Developmental changes of functional and directed resting-state connectivities associated with neuronal oscillations in EEG

Several studies demonstrated that resting-state EEG power differs tremendously between school-aged children and adults. Low-frequency oscillations (delta and theta, <7 Hz) are dominant in children but become less prominent in the adult brain, where higher-frequency alpha oscillations (8-12 Hz) dominate the mature brain rhythm. However, this assessment of developmental effects with EEG power mapping is restricted to the scalp level and blind to the information flow between brain regions, thus limiting insights about brain development. In contrast dynamic source synchronization provides a tool to study inter-regional directionality on the cortical and sub-cortical source level. In this study we investigated functional and directed connectivities (information flow) with renormalized partial directed coherence during resting state EEG (eyes open and eyes closed) recordings in 17 school-aged children and 17 young adults. First, we found higher spectral mean source power in children relative to adults, irrespective of the examined frequency band and resting state. We further found that coherence values were stronger in adults compared to children in all frequency bands. The directed within-group coherence analysis indicated information flow from frontal to parietal sources in children, while information flow from parietal to frontal was observed in adults. In addition, significant thalamocortical connectivity was unidirectional (i.e., outflow to cortical regions) in adults, but bidirectional in children. Group comparison confirmed the results of the single subject analyses for both functional and directed connectivities. Our results suggest that both functional and directed connectivities are sensitive to brain maturation as the distribution and directionality of functional connections differ between the developing and adult brains.

[1]  Robert Turner,et al.  A Method for Removing Imaging Artifact from Continuous EEG Recorded during Functional MRI , 2000, NeuroImage.

[2]  H. Lyytinen,et al.  Brain sensitivity to print emerges when children learn letter–speech sound correspondences , 2010, Proceedings of the National Academy of Sciences.

[3]  P. V. van Rijen,et al.  Measurement of the Conductivity of Skull, Temporarily Removed During Epilepsy Surgery , 2004, Brain Topography.

[4]  M. Deschenes,et al.  The thalamus as a neuronal oscillator , 1984, Brain Research Reviews.

[5]  J G Beaumont,et al.  Asymmetry in EEG alpha coherence and power: effects of task and sex. , 1978, Electroencephalography and clinical neurophysiology.

[6]  Alfons Schnitzler,et al.  Modality specific functional interaction in sensorimotor synchronization , 2009, Human brain mapping.

[7]  Arnold Neumaier,et al.  Algorithm 808: ARfit—a matlab package for the estimation of parameters and eigenmodes of multivariate autoregressive models , 2001, TOMS.

[8]  M. Butz,et al.  Synchronized brain network underlying postural tremor in Wilson's disease , 2006, Movement disorders : official journal of the Movement Disorder Society.

[9]  Krish D. Singh,et al.  A new approach to neuroimaging with magnetoencephalography , 2005, Human brain mapping.

[10]  Febo Cincotti,et al.  Functional frontoparietal connectivity during short-term memory as revealed by high-resolution EEG coherence analysis. , 2004, Behavioral neuroscience.

[11]  A. Schnitzler,et al.  The neural basis of intermittent motor control in humans , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[12]  Michelle K. Jetha,et al.  Electrophysiological changes during adolescence: A review , 2010, Brain and Cognition.

[13]  D. Lehmann,et al.  Reference-free identification of components of checkerboard-evoked multichannel potential fields. , 1980, Electroencephalography and clinical neurophysiology.

[14]  D. Tucker,et al.  Functional connections among cortical regions: topography of EEG coherence. , 1986, Electroencephalography and clinical neurophysiology.

[15]  R. Thatcher,et al.  Human cerebral hemispheres develop at different rates and ages. , 1987, Science.

[16]  P. Huttenlocher Morphometric study of human cerebral cortex development , 1990, Neuropsychologia.

[17]  Robert J Barry,et al.  EEG coherence in children with attention-deficit/hyperactivity disorder and comorbid reading disabilities. , 2009, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[18]  Maria G. Knyazeva,et al.  Interhemispheric interaction in children of 7–8: Analysis of EEG coherence and finger tapping parameters , 1994, Behavioural Brain Research.

[19]  T. Koenig,et al.  Developmental Changes of BOLD Signal Correlations with Global Human EEG Power and Synchronization during Working Memory , 2012, PloS one.

[20]  Louis Lemieux,et al.  Identification of EEG Events in the MR Scanner: The Problem of Pulse Artifact and a Method for Its Subtraction , 1998, NeuroImage.

[21]  Stefan Haufe,et al.  A critical assessment of connectivity measures for EEG data: A simulation study , 2013, NeuroImage.

