Abstract
In network analysis, the so‐called “rich club” describes the core areas of the brain that are more densely interconnected among themselves than expected by chance, and has been identified as a fundamental aspect of the human brain connectome. This is the first in‐depth diffusion imaging study to investigate the rich club along with other organizational changes in the brain's anatomical network in behavioral frontotemporal dementia (bvFTD), and a matched cohort with early‐onset Alzheimer's disease (EOAD). Our study sheds light on how bvFTD and EOAD affect connectivity of white matter fiber pathways in the brain, revealing differences and commonalities in the connectome among the dementias. To analyze the breakdown in connectivity, we studied three groups: 20 bvFTD, 23 EOAD, and 37 healthy elderly controls. All participants were scanned with diffusion‐weighted magnetic resonance imaging (MRI), and based on whole‐brain probabilistic tractography and cortical parcellations, we analyzed the rich club of the brain's connectivity network. This revealed distinct patterns of disruption in both forms of dementia. In the connectome, we detected less disruption overall in EOAD than in bvFTD [false discovery rate (FDR) critical P perm = 5.7 × 10−3, 10,000 permutations], with more involvement of richly interconnected areas of the brain (chi‐squared P = 1.4 × 10−4)—predominantly posterior cognitive alterations. In bvFTD, we found a greater spread of disruption including the rich club (FDR critical P perm = 6 × 10−4), but especially more peripheral alterations (chi‐squared P = 6.5 × 10−3), particularly in medial frontal areas of the brain, in line with the known behavioral socioemotional deficits seen in these patients. Hum Brain Mapp 37:868–883, 2016. © 2015 The Authors. Human Brain Mapping Published by Wiley Periodicals, Inc.
Highlights
The human nervous system is a network of connections that supports complex communication between numerous brain regions
The UwFA curve was higher in behavioral frontotemporal dementia (bvFTD) compared to controls (FDR critical Pperm 5 7.5 3 1023) at k 5 5–27, while the UwMD curve, expected to have an opposing effect, was lower in bvFTD, relative to controls (FDR critical Pperm 5 0.015), at k 5 5–17
We found disrupted levels of connectivity in patients with dementia, bvFTD, and earlyonset Alzheimer’s disease (EOAD) (Fig. 2), based on an in-depth analysis of the weighted rich club organization of the brain
Summary
The human nervous system is a network of connections that supports complex communication between numerous brain regions. Using emerging network-sensitive neuroimaging techniques, such as diffusion-weighted imaging (DWI), we are able to reconstruct the gross organization of the human brain as a structural network of connections that make up the “connectome”, revealing the architectural properties of the nervous system. Studies of the human connectome have advanced neuroscience by shedding light on the cognitive and behavioral characteristics [Toga and Thompson, 2013] of the healthy and diseased living brain. Neurodegenerative diseases may target specific neural networks with a characteristic profile of anatomical progression [Braak and Braak, 1991; Zhou et al, 2012]. In late-onset Alzheimer’s disease (LOAD), pathology may emerge first in the more central and interconnected areas of the brain’s network, known as “hubs” [Buckner et al, 2005]. Network hubs form a highcapacity central core, or rich club, and rich club connec-
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