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      Criticality in Large-Scale Brain fMRI Dynamics Unveiled by a Novel Point Process Analysis

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          Abstract

          Functional magnetic resonance imaging (fMRI) techniques have contributed significantly to our understanding of brain function. Current methods are based on the analysis of gradual and continuous changes in the brain blood oxygenated level dependent (BOLD) signal. Departing from that approach, recent work has shown that equivalent results can be obtained by inspecting only the relatively large amplitude BOLD signal peaks, suggesting that relevant information can be condensed in discrete events. This idea is further explored here to demonstrate how brain dynamics at resting state can be captured just by the timing and location of such events, i.e., in terms of a spatiotemporal point process. The method allows, for the first time, to define a theoretical framework in terms of an order and control parameter derived from fMRI data, where the dynamical regime can be interpreted as one corresponding to a system close to the critical point of a second order phase transition. The analysis demonstrates that the resting brain spends most of the time near the critical point of such transition and exhibits avalanches of activity ruled by the same dynamical and statistical properties described previously for neuronal events at smaller scales. Given the demonstrated functional relevance of the resting state brain dynamics, its representation as a discrete process might facilitate large-scale analysis of brain function both in health and disease.

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          Most cited references32

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          Correspondence of the brain's functional architecture during activation and rest.

          Neural connections, providing the substrate for functional networks, exist whether or not they are functionally active at any given moment. However, it is not known to what extent brain regions are continuously interacting when the brain is "at rest." In this work, we identify the major explicit activation networks by carrying out an image-based activation network analysis of thousands of separate activation maps derived from the BrainMap database of functional imaging studies, involving nearly 30,000 human subjects. Independently, we extract the major covarying networks in the resting brain, as imaged with functional magnetic resonance imaging in 36 subjects at rest. The sets of major brain networks, and their decompositions into subnetworks, show close correspondence between the independent analyses of resting and activation brain dynamics. We conclude that the full repertoire of functional networks utilized by the brain in action is continuously and dynamically "active" even when at "rest."
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            Geometry from a Time Series

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              Frequencies contributing to functional connectivity in the cerebral cortex in "resting-state" data.

              In subjects performing no specific cognitive task ("resting state"), time courses of voxels within functionally connected regions of the brain have high cross-correlation coefficients ("functional connectivity"). The purpose of this study was to measure the contributions of low frequencies and physiological noise to cross-correlation maps. In four healthy volunteers, task-activation functional MR imaging and resting-state data were acquired. We obtained four contiguous slice locations in the "resting state" with a high sampling rate. Regions of interest consisting of four contiguous voxels were selected. The correlation coefficient for the averaged time course and every other voxel in the four slices was calculated and separated into its component frequency contributions. We calculated the relative amounts of the spectrum that were in the low-frequency (0 to 0.1 Hz), the respiratory-frequency (0.1 to 0.5 Hz), and cardiac-frequency range (0.6 to 1.2 Hz). For each volunteer, resting-state maps that resembled task-activation maps were obtained. For the auditory and visual cortices, the correlation coefficient depended almost exclusively on low frequencies (<0.1 Hz). For all cortical regions studied, low-frequency fluctuations contributed more than 90% of the correlation coefficient. Physiological (respiratory and cardiac) noise sources contributed less than 10% to any functional connectivity MR imaging map. In blood vessels and cerebrospinal fluid, physiological noise contributed more to the correlation coefficient. Functional connectivity in the auditory, visual, and sensorimotor cortices is characterized predominantly by frequencies slower than those in the cardiac and respiratory cycles. In functionally connected regions, these low frequencies are characterized by a high degree of temporal coherence.
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                Author and article information

                Journal
                Front Physiol
                Front Physiol
                Front. Physio.
                Frontiers in Physiology
                Frontiers Research Foundation
                1664-042X
                04 January 2012
                08 February 2012
                2012
                : 3
                : 15
                Affiliations
                [1] 1simpleDepartamento de Física, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires Buenos Aires, Argentina
                [2] 2simpleDepartment of Neurology and Brain Imaging Center, Goethe-University Frankfurt Frankfurt am Main, Germany
                [3] 3simpleConsejo Nacional de Investigaciones Científicas y Tecnológicas Buenos Aires, Argentina
                [4] 4simpleDepartamento de Matemática y Ciencias, Universidad de San Andrés Buenos Aires, Argentina
                [5] 5simpleFacultad de Ciencias Médicas, Universidad Nacional de Rosario Rosario, Argentina
                [6] 6simpleDavid Geffen School of Medicine, University of California Los Angeles Los Angeles, CA, USA
                Author notes

                Edited by: Zbigniew R. Struzik, The University of Tokyo, Japan

                Reviewed by: Riccardo Barbieri, Massachusetts Institute of Technology, USA; Masanori Shimono, Indiana University, USA

                *Correspondence: Dante R. Chialvo, Department of Physiology, Northwestern University, 303 East Chicago Avenue, Chicago, IL 60611, USA. e-mail: dchialvo@ 123456ucla.edu

                This article was submitted to Frontiers in Fractal Physiology, a specialty of Frontiers in Physiology.

                Article
                10.3389/fphys.2012.00015
                3274757
                22347863
                819f22e9-e87d-4280-a659-6ef7a8ce151d
                Copyright © 2012 Tagliazucchi, Balenzuela, Fraiman and Chialvo.

                This is an open-access article distributed under the terms of the Creative Commons Attribution Non Commercial License, which permits non-commercial use, distribution, and reproduction in other forums, provided the original authors and source are credited.

                History
                : 12 December 2011
                : 23 January 2012
                Page count
                Figures: 7, Tables: 1, Equations: 2, References: 61, Pages: 12, Words: 9236
                Categories
                Physiology
                Original Research

                Anatomy & Physiology
                brain dynamics,fmri,point processes,criticality
                Anatomy & Physiology
                brain dynamics, fmri, point processes, criticality

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