Complexity changes in functional state dynamics suggest focal connectivity reductions

Front Hum Neurosci. 2022 Sep 23:16:958706. doi: 10.3389/fnhum.2022.958706. eCollection 2022.

Abstract

The past two decades have seen an explosion in the methods and directions of neuroscience research. Along with many others, complexity research has rapidly gained traction as both an independent research field and a valuable subdiscipline in computational neuroscience. In the past decade alone, several studies have suggested that psychiatric disorders affect the spatiotemporal complexity of both global and region-specific brain activity (Liu et al., 2013; Adhikari et al., 2017; Li et al., 2018). However, many of these studies have not accounted for the distributed nature of cognition in either the global or regional complexity estimates, which may lead to erroneous interpretations of both global and region-specific entropy estimates. To alleviate this concern, we propose a novel method for estimating complexity. This method relies upon projecting dynamic functional connectivity into a low-dimensional space which captures the distributed nature of brain activity. Dimension-specific entropy may be estimated within this space, which in turn allows for a rapid estimate of global signal complexity. Testing this method on a recently acquired obsessive-compulsive disorder dataset reveals substantial increases in the complexity of both global and dimension-specific activity versus healthy controls, suggesting that obsessive-compulsive patients may experience increased disorder in cognition. To probe the potential causes of this alteration, we estimate subject-level effective connectivity via a Hopf oscillator-based model dynamic model, the results of which suggest that obsessive-compulsive patients may experience abnormally high connectivity across a broad network in the cortex. These findings are broadly in line with results from previous studies, suggesting that this method is both robust and sensitive to group-level complexity alterations.

Keywords: Hopf bifurcation; LEiDA; Shannon entropy; eigendecomposition; independent component analysis; network-based statistic; obsessive-compulsive disorder; whole-brain model.

Grants and funding

This work was funded by ICVS Scientific Microscopy Platform, member of the National infrastructure PPBI-Portuguese Platform of Bioimaging (PPBI-POCI01 0145-FEDER-022122); by National funds, through the Foundation for Science and Technology (FCT)-project UIDB/50026/2020 and UIDP/50026/2020; and by the project NORTE-01-0145-FEDER-000039, supported by Norte Portugal Regional Operational Programme (NORTE 2020), under the PORTUGAL 2020 Partnership Agreement, through the European Regional Development Fund (ERDF). GD and DB were supported by the Spanish national research project (ref. PID2019-105772GB-I00/AEI/10.13039/501100011033) funded by the Spanish Ministry of Science, Innovation and Universities (MCIU) and State Research Agency (AEI).