[22]  Ricardo Nitrini,et al.  [EEG alpha band coherence analysis in healthy adults: preliminary results]. , 2005, Arquivos de neuro-psiquiatria.

[23]  P. Yakovlev,et al.  The myelogenetic cycles of regional maturation of the brain , 1967 .

[24]  Mingzhou Ding,et al.  Evaluating causal relations in neural systems: Granger causality, directed transfer function and statistical assessment of significance , 2001, Biological Cybernetics.

[25]  J Gross,et al.  REPRINTS , 1962, The Lancet.

[26]  Michael C. Stevens,et al.  The developmental cognitive neuroscience of functional connectivity , 2009, Brain and Cognition.

[27]  R. Barry,et al.  Age and gender effects in EEG coherence: I. Developmental trends in normal children , 2004, Clinical Neurophysiology.

[28]  E. Gordon,et al.  Brain maturation in adolescence: Concurrent changes in neuroanatomy and neurophysiology , 2007, Human brain mapping.

[29]  N. Japaridze,et al.  Dynamic imaging of coherent sources , 2013, Zeitschrift für Epileptologie.

[30]  R. Oostenveld,et al.  Frontal theta EEG activity correlates negatively with the default mode network in resting state. , 2008, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[31]  Sacha Jennifer van Albada,et al.  Neurophysiological changes with age probed by inverse modeling of EEG spectra , 2010, Clinical Neurophysiology.

[32]  G. Deuschl,et al.  Imaging coherent sources of tremor related EEG activity in patients with Parkinson's disease , 2008, 2008 30th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[33]  Theo Gasser,et al.  EEG Power and Coherence in Children with Educational Problems , 2003, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[34]  Ronald A. Cohen,et al.  Diffusion tensor imaging of the corpus callosum: a cross-sectional study across the lifespan , 2007, International Journal of Developmental Neuroscience.

[35]  G. Wang,et al.  Directed coherence as a measure of interhemispheric correlation of EEG. , 1992, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[36]  M. Hallett,et al.  Identifying true brain interaction from EEG data using the imaginary part of coherency , 2004, Clinical Neurophysiology.

[37]  T. Gasser,et al.  Development of the EEG of school-age children and adolescents. I. Analysis of band power. , 1988, Electroencephalography and clinical neurophysiology.

[38]  Mark S. Cohen,et al.  Simultaneous EEG and fMRI of the alpha rhythm , 2002, Neuroreport.

[39]  H. Berger Über das Elektrenkephalogramm des Menschen , 1929, Archiv für Psychiatrie und Nervenkrankheiten.

[40]  M. Witter,et al.  Deficits of memory, executive functioning and attention following infarction in the thalamus; a study of 22 cases with localised lesions , 2003, Neuropsychologia.

[41]  R. Thatcher,et al.  Cortico-cortical associations and EEG coherence: a two-compartmental model. , 1986, Electroencephalography and clinical neurophysiology.

[42]  P. Rappelsberger,et al.  EEG cohererence and reference signals: experimental results and mathematical explanations , 1998, Medical and Biological Engineering and Computing.

[43]  Julia P. Owen,et al.  Removal of Spurious Coherence in MEG Source-Space Coherence Analysis , 2011, IEEE Transactions on Biomedical Engineering.

[44]  Peter C. M. Molenaar,et al.  Frequency domain simultaneous source and source coherence estimation with an application to MEG , 2004, IEEE Transactions on Biomedical Engineering.

[45]  T. Gasser,et al.  EEG power and coherence while male adults watch emotional video films. , 1990, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[46]  Koichi Sameshima,et al.  Using partial directed coherence to describe neuronal ensemble interactions , 1999, Journal of Neuroscience Methods.

[47]  Muthuraman Muthuraman,et al.  Oscillating central motor networks in pathological tremors and voluntary movements. What makes the difference? , 2012, NeuroImage.

[48]  Robert Oostenveld,et al.  FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data , 2010, Comput. Intell. Neurosci..

[49]  W. Drongelen,et al.  Localization of brain electrical activity via linearly constrained minimum variance spatial filtering , 1997, IEEE Transactions on Biomedical Engineering.

[50]  G. Wang,et al.  EEG analysis of epilepsy by directed coherence method. A data processing approach. , 1996, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[51]  Bart Vanrumste,et al.  Review on solving the forward problem in EEG source analysis , 2007, Journal of NeuroEngineering and Rehabilitation.

