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Baum, G. L.

Publications and source records attributed to Baum, G. L..

9 recordsLinked to original sources

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.

neuroscience↗

Transmit Field Bias Correction of T1w/T2w Myelin Maps

T1-weighted divided by T2-weighted (T1w/T2w) myelin maps were initially developed for neuroanatomical analyses such as identifying cortical areas, but they are increasingly used in statistical comparisons across individuals and groups with other variables of interest. Existing T1w/T2w myelin maps contain radiofrequency transmit field (B1+) biases, which may be correlated with these variables of interest, leading to potentially spurious results. Here we propose two empirical methods for correcting these transmit field biases using either explicit measures of the transmit field or alternatively a pseudo-transmit approach that is highly correlated with the transmit field at 3T. We find that the resulting corrected T1w/T2w myelin maps are both better neuroanatomical measures (e.g., for use in cross-species comparisons), and more appropriate for statistical comparisons of relative T1w/T2w differences across individuals and groups (e.g., sex, age, or body-mass-index) within a consistently acquired study at 3T. We recommend that investigators who use the T1w/T2w approach for mapping cortical myelin use these B1+ transmit field corrected myelin maps going forward.

neuroscience↗

Efficient Coding in the Economics of Human Brain Connectomics

In systems neuroscience, most models posit that brain regions communicate information under constraints of efficiency. Yet, evidence for efficient communication in structural brain networks characterized by hierarchical organization and highly connected hubs remains sparse. The principle of efficient coding proposes that the brain transmits maximal information in a metabolically economical or compressed form to improve future behavior. To determine how structural connectivity supports efficient coding, we develop a theory specifying minimum rates of message transmission between brain regions to achieve an expected fidelity, and we test five predictions from the theory based on random walk communication dynamics. In doing so, we introduce the metric of compression efficiency, which quantifies the trade-off between lossy compression and transmission fidelity in structural networks. In a large sample of youth (n = 1,042; age 8-23 years), we analyze structural networks derived from diffusion weighted imaging and metabolic expenditure operationalized using cerebral blood flow. We show that structural networks strike compression efficiency trade-offs consistent with theoretical predictions. We find that compression efficiency prioritizes fidelity with development, heightens when metabolic resources and myelination guide communication, explains advantages of hierarchical organization, links higher input fidelity to disproportionate areal expansion, and shows that hubs integrate information by lossy compression. Lastly, compression efficiency is predictive of behavior--beyond the conventional network efficiency metric--for cognitive domains including executive function, memory, complex reasoning, and social cognition. Our findings elucidate how macroscale connectivity supports efficient coding, and serve to foreground communication processes that utilize random walk dynamics constrained by network connectivity. Author SummaryMacroscale communication between interconnected brain regions underpins most aspects of brain function and incurs substantial metabolic cost. Understanding efficient and behaviorally meaningful information transmission dependent on structural connectivity has remained challenging. We validate a model of communication dynamics atop the macroscale human structural connectome, finding that structural networks support dynamics that strike a balance between information transmission fidelity and lossy compression. Notably, this balance is predictive of behavior and explanatory of biology. In addition to challenging and reformulating the currently held view that communication occurs by routing dynamics along metabolically efficient direct anatomical pathways, our results suggest that connectome architecture and behavioral demands yield communication dynamics that accord to neurobiological and information theoretical principles of efficient coding and lossy compression.

neuroscience↗

Development of structure-function coupling in human brain networks during youth

The protracted development of structural and functional brain connectivity within distributed association networks coincides with improvements in higher-order cognitive processes such as working memory. However, it remains unclear how white matter architecture develops during youth to directly support coordinated neural activity. Here, we characterize the development of structure-function coupling using diffusion-weighted imaging and n-back fMRI data in a sample of 727 individuals (ages 8-23 years). We found that spatial variability in structure-function coupling aligned with cortical hierarchies of functional specialization and evolutionary expansion. Furthermore, hierarchy-dependent age effects on structure-function coupling localized to transmodal cortex in both cross-sectional data and a subset of participants with longitudinal data (n=294). Moreover, structure-function coupling in rostrolateral prefrontal cortex was associated with executive performance, and partially mediated age-related improvements in executive function. Together, these findings delineate a critical dimension of adolescent brain development, whereby the coupling between structural and functional connectivity remodels to support functional specialization and cognition.

neuroscience↗

Individual Variation in Control Network Topography Supports Executive Function in Youth

The spatial distribution of large-scale functional networks on the anatomic cortex differs between individuals, and is particularly variable in networks responsible for executive function. However, it remains unknown how this functional topography evolves in development and supports cognition. Capitalizing upon advances in machine learning and a large sample of youth (n=693, ages 8-23y) imaged with 27 minutes of high-quality fMRI data, we delineate how functional topography evolves during youth. We found that the functional topography of association networks is refined with age, allowing accurate prediction of an unseen individuals brain maturity. Furthermore, the cortical representation of executive networks predicts individual differences in executive function. Finally, variability of functional topography is associated with fundamental properties of brain organization including evolutionary expansion, cortical myelination, and cerebral blood flow. Our results emphasize the importance of considering both the plasticity and diversity of functional neuroanatomy during development, and suggest advances in personalized therapeutics.

neuroscience↗

Advantages of Multi-shell Diffusion Models for Studies of Brain Development in Youth

