Abstract

With recent advances in computational analyses of structural neuroimaging, it is possible to comprehensively map neural connectivity, i.e., the brain connectome. The architectural organization of the connectome is believed to play an important role in several biological processes. Central to the conformation of the connectome are connectivity hubs, which are likely to be organized in accordance with the rich club phenomenon, as evidenced by graph theory analyses of neural architecture. It is yet unclear whether rich club connectivity hubs are consistently organized in the same anatomical framework across healthy adults. We constructed the brain connectome from 43 healthy adults, based on T1-weighted and diffusion tensor MRI data. Probabilistic fiber tractography was used to evaluate connectivity between each possible pair of cortical anatomical regions of interest. Connectivity hubs were identified in accordance with the rich club phenomenon applied to binarized matrices, and the variability in frequency of hub participation was assessed node-wise across all subjects. The anatomical location of nodes participating in rich club networks was fairly consistent across subjects. The most common locations for rich club nodes were identified in integrative areas, such as the cingulate and pericingulate regions, medial aspect of the occipital areas and precuneus; or else, they were found in important and specialized brain regions (such as the oribitofrontal cortex, caudate, fusiform gyrus, and hippocampus). Marked anatomical consistency exists across healthy brains in terms of nodal participation and location of rich club networks. The consistency of connections between integrative areas and specialized brain regions highlights a fundamental connectivity pattern shared among healthy brains. We propose that approaching brain connectivity with this framework of anatomical consistencies may have clinical implications for early detection of individual variability.

Highlights

  • Recent advances in neuroimaging make it possible to chart the organization of neural connectivity across the entire human brain using magnetic resonance (MRI) diffusion tensor imagingIndividual rich club networks (DTI) (Hagmann et al, 2008)

  • MRI Acquisition All subjects underwent MRI scanning performed on a Verio 3 Tesla MRI scanner (Siemens Medical, Erlangen, Germany), yielding T1- and diffusion-weighted images (DWIs) obtained using a unique protocol across, as follows: (1) T1 weighted images: 3D magnetization-prepared rapid gradient echo (MPRAGE) sequences with parameters: repetition time (TR) = 2250 ms, echo time (TE) = 4.18 ms, flip angle = 6◦, FOV = 256 × 256 mm, matrix size = 256 × 256, slice thickness: 1 mm and 192 sagittal slices; (2) DWI: twice-refocused, singleshot echo planar sequence with diffusion weightings b-value = 0, 1000, and 2000 s/mm2 applied along 30 non-collinear directions

  • Demonstrated that the following nodes were more likely to be involved in the rich club network: right lateral occipital, right pericalcarine, right caudal anterior cingulate, left posterior cingulate, right posterior cingulate, right lateral orbitofrontal, right fusiform, right caudate, left supramarginal, left lateral orbitofrontal, left inferior temporal, right middle temporal, right lingual, right hippocampus, left precuneus, left hippocampus, left caudate, left caudal middle frontal regions

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Summary

Introduction

Recent advances in neuroimaging make it possible to chart the organization of neural connectivity across the entire human brain using magnetic resonance (MRI) diffusion tensor imagingIndividual rich club networks (DTI) (Hagmann et al, 2008). Known as brain connectomes (Sporns et al, 2005; Sporns, 2011), the generation of whole brain maps of neural architecture is becoming increasingly popular as evidence accumulates in favor of the view that the disruption of structural connectivity is central to the neurobiology of many neurological and psychiatric illnesses (Buckner et al, 2009; Seeley et al, 2009; van den Heuvel and Sporns, 2011). Hubs are expected to function as the basis of the brain’s integrative capacity (van den Heuvel and Sporns, 2011; Sporns, 2013), and possess a high degree of connectivity, short neuronal path lengths, and high centrality (van den Heuvel and Sporns, 2011). Assuming that central hubs of the connectome are more likely to be highly interconnected, rich-club nodes characteristically show higher connectivity with each other, beyond what would be expected by chance given their degrees (i.e., number of connections with other nodes)

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