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Emerging concepts for the dynamical organization of resting-state activity in the brain

Nature Reviews Neuroscience volume 12, pages 4356 (2011) | Download Citation

Abstract

A broad body of experimental work has demonstrated that apparently spontaneous brain activity is not random. At the level of large-scale neural systems, as measured with functional MRI (fMRI), this ongoing activity reflects the organization of a series of highly coherent functional networks. These so-called resting-state networks (RSNs) closely relate to the underlying anatomical connectivity but cannot be understood in those terms alone. Here we review three large-scale neural system models of primate neocortex that emphasize the key contributions of local dynamics, signal transmission delays and noise to the emerging RSNs. We propose that the formation and dissolution of resting-state patterns reflects the exploration of possible functional network configurations around a stable anatomical skeleton.

Key points

  • Spontaneous ongoing global activity of the brain at rest is highly structured in spatiotemporal patterns called resting-state networks.

  • Resting-state networks are related to the underlying neuroanatomical structure, but they emerge as a result of the interplay between dynamics and structure.

  • Resting-state networks therefore reflect the intrinsic properties of the brain network. These include neuroanatomical structure, local neuronal dynamics, signal transmission delays and genuine noise.

  • The formation and dissolution of resting-state networks reflects the exploration of possible functional network configurations around a stable anatomical framework.

  • Brain networks generally possess a small-world construction, in which there are multiple ways for different network elements to interact. This anatomical architecture provides the landscape within which different possible network configurations occur. In the absence of external stimulation, noise drives the network dynamics such that the system will visit these network configurations spontaneously.

  • Resting-state networks were originally characterized by indirect and slow measures of neuronal activity (for example, by blood oxygen level-dependent (BOLD) functional MRI (fMRI)). However, it is now clear that large-scale resting-state networks correlate with neuronal rhythms at faster frequencies.

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Acknowledgements

We are grateful for funding received from the James S. McDonnell Foundation (grant Brain NRG [JSMF22002082]).

Author information

Affiliations

  1. Institució Catalana de Recerca i Estudis Avançats (ICREA), Universitat Pompeu Fabra, Computational Neuroscience, Plaça de la Mercè, 10–12, 08002 Barcelona, Spain.

    • Gustavo Deco
  2. Theoretical Neuroscience Group, Institut des Sciences du Mouvement UMR6233 CNRS, Marseille, France, and Center for Complex Systems and Brain Sciences, Physics Department, Florida Atlantic University, USA.

    • Viktor K. Jirsa
  3. Rotman Research Institute of Baycrest Centre, University of Toronto, 3560 Bathurst Street, Toronto, Ontario M6A 2E1 Canada.

    • Anthony R. McIntosh

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Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Gustavo Deco.

Glossary

Oxygen extraction

A quantitative medical imaging method to determine the regional consumption of oxygen in brain tissue.

BOLD fMRI

Blood oxygen level-dependent (BOLD) functional MRI (fMRI) is a relatively new neuroimaging tool to map activity in the brain in vivo. Signal changes are dependent on the relative changes in blood oxygen levels in the brain capillary beds.

Functional connectivity

The relationship between activity in two or more neural sources. This usually refers to the temporal correlation between sources but has been extended to include correlations across trials or different experimental subjects. Functional connectivity methods include estimation of correlation coefficients and coherence. The estimation cannot be used to infer the direction of the relation between sources.

Diffusion spectrum imaging

An MRI technique that is similar to DTI, but with the added capability of resolving multiple directions of diffusion in each voxel of white matter. This allows multiple groups of fibres at each location, including intersecting fibre pathways, to be mapped.

Graph theory

A branch of mathematics that deals with the formal description and analysis of graphs. A graph is defined as a set of nodes (vertices) linked by connections (edges). The connections may be directed or undirected. A graph provides an abstract representation of the system's elements and their interaction.

Small-world architecture

A term derived from graph theory estimation referring to a network that combines high levels of local clustering among nodes (to form families or cliques) and short paths that globally link all nodes of the network.

Diffusion tensor imaging

(Often abbreviated to DTI.) An MRI technique that takes advantage of the restricted diffusion of water through myelinated nerve fibres in the brain to infer the anatomical connectivity between brain areas.

Neural field

Values of neural activity that are defined over a continuous physical space, typically the two- or three-dimensional cortical sheet.

Transient

In dynamical systems this refers to time-dependent states evolving towards an attractor.

Balloon–Windkessel haemodynamic model

A dynamical model in which neural activity (the BOLD signal) is transduced into brain perfusion changes. In this model, the BOLD signal is taken to be a static nonlinear function of normalized total deoxyhaemoglobin voxel content, normalized venous volume, resting net oxygen extraction fraction by the capillary bed and resting blood volume fraction.

Stability

In dynamical systems refers to a state that, if it is perturbed, will return after a time to the same configuration.

Instability

In dynamical systems refers to a state that, if it is perturbed, will escape away from the original configuration.

Carrier wave

A wave of a higher frequency that is modulated with another signal of a lower frequency, typically for the purpose of conveying information.

Hopf bifurcation

In nonlinear dynamics, a local bifurcation in which an initially stable fixed point of a dynamical system loses its stability in an oscillatory fashion.

Attractor

In dynamical systems refers to a set towards which a system evolves. Geometrically, this set may be a point, a curve or a manifold.

Metastability

In dynamical systems refers to a state that falls outside the natural equilibrium state of the system, but that persists for an extended period of time.

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https://doi.org/10.1038/nrn2961

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