The evolution of whole-brain turbulent dynamics during recovery from traumatic brain injury

Author:

Martínez-Molina Noelia123ORCID,Escrichs Anira1,Sanz-Perl Yonatan1,Sihvonen Aleksi J.2345,Särkämö Teppo23,Kringelbach Morten L.678,Deco Gustavo19

Affiliation:

1. Computational Neuroscience Group, Center for Brain and Cognition, Department of Information and Communication Technologies, Universitat Pompeu Fabra, Barcelona, Catalonia, Spain

2. Cognitive Brain Research Unit, Department of Psychology and Logopedics, Faculty of Medicine, University of Helsinki, Helsinki, Finland

3. Centre of Excellence in Music, Mind, Body and Brain, University of Helsinki, Helsinki, Finland

4. School of Health and Rehabilitation Sciences, Queensland Aphasia Research Centre and UQ Centre for Clinical Research, University of Queensland, Brisbane, Australia

5. Department of Neurology, University of Helsinki, and Helsinki University Hospital, Helsinki, Finland

6. Centre for Eudaimonia and Human Flourishing, Linacre College, University of Oxford, Oxford, United Kingdom

7. Department of Psychiatry, University of Oxford, Oxford, United Kingdom

8. Center for Music in the Brain, Department of Clinical Medicine, Aarhus University, Aarhus, Denmark

9. Institució Catalana de la Recerca i Estudis Avançats (ICREA), Barcelona, Catalonia, Spain

Abstract

Abstract It has been previously shown that traumatic brain injury (TBI) is associated with reductions in metastability in large-scale networks in resting-state fMRI (rsfMRI). However, little is known about how TBI affects the local level of synchronization and how this evolves during the recovery trajectory. Here, we applied a novel turbulent dynamics framework to investigate whole-brain dynamics using an rsfMRI dataset from a cohort of moderate to severe TBI patients and healthy controls (HCs). We first examined how several measures related to turbulent dynamics differ between HCs and TBI patients at 3, 6, and 12 months post-injury. We found a significant reduction in these empirical measures after TBI, with the largest change at 6 months post-injury. Next, we built a Hopf whole-brain model with coupled oscillators and conducted in silico perturbations to investigate the mechanistic principles underlying the reduced turbulent dynamics found in the empirical data. A simulated attack was used to account for the effect of focal lesions. This revealed a shift to lower coupling parameters in the TBI dataset and, critically, decreased susceptibility and information-encoding capability. These findings confirm the potential of the turbulent framework to characterize longitudinal changes in whole-brain dynamics and in the reactivity to external perturbations after TBI.

Funder

BdP Programme

H2020 Marie Skłodowska-Curie Actions

Human Brain Mapping Project

Suomen Kulttuurirahasto

Orionin Tutkimussäätiö

Signe ja Ane Gyllenbergin Säätiö

Academy of Finland

H2020 European Research Council

Danish National Research Foundation

Ministerio de Ciencia e Innovación

Publisher

MIT Press

Subject

Applied Mathematics,Artificial Intelligence,Computer Science Applications,General Neuroscience

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