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      Neuronal Networks during Burst Suppression as Revealed by Source Analysis

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          Abstract

          Introduction

          Burst-suppression (BS) is an electroencephalography (EEG) pattern consisting of alternant periods of slow waves of high amplitude (burst) and periods of so called flat EEG (suppression). It is generally associated with coma of various etiologies (hypoxia, drug-related intoxication, hypothermia, and childhood encephalopathies, but also anesthesia). Animal studies suggest that both the cortex and the thalamus are involved in the generation of BS. However, very little is known about mechanisms of BS in humans. The aim of this study was to identify the neuronal network underlying both burst and suppression phases using source reconstruction and analysis of functional and effective connectivity in EEG.

          Material/Methods

          Dynamic imaging of coherent sources (DICS) was applied to EEG segments of 13 neonates and infants with burst and suppression EEG pattern. The brain area with the strongest power in the analyzed frequency (1–4 Hz) range was defined as the reference region. DICS was used to compute the coherence between this reference region and the entire brain. The renormalized partial directed coherence (RPDC) was used to describe the informational flow between the identified sources.

          Results/Conclusion

          Delta activity during the burst phases was associated with coherent sources in the thalamus and brainstem as well as bilateral sources in cortical regions mainly frontal and parietal, whereas suppression phases were associated with coherent sources only in cortical regions. Results of the RPDC analyses showed an upwards informational flow from the brainstem towards the thalamus and from the thalamus to cortical regions, which was absent during the suppression phases. These findings may support the theory that a “cortical deafferentiation” between the cortex and sub-cortical structures exists especially in suppression phases compared to burst phases in burst suppression EEGs. Such a deafferentiation may play a role in the poor neurological outcome of children with these encephalopathies.

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          Most cited references53

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          Identifying true brain interaction from EEG data using the imaginary part of coherency.

          The main obstacle in interpreting EEG/MEG data in terms of brain connectivity is the fact that because of volume conduction, the activity of a single brain source can be observed in many channels. Here, we present an approach which is insensitive to false connectivity arising from volume conduction. We show that the (complex) coherency of non-interacting sources is necessarily real and, hence, the imaginary part of coherency provides an excellent candidate to study brain interactions. Although the usual magnitude and phase of coherency contain the same information as the real and imaginary parts, we argue that the Cartesian representation is far superior for studying brain interactions. The method is demonstrated for EEG measurements of voluntary finger movement. We found: (a) from 5 s before to movement onset a relatively weak interaction around 20 Hz between left and right motor areas where the contralateral side leads the ipsilateral side; and (b) approximately 2-4 s after movement, a stronger interaction also at 20 Hz in the opposite direction. It is possible to reliably detect brain interaction during movement from EEG data. The method allows unambiguous detection of brain interaction from rhythmic EEG/MEG data.
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            Dynamic imaging of coherent sources: Studying neural interactions in the human brain.

            Functional connectivity between cortical areas may appear as correlated time behavior of neural activity. It has been suggested that merging of separate features into a single percept ("binding") is associated with coherent gamma band activity across the cortical areas involved. Therefore, it would be of utmost interest to image cortico-cortical coherence in the working human brain. The frequency specificity and transient nature of these interactions requires time-sensitive tools such as magneto- or electroencephalography (MEG/EEG). Coherence between signals of sensors covering different scalp areas is commonly taken as a measure of functional coupling. However, this approach provides vague information on the actual cortical areas involved, owing to the complex relation between the active brain areas and the sensor recordings. We propose a solution to the crucial issue of proceeding beyond the MEG sensor level to estimate coherences between cortical areas. Dynamic imaging of coherent sources (DICS) uses a spatial filter to localize coherent brain regions and provides the time courses of their activity. Reference points for the computation of neural coupling may be based on brain areas of maximum power or other physiologically meaningful information, or they may be estimated starting from sensor coherences. The performance of DICS is evaluated with simulated data and illustrated with recordings of spontaneous activity in a healthy subject and a parkinsonian patient. Methods for estimating functional connectivities between brain areas will facilitate characterization of cortical networks involved in sensory, motor, or cognitive tasks and will allow investigation of pathological connectivities in neurological disorders.
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              Partial directed coherence: a new concept in neural structure determination.

              This paper introduces a new frequency-domain approach to describe the relationships (direction of information flow) between multivariate time series based on the decomposition of multivariate partial coherences computed from multivariate autoregressive models. We discuss its application and compare its performance to other approaches to the problem of determining neural structure relations from the simultaneous measurement of neural electrophysiological signals. The new concept is shown to reflect a frequency-domain representation of the concept of Granger causality.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                30 April 2015
                2015
                : 10
                : 4
                : e0123807
                Affiliations
                [1 ]Department of Neuropediatrics, Christian-Albrechts-University, Kiel, Germany
                [2 ]Department of Neurology, Christian-Albrechts-University, Kiel, Germany
                [3 ]Department of Neurophysiology, Great Ormond Street Hospital for Children, London, United Kingdom
                [4 ]Institute of Medical Psychology and Medical Sociology, Christian-Albrechts-University of Kiel, Kiel, Germany
                University of British Columbia, CANADA
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: NJ CR GD US MS. Performed the experiments: NJ CR MM. Analyzed the data: NJ CR MM ARA KGM. Contributed reagents/materials/analysis tools: RP FM. Wrote the paper: NJ US MS FM.

                Article
                PONE-D-14-50150
                10.1371/journal.pone.0123807
                4415810
                25927439
                7e3da103-7e5c-465e-a246-0156b6d072c5
                Copyright @ 2015

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

                History
                : 12 November 2014
                : 6 March 2015
                Page count
                Figures: 5, Tables: 1, Pages: 18
                Funding
                Funding provided by D3 and D2 subproject of Sonderforschungsbereich (SFB) 855 of the German Science Society (DFG), Japaridze N., Muthuraman M., Anwar A. R.2, Mideksa K. G., Siniatchkin M.4, http://www.sfb855.uni-kiel.de/ and EU FP7 project DESIRE “Development & Epilepsy”, WP2 & WP4, Japaridze N., http://epilepsydesireproject.eu/. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Custom metadata
                Due to ethical restrictions data are available upon request. Interested researchers may submit requests for confidential data to the corresponding author, Natia Japaridze ( n.japaridze@ 123456pedneuro.uni-kiel.de ).

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