gene expression data demonstrates that myelination and synaptic processes are dominant contributors to this postnatal microstructural tissue growth. Using visual cortex as a model system, we find hierarchical microstructural growth: higher-level visual areas have less mature tissue at birth than earlier visual areas but grow at faster rates. This overturns the prevailing view that visual areas that are most mature at birth develop fastest. Together, in vivo, longitudinal, and quantitative measurements, which we validated with ex vivo transcriptomic data, shed new light on the rate, sequence, and specific biological mechanisms of developing cortical systems. Importantly, our findings propose a new hypothesis that cortical myelination is a key factor in cortical development during early infancy, which has significant implications for diagnosis of neurodevelopmental disorders and delays in infants.

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Holistic face recognition is an emergent phenomenon of spatial integration in face-selective regions

Spatial processing by receptive fields is a core property of the visual system. However, it is unknown how spatial coding in high-level regions contributes to recognition behavior. As face inversion is thought to disrupt typical holistic processing of information in faces, we mapped population receptive fields (pRFs) with upright and inverted faces in the human visual system. In face-selective regions, but not primary visual cortex, pRFs and overall visual field coverage were smaller and shifted downward in response to face inversion. From these measurements, we successfully predicted the relative behavioral detriment of face inversion at different positions in the visual field. This correspondence between neural measurements and behavior demonstrates how spatial integration in face-selective regions enables holistic processing. These results not only show that spatial processing in high-level visual regions is dynamically used towards recognition, but also suggest a powerful approach for bridging neural computations by receptive fields to behavior.

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Cortical recycling in high-level visual cortex during childhood development

Human ventral temporal cortex (VTC) contains category-selective regions that respond preferentially to ecologically-relevant categories such as faces, bodies, places, and words, which are causally involved in the perception of these categories. How do these regions develop during childhood? We used functional MRI to measure longitudinal development of category-selectivity in school-age children over 1 to 5 years. We discovered that from young childhood to the teens, face- and word-selective regions in VTC expand and become more category-selective, but limb-selective regions shrink and lose their preference for limbs. Critically, as a child develops, increases in face- and word-selectivity are directly linked to decreases in limb-selectivity, revealing that during childhood limb-selectivity in VTC is repurposed into word- and face-selectivity. These data provide evidence for cortical recycling during childhood development. This has important implications for understanding typical as well as atypical brain development and necessitates a rethinking of how cortical function develops during childhood.

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