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Brain network integration dynamics are associated with loss and recovery of consciousness induced by sevoflurane

Andrea I. Luppi, Daniel Golkowski, Andreas Ranft, Rüdiger Ilg, Denis Jordan, David Menon, Emmanuel A. Stamatakis

Human Brain Mapping March 19, 2021 DOI: 10.1002/hbm.25405 via OpenAlex

Summary

The human brain alternates between states of high integration and segregation, which are thought to support consciousness. Using dynamic functional connectivity and graph theory on resting-state fMRI data from healthy volunteers, the authors show that the integrated state is especially vulnerable to the anaesthetic sevoflurane. At higher doses (3% vol and burst-suppression), anaesthesia reduces the complexity and small-world character of integrated brain states and disrupts the temporal balance between integration and segregation. These effects reverse upon recovery, linking them to consciousness. Reduced anticorrelations between the default mode and executive control networks also reconfigure dynamically depending on the brain's integration state. The breakdown of the integrated sub-state may serve as a generalisable biomarker of loss and recovery of consciousness.

Study at a glance

Characteristics Observational cohort Peer reviewed
Population Healthy volunteers
Topics Default mode network
Keywords Consciousness Neuroscience Dynamic functional connectivity Functional integration
Citations 72
Key finding The integrated sub-state of brain connectivity is especially vulnerable to anaesthesia, and its breakdown represents a generalisable biomarker of loss and recovery of consciousness.

Abstract

Abstract The dynamic interplay of integration and segregation in the brain is at the core of leading theoretical accounts of consciousness. The human brain dynamically alternates between a sub‐state where integration predominates, and a predominantly segregated sub‐state, with different roles in supporting cognition and behaviour. Here, we combine graph theory and dynamic functional connectivity to compare resting‐state functional MRI data from healthy volunteers before, during, and after loss of responsiveness induced with different concentrations of the inhalational anaesthetic, sevoflurane. We show that dynamic states characterised by high brain integration are especially vulnerable to general anaesthesia, exhibiting attenuated complexity and diminished small‐world character. Crucially, these effects are reversed upon recovery, demonstrating their association with consciousness. Higher doses of sevoflurane (3% vol and burst‐suppression) also compromise the temporal balance of integration and segregation in the human brain. Additionally, we demonstrate that reduced anticorrelations between the brain's default mode and executive control networks dynamically reconfigure depending on the brain's state of integration or segregation. Taken together, our results demonstrate that the integrated sub‐state of brain connectivity is especially vulnerable to anaesthesia, in terms of both its complexity and information capacity, whose breakdown represents a generalisable biomarker of loss of consciousness and its recovery.

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