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      Individual Human Brain Areas Can Be Identified from Their Characteristic Spectral Activation Fingerprints

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      PLoS Biology
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          Abstract

          The human brain can be parcellated into diverse anatomical areas. We investigated whether rhythmic brain activity in these areas is characteristic and can be used for automatic classification. To this end, resting-state MEG data of 22 healthy adults was analysed. Power spectra of 1-s long data segments for atlas-defined brain areas were clustered into spectral profiles (“fingerprints”), using k-means and Gaussian mixture (GM) modelling. We demonstrate that individual areas can be identified from these spectral profiles with high accuracy. Our results suggest that each brain area engages in different spectral modes that are characteristic for individual areas. Clustering of brain areas according to similarity of spectral profiles reveals well-known brain networks. Furthermore, we demonstrate task-specific modulations of auditory spectral profiles during auditory processing. These findings have important implications for the classification of regional spectral activity and allow for novel approaches in neuroimaging and neurostimulation in health and disease.

          Abstract

          Oscillatory activity in anatomically defined brain areas is organized according to several different spectral modes; these modes are characteristic and can be used for automatic classification.

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          Most cited references34

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          Structural and functional brain networks: from connections to cognition.

          How rich functionality emerges from the invariant structural architecture of the brain remains a major mystery in neuroscience. Recent applications of network theory and theoretical neuroscience to large-scale brain networks have started to dissolve this mystery. Network analyses suggest that hierarchical modular brain networks are particularly suited to facilitate local (segregated) neuronal operations and the global integration of segregated functions. Although functional networks are constrained by structural connections, context-sensitive integration during cognition tasks necessarily entails a divergence between structural and functional networks. This degenerate (many-to-one) function-structure mapping is crucial for understanding the nature of brain networks. The emergence of dynamic functional networks from static structural connections calls for a formal (computational) approach to neuronal information processing that may resolve this dialectic between structure and function.
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            Electrophysiological signatures of resting state networks in the human brain.

            Functional neuroimaging and electrophysiological studies have documented a dynamic baseline of intrinsic (not stimulus- or task-evoked) brain activity during resting wakefulness. This baseline is characterized by slow (<0.1 Hz) fluctuations of functional imaging signals that are topographically organized in discrete brain networks, and by much faster (1-80 Hz) electrical oscillations. To investigate the relationship between hemodynamic and electrical oscillations, we have adopted a completely data-driven approach that combines information from simultaneous electroencephalography (EEG) and functional magnetic resonance imaging (fMRI). Using independent component analysis on the fMRI data, we identified six widely distributed resting state networks. The blood oxygenation level-dependent signal fluctuations associated with each network were correlated with the EEG power variations of delta, theta, alpha, beta, and gamma rhythms. Each functional network was characterized by a specific electrophysiological signature that involved the combination of different brain rhythms. Moreover, the joint EEG/fMRI analysis afforded a finer physiological fractionation of brain networks in the resting human brain. This result supports for the first time in humans the coalescence of several brain rhythms within large-scale brain networks as suggested by biophysical studies.
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              Neural synchrony in brain disorders: relevance for cognitive dysfunctions and pathophysiology.

              Following the discovery of context-dependent synchronization of oscillatory neuronal responses in the visual system, novel methods of time series analysis have been developed for the examination of task- and performance-related oscillatory activity and its synchronization. Studies employing these advanced techniques revealed that synchronization of oscillatory responses in the beta- and gamma-band is involved in a variety of cognitive functions, such as perceptual grouping, attention-dependent stimulus selection, routing of signals across distributed cortical networks, sensory-motor integration, working memory, and perceptual awareness. Here, we review evidence that certain brain disorders, such as schizophrenia, epilepsy, autism, Alzheimer's disease, and Parkinson's are associated with abnormal neural synchronization. The data suggest close correlations between abnormalities in neuronal synchronization and cognitive dysfunctions, emphasizing the importance of temporal coordination. Thus, focused search for abnormalities in temporal patterning may be of considerable clinical relevance.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS Biol
                PLoS Biol
                plos
                plosbiol
                PLoS Biology
                Public Library of Science (San Francisco, CA USA )
                1544-9173
                1545-7885
                29 June 2016
                June 2016
                29 June 2016
                : 14
                : 6
                : e1002498
                Affiliations
                [001]Centre for Cognitive Neuroimaging, Institute of Neuroscience and Psychology, University of Glasgow, Glasgow, United Kingdom
                University Medical Center Hamburg-Eppendorf, GERMANY
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: JG. Analyzed the data: AK JG. Contributed reagents/materials/analysis tools: AK JG. Wrote the paper: AK JG.

                Article
                PBIOLOGY-D-16-00483
                10.1371/journal.pbio.1002498
                4927181
                27355236
                baa4d17d-6e81-45ea-bc8b-2ab17b4ab74f
                © 2016 Keitel, Gross

                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
                : 1 March 2016
                : 2 June 2016
                Page count
                Figures: 6, Tables: 0, Pages: 22
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100004440, Wellcome Trust;
                Award ID: 098433
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100000268, Biotechnology and Biological Sciences Research Council;
                Award ID: BB/L027534/1
                AK is supported by the Biotechnology and Biological Sciences Research Council (grant number: BB/L027534/1, URL: http://www.bbsrc.ac.uk/). JG is supported by the Wellcome Trust (Joint Senior Investigator Grant, 098433, URL: www.wellcome.ac.uk/). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Anatomy
                Brain
                Medicine and Health Sciences
                Anatomy
                Brain
                Biology and Life Sciences
                Neuroscience
                Brain Mapping
                Magnetoencephalography
                Research and Analysis Methods
                Imaging Techniques
                Neuroimaging
                Magnetoencephalography
                Biology and Life Sciences
                Neuroscience
                Neuroimaging
                Magnetoencephalography
                Computer and Information Sciences
                Neural Networks
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                Neuroscience
                Neural Networks
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                Neuroscience
                Physical Sciences
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                Geometry
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                Research and Analysis Methods
                Mathematical and Statistical Techniques
                Statistical Methods
                Regression Analysis
                Linear Regression Analysis
                Physical Sciences
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                Statistics (Mathematics)
                Statistical Methods
                Regression Analysis
                Linear Regression Analysis
                Medicine and Health Sciences
                Diagnostic Medicine
                Diagnostic Radiology
                Magnetic Resonance Imaging
                Research and Analysis Methods
                Imaging Techniques
                Diagnostic Radiology
                Magnetic Resonance Imaging
                Medicine and Health Sciences
                Radiology and Imaging
                Diagnostic Radiology
                Magnetic Resonance Imaging
                Engineering and Technology
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                Custom metadata
                The Matlab-based script, as well as clean data and LCMV filters for all participants, can be downloaded from the MEG web site of the Centre for Cognitive Neuroimaging, Institute of Neuroscience and Psychology, University of Glasgow: http://meg.psy.gla.ac.uk/.

                Life sciences
                Life sciences

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