Reduced emergent character of neural dynamics in patients with a disrupted connectome
Andrea I. Luppi,
Pedro A.M. Mediano,
Fernando E. Rosas,
Judith Allanson,
John D. Pickard,
Guy B. Williams,
Michael M. Craig,
Paola Finoia,
Alexander R.D. Peattie,
Peter Coppola,
David K. Menon,
Daniel Bor,
Emmanuel A. Stamatakis
Affiliations
Andrea I. Luppi
Division of Anaesthesia, School of Clinical Medicine, University of Cambridge, UK; Department of Clinical Neurosciences, University of Cambridge, Cambridge, UK; Leverhulme Centre for the Future of Intelligence, Cambridge, UK; The Alan Turing Institute, London, UK; Corresponding author at: Division of Anaesthesia, School of Clinical Medicine, University of Cambridge, UK.
Pedro A.M. Mediano
Department of Computing, Imperial College London, London, UK; Department of Psychology, University of Cambridge, Cambridge, UK
Fernando E. Rosas
Department of Brain Science, Center for Psychedelic Research, Imperial College London, London, UK; Data Science Institute, Imperial College London, London, UK; Centre for Complexity Science, Imperial College London, London, UK; Center for Eudaimonia and Human Flourishing, University of Oxford, Oxford, UK; Department of Informatics, University of Sussex, Brighton, UK
Judith Allanson
Department of Clinical Neurosciences, University of Cambridge, Cambridge, UK; Department of Neurosciences, Addenbrooke's Hospital, Cambridge University Hospitals NHS Foundation, Cambridge, UK
John D. Pickard
Department of Clinical Neurosciences, University of Cambridge, Cambridge, UK
Guy B. Williams
Department of Clinical Neurosciences, University of Cambridge, Cambridge, UK; Wolfson Brain Imaging Centre, University of Cambridge, Cambridge, UK
Michael M. Craig
Division of Anaesthesia, School of Clinical Medicine, University of Cambridge, UK; Department of Clinical Neurosciences, University of Cambridge, Cambridge, UK
Paola Finoia
Department of Clinical Neurosciences, University of Cambridge, Cambridge, UK
Alexander R.D. Peattie
Division of Anaesthesia, School of Clinical Medicine, University of Cambridge, UK; Department of Clinical Neurosciences, University of Cambridge, Cambridge, UK
Peter Coppola
Division of Anaesthesia, School of Clinical Medicine, University of Cambridge, UK; Department of Clinical Neurosciences, University of Cambridge, Cambridge, UK
David K. Menon
Division of Anaesthesia, School of Clinical Medicine, University of Cambridge, UK; Wolfson Brain Imaging Centre, University of Cambridge, Cambridge, UK
Daniel Bor
Department of Psychology, University of Cambridge, Cambridge, UK; Department of Psychology, Queen Mary University of London, UK
Emmanuel A. Stamatakis
Division of Anaesthesia, School of Clinical Medicine, University of Cambridge, UK; Department of Clinical Neurosciences, University of Cambridge, Cambridge, UK
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.
