Systematic network lesioning reveals the core white matter scaffold of the human brain

Department of Neurology, Keck School of Medicine, Institute for Neuroimaging and Informatics, University of Southern California, Los Angeles, CA, USA

Brain connectivity loss due to traumatic brain injury, stroke or multiple sclerosis can have serious consequences on life quality and a measurable impact upon neural and cognitive function. Though brain network properties are known to be affected disproportionately by injuries to certain gray matter regions, the manner in which white matter (WM) insults affect such properties remains poorly understood. Here, network-theoretic analysis allows us to identify the existence of a macroscopic neural connectivity core in the adult human brain which is particularly sensitive to network lesioning. The systematic lesion analysis of brain connectivity matrices from diffusion neuroimaging over a large sample (N = 110) reveals that the global vulnerability of brain networks can be predicated upon the extent to which injuries disrupt this connectivity core, which is found to be quite distinct from the set of connections between rich club nodes in the brain. Thus, in addition to connectivity within the rich club, the brain as a network also contains a distinct core scaffold of network edges consisting of WM connections whose damage dramatically lowers the integrative properties of brain networks. This pattern of core WM fasciculi whose injury results in major alterations to overall network integrity presents new avenues for clinical outcome prediction following brain injury by relating lesion locations to connectivity core disruption and implications for recovery. The findings of this study contribute substantially to current understanding of the human WM connectome, its sensitivity to injury, and clarify a long-standing debate regarding the relative prominence of gray vs. WM regions in the context of brain structure and connectomic architecture.

Keywords: connectomics, traumatic brain injury, brain network, neurotrauma, neuroimaging, MRI, DTI

Citation: Irimia A and Van Horn JD (2014) Systematic network lesioning reveals the core white matter scaffold of the human brain. Front. Hum. Neurosci. 8:51. doi: 10.3389/fnhum.2014.00051

Received: 17 October 2013; Paper pending published: 23 November 2013;
Accepted: 23 January 2014; Published online: 11 February 2014.

Edited by:

Shuhei Yamaguchi, Shimane University, Japan

Reviewed by:

Keiichi Onoda, Shimane University, Japan
Boris Bernhardt, Max Planck Institute for Human Cognitive and Brain Sciences, Germany

Copyright © 2014 Irimia and Van Horn. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: John D. Van Horn, Department of Neurology, Keck School of Medicine, Institute for Neuroimaging and Informatics, University of Southern California, 2001 North Soto Street, Room 102, MC 9232, Los Angeles, CA 90089-9235, USA e-mail: jvanhorn@usc.edu