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Symmetry breaking organizes the brain's resting state manifold

. 2024 Dec 30 ; 14 (1) : 31970. [epub] 20241230

Language English Country England, Great Britain Media electronic

Document type Journal Article, Research Support, Non-U.S. Gov't

Grant support
945539 HORIZON EUROPE Framework Programme
ANR-22-PESN-0012 Agence Nationale de la Recherche
ANR-22-PESN-0012 Agence Nationale de la Recherche

Links

PubMed 39738729
PubMed Central PMC11686292
DOI 10.1038/s41598-024-83542-w
PII: 10.1038/s41598-024-83542-w
Knihovny.cz E-resources

Spontaneously fluctuating brain activity patterns that emerge at rest have been linked to the brain's health and cognition. Despite detailed descriptions of the spatio-temporal brain patterns, our understanding of their generative mechanism is still incomplete. Using a combination of computational modeling and dynamical systems analysis we provide a mechanistic description of the formation of a resting state manifold via the network connectivity. We demonstrate that the symmetry breaking by the connectivity creates a characteristic flow on the manifold, which produces the major data features across scales and imaging modalities. These include spontaneous high-amplitude co-activations, neuronal cascades, spectral cortical gradients, multistability, and characteristic functional connectivity dynamics. When aggregated across cortical hierarchies, these match the profiles from empirical data. The understanding of the brain's resting state manifold is fundamental for the construction of task-specific flows and manifolds used in theories of brain function. In addition, it shifts the focus from the single recordings towards the brain's capacity to generate certain dynamics characteristic of health and pathology.

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Honey, C. J., Kötter, R., Breakspear, M. & Sporns, O. Network structure of cerebral cortex shapes functional connectivity on multiple time scales. Proc. Natl. Acad. Sci. U.S.A.104, 10240–10245 (2007). PubMed PMC

Ghosh, A., Rho, Y., McIntosh, A. R., Kötter, R. & Jirsa, V. K. Noise during rest enables the exploration of the brain’s dynamic repertoire. PLoS Comput. Biol.4, e1000196 (2008). PubMed PMC

Deco, G., Jirsa, V. K. & McIntosh, A. R. Resting brains never rest: Computational insights into potential cognitive architectures. Trends Neurosci.36, 268–274 (2013). PubMed

Cabral, J., Kringelbach, M. L. & Deco, G. Functional connectivity dynamically evolves on multiple time-scales over a static structural connectome: Models and mechanisms. Neuroimage160, 84–96 (2017). PubMed

Gusnard, D. A., Raichle, M. E. & Raichle, M. E. Searching for a baseline: Functional imaging and the resting human brain. Nat. Rev. Neurosci.2, 685–694 (2001). PubMed

Damoiseaux, J. S. et al. Consistent resting-state networks across healthy subjects. Proc. Natl. Acad. Sci. U.S.A.103, 13848–13853 (2006). PubMed PMC

Deco, G., Jirsa, V. K. & McIntosh, A. R. Emerging concepts for the dynamical organization of resting-state activity in the brain. Nat. Rev. Neurosci.12, 43–56 (2011). PubMed

Hutchison, R. M. et al. Dynamic functional connectivity: Promise, issues, and interpretations. Neuroimage80, 360–378 (2013). PubMed PMC

Preti, M. G., Bolton, T. A. & Van De Ville, D. The dynamic functional connectome: State-of-the-art and perspectives. Neuroimage160, 41–54 (2017). PubMed

Shine, J. M. et al. The dynamics of functional brain networks: Integrated network states during cognitive task performance. Neuron92, 544–554 (2016). PubMed PMC

Cavanna, F., Vilas, M. G., Palmucci, M. & Tagliazucchi, E. Dynamic functional connectivity and brain metastability during altered states of consciousness. Neuroimage180, 383–395 (2018). PubMed

Battaglia, D. et al. Dynamic functional connectivity between order and randomness and its evolution across the human adult lifespan. Neuroimage222, 117156 (2020). PubMed

Petkoski, S., Ritter, P. & Jirsa, V. K. White-matter degradation and dynamical compensation support age-related functional alterations in human brain. Cereb. Cortexbhac500, 1–16 (2023). PubMed PMC

