The spatiospectral characterization of brain networks: Fusing concurrent EEG spectra and fMRI maps

Different imaging modalities capture different aspects of brain activity. Functional magnetic resonance imaging (fMRI) reveals intrinsic networks whose BOLD signals have periods from 100 s (0.01 Hz) to about 10s (0.1 Hz). Electroencephalographic (EEG) recordings, in contrast, commonly reflect cortical electrical fluctuations with periods up to 20 ms (50 Hz) or above. We examined the correspondence between intrinsic fMRI and EEG network activity at rest in order to characterize brain networks both spatially (with fMRI) and spectrally (with EEG). Brain networks were separately identified within the concurrently recorded fMRI and EEG at the aggregate group level with group independent component analysis and the association between spatial fMRI and frequency by spatial EEG sources was examined by deconvolving their component time courses. The two modalities are considered linked if the estimated impulse response function (IRF) is significantly non-zero at biologically plausible delays. We found that negative associations were primarily present within two of five alpha components, which highlights the importance of considering multiple alpha sources in EEG-fMRI. Positive associations were primarily present within the lower (e.g. delta and theta) and higher (e.g. upper beta and lower gamma) spectral regions, sometimes within the same fMRI components. Collectively, the results demonstrate a promising approach to characterize brain networks spatially and spectrally, and reveal that positive and negative associations appear within partially distinct regions of the EEG spectrum.

[1]  E. Harth,et al.  Electric Fields of the Brain: The Neurophysics of Eeg , 2005 .

[2]  R. Sekuler,et al.  Intracranial electroencephalography reveals two distinct similarity effects during item recognition , 2009, Brain Research.

[3]  A. Kleinschmidt,et al.  Intrinsic Connectivity Networks, Alpha Oscillations, and Tonic Alertness: A Simultaneous Electroencephalography/Functional Magnetic Resonance Imaging Study , 2010, The Journal of Neuroscience.

[4]  T. Sejnowski,et al.  Removing electroencephalographic artifacts by blind source separation. , 2000, Psychophysiology.

[5]  David Zhang,et al.  Directional independent component analysis with tensor representation , 2008, 2008 IEEE Conference on Computer Vision and Pattern Recognition.

[6]  S. Debener,et al.  Mining EEG-fMRI using independent component analysis. , 2009, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[7]  A. Engel,et al.  Spectral fingerprints of large-scale neuronal interactions , 2012, Nature Reviews Neuroscience.

[8]  Seungjin Choi,et al.  Independent Component Analysis , 2009, Handbook of Natural Computing.

[9]  J C Mazziotta,et al.  Automated labeling of the human brain: A preliminary report on the development and evaluation of a forward‐transform method , 1997, Human brain mapping.

[10]  Vince D. Calhoun,et al.  Reactivity of hemodynamic responses and functional connectivity to different states of alpha synchrony: A concurrent EEG-fMRI study , 2010, NeuroImage.

[11]  J. Szaflarski,et al.  Simultaneous EEG/Functional Magnetic Resonance Imaging at 4 Tesla: Correlates of Brain Activity to Spontaneous Alpha Rhythm During Relaxation , 2008, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[12]  S. Makeig,et al.  Mining event-related brain dynamics , 2004, Trends in Cognitive Sciences.

[13]  Rex E. Jung,et al.  A Baseline for the Multivariate Comparison of Resting-State Networks , 2011, Front. Syst. Neurosci..

[14]  D. C. Mccarthy,et al.  Hippocampal and neocortical gamma oscillations predict memory formation in humans. , 2006, Cerebral cortex.

[15]  Terrence J. Sejnowski,et al.  An Information-Maximization Approach to Blind Separation and Blind Deconvolution , 1995, Neural Computation.

[16]  R. Eckhorn,et al.  Coherent oscillations: A mechanism of feature linking in the visual cortex? , 1988, Biological Cybernetics.

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

[18]  W. Singer,et al.  Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties , 1989, Nature.

[19]  C. Schroeder,et al.  Low-frequency neuronal oscillations as instruments of sensory selection , 2009, Trends in Neurosciences.

[20]  Stephen M Smith,et al.  Correspondence of the brain's functional architecture during activation and rest , 2009, Proceedings of the National Academy of Sciences.

[21]  O. Tervonen,et al.  The effect of model order selection in group PICA , 2010, Human brain mapping.

[22]  Dirk Ostwald,et al.  Functional source separation improves the quality of single trial visual evoked potentials recorded during concurrent EEG-fMRI , 2010, NeuroImage.

[23]  A. Kleinschmidt,et al.  Electroencephalographic signatures of attentional and cognitive default modes in spontaneous brain activity fluctuations at rest , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[24]  C. F. Beckmann,et al.  Tensorial extensions of independent component analysis for multisubject FMRI analysis , 2005, NeuroImage.

[25]  Karl J. Friston,et al.  Nonlinear Responses in fMRI: The Balloon Model, Volterra Kernels, and Other Hemodynamics , 2000, NeuroImage.

[26]  Vince D. Calhoun,et al.  EEGIFT: Group Independent Component Analysis for Event-Related EEG Data , 2011, Comput. Intell. Neurosci..

[27]  M. D’Esposito,et al.  The Variability of Human, BOLD Hemodynamic Responses , 1998, NeuroImage.

[28]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[29]  J. Voipio,et al.  Full-band EEG (FbEEG): an emerging standard in electroencephalography , 2005, Clinical Neurophysiology.

[30]  G. Buzsáki Rhythms of the brain , 2006 .

[31]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[32]  G. Srivastava,et al.  ICA-based procedures for removing ballistocardiogram artifacts from EEG data acquired in the MRI scanner , 2005, NeuroImage.