[52]  M. Corbetta,et al.  Electrophysiological signatures of resting state networks in the human brain , 2007, Proceedings of the National Academy of Sciences.

[53]  Christoph M. Michel,et al.  The behavioral significance of coherent resting-state oscillations after stroke , 2012, NeuroImage.

[54]  Kathryn L. Mills,et al.  Altered Cortico-Striatal–Thalamic Connectivity in Relation to Spatial Working Memory Capacity in Children with ADHD , 2012, Front. Psychiatry.

[55]  Roberto Spreafico,et al.  Partial Directed Coherence estimated on Stereo-EEG signals in patients with Taylor's type focal cortical dysplasia , 2010, 2010 Annual International Conference of the IEEE Engineering in Medicine and Biology.

[56]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[57]  R. Llinás,et al.  The functional states of the thalamus and the associated neuronal interplay. , 1988, Physiological reviews.

[58]  T. Sejnowski,et al.  Removal of eye activity artifacts from visual event-related potentials in normal and clinical subjects , 2000, Clinical Neurophysiology.

[59]  Wolfgang Klimesch,et al.  Individual differences in brain dynamics: important implications for the calculation of event-related band power , 1998, Biological Cybernetics.

[60]  J. Mazziotta,et al.  Positron emission tomography study of human brain functional development , 1987, Annals of neurology.

[61]  Helmut Laufs,et al.  Where the BOLD signal goes when alpha EEG leaves , 2006, NeuroImage.

[62]  G. Deuschl,et al.  Source Analysis of Beta-Synchronisation and Cortico-Muscular Coherence after Movement Termination Based on High Resolution Electroencephalography , 2012, PloS one.

[63]  O. Muzik,et al.  Thalamocortical Connectivity in Healthy Children: Asymmetries and Robust Developmental Changes between Ages 8 and 17 Years , 2011, American Journal of Neuroradiology.

[64]  J. R. Rosenberg,et al.  The Fourier approach to the identification of functional coupling between neuronal spike trains. , 1989, Progress in biophysics and molecular biology.

[65]  Robert J Barry,et al.  Adjusting EEG coherence for inter-electrode distance effects: an exploration in normal children. , 2005, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[66]  Christoph M. Michel,et al.  Electrical Neuroimaging: Imaging the electric neuronal generators of EEG/MEG , 2009 .

[67]  Thomas F. Nugent,et al.  Dynamic mapping of human cortical development during childhood through early adulthood. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[68]  Mitchell K. Byrne,et al.  EEG coherence in adults with attention-deficit/hyperactivity disorder. , 2008, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[69]  Andreas Kleinschmidt,et al.  EEG-correlated fMRI of human alpha activity , 2003, NeuroImage.

[70]  G. Deuschl,et al.  The central oscillatory network of essential tremor , 2010, 2010 Annual International Conference of the IEEE Engineering in Medicine and Biology.

[71]  T Fernández,et al.  Maturation of the coherence of EEG activity in normal and learning-disabled children. , 1992, Electroencephalography and clinical neurophysiology.

[72]  R Verleger,et al.  EEG coherence at rest and during a visual task in two groups of children. , 1987, Electroencephalography and clinical neurophysiology.

[73]  M. Eichler,et al.  Assessing the strength of directed influences among neural signals using renormalized partial directed coherence , 2009, Journal of Neuroscience Methods.

[74]  M. Fuchs,et al.  Development of Volume Conductor and Source Models to Localize Epileptic Foci , 2007, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[75]  A. Connelly,et al.  Developmental changes in cerebral grey and white matter volume from infancy to adulthood , 2010, International Journal of Developmental Neuroscience.

[76]  W. Klimesch,et al.  Lifespan differences in cortical dynamics of auditory perception. , 2009, Developmental science.

[77]  Arnold Neumaier,et al.  Estimation of parameters and eigenmodes of multivariate autoregressive models , 2001, TOMS.

[78]  Michael D. Greicius,et al.  Development of functional and structural connectivity within the default mode network in young children , 2010, NeuroImage.

[79]  M. Butz,et al.  Oscillatory coupling in writing and writer’s cramp , 2006, Journal of Physiology-Paris.

[80]  P. Nunez,et al.  Spatial filtering and neocortical dynamics: estimates of EEG coherence , 1998, IEEE Transactions on Biomedical Engineering.

[81]  Jan Kujala,et al.  Localization of correlated network activity at the cortical level with MEG , 2008, NeuroImage.

[82]  Helmut Laufs,et al.  Endogenous brain oscillations and related networks detected by surface EEG‐combined fMRI , 2008, Human brain mapping.

