Unexpected hubness: a proof-of-concept study of the human connectome using pagerank centrality and implications for intr

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CLINICAL STUDY

Unexpected hubness: a proof‑of‑concept study of the human connectome using pagerank centrality and implications for intracerebral neurosurgery Jacky T. Yeung1 · Hugh M. Taylor2 · Isabella M. Young3 · Peter J. Nicholas2 · Stéphane Doyen2 · Michael E. Sughrue1,2  Received: 9 September 2020 / Accepted: 4 November 2020 © Springer Science+Business Media, LLC, part of Springer Nature 2020

Abstract Introduction  Understanding the human connectome by parcellations allows neurosurgeons to foretell the potential effects of lesioning parts of the brain during intracerebral surgery. However, it is unclear whether there exist variations among individuals such that brain regions that are thought to be dispensable may serve as important networking hubs. Methods  We obtained diffusion neuroimaging data from two healthy cohorts (OpenNeuro and SchizConnect) and applied a parcellation scheme to them. We ranked the parcellations on average using PageRank centrality in each cohort. Using the OpenNeuro cohort, we focused on parcellations in the lower 50% ranking that displayed top quartile ranking at the individual level. We then queried whether these select parcellations with over 3% prevalence would be reproducible in the same manner in the SchizConnect cohort. Results  In the OpenNeuro (n = 68) and SchizConnect cohort (n = 195), there were 27.9% and 43.1% of parcellations, respectively, in the lower half of all ranks that displayed top quartile ranks. We noted three outstanding parcellations (L_V6, L_a10p, and L_7PL) in the OpenNeuro cohort that also appeared in the SchizConnect cohort. In the larger Schizconnect cohort, L_V6, L_a10p, and L_7PL had unexpected hubness in 3.08%, 5.13%, and 8.21% of subjects, respectively. Conclusions  We demonstrated that lowly-ranked parcellations may serve as important hubs in a subset of individuals, highlighting the importance of studying parcellation ranks at the personalized level in planning supratentorial neurosurgery. Keywords  Unexpected hubness · Centrality · Hubs · Connectome · Connectomics Abbreviations DVAR Spatial standard deviation of successive difference images ROI Regions of interest HCP Human connectome project SFL Superior frontal lobe

Electronic supplementary material  The online version of this article (https​://doi.org/10.1007/s1106​0-020-03659​-6) contains supplementary material, which is available to authorized users. * Michael E. Sughrue [email protected] 1



Centre for Minimally Invasive Neurosurgery, Suite 19, Level 7 Prince of Wales Private Hospital, Barker Street, Randwick, NSW 2031, Australia

2



Omniscient Neurotechnology, Sydney, Australia

3

Cingulum Health, Sydney, Australia



TE1p Posterior portions of the middle and inferior temporal gyrus TGd Temporal gyrus dorsal

Introduction Eloquence is traditionally regarded as one of the most important considerations in intracerebral neurosurgery [1, 2]. The transgression of a neurologically eloquent area will result in undesired clinical outcomes and alteration of neurological functions [3]