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

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.

Noelia Martínez-Molina, BdP Programme, Award ID: 2019-BP-00032. Yonatan Sanz-Perl, H2020 Marie Skłodowska-Curie Actions (https://dx.doi.org/10.13039/100010665), Award ID: 896354. Anira Escrichs, Human Brain Mapping Project, Award ID: 945539. Aleksi J. Sihvonen, Suomen Kulttuurirahasto (https://dx.doi.org/10.13039/501100003125), Award ID: 191230. Aleksi J. Sihvonen, Orionin Tutkimussäätiö (https://dx.doi.org/10.13039/501100007083). Aleksi J. Sihvonen, Signe ja Ane Gyllenbergin Säätiö (https://dx.doi.org/10.13039/501100004325). Teppo Särkämö, Academy of Finland (https://dx.doi.org/10.13039/501100002341), Award ID: 338448 & 346211. Teppo Särkämö, H2020 European Research Council (https://dx.doi.org/10.13039/100010663), Award ID: 803466. Morten L. Kringelbach, Danish National Research Foundation, Award ID: DNRF117. Morten L. Kringelbach is the founder of the Centre for Eudaimonia and Human Flourishing at Linacre College, funded by the Pettit and Carlsberg Foundations. Gustavo Deco, Ministerio de Ciencia e Innovación (https://dx.doi.org/10.13039/501100004837), Award ID: PID2019-105772GB-I00 MCIU AEI.