[83]  Tuomo Starck,et al.  Age-Related Differences in Functional Nodes of the Brain Cortex – A High Model Order Group ICA Study , 2010, Front. Syst. Neurosci..

[84]  Manuel Schabus,et al.  Fronto-parietal EEG coherence in theta and upper alpha reflect central executive functions of working memory. , 2005, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[85]  S. Petersen,et al.  The maturing architecture of the brain's default network , 2008, Proceedings of the National Academy of Sciences.

[86]  H. Freund,et al.  The cerebral oscillatory network of parkinsonian resting tremor. , 2003, Brain : a journal of neurology.

[87]  Yoko Yamaguchi,et al.  Long-range EEG phase synchronization during an arithmetic task indexes a coherent cortical network simultaneously measured by fMRI , 2005, NeuroImage.

[88]  Hellmuth Obrig,et al.  Correlates of alpha rhythm in functional magnetic resonance imaging and near infrared spectroscopy , 2003, NeuroImage.

[89]  R. V. Uitert,et al.  Can a Spherical Model Substitute for a Realistic Head Model in Forward and Inverse MEG Simulations ? , 2002 .

[90]  K. Sekihara,et al.  Generalized Wiener estimation of three-dimensional current distribution from biomagnetic measurements , 1996, IEEE Transactions on Biomedical Engineering.

[91]  B Schack,et al.  The sensitivity of instantaneous coherence for considering elementary comparison processing. Part II: Similarities and differences between EEG and MEG coherences. , 1999, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[92]  G Fein,et al.  Common reference coherence data are confounded by power and phase effects. , 1988, Electroencephalography and clinical neurophysiology.

[93]  Paulo Caramelli,et al.  Estudo da coerência do eletrencefalograma na banda de frequência alfa em indivíduos adultos normais: resultados preliminares em 10 casos , 2005 .

[94]  S. Petersen,et al.  Development of distinct control networks through segregation and integration , 2007, Proceedings of the National Academy of Sciences.

[95]  Alfons Schnitzler,et al.  Functional network interactions during sensorimotor synchronization in musicians and non-musicians , 2010, NeuroImage.

[96]  H. Akaike A new look at the statistical model identification , 1974 .

[97]  P. Achermann,et al.  Developmental changes in brain connectivity assessed using the sleep EEG , 2010, Neuroscience.

[98]  Daniel Brandeis,et al.  Brain state regulation during normal development: Intrinsic activity fluctuations in simultaneous EEG–fMRI , 2012, NeuroImage.

[99]  Daniel Brandeis,et al.  EEG–BOLD correlations during (post-)adolescent brain maturation , 2011, NeuroImage.

[100]  J. R. Rosenberg,et al.  An extended difference of coherence test for comparing and combining several independent coherence estimates: theory and application to the study of motor units and physiological tremor , 1997, Journal of Neuroscience Methods.

[101]  Hualou Liang,et al.  Short-window spectral analysis of cortical event-related potentials by adaptive multivariate autoregressive modeling: data preprocessing, model validation, and variability assessment , 2000, Biological Cybernetics.

[102]  O. Jensen,et al.  Neuromagnetic localization of rhythmic activity in the human brain: a comparison of three methods , 2005, NeuroImage.

[103]  Wolf Singer,et al.  Distributed processing and temporal codes in neuronal networks , 2009, Cognitive Neurodynamics.

[104]  F. H. Lopes da Silva,et al.  Model of brain rhythmic activity , 1974, Kybernetik.

[105]  P. Nunez,et al.  EEG and MEG coherence: Measures of functional connectivity at distinct spatial scales of neocortical dynamics , 2007, Journal of Neuroscience Methods.

[106]  J. D. Munck A linear discretization of the volume conductor boundary integral equation using analytically integrated elements (electrophysiology application) , 1992 .

[107]  Irwin Feinberg,et al.  Sleep EEG changes during adolescence: An index of a fundamental brain reorganization , 2010, Brain and Cognition.

[108]  Jeff H. Duyn,et al.  Large-scale spontaneous fluctuations and correlations in brain electrical activity observed with magnetoencephalography , 2010, NeuroImage.

[109]  H. Berger,et al.  Über das Elektrenkephalogramm des Menschen , 1937, Archiv für Psychiatrie und Nervenkrankheiten.

[110]  Robert Oostenveld,et al.  Imaging the human motor system’s beta-band synchronization during isometric contraction , 2008, NeuroImage.

[111]  Jonathan D. Power,et al.  Prediction of Individual Brain Maturity Using fMRI , 2010, Science.