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Reduced emergent character of neural dynamics in patients with a disrupted connectome.

Published version
Peer-reviewed

Type

Article

Change log

Authors

Luppi, Andrea I 
Mediano, Pedro AM 
Rosas, Fernando E 
Allanson, Judith 
Pickard, John D 

Abstract

High-level brain functions are widely believed to emerge from the orchestrated activity of multiple neural systems. However, lacking a formal definition and practical quantification of emergence for experimental data, neuroscientists have been unable to empirically test this long-standing conjecture. Here we investigate this fundamental question by leveraging a recently proposed framework known as "Integrated Information Decomposition," which establishes a principled information-theoretic approach to operationalise and quantify emergence in dynamical systems - including the human brain. By analysing functional MRI data, our results show that the emergent and hierarchical character of neural dynamics is significantly diminished in chronically unresponsive patients suffering from severe brain injury. At a functional level, we demonstrate that emergence capacity is positively correlated with the extent of hierarchical organisation in brain activity. Furthermore, by combining computational approaches from network control theory and whole-brain biophysical modelling, we show that the reduced capacity for emergent and hierarchical dynamics in severely brain-injured patients can be mechanistically explained by disruptions in the patients' structural connectome. Overall, our results suggest that chronic unresponsiveness resulting from severe brain injury may be related to structural impairment of the fundamental neural infrastructures required for brain dynamics to support emergence.

Description

Keywords

Disorders of consciousness, Emergence, Hierarchy, Information decomposition, Network control theory, Whole-brain modelling, Humans, Connectome, Brain, Magnetic Resonance Imaging, Nervous System Physiological Phenomena, Brain Injuries

Journal Title

Neuroimage

Conference Name

Journal ISSN

1053-8119
1095-9572

Volume Title

269

Publisher

Elsevier BV
Sponsorship
Medical Research Council (MR/M009041/1)
Wellcome Trust (210920/Z/18/Z)