Braun, U. et al. From maps to multi-dimensional network mechanisms of mental disorders. Neuron97, 14–31 (2018). PubMed PMC

Jones, D. T. et al. Non-stationarity in the "resting brain’s" modular architecture. PLoS ONE7, e39731 (2012). PubMed PMC

Zalesky, A., Fornito, A., Cocchi, L., Gollo, L. L. & Breakspear, M. Time-resolved resting-state brain networks. Proc. Natl. Acad. Sci. USA111, 10341–10346 (2014). PubMed PMC

Baker, A. P. et al. Fast transient networks in spontaneous human brain activity. Elife3, e01867 (2014). PubMed PMC

Beim Graben, P. et al. Metastable resting state brain dynamics. Front. Comput. Neurosci.13, 62 (2019). PubMed PMC

Tagliazucchi, E., Balenzuela, P., Fraiman, D. & Chialvo, D. R. Criticality in large-scale brain FMRI dynamics unveiled by a novel point process analysis. Front. Physiol.3, 15 (2012). PubMed PMC

Liu, X., Zhang, N., Chang, C. & Duyn, J. H. Co-activation patterns in resting-state fMRI signals. Neuroimage180, 485–494 (2018). PubMed PMC

Esfahlani, F. Z. et al. High-amplitude cofluctuations in cortical activity drive functional connectivity. Proc. Natl. Acad. Sci. USA117, 28393–28401 (2020). PubMed PMC

Gu, Y. et al. Brain activity fluctuations propagate as waves traversing the cortical hierarchy. Cereb. Cortex31, 3986–4005 (2021). PubMed PMC

Mišić, B. et al. Network-level structure-function relationships in human neocortex. Cereb. Cortex26, 3285–3296 (2016). PubMed PMC

Breakspear, M. Dynamic models of large-scale brain activity. Nat. Neurosci.20, 340–352 (2017). PubMed

O’Byrne, J. & Jerbi, K. How critical is brain criticality?. Trends Neurosci.45(11), 820–837 (2022). PubMed

Deco, G., Jirsa, V., McIntosh, A. R., Sporns, O. & Kötter, R. Key role of coupling, delay, and noise in resting brain fluctuations. Proc. Natl. Acad. Sci. USA106, 10302–10307 (2009). PubMed PMC

Deco, G. et al. Dynamical consequences of regional heterogeneity in the brain’s transcriptional landscape. Sci. Adv.7, eabf4752 (2021). PubMed PMC

Melozzi, F. et al. Individual structural features constrain the mouse functional connectome. Proc. Natl. Acad. Sci. USA116(52), 26961–26969 (2019). PubMed PMC

Shine, J. M. et al. The dynamic basis of cognition: an integrative core under the control of the ascending neuromodulatory system (2018).

Roberts, J. A. et al. Metastable brain waves. Nat. Commun.10, 1056 (2019). PubMed PMC

Courtiol, J., Guye, M., Bartolomei, F., Petkoski, S. & Jirsa, V. K. Dynamical mechanisms of interictal resting-state functional connectivity in epilepsy. J. Neurosci.40, 5572–5588 (2020). PubMed PMC

Hansen, E. C. A., Battaglia, D., Spiegler, A., Deco, G. & Jirsa, V. K. Functional connectivity dynamics: Modeling the switching behavior of the resting state. Neuroimage105, 525–535 (2015). PubMed

Machamer, P., Darden, L. & Craver, C. F. Thinking about mechanisms. Philos. Sci.67, 1–25 (2000).

Jirsa, V. in Selbstorganisation–ein Paradigma f ü r die Humanwissenschaften 89–102 (Springer, 2020).

Pillai, A. S. & Jirsa, V. K. Symmetry breaking in space-time hierarchies shapes brain dynamics and behavior. Neuron94, 1010–1026 (2017). PubMed

Huys, R., Perdikis, D. & Jirsa, V. K. Functional architectures and structured flows on manifolds: A dynamical framework for motor behavior. Psychol. Rev.121, 302–336 (2014). PubMed

McIntosh, A. R. & Jirsa, V. K. The hidden repertoire of brain dynamics and dysfunction. Netw Neurosci3, 994–1008 (2019). PubMed PMC

