Loss of consciousness reduces the stability of brain hubs and the heterogeneity of brain dynamics

Ane López-González,Rajanikant Panda,Jitka Annen,Steven Laureys,Gustavo Deco,Anira Escrichs,Gorka Zamora-López,Charlotte Martial,Aurore Thibaut,Adrián Ponce-Alvarez,Morten L Kringelbach,Olivia Gosseries

doi:10.1038/s42003-021-02537-9

Abstract

Low-level states of consciousness are characterized by disruptions of brain activity that sustain arousal and awareness. Yet, how structural, dynamical, local and network brain properties interplay in the different levels of consciousness is unknown. Here, we study fMRI brain dynamics from patients that suffered brain injuries leading to a disorder of consciousness and from healthy subjects undergoing propofol-induced sedation. We show that pathological and pharmacological low-level states of consciousness display less recurrent, less connected and more segregated synchronization patterns than conscious state. We use whole-brain models built upon healthy and injured structural connectivity to interpret these dynamical effects. We found that low-level states of consciousness were associated with reduced network interactions, together with more homogeneous and more structurally constrained local dynamics. Notably, these changes lead the structural hub regions to lose their stability during low-level states of consciousness, thus attenuating the differences between hubs and non-hubs brain dynamics.

Highlights

Low-level states of consciousness are characterized by disruptions of brain activity that sustain arousal and awareness
We found that the average integration across time was significantly lower for Minimally Conscious State (MCS) and Unresponsiveness Wakefulness Syndrome (UWS), compared to control subjects (CNT), for S and R compared to W, and for S compared to R (Fig. 1d, see Table 1 for statistics)
We have shown that reduction of consciousness is characterized by brain dynamics with less recurrent, less connected and more segregated patterns of phasesynchronization than for conscious states

Summary

Introduction

Low-level states of consciousness are characterized by disruptions of brain activity that sustain arousal and awareness. Wakefulness is usually evaluated by eye opening, and awareness by the responsiveness of the patients and their ability to interact with the environment, as a proxy for subjective experience The study of these different levels of consciousness has proven to be essential to understand the neural correlates of consciousness, yet, the underlying mechanisms remain largely unknown. Graph theory studies have shown that the modular and hierarchical organization of the human connectome facilitates the efficiency and robustness of information transmission[3,12] For these reasons, consciousness has been considered to result from the interplay between dynamics and connectivity allowing the coordination of brain-wide activity to ensure the conscious functioning of the brain[13,14,15,16]. It allows us to study how network dynamics depend on the local activity of brain regions that have an important place in the structural network, such as highly connected nodes, usually referred to as “hubs”

Objectives

Methods

Results

Conclusion