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.

Central European Institute of Technology Masaryk University Brno Czech Republic

Department of Neurology University of Minnesota Minneapolis MN USA

Department of Psychiatry and Behavioral Sciences University of Minnesota Minneapolis MN USA

INSERM INS Institut de Neurosciences des Systèmes Aix Marseille University 13005 Marseille France

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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. PubMed DOI 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. PubMed DOI PMC

Deco, G., Jirsa, V. K. & McIntosh, A. R. Resting brains never rest: Computational insights into potential cognitive architectures. PubMed DOI

Cabral, J., Kringelbach, M. L. & Deco, G. Functional connectivity dynamically evolves on multiple time-scales over a static structural connectome: Models and mechanisms. PubMed DOI

Gusnard, D. A., Raichle, M. E. & Raichle, M. E. Searching for a baseline: Functional imaging and the resting human brain. PubMed DOI

Damoiseaux, J. S. et al. Consistent resting-state networks across healthy subjects. PubMed DOI PMC

Deco, G., Jirsa, V. K. & McIntosh, A. R. Emerging concepts for the dynamical organization of resting-state activity in the brain. PubMed DOI

Hutchison, R. M. et al. Dynamic functional connectivity: Promise, issues, and interpretations. PubMed DOI PMC

Preti, M. G., Bolton, T. A. & Van De Ville, D. The dynamic functional connectome: State-of-the-art and perspectives. PubMed DOI

Shine, J. M. et al. The dynamics of functional brain networks: Integrated network states during cognitive task performance. PubMed DOI PMC

Cavanna, F., Vilas, M. G., Palmucci, M. & Tagliazucchi, E. Dynamic functional connectivity and brain metastability during altered states of consciousness. PubMed DOI

Battaglia, D. et al. Dynamic functional connectivity between order and randomness and its evolution across the human adult lifespan. PubMed DOI

Petkoski, S., Ritter, P. & Jirsa, V. K. White-matter degradation and dynamical compensation support age-related functional alterations in human brain. PubMed PMC

Braun, U. et al. From maps to multi-dimensional network mechanisms of mental disorders. PubMed DOI PMC

Jones, D. T. et al. Non-stationarity in the "resting brain’s" modular architecture. PubMed DOI PMC

Zalesky, A., Fornito, A., Cocchi, L., Gollo, L. L. & Breakspear, M. Time-resolved resting-state brain networks. PubMed DOI PMC

Baker, A. P. et al. Fast transient networks in spontaneous human brain activity. PubMed DOI PMC

Beim Graben, P. et al. Metastable resting state brain dynamics. PubMed DOI PMC

Tagliazucchi, E., Balenzuela, P., Fraiman, D. & Chialvo, D. R. Criticality in large-scale brain FMRI dynamics unveiled by a novel point process analysis. PubMed DOI PMC

Liu, X., Zhang, N., Chang, C. & Duyn, J. H. Co-activation patterns in resting-state fMRI signals. PubMed DOI PMC

Esfahlani, F. Z. et al. High-amplitude cofluctuations in cortical activity drive functional connectivity. PubMed DOI PMC

Gu, Y. et al. Brain activity fluctuations propagate as waves traversing the cortical hierarchy. PubMed DOI PMC

Mišić, B. et al. Network-level structure-function relationships in human neocortex. PubMed DOI PMC

Breakspear, M. Dynamic models of large-scale brain activity. PubMed DOI

O’Byrne, J. & Jerbi, K. How critical is brain criticality?. PubMed DOI

Deco, G., Jirsa, V., McIntosh, A. R., Sporns, O. & Kötter, R. Key role of coupling, delay, and noise in resting brain fluctuations. PubMed DOI PMC

Deco, G. et al. Dynamical consequences of regional heterogeneity in the brain’s transcriptional landscape. PubMed DOI PMC

Melozzi, F. et al. Individual structural features constrain the mouse functional connectome. PubMed DOI PMC

Shine, J. M. et al.