Woodman, M. M. & Jirsa, V. K. Emergent dynamics from spiking neuron networks through symmetry breaking of connectivity. PLoS ONE8, e64339 (2013). PubMed PMC

Watanabe, T. et al. A pairwise maximum entropy model accurately describes resting-state human brain networks. Nat. Commun.4, 1–10 (2013). PubMed PMC

Watanabe, T. et al. Energy landscapes of resting-state brain networks. Front. Neuroinform.8, 12 (2014). PubMed PMC

Gu, S. et al. The energy landscape of neurophysiological activity implicit in brain network structure. Sci. Rep.8, 2507 (2018). PubMed PMC

Ashourvan, A., Gu, S., Mattar, M. G., Vettel, J. M. & Bassett, D. S. The energy landscape underpinning module dynamics in the human brain connectome. Neuroimage157, 364–380 (2017). PubMed PMC

Vohryzek, J., Deco, G., Cessac, B., Kringelbach, M. L. & Cabral, J. Ghost attractors in spontaneous brain activity: Recurrent excursions into functionally-relevant BOLD phase-locking states. Front. Syst. Neurosci.14, 20 (2020). PubMed PMC

Rabuffo, G., Fousek, J., Bernard, C. & Jirsa, V. Neuronal Cascades shape whole-brain functional dynamics at rest. eNeuro8 (2021). PubMed PMC

Cornblath, E. J. et al. Temporal sequences of brain activity at rest are constrained by white matter structure and modulated by cognitive demands. Commun. Biol.3, 261 (2020). PubMed PMC

Wong, K.-F. & Wang, X.-J. A recurrent network mechanism of time integration in perceptual decisions. J. Neurosci.26, 1314–1328 (2006). PubMed PMC

Sanz-Leon, P. et al. The Virtual Brain: A simulator of primate brain network dynamics. Front. Neuroinf.7, 10 (2013). PubMed PMC

Montbrió, E., Pazó, D. & Roxin, A. Macroscopic description for networks of spiking neurons. Phys. Rev. X5, 021028 (2015).

Van Essen, D. C. et al. The WU-Minn human connectome project: An overview. Neuroimage80, 62–79 (2013). PubMed PMC

Stephan, K. E., Weiskopf, N., Drysdale, P. M., Robinson, P. A. & Friston, K. J. Comparing hemodynamic models with DCM. Neuroimage38, 387–401 (2007). PubMed PMC

Lurie, D. J. et al. Questions and controversies in the study of time-varying functional connectivity in resting fMRI. Netw. Neurosci.4, 30–69 (2020). PubMed PMC

Schirner, M., McIntosh, A. R., Jirsa, V., Deco, G. & Ritter, P. Hybrid brain model data. 10.17605/OSF.IO/MNDT8. Available at Open Science Framework Repository under a CC0 1.0 Universal license (2017).

Tenenbaum, J. B., de Silva, V. & Langford, J. C. A global geometric framework for nonlinear dimensionality reduction. Science290(2319–2323), 1095–9203. 10.1126/science.290.5500.2319 (2000). PubMed

Mesulam, M. M. From sensation to cognition. Brain121(Pt 6), 1013–1052 (1998). PubMed

Suárez, L. E., Markello, R. D., Betzel, R. F. & Misic, B. Linking structure and function in macroscale brain networks. Trends Cogn. Sci.24, 302–315. 10.1016/j.tics.2020.01.008 (2020). PubMed

Margulies, D. S. et al. Situating the default-mode network along a principal gradient of macroscale cortical organization. Proc. Natl. Acad. Sci. USA113, 12574–12579 (2016). PubMed PMC

Beggs, J. M. & Plenz, D. Neuronal avalanches in neocortical circuits. J. Neurosci.23, 11167–11177 (2003). PubMed PMC

Deco, G. & Jirsa, V. K. Ongoing cortical activity at rest: Criticality, multistability, and ghost attractors. J. Neurosci.32, 3366–3375 (2012). PubMed PMC

Haimovici, A., Tagliazucchi, E., Balenzuela, P. & Chialvo, D. R. Brain organization into resting state networks emerges at criticality on a model of the human connectome. Phys. Rev. Lett.110, 178101 (2013). PubMed