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

[34]  Natasha M. Maurits,et al.  Correlating the alpha rhythm to BOLD using simultaneous EEG/fMRI: Inter-subject variability , 2006, NeuroImage.

[35]  T. Curran,et al.  Functional role of gamma and theta oscillations in episodic memory , 2010, Neuroscience & Biobehavioral Reviews.

[36]  Kenneth Hugdahl,et al.  Prediction of human errors by maladaptive changes in event-related brain networks , 2008, Proceedings of the National Academy of Sciences.

[37]  Darren Price,et al.  Investigating the electrophysiological basis of resting state networks using magnetoencephalography , 2011, Proceedings of the National Academy of Sciences.

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

[39]  Terrence J. Sejnowski,et al.  Independent Component Analysis Using an Extended Infomax Algorithm for Mixed Subgaussian and Supergaussian Sources , 1999, Neural Computation.

[40]  Karl J. Friston,et al.  Spatial registration and normalization of images , 1995 .

[41]  Tülay Adali,et al.  Comparison of multi‐subject ICA methods for analysis of fMRI data , 2010, Human brain mapping.

[42]  H. Petsche,et al.  Phase-coupling of theta-gamma EEG rhythms during short-term memory processing. , 2002, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[43]  W. Klimesch,et al.  EEG alpha oscillations: The inhibition–timing hypothesis , 2007, Brain Research Reviews.

[44]  J L Lancaster,et al.  Automated Talairach Atlas labels for functional brain mapping , 2000, Human brain mapping.

[45]  Fernando Henrique Lopes da Silva,et al.  Interactions between different EEG frequency bands and their effect on alpha–fMRI correlations , 2009, NeuroImage.

[46]  J. Steffener,et al.  Investigating Hemodynamic Response Variability at the Group Level using Basis Functions , 2009, NeuroImage.

[47]  C. Schroeder,et al.  Neuronal Mechanisms and Attentional Modulation of Corticothalamic Alpha Oscillations , 2011, The Journal of Neuroscience.

[48]  P. Nunez,et al.  Spatial‐temporal structures of human alpha rhythms: Theory, microcurrent sources, multiscale measurements, and global binding of local networks , 2001, Human brain mapping.

[49]  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.

[50]  M. Corbetta,et al.  Large-scale cortical correlation structure of spontaneous oscillatory activity , 2012, Nature Neuroscience.

[51]  M. Berger,et al.  High Gamma Power Is Phase-Locked to Theta Oscillations in Human Neocortex , 2006, Science.

[52]  O. Tervonen,et al.  Functional segmentation of the brain cortex using high model order group-PICA. , 2009, NeuroImage.

[53]  Mark D'Esposito,et al.  Variation of BOLD hemodynamic responses across subjects and brain regions and their effects on statistical analyses , 2004, NeuroImage.

[54]  Mingzhou Ding,et al.  Attentional Modulation of Alpha Oscillations in Macaque Inferotemporal Cortex , 2011, The Journal of Neuroscience.

[55]  P. Rossini,et al.  Hand sensory–motor cortical network assessed by functional source separation , 2008, Human brain mapping.

[56]  C Porcaro,et al.  Functional Source Separation Improves the Quality of Single Trial Evoked Potentials for EEG-fMRI Analysis , 2009, NeuroImage.

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

[58]  Fernando Henrique Lopes da Silva,et al.  The hemodynamic response of the alpha rhythm: An EEG/fMRI study , 2007, NeuroImage.

[59]  R. Oostenveld,et al.  Neuronal Dynamics Underlying High- and Low-Frequency EEG Oscillations Contribute Independently to the Human BOLD Signal , 2011, Neuron.

[60]  J. Pekar,et al.  A method for making group inferences from functional MRI data using independent component analysis , 2001, Human brain mapping.

[61]  J. Martinerie,et al.  The brainweb: Phase synchronization and large-scale integration , 2001, Nature Reviews Neuroscience.

[62]  Robert Tibshirani,et al.  An Introduction to the Bootstrap , 1994 .

[63]  Herrmann Christoph,et al.  Gamma amplitudes are coupled to theta phase in human EEG during visual perception , 2010 .

[64]  Yoko Yamaguchi,et al.  A long-range cortical network emerging with theta oscillation in a mental task , 2004, Neuroreport.

[65]  L. Freire,et al.  Motion Correction Algorithms May Create Spurious Brain Activations in the Absence of Subject Motion , 2001, NeuroImage.

[66]  P M Rossini,et al.  A neurally-interfaced hand prosthesis tuned inter-hemispheric communication. , 2012, Restorative neurology and neuroscience.

[67]  Dieter Vaitl,et al.  Relationship between regional hemodynamic activity and simultaneously recorded EEG‐theta associated with mental arithmetic‐induced workload , 2007, Human brain mapping.

[68]  E. Niedermeyer Alpha rhythms as physiological and abnormal phenomena. , 1997, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[69]  W. Pritchard,et al.  The brain in fractal time: 1/f-like power spectrum scaling of the human electroencephalogram. , 1992, The International journal of neuroscience.

[70]  Gareth R. Barnes,et al.  The relationship between the visual evoked potential and the gamma band investigated by blind and semi-blind methods , 2011, NeuroImage.

[71]  Todd C. Handy,et al.  Event-related potentials : a methods handbook , 2005 .

[72]  B. Feige,et al.  Cortical and subcortical correlates of electroencephalographic alpha rhythm modulation. , 2005, Journal of neurophysiology.

[73]  B. Biswal,et al.  Functional connectivity in the motor cortex of resting human brain using echo‐planar mri , 1995, Magnetic resonance in medicine.