How hot is the hot zone? Computational modelling clarifies the role of parietal and frontoparietal connectivity during anaesthetic-induced loss of consciousness

Research output: Contribution to journalArticlepeer-review

Authors

  • Riku Ihalainen
  • Olivia Gosseries
  • Frederick van de Steen
  • Federico Raimondo
  • Rajanikant Panda
  • Vincent Bonhomme
  • Daniele Marinazzo
  • Steven Laureys
  • Srivas Chennu

Colleges, School and Institutes

Abstract

In recent years, specific cortical networks have been proposed to be crucial for sustaining consciousness, including the posterior hot zone and frontoparietal resting state networks (RSN). Here, we computationally evaluate the relative contributions of three RSNs – the default mode network (DMN), the salience network (SAL), and the central executive network (CEN) – to consciousness and its loss during propofol anaesthesia. Specifically, we use dynamic causal modelling (DCM) of 10 min of high-density EEG recordings (N = 10, 4 males) obtained during behavioural responsiveness, unconsciousness and post-anaesthetic recovery to characterise differences in effective connectivity within frontal areas, the posterior ‘hot zone’, frontoparietal connections, and between-RSN connections. We estimate – for the first time – a large DCM model (LAR) of resting EEG, combining the three RSNs into a rich club of interconnectivity. Consistent with the hot zone theory, our findings demonstrate reductions in inter-RSN connectivity in the parietal cortex. Within the DMN itself, the strongest reductions are in feed-forward frontoparietal and parietal connections at the precuneus node. Within the SAL and CEN, loss of consciousness generates small increases in bidirectional connectivity. Using novel DCM leave-one-out cross-validation, we show that the most consistent out-of-sample predictions of the state of consciousness come from a key set of frontoparietal connections. This finding also generalises to unseen data collected during post-anaesthetic recovery. Our findings provide new, computational evidence for the importance of the posterior hot zone in explaining the loss of consciousness, highlighting also the distinct role of frontoparietal connectivity in underpinning conscious responsiveness, and consequently, suggest a dissociation between the mechanisms most prominently associated with explaining the contrast between conscious awareness and unconsciousness, and those maintaining consciousness.

Bibliographic note

Funding Information: This work was supported by the UK Engineering and Physical Sciences Research Council (EP/P033199/1), Belgian National Funds for Scientific Research (FRS-FNRS), the University and University Hospital of Liege, the Fund Generet, the King Baudouin Foundation, the AstraZeneca Foundation, the European Union's Horizon 2020 Framework Programme for Research and Innovation under the Specific Grant Agreement No. 945539 (Human Brain Project SGA3), DOCMA project (EU-H2020-MSCA–RISE–778234), the BIAL Foundation, the European Space Agency (ESA) and the Belgian Federal Science Policy Office (BELSPO) in the framework of the PRODEX Programme, the centre-TBI project (FP7-HEALTH- 602150), the Public Utility Foundation ‘Université Européenne du Travail’, “Fondazione Europea di Ricerca Biomedica”, the Mind Science Foundation, the European Commission, and the Special Research Fund of Ghent University. O.G. is research associate and S.L. is research director at the F.R.S-FNRS. Funding Information: We gratefully acknowledge support from the University of Kent’s High Performance Computing facility. Funding Information: We gratefully acknowledge support from the University of Kent's High Performance Computing facility. This work was supported by the UK Engineering and Physical Sciences Research Council (EP/P033199/1), Belgian National Funds for Scientific Research (FRS-FNRS), the University and University Hospital of Liege, the Fund Generet, the King Baudouin Foundation, the AstraZeneca Foundation, the European Union's Horizon 2020 Framework Programme for Research and Innovation under the Specific Grant Agreement No. 945539 (Human Brain Project SGA3), DOCMA project (EU-H2020-MSCA?RISE?778234), the BIAL Foundation, the European Space Agency (ESA) and the Belgian Federal Science Policy Office (BELSPO) in the framework of the PRODEX Programme, the centre-TBI project (FP7-HEALTH- 602150), the Public Utility Foundation ?Universit? Europ?enne du Travail?, ?Fondazione Europea di Ricerca Biomedica?, the Mind Science Foundation, the European Commission, and the Special Research Fund of Ghent University. O.G. is research associate and S.L. is research director at the F.R.S-FNRS. Publisher Copyright: © 2021 Copyright: Copyright 2021 Elsevier B.V., All rights reserved.

Details

Original languageEnglish
Article number117841
Number of pages58
JournalNeuroImage
Volume231
Early online date9 Feb 2021
Publication statusPublished - 1 May 2021

Keywords

  • Anesthesia, Consciousness, EEG, Effective Connectivity, Dynamic Causal Modelling, Anaesthesia, Dynamic causal modelling, Effective connectivity

ASJC Scopus subject areas