Sporns, O., Faskowitz, J., Teixeira, A. S., Cutts, S. A. & Betzel, R. F. Dynamic expression of brain functional systems disclosed by fine-scale analysis of edge time series. Netw. Neurosci.5, 405–433 (2021). PubMed PMC

Pope, M., Fukushima, M., Betzel, R. F. & Sporns, O. Modular origins of high-amplitude cofluctuations in fine-scale functional connectivity dynamics. Proc. Natl. Acad. Sci. USA118, e2109380118 (2021). PubMed PMC

Cocchi, L., Gollo, L. L., Zalesky, A. & Breakspear, M. Criticality in the brain: A synthesis of neurobiology, models and cognition. Prog. Neurobiol.158, 132–152 (2017). PubMed

Kong, X. et al. Sensory-motor cortices shape functional connectivity dynamics in the human brain. Nat. Commun.12, 6373 (2021). PubMed PMC

Fox, M. D. & Raichle, M. E. Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat. Rev. Neurosci.8, 700–711 (2007). PubMed

Mitra, A. et al. Spontaneous infra-slow brain activity has unique spatiotemporal dynamics and laminar structure. Neuron98, 297–305 (2018). PubMed PMC

Huntenburg, J. M., Bazin, P.-L. & Margulies, D. S. Large-scale gradients in human cortical organization. Trends Cogn. Sci.22, 21–31 (2018). PubMed

Ashwin, P., Creaser, J. & Tsaneva-Atanasova, K. Fast and slow domino regimes in transient network dynamics. Phys. Rev. E96, 052309 (2017). PubMed

Ashwin, P., Creaser, J. & Tsaneva-Atanasova, K. Sequential escapes: Onset of slow domino regime via a saddle connection. Eur. Phys. J. Spec. Top.227, 1091–1100 (2018).

Deco, G., Senden, M. & Jirsa, V. How anatomy shapes dynamics: A semi-analytical study of the brain at rest by a simple spin model. Front. Comput. Neurosci.6, 68 (2012). PubMed PMC

Kim, J., Joshi, A., Frank, L. & Ganguly, K. Cortical–hippocampal coupling during manifold exploration in motor cortex. Nature (2022). PubMed PMC

Chaudhuri, R., Gerçek, B., Pandey, B., Peyrache, A. & Fiete, I. The intrinsic attractor manifold and population dynamics of a canonical cognitive circuit across waking and sleep. Nat. Neurosci.22, 1512–1520 (2019). PubMed

Favaretto, C. et al. Subcortical-cortical dynamical states of the human brain and their breakdown in stroke. Nat. Commun.13, 5069 (2022). PubMed PMC

Rué-Queralt, J. et al. Decoding brain states on the intrinsic manifold of human brain dynamics across wakefulness and sleep. Commun. Biol.4, 1–11 (2021). PubMed PMC

Gao, S., Mishne, G. & Scheinost, D. Nonlinear manifold learning in functional magnetic resonance imaging uncovers a low-dimensional space of brain dynamics. Hum. Brain Mapp.42, 4510–4524 (2021). PubMed PMC

Michel, C. M. & Koenig, T. EEG microstates as a tool for studying the temporal dynamics of whole-brain neuronal networks: A review. Neuroimage180, 577–593 (2018). PubMed

Britz, J., Van De Ville, D. & Michel, C. M. BOLD correlates of EEG topography reveal rapid resting-state network dynamics. Neuroimage52, 1162–1170 (2010). PubMed

Bréchet, L. et al. Capturing the spatiotemporal dynamics of self-generated, task-initiated thoughts with EEG and fMRI. Neuroimage194, 82–92 (2019). PubMed

Drew, P. J., Mateo, C., Turner, K. L., Yu, X. & Kleinfeld, D. Ultra-slow oscillations in fMRI and resting-state connectivity: Neuronal and vascular contributions and technical confounds. Neuron107, 782–804 (2020). PubMed PMC

Wang, X.-J. Macroscopic gradients of synaptic excitation and inhibition in the neocortex. Nat. Rev. Neurosci.21, 169–178 (2020). PubMed PMC

Chaudhuri, R., Knoblauch, K., Gariel, M. A., Kennedy, H. & Wang, X. J. A large-scale circuit mechanism for hierarchical dynamical processing in the primate cortex. Neuron88, 419–431 (2015). PubMed PMC

