Population-averaged atlas of the macroscale human structural connectome and its network topology
Fang‐Cheng YehSandip S. PanesarDavid FernandesAntonio MeolaMasanori YoshinoJuan Fernandez‐MirandaJean M. VettelTimothy Verstynen
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Diffusion MRI tractography is the most widely used macroscale method for mapping connectomes in vivo . However, tractography is prone to various errors and biases, and thus tractography‐derived connectomes require careful validation. Here, we critically review studies that have developed or utilized phantoms and tracer maps to validate tractography‐derived connectomes, either quantitatively or qualitatively. We identify key factors impacting connectome reconstruction accuracy, including streamline seeding, propagation and filtering methods, and consider the strengths and limitations of state‐of‐the‐art connectome phantoms and associated validation studies. These studies demonstrate the inherent limitations of current fiber orientation models and tractography algorithms and their impact on connectome reconstruction accuracy. Reconstructing connectomes with both high sensitivity and high specificity is challenging, given that some tractography methods can generate an abundance of spurious connections, while others can overlook genuine fiber bundles. We argue that streamline filtering can minimize spurious connections and potentially improve the biological plausibility of connectomes derived from tractography. We find that algorithmic choices such as the tractography seeding methodology, angular threshold, and streamline propagation method can substantially impact connectome reconstruction accuracy. Hence, careful application of tractography is necessary to reconstruct accurate connectomes. Improvements in diffusion MRI acquisition techniques will not necessarily overcome current tractography limitations without accompanying modeling and algorithmic advances.
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Abstract Tractography combined with regions of interest (ROIs) has been used to non-invasively study the structural connectivity of the cortex as well as to assess the reliability of these connections. However, the subcortical connectome (subcortex to subcortex) has not been comprehensively examined, in part due to the difficulty of performing tractography in this complex and compact region. In this study, we performed an in vivo investigation using tractography to assess the feasibility and reliability of mapping known connections between structures of the subcortex using the test-retest dataset from the Human Connectome Project (HCP). We further validated our observations using a separate unrelated subjects dataset from the HCP. Quantitative assessment was performed by computing tract densities and spatial overlap of identified connections between subcortical ROIs. Further, known connections between structures of the basal ganglia and thalamus were identified and visually inspected, comparing tractography reconstructed trajectories with descriptions from tract-tracing studies. Our observations demonstrate both the feasibility and reliability of using a data-driven tractography-based approach to map the subcortical connectome in vivo .
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The human cerebral cortex consists of approximately 1010 neurons that are organized into a complex network of local circuits and long-range connections. During the past years there has been an increasing interest from the neuro-scientific community towards the study of this network, referred to as the human connectome. Due to its ability to probe the tissue microstructure in vivo and non invasively, diffusion MRI has revealed to be a helpful tool for the analysis of brain axonal pathways at the millimeter scale. Whereas the neuronal level remains unreachable, diffusion MRI enables the mapping of a low-resolution estimate of the human connectome, which should give a new breath to the study of normal or pathologic neuroanatomy. After a short introduction on diffusion MRI and tractography, the process by which fiber tracts are reconstructed from the diffusion images, we present a methodology allowing the creation of normalized whole-brain structural connection matrices derived from tractography and representing the human connectome. Based on the developed framework we then investigate the potential of front propagation algorithms in tractography. We compare their performance with classical tractography approaches on several well-known associative fiber pathways, and we discuss their advantages and limitations. Several solutions are proposed in order to evaluate and validate the connectome-related methodology. We develop a method to estimate the respective contributions of diffusion contrast versus other effects to a tractography result. Using this methodology, we show that whereas we can have a strong confidence in mid- and long-range connections, short-range connectivity has to be interpreted with care. Next, we demonstrate the strong relationship between the structural connectivity obtained from diffusion MR tractography and the functional connectivity measured with functional MRI. Then, we compare the performance of several diffusion MRI techniques through connectome-based measurements. We find that diffusion spectrum imaging is more sensitive and therefore enhances the results of tractography. Finally, we present two network-oriented applications. We use the human connectome to reveal the small-world architecture of the brain, a very efficient network topology in terms of wiring and power supply. We identify the cortical areas that belong to the core of structural connectivity. We show that these regions also belong to the default mode network, a set of dynamically coupled brain regions that are found to be more highly activated at rest. As a conclusion, we emphasize the potential of human connectome mapping for clinical applications and pathological studies.
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Abstract This article presents a novel approach for understanding information exchange efficiency and its decay across hierarchies of modularity, from local to global, of the structural human brain connectome. Magnetic resonance imaging techniques have allowed us to study the human brain connectivity as a graph, which can then be analyzed using a graph‐theoretical approach. Collectively termed brain connectomics, these sophisticated mathematical techniques have revealed that the brain connectome, like many networks, is highly modular and brain regions can thus be organized into communities or modules. Here, using tractography‐informed structural connectomes from 46 normal healthy human subjects, we constructed the hierarchical modularity of the structural connectome using bifurcating dendrograms. Moving from fine to coarse (i.e., local to global) up the connectome's hierarchy, we computed the rate of decay of a new metric that hierarchically preferentially weighs the information exchange between two nodes in the same module. By computing “embeddedness”‐the ratio between nodal efficiency and this decay rate, one could thus probe the relative scale‐invariant information exchange efficiency of the human brain. Results suggest that regions that exhibit high embeddedness are those that comprise the limbic system, the default mode network, and the subcortical nuclei. This supports the presence of near‐decomposability overall yet relative embeddedness in select areas of the brain. The areas we identified as highly embedded are varied in function but are arguably linked in the evolutionary role they play in memory, emotion and behavior. Hum Brain Mapp 36:3653–3665, 2015 . © 2015 Wiley Periodicals, Inc.
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The methodological development in the mapping of the brain structural connectome from diffusion-weighted magnetic resonance imaging (DW-MRI) has raised many hopes in the neuroscientific community. Indeed, the knowledge of the connections between different brain regions is fundamental to study brain anatomy and function. The reliability of the structural connectome is therefore of paramount importance. In the search for accuracy, researchers have given particular attention to linking white matter tractography methods – used for estimating the connectome – with information about the microstructure of the nervous tissue. The creation and validation of methods in this context were hampered by a lack of practical numerical phantoms. To achieve this, we created a numerical phantom that mimics complex anatomical fibre pathway trajectories while also accounting for microstructural features such as axonal diameter distribution, myelin presence, and variable packing densities. The substrate has a micrometric resolution and an unprecedented size of 1 cubic millimetre to mimic an image acquisition matrix of 40×40×40 voxels. DW-MRI images were obtained from Monte Carlo simulations of spin dynamics to enable the validation of quantitative tractography. The phantom is composed of 12,196 synthetic tubular fibres with diameters ranging from 1.4 µm to 4.2 µm, interconnecting sixteen regions of interest. The simulated images capture the microscopic properties of the tissue (e.g. fibre diameter, water diffusing within and around fibres, free water compartment), while also having desirable macroscopic properties resembling the anatomy, such as the smoothness of the fibre trajectories. While previous phantoms were used to validate either tractography or microstructure, this phantom can enable a better assessment of the connectome estimation's reliability on the one side, and its adherence to the actual microstructure of the nervous tissue on the other.
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