The trade-off between wiring cost and network topology in white matter structural networks in health and migraine

Abstract

The human brain organization of cortical networks has optimized trade-off architecture for the economical minimization of connection distance and maximizing valuable topological properties; however, whether this network configuration is disrupted in chronic migraine remains unknown. Here, employing the diffusion tensor imaging and graph theory approaches to construct white matter networks in 26 patients with migraine (PM) and 26 gender-matched healthy controls (HC), we investigated relationships between structural connectivity, cortical network architecture and anatomical distance in the two groups separately. Compared with the HC group, the patients showed longer global distance connection in PM, with proportionally less short-distance and more medium-distance; correspondingly, the patients showed abnormal global topology in their structural networks, mainly presented as a higher clustering coefficient. Moreover, the abnormal association between these two network features was also found. Intriguingly, the network measure that combined the nodal anatomical distance and network topology could distinguish PM from HC with high accuracy of 90.4%. We also demonstrated a high reproducibility of our findings across different parcellation schemes. Our results demonstrated that long-term migraine may result in a abnormal optimization of a trade-off between wiring cost and network topology in white matter structural networks and highlights the potential for combining spatial and topological aspects as a network marker, which may provide valuable insights into the understanding of brain network reorganization that could be attributed to the underlying pathophysiology resulting from migraine.

Keywords: AAL; Anatomical distance; C; DCS; DTI; FA; FACT; FDT; FMRIB software Library; FMRIB's Diffusion Toolbox; FOV; FSGPR; FSL; Fast Spoiled Gradient Recalled sequence; HC; L; Migraine; PH; PM; Q; ROC; ROIs; Structural connectivity; TE; TR; Trade-off architecture; White matter network; automated anatomical labeling atlas; average of the clustering coefficient; average of the shortest path lengths; diffusion tensor imaging; distance-related connection strength; dlPFC; dorsolateral prefrontal cortex; echo time; fiber assignment by continuous tracking algorithm; field of view; fractional anisotropy; healthy controls; migraine patients; modularity; parahippocampal gyrus; receiver operating characteristic; region of interests; repetition time.