Spectral signatures of reorganised brain networks in disorders of consciousness.

Srivas Chennu,Martin M Monti,Francisco Olivares,Evelyn Kamau,Valdas Noreika,Judith Allanson,Daniela Cabezas-Soto,Guy B Williams,Tristan A Bekinschtein,David K Menon,Andrés Canales-Johnson,Adrian M Owen,John D Pickard,Paola Finoia,Aurina Arnatkeviciute

doi:10.1371/journal.pcbi.1003887

Abstract

Theoretical advances in the science of consciousness have proposed that it is concomitant with balanced cortical integration and differentiation, enabled by efficient networks of information transfer across multiple scales. Here, we apply graph theory to compare key signatures of such networks in high-density electroencephalographic data from 32 patients with chronic disorders of consciousness, against normative data from healthy controls. Based on connectivity within canonical frequency bands, we found that patient networks had reduced local and global efficiency, and fewer hubs in the alpha band. We devised a novel topographical metric, termed modular span, which showed that the alpha network modules in patients were also spatially circumscribed, lacking the structured long-distance interactions commonly observed in the healthy controls. Importantly however, these differences between graph-theoretic metrics were partially reversed in delta and theta band networks, which were also significantly more similar to each other in patients than controls. Going further, we found that metrics of alpha network efficiency also correlated with the degree of behavioural awareness. Intriguingly, some patients in behaviourally unresponsive vegetative states who demonstrated evidence of covert awareness with functional neuroimaging stood out from this trend: they had alpha networks that were remarkably well preserved and similar to those observed in the controls. Taken together, our findings inform current understanding of disorders of consciousness by highlighting the distinctive brain networks that characterise them. In the significant minority of vegetative patients who follow commands in neuroimaging tests, they point to putative network mechanisms that could support cognitive function and consciousness despite profound behavioural impairment.

Highlights

There has been considerable recent interest in the view that consciousness is a phenomenon emerging from the dynamic equilibrium between differentiated and integrated information processing in the brain [1,2,3,4]
Using a novel metric termed modular span that embedded topologically derived modules in topographical space, we established that the alpha network modules in patients were spatially limited, with a prominent absence of the structured long-distance connectivity commonly observed in healthy networks
We noted the presence of robust connectivity patterns that were commonly structured across patients, suggesting that there could be some degree of reorganisation, rather than just disorganisation, of brain networks in disorders of consciousness (DoC)

Summary

Introduction

There has been considerable recent interest in the view that consciousness is a phenomenon emerging from the dynamic equilibrium between differentiated and integrated information processing in the brain [1,2,3,4] This view has inspired research into ways of quantifying the characteristics of information exchange in the brain at rest, and how this modulated in natural sleep, pharmacological sedation, and pathological coma and disorders of consciousness (DoC; including the vegetative and minimally conscious states, VS and MCS). Recent advances in the use of neuroimaging to better ascertain brain function in DoC have yielded some surprises, and indicated that a significant minority of patients are able to volitionally modulate brain activity in ways that would

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