Wang, P. et al. Inversion of a large-scale circuit model reveals a cortical hierarchy in the dynamic resting human brain. Sci. Adv.5, eaat7854 (2019). PubMed PMC

Shine, J. M. The thalamus integrates the macrosystems of the brain to facilitate complex, adaptive brain network dynamics (2020). PubMed

Kringelbach, M. L. et al. Dynamic coupling of whole-brain neuronal and neurotransmitter systems. Proc. Natl. Acad. Sci.117, 9566–9576 (2020). PubMed PMC

Aquino, K. M. et al. On the intersection between data quality and dynamical modelling of large-scale fMRI signals. Neuroimage256, 119051 (2022). PubMed

Van De Ville, D., Farouj, Y., Preti, M. G., Liégeois, R. & Amico, E. When makes you unique: Temporality of the human brain fingerprint. Sci. Adv.7, eabj0751 (2021). PubMed PMC

Palva, J. M. & Palva, S. Infra-slow fluctuations in electrophysiological recordings, blood-oxygenation-level-dependent signals, and psychophysical time series. Neuroimage62, 2201–2211 (2012). PubMed

Destexhe, A., Hughes, S. W., Rudolph, M. & Crunelli, V. Are corticothalamic ‘up’states fragments of wakefulness?. Trends Neurosci.30, 334–342 (2007). PubMed PMC

Lavanga, M. et al. The virtual aging brain: Causal inference supports interhemispheric dedifferentiation in healthy aging. Neuroimage283, 120403 (2023). PubMed

Amunts, K., Mohlberg, H., Bludau, S. & Zilles, K. Julich-Brain: A 3D probabilistic atlas of the human brain’s cytoarchitecture. Science369, 988–992 (2020). PubMed

Schirner, M. et al. Brain simulation as a cloud service: The Virtual Brain on EBRAINS. Neuroimage251, 118973 (2022). PubMed

Müller, E. J., Munn, B. R. & Shine, J. M. Diffuse neural coupling mediates complex network dynamics through the formation of quasi-critical brain states. Nat. Commun.11, 6337 (2020). PubMed PMC

Munn, B. R., Müller, E. J., Wainstein, G. & Shine, J. M. The ascending arousal system shapes neural dynamics to mediate awareness of cognitive states. Nat. Commun.12, 6016 (2021). PubMed PMC

Cisek, P. Resynthesizing behavior through phylogenetic refinement. Atten. Percept. Psychophys.81, 2265–2287 (2019). PubMed PMC

Domhof, J. W. M., Jung, K., Eickhoff, S. B. & Popovych, O. V. Parcellation-induced variation of empirical and simulated brain connectomes at group and subject levels. Netw. Neurosci.5, 798–830 (2021). PubMed PMC

Hashemi, M. et al. Simulation-based inference on virtual brain models of disorders. Mach. Learn. Sci. Technol.5, 035019 (2024).

Sanz-Leon, P., Knock, S. A., Spiegler, A. & Jirsa, V. K. Mathematical framework for large-scale brain network modeling in The Virtual Brain. Neuroimage111, 385–430 (2015). PubMed

Trebaul, L. et al. Probabilistic functional tractography of the human cortex revisited. Neuroimage181, 414–429 (2018). PubMed PMC

Desikan, R. S. et al. An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage31, 968–980 (2006). PubMed

Allen, E. A. et al. Tracking whole-brain connectivity dynamics in the resting state. Cereb. Cortex24, 663–676 (2014). PubMed PMC

Preti, M. G. & Van De Ville, D. Decoupling of brain function from structure reveals regional behavioral specialization in humans. Nat. Commun.10, 4747 (2019). PubMed PMC

Yamapi, R., Filatrella, G. & Aziz-Alaoui, M. A. Global stability analysis of birhythmicity in a self-sustained oscillator. Chaos20, 013114 (2010). PubMed

Vos de Wael, R. BrainSpace: A toolbox for the analysis of macroscale gradients in neuroimaging and connectomics datasets. Commun. Biol.3, 103 (2020). PubMed PMC

Domhof, J. W. M., Jung, K., Eickhoff, S. B. & Popovych, O. V. Parcellation-based resting-state blood-oxygen-level-dependent (BOLD) signals of a healthy cohort (v1.0) (2022).

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