Diffusion tensor imaging (DTI) has advanced our understanding of how brain microstructure evolves over development. However, the proliferation of multi-shell diffusion imaging sequences has coincided with notable advances in the modeling of neuronal diffusion patterns, such as Neurite Orientation Dispersion and Density Imaging (NODDI) and Laplacian-regularized Mean Apparent Propagator MRI (MAPL). The relative utility of these newer diffusion models for understanding brain maturation remains sparsely investigated. Additionally, despite evidence that motion artifact is a major confound for studies of development, the relative vulnerability of these models to in-scanner motion has not been described. Accordingly, in a sample of 123 youth (ages 12-30) we evaluated DTI, NODDI, and MAPL for associations with age and in-scanner head motion at multiple scales, including mean white matter values, voxelwise analyses, and tractography-based structural brain networks. Our results reveal that multi-shell diffusion imaging sequences can be leveraged to robustly characterize neurodevelopment, even within the framework of DTI. However, these metrics of diffusion are variably impacted by motion, highlighting the importance of modeling choices for studies of movement-prone populations. Our findings suggest that while traditional DTI is sensitive to neurodevelopmental trends, contemporary modeling techniques confer key advantages for neurodevelopmental inquiries.

neuroscience↗

Optimization of Energy State Transition Trajectory Supports the Development of Executive Function During Youth

Executive function develops rapidly during adolescence, and failures of executive function are associated with both risk-taking behaviors and psychopathology. However, it remains relatively unknown how structural brain networks mature during this critical period to facilitate energetically demanding transitions to activate the frontoparietal system, which is critical for executive function. In a sample of 946 human youths (ages 8-23 yr) who completed diffusion imaging as part of the Philadelphia Neurodevelopment Cohort, we capitalized upon recent advances in network control theory in order to calculate the control energy necessary to activate the frontoparietal system given the existing structural network topology. We found that the control energy required to activate the frontoparietal system declined with development. Moreover, we found that this control energy pattern contains sufficient information to make accurate predictions about individuals brain maturity. Finally, the control energy costs of the cingulate cortex were negatively correlated with executive performance, and partially mediated the development of executive performance with age. These results could not be explained by changes in general network control properties or in network modularity. Taken together, our results reveal a mechanism by which structural networks develop during adolescence to facilitate the instantiation of activation states necessary for executive function.\n\nSIGNIFICANCE STATEMENTExecutive function undergoes protracted development during youth, but it is unknown how structural brain networks mature to facilitate the activation of the frontoparietal cortex that is critical for executive processes. Here, we leverage recent advances in network control theory to establish that structural brain networks evolve in adolescence to lower the energetic cost of activating the frontoparietal system. Our results suggest a new mechanistic framework for understanding how brain network maturation supports cognition, with clear implications for disorders marked by executive dysfunction, such as ADHD and psychosis.

neuroscience↗

Context-dependent architecture of brain state dynamics is explained by white matter connectivity and theories of network control

A diverse white matter network and finely tuned neuronal membrane properties allow the brain to transition seamlessly between cognitive states. However, it remains unclear how static structural connections guide the temporal progression of large-scale brain activity patterns in different cognitive states. Here, we deploy an unsupervised machine learning algorithm to define brain states as time point level activity patterns from functional magnetic resonance imaging data acquired during passive visual fixation (rest) and an n-back working memory task. We find that brain states are composed of interdigitated functional networks and exhibit context-dependent dynamics. Using diffusion-weighted imaging acquired from the same subjects, we show that structural connectivity constrains the temporal progression of brain states. We also combine tools from network control theory with geometrically conservative null models to demonstrate that brains are wired to support states of high activity in default mode areas, while requiring relatively low energy. Finally, we show that brain state dynamics change throughout development and explain working memory performance. Overall, these results elucidate the structural underpinnings of cognitively and developmentally relevant spatiotemporal brain dynamics.

neuroscience↗

The Impact of In-Scanner Head Motion on Structural Connectivity Derived from Diffusion Tensor Imaging

Multiple studies have shown that data quality is a critical confound in the construction of brain networks derived from functional MRI. This problem is particularly relevant for studies of human brain development where important variables (such as participant age) are correlated with data quality. Nevertheless, the impact of head motion on estimates of structural connectivity derived from diffusion tractography methods remains poorly characterized. Here, we evaluated the impact of in-scanner head motion on structural connectivity using a sample of 949 participants (ages 8-23 years old) who passed a rigorous quality assessment protocol for diffusion tensor imaging (DTI) acquired as part of the Philadelphia Neurodevelopmental Cohort. Structural brain networks were constructed for each participant using both deterministic and probabilistic tractography. We hypothesized that subtle variation in head motion would systematically bias estimates of structural connectivity and confound developmental inference, as observed in previous studies of functional connectivity. Even following quality assurance and retrospective correction for head motion, eddy currents, and field distortions, in-scanner head motion significantly impacted the strength of structural connectivity in a consistency-and length-dependent manner. Specifically, increased head motion was associated with reduced estimates of structural connectivity for high-consistency network edges, which included both short-and long-range connections. In contrast, motion inflated estimates of structural connectivity for low-consistency network edges that were primarily shorter-range. Finally, we demonstrate that age-related differences in head motion can both inflate and obscure developmental inferences on structural connectivity. Taken together, these data delineate the systematic impact of head motion on structural connectivity, and provide a critical context for identifying motion-related confounds in studies of structural brain network development.

neuroscience↗