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

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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.

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Data availability

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

Abbreviations

DVAR:

Spatial standard deviation of successive difference images

ROI:

Regions of interest

HCP:

Human connectome project

SFL:

Superior frontal lobe

TE1p:

Posterior portions of the middle and inferior temporal gyrus

TGd:

Temporal gyrus dorsal

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Acknowledgements

Some of the data used in preparation of this article were obtained from the SchizConnect database (https://schizconnect.org) As such, the investigators within SchizConnect contributed to the design and implementation of SchizConnect and/or provided data but did not participate in analysis or writing of this report. Data collection and sharing for this SchizConnect project was funded by NIMH cooperative agreement 1U01 MH097435.

Funding

No funding was received to conduct this study or assist with the preparation of this manuscript.

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Authors and Affiliations

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

    Jacky T. Yeung & Michael E. Sughrue

  2. Omniscient Neurotechnology, Sydney, Australia

    Hugh M. Taylor, Peter J. Nicholas, Stéphane Doyen & Michael E. Sughrue

  3. Cingulum Health, Sydney, Australia

    Isabella M. Young

Authors
  1. Jacky T. Yeung
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  2. Hugh M. Taylor
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Correspondence to Michael E. Sughrue.

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Hugh Taylor, Peter Nicholas, Stephane Doyen and Michael Sughrue are employees of Omniscient Neurotechnologies. No other authors report any conflict of interest.

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Yeung, J.T., Taylor, H.M., Young, I.M. et al. Unexpected hubness: a proof-of-concept study of the human connectome using pagerank centrality and implications for intracerebral neurosurgery. J Neurooncol 151, 249–256 (2021). https://doi.org/10.1007/s11060-020-03659-6

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  • DOI: https://doi.org/10.1007/s11060-020-03659-6

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