A connectivity-constrained computational account of topographic organization in primate high-level visual cortex

Inferotemporal (IT) cortex in humans and other primates is topographically organized, containing multiple hierarchically organized areas selective for particular domains, such as faces and scenes. This organization is commonly viewed in terms of evolved domain-specific visual mechanisms. Here, we develop an alternative, domain-general and developmental account of IT cortical organization. The account is instantiated in interactive topographic networks (ITNs), a class of computational models in which a hierarchy of model IT areas, subject to biologically plausible connectivity-based constraints, learns high-level visual representations optimized for multiple domains. We find that minimizing a wiring cost on spatially organized feedforward and lateral connections, alongside realistic constraints on the sign of neuronal connectivity within model IT, results in a hierarchical, topographic organization. This organization replicates a number of key properties of primate IT cortex, including the presence of domain-selective spatial clusters preferentially involved in the representation of faces, objects, and scenes; columnar responses across separate excitatory and inhibitory units; and generic spatial organization whereby the response correlation of pairs of units falls off with their distance. We thus argue that topographic domain selectivity is an emergent property of a visual system optimized to maximize behavioral performance under generic connectivity-based constraints.

Graded Variation In Cortical T1w/T2w Myelination During Adolescence

Myelination influences brain connectivity during sensitive periods of development by enhancing neural signaling speed and regulating synapse formation to reduce plasticity. However, in vivo studies characterizing the maturational timing of cortical myelination during human development remain scant. Here, we take advantage of recent advances in high-resolution cortical T1w/T2w myelin mapping methods, including principled correction of B1+ transmit field effects, using data from the Human Connectome Project in Development (N=628, ages 8-21) to characterize the maturational timing of myelination from childhood through early adulthood throughout the cerebral neocortex. We apply Bayesian spline models and functional latent clustering analysis to demonstrate graded variation in the rate of cortical T1w/T2w myelin growth in neocortical areas that is strongly correlated with the sensorimotor-association (S-A) axis of cortical organization reported by others. In sensorimotor areas T1w/T2w myelin starts at high levels at early ages, increases at a fast pace, and decelerates at later ages (18-21). In intermediate multimodal areas along the S-A axis, T1w/T2w myelin tends to start at intermediate levels and increase linearly at an intermediate pace. In transmodal/paralimbic association areas high along the S-A axis, T1w/T2w myelin tends to start at low levels and increase linearly at the slowest pace. These data provide evidence for graded variation along the S-A axis in the rate of cortical myelination during adolescence, which could reflect ongoing plasticity underlying the development of complex information processing and psychological functioning.Significance StatementMyelin is a lipid membrane that is essential to healthy brain function. Myelin wraps axons to increase neural signaling speed, enabling complex neuronal functioning underlying learning and cognition. Here we characterize the developmental timing of myelination across the cerebral cortex during adolescence using recent advances in non-invasive myelin mapping. Our results provide new evidence demonstrating graded variation across the cortex in the timing of myelination during adolescence, with rapid myelination in lower-order sensory areas and gradual myelination in higher-order association areas. This spatial pattern of microstructural brain development closely parallels the sensorimotor-to-association axis of cortical organization and plasticity during ontogeny.

Dissociable Multi-scale Patterns of Development in Personalized Brain Networks

The brain is organized into networks at multiple resolutions, or scales, yet studies of functional network development typically focus on a single scale. Here, we derived personalized functional networks across 29 scales in a large sample of youths (n=693, ages 8-23 years) to identify multi-scale patterns of network re-organization related to neurocognitive development. We found that developmental shifts in inter-network coupling systematically adhered to and strengthened a functional hierarchy of cortical organization. Furthermore, we observed that scale-dependent effects were present in lower-order, unimodal networks, but not higher-order, transmodal networks. Finally, we found that network maturation had clear behavioral relevance: the development of coupling in unimodal and transmodal networks dissociably mediated the emergence of executive function. These results delineate maturation of multi-scale brain networks, which varies according to a functional hierarchy and impacts cognitive development.

Shifting gradients of macroscale cortical organization mark the transition from childhood to adolescence

The transition from childhood to adolescence is marked by pronounced shifts in brain structure and function that coincide with the development of physical, cognitive, and social abilities. Prior work in adult populations has characterized the topographical organization of the cortex, revealing macroscale functional gradients that extend from unimodal (somatosensory/motor and visual) regions through the cortical association areas that underpin complex cognition in humans. However, the presence of these core functional gradients across development as well as their maturational course have yet to be established. Here, leveraging 378 resting-state functional MRI scans from 190 healthy individuals aged 6 to 17 y old, we demonstrate that the transition from childhood to adolescence is reflected in the gradual maturation of gradient patterns across the cortical sheet. In children, the overarching organizational gradient is anchored within the unimodal cortex, between somatosensory/motor and visual territories. Conversely, in adolescence, the principal gradient of connectivity transitions into an adult-like spatial framework, with the default network at the opposite end of a spectrum from primary sensory and motor regions. The observed gradient transitions are gradually refined with age, reaching a sharp inflection point in 13 and 14 y olds. Functional maturation was nonuniformly distributed across cortical networks. Unimodal networks reached their mature positions early in development, while association regions, in particular the medial prefrontal cortex, reached a later peak during adolescence. These data reveal age-dependent changes in the macroscale organization of the cortex and suggest the scheduled maturation of functional gradient patterns may be critically important for understanding how cognitive and behavioral capabilities are refined across development.

Schizophrenia polygenic risk during typical development reflects multiscale cortical organization

Schizophrenia is widely recognized as a neurodevelopmental disorder, but determining neurodevelopmental features of schizophrenia requires a departure from classic case-control designs. Polygenic risk scoring for schizophrenia (PRS-SCZ) enables investigation of the influence of genetic risk for schizophrenia on cortical anatomy during neurodevelopment and prior to disease onset. PRS-SCZ and cortical morphometry were assessed in typically developing children (3-21 years) using T1-weighted MRI and whole genome genotyping (n=390) from the Pediatric Imaging, Neurocognition and Genetics (PING) cohort. Then, we sought to contextualise the findings using (i) age-matched transcriptomics, (ii) gradients of cortical differentiation and (iii) case-control differences of major psychiatric disorders. Higher PRS-SCZ was associated with greater cortical thickness in typically developing children, while surface area and cortical volume showed only subtle associations. Greater cortical thickness was most prominent in areas with heightened gene expression for dendrites and synapses. The pattern of PRS-SCZ associations with cortical thickness reflected functional specialisation in the cortex and was spatially related to cortical abnormalities of patient populations of schizophrenia, bipolar disorder, and major depression. Finally, age interaction models indicated PRS-SCZ effects on cortical thickness were most pronounced between ages 3 and 6, suggesting an influence of PRS-SCZ on cortical maturation early in life. Integrating imaging-genetics with multi-scale mapping of cortical organization, our work contributes to an emerging understanding of how risk for schizophrenia and related disorders manifest in early life.

The primitive brain of early Homo

The brains of modern humans differ from those of great apes in size, shape, and cortical organization, notably in frontal lobe areas involved in complex cognitive tasks, such as social cognition, tool use, and language. When these differences arose during human evolution is a question of ongoing debate. Here, we show that the brains of early Homo from Africa and Western Asia (Dmanisi) retained a primitive, great ape–like organization of the frontal lobe. By contrast, African Homo younger than 1.5 million years ago, as well as all Southeast Asian Homo erectus, exhibited a more derived, humanlike brain organization. Frontal lobe reorganization, once considered a hallmark of earliest Homo in Africa, thus evolved comparatively late, and long after Homo first dispersed from Africa.