Perturbation of whole-brain dynamics in silico reveals mechanistic differences between brain states

Gustavo Deco, Joana Cabral, Victor M. Saenger, Melanie Boly, Enzo Tagliazucchi, Helmut Laufs, Eus Van Someren, Beatrice Jobst, Angus Stevner, Morten L. Kringelbach*

*Corresponding author for this work

Research output: Contribution to JournalArticleAcademicpeer-review

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Abstract

Human neuroimaging research has revealed that wakefulness and sleep involve very different activity patterns. Yet, it is not clear why brain states differ in their dynamical complexity, e.g. in the level of integration and segregation across brain networks over time. Here, we investigate the mechanisms underlying the dynamical stability of brain states using a novel off-line in silico perturbation protocol. We first adjust a whole-brain computational model to the basal dynamics of wakefulness and deep sleep recorded with fMRI in two independent human fMRI datasets. Then, the models of sleep and awake brain states are perturbed using two distinct multifocal protocols either promoting or disrupting synchronization in randomly selected brain areas. Once perturbation is halted, we use a novel measure, the Perturbative Integration Latency Index (PILI), to evaluate the recovery back to baseline. We find a clear distinction between models, consistently showing larger PILI in wakefulness than in deep sleep, corroborating previous experimental findings. In the models, larger recoveries are associated to a critical slowing down induced by a shift in the model's operation point, indicating that the awake brain operates further from a stable equilibrium than deep sleep. This novel approach opens up for a new level of artificial perturbative studies unconstrained by ethical limitations allowing for a deeper investigation of the dynamical properties of different brain states.

Original languageEnglish
Pages (from-to)46-56
Number of pages11
JournalNeuroImage
Volume169
Early online date7 Dec 2017
DOIs
Publication statusPublished - 1 Apr 2018

Funding

GD was supported by the ERC Advanced Grant: DYSTRUCTURE (n. 295129 ), by the Spanish Research Project SAF2010-16085 and the FP7-ICT BrainScales. MLK and JC were supported by the ERC Consolidator Grant: CAREGIVING (n. 615539 ) and Center for Music in the Brain, funded by the Danish National Research Foundation ( DNRF117 ). JC was supported under the project NORTE-01-0145-FEDER-000023, supported by the Northern Portugal Regional Operational Programme ( NORTE 2020 ), under the Portugal 2020 Partnership Agreement, through the European Regional Development Fund (FEDER). Appendix A

FundersFunder number
Center for Music
FP7-ICT Brainscales
Northern Portugal Regional Operational Programme
Seventh Framework Programme615539, 295129, 269921
European Research CouncilSAF2010-16085
Danmarks GrundforskningsfondNORTE-01-0145-FEDER-000023, DNRF117
European Regional Development Fund

    Keywords

    • Brain state
    • Perturbation
    • Sleep
    • Whole brain modeling

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