Roberts, J. A. et al. Metastable brain waves. PubMed DOI PMC

Courtiol, J., Guye, M., Bartolomei, F., Petkoski, S. & Jirsa, V. K. Dynamical mechanisms of interictal resting-state functional connectivity in epilepsy. PubMed DOI 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. PubMed DOI

Machamer, P., Darden, L. & Craver, C. F. Thinking about mechanisms. DOI

Jirsa, V. in

Pillai, A. S. & Jirsa, V. K. Symmetry breaking in space-time hierarchies shapes brain dynamics and behavior. PubMed DOI

Huys, R., Perdikis, D. & Jirsa, V. K. Functional architectures and structured flows on manifolds: A dynamical framework for motor behavior. PubMed DOI

McIntosh, A. R. & Jirsa, V. K. The hidden repertoire of brain dynamics and dysfunction. PubMed DOI PMC

Woodman, M. M. & Jirsa, V. K. Emergent dynamics from spiking neuron networks through symmetry breaking of connectivity. PubMed DOI PMC

Watanabe, T. et al. A pairwise maximum entropy model accurately describes resting-state human brain networks. PubMed DOI PMC

Watanabe, T. et al. Energy landscapes of resting-state brain networks. PubMed DOI PMC

Gu, S. et al. The energy landscape of neurophysiological activity implicit in brain network structure. PubMed DOI 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. PubMed DOI 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. PubMed DOI PMC

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

Wong, K.-F. & Wang, X.-J. A recurrent network mechanism of time integration in perceptual decisions. PubMed DOI PMC

Sanz-Leon, P. et al. The Virtual Brain: A simulator of primate brain network dynamics. PubMed DOI PMC

Montbrió, E., Pazó, D. & Roxin, A. Macroscopic description for networks of spiking neurons.

Van Essen, D. C. et al. The WU-Minn human connectome project: An overview. PubMed DOI PMC

Stephan, K. E., Weiskopf, N., Drysdale, P. M., Robinson, P. A. & Friston, K. J. Comparing hemodynamic models with DCM. PubMed DOI PMC

Lurie, D. J. et al. Questions and controversies in the study of time-varying functional connectivity in resting fMRI. PubMed DOI 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. PubMed DOI

Mesulam, M. M. From sensation to cognition. PubMed DOI

Suárez, L. E., Markello, R. D., Betzel, R. F. & Misic, B. Linking structure and function in macroscale brain networks. PubMed DOI

Margulies, D. S. et al. Situating the default-mode network along a principal gradient of macroscale cortical organization. PubMed DOI PMC

Beggs, J. M. & Plenz, D. Neuronal avalanches in neocortical circuits. PubMed DOI PMC

Deco, G. & Jirsa, V. K. Ongoing cortical activity at rest: Criticality, multistability, and ghost attractors. PubMed DOI 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. PubMed DOI

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. PubMed DOI PMC

Pope, M., Fukushima, M., Betzel, R. F. & Sporns, O. Modular origins of high-amplitude cofluctuations in fine-scale functional connectivity dynamics. PubMed DOI PMC

Cocchi, L., Gollo, L. L., Zalesky, A. & Breakspear, M. Criticality in the brain: A synthesis of neurobiology, models and cognition. PubMed DOI

Kong, X. et al. Sensory-motor cortices shape functional connectivity dynamics in the human brain. PubMed DOI PMC

Fox, M. D. & Raichle, M. E. Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. PubMed DOI

Mitra, A. et al. Spontaneous infra-slow brain activity has unique spatiotemporal dynamics and laminar structure. PubMed DOI PMC

Huntenburg, J. M., Bazin, P.-L. & Margulies, D. S. Large-scale gradients in human cortical organization. PubMed DOI

Ashwin, P., Creaser, J. & Tsaneva-Atanasova, K. Fast and slow domino regimes in transient network dynamics. PubMed DOI

Ashwin, P., Creaser, J. & Tsaneva-Atanasova, K. Sequential escapes: Onset of slow domino regime via a saddle connection. DOI

Deco, G., Senden, M. & Jirsa, V. How anatomy shapes dynamics: A semi-analytical study of the brain at rest by a simple spin model. PubMed DOI PMC

Kim, J., Joshi, A., Frank, L. & Ganguly, K. Cortical–hippocampal coupling during manifold exploration in motor cortex. 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. PubMed DOI

Favaretto, C. et al. Subcortical-cortical dynamical states of the human brain and their breakdown in stroke. PubMed DOI PMC

Rué-Queralt, J. et al. Decoding brain states on the intrinsic manifold of human brain dynamics across wakefulness and sleep. PubMed DOI PMC

Gao, S., Mishne, G. & Scheinost, D. Nonlinear manifold learning in functional magnetic resonance imaging uncovers a low-dimensional space of brain dynamics. PubMed DOI PMC

Michel, C. M. & Koenig, T. EEG microstates as a tool for studying the temporal dynamics of whole-brain neuronal networks: A review. PubMed DOI

Britz, J., Van De Ville, D. & Michel, C. M. BOLD correlates of EEG topography reveal rapid resting-state network dynamics. PubMed DOI

Bréchet, L. et al. Capturing the spatiotemporal dynamics of self-generated, task-initiated thoughts with EEG and fMRI. PubMed DOI

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. PubMed DOI PMC

Wang, X.-J. Macroscopic gradients of synaptic excitation and inhibition in the neocortex. PubMed DOI 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. PubMed DOI PMC

Wang, P. et al. Inversion of a large-scale circuit model reveals a cortical hierarchy in the dynamic resting human brain. PubMed DOI PMC

Shine, J. M. PubMed

Kringelbach, M. L. et al. Dynamic coupling of whole-brain neuronal and neurotransmitter systems. PubMed DOI PMC

Aquino, K. M. et al. On the intersection between data quality and dynamical modelling of large-scale fMRI signals. PubMed DOI

Van De Ville, D., Farouj, Y., Preti, M. G., Liégeois, R. & Amico, E. When makes you unique: Temporality of the human brain fingerprint. PubMed DOI PMC

Palva, J. M. & Palva, S. Infra-slow fluctuations in electrophysiological recordings, blood-oxygenation-level-dependent signals, and psychophysical time series. PubMed DOI

Destexhe, A., Hughes, S. W., Rudolph, M. & Crunelli, V. Are corticothalamic ‘up’states fragments of wakefulness?. PubMed DOI PMC

Lavanga, M. et al. The virtual aging brain: Causal inference supports interhemispheric dedifferentiation in healthy aging. PubMed DOI

Amunts, K., Mohlberg, H., Bludau, S. & Zilles, K. Julich-Brain: A 3D probabilistic atlas of the human brain’s cytoarchitecture. PubMed DOI

Schirner, M. et al. Brain simulation as a cloud service: The Virtual Brain on EBRAINS. PubMed DOI

Müller, E. J., Munn, B. R. & Shine, J. M. Diffuse neural coupling mediates complex network dynamics through the formation of quasi-critical brain states. PubMed DOI 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. PubMed DOI PMC

Cisek, P. Resynthesizing behavior through phylogenetic refinement. PubMed DOI 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. PubMed DOI PMC

Hashemi, M. et al. Simulation-based inference on virtual brain models of disorders. DOI

Sanz-Leon, P., Knock, S. A., Spiegler, A. & Jirsa, V. K. Mathematical framework for large-scale brain network modeling in The Virtual Brain. PubMed DOI

Trebaul, L. et al. Probabilistic functional tractography of the human cortex revisited. PubMed DOI 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. PubMed DOI

Allen, E. A. et al. Tracking whole-brain connectivity dynamics in the resting state. PubMed DOI PMC

Preti, M. G. & Van De Ville, D. Decoupling of brain function from structure reveals regional behavioral specialization in humans. PubMed DOI PMC

Yamapi, R., Filatrella, G. & Aziz-Alaoui, M. A. Global stability analysis of birhythmicity in a self-sustained oscillator. PubMed DOI

Vos de Wael, R. BrainSpace: A toolbox for the analysis of macroscale gradients in neuroimaging and connectomics datasets. PubMed DOI PMC

Domhof, J. W. M., Jung, K., Eickhoff, S. B. & Popovych, O. V.

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