EEG-fMRI Fusion of Paradigm-Free Activity Using Kalman Filtering

We address here the use of EEG and fMRI, and their combination, in order to estimate the full spatiotemporal patterns of activity on the cortical surface in the absence of any particular assumptions on this activity such as stimulation times. For handling such a high-dimension inverse problem, we propose the use of (1) a global forward model of how these measures are functions of the neural activity of a large number of sources distributed on the cortical surface, formalized as a dynamical system, and (2) adaptive filters, as a natural solution to solve this inverse problem iteratively along the temporal dimension. This estimation framework relies on realistic physiological models, uses EEG and fMRI in a symmetric manner, and takes into account both their temporal and spatial information. We use the Kalman filter and smoother to perform such an estimation on realistic artificial data and demonstrate that the algorithm can handle the high dimensionality of these data and that it succeeds in solving this inverse problem, combining efficiently the information provided by the two modalities (this information being naturally predominantly temporal for EEG and spatial for fMRI). It performs particularly well in reconstructing a random temporally and spatially smooth activity spread over the cortex. The Kalman filter and smoother show some limitations, however, which call for the development of more specific adaptive filters. First, they do not cope well with the strong nonlinearity in the model that is necessary for an adequate description of the relation between cortical electric activities and the metabolic demand responsible for fMRI signals. Second, they fail to estimate a sparse activity (i.e., presenting sharp peaks at specific locations and times). Finally their computational cost remains high. We use schematic examples to explain these limitations and propose further developments of our method to overcome them.

[1]  Thomas Deneux,et al.  Hemodynamic Models: Investigation and Application to Brain Imaging Analysis. (Modèles Hémodynamiques: Investigation et Application à l'Analyse en Imagerie Cérébrale) , 2006 .

[2]  J Riera,et al.  Fusing EEG and fMRI based on a bottom-up model: inferring activation and effective connectivity in neural masses , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[3]  Karl J. Friston,et al.  Effective connectivity: Influence, causality and biophysical modeling , 2011, NeuroImage.

[4]  Louis Lemieux,et al.  Comparison of Spike-Triggered Functional MRI BOLD Activation and EEG Dipole Model Localization , 2001, NeuroImage.

[5]  J J Riera,et al.  Evaluation of inverse methods and head models for EEG source localization using a human skull phantom , 2001, Physics in medicine and biology.

[6]  Neil J. Gordon,et al.  A tutorial on particle filters for online nonlinear/non-Gaussian Bayesian tracking , 2002, IEEE Trans. Signal Process..

[7]  Jean-Michel Morel,et al.  Variational methods in image segmentation , 1995 .

[8]  J. Gotman,et al.  Quality of EEG in simultaneous EEG-fMRI for epilepsy , 2003, Clinical Neurophysiology.

[9]  R. Ilmoniemi,et al.  Magnetoencephalography-theory, instrumentation, and applications to noninvasive studies of the working human brain , 1993 .

[10]  Geoffray Adde,et al.  Image Processing Methods Applied to the Magneto-Electro-Encephalography Inverse Problem , 2005 .

[11]  J. Gotman,et al.  Combining EEG and fMRI in Epilepsy: Methodological Challenges and Clinical Results , 2004, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[12]  Robert A. Frazor,et al.  Standing Waves and Traveling Waves Distinguish Two Circuits in Visual Cortex , 2007, Neuron.

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

[14]  C C Wood,et al.  Mapping function in the human brain with magnetoencephalography, anatomical magnetic resonance imaging, and functional magnetic resonance imaging. , 1995, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[15]  Naoki Miura,et al.  A state-space model of the hemodynamic approach: nonlinear filtering of BOLD signals , 2004, NeuroImage.

[16]  R. Malach,et al.  Intersubject Synchronization of Cortical Activity During Natural Vision , 2004, Science.

[17]  Laura Astolfi,et al.  Multimodal integration of EEG, MEG and fMRI data for the solution of the neuroimage puzzle. , 2004, Magnetic resonance imaging.

[18]  Greg Welch,et al.  An Introduction to Kalman Filter , 1995, SIGGRAPH 2001.

[19]  Pierre Kornprobst,et al.  Mathematical problems in image processing - partial differential equations and the calculus of variations, 2nd Edition , 2010, Applied mathematical sciences.

[20]  Olivier Faugeras,et al.  Using nonlinear models in fMRI data analysis: Model selection and activation detection , 2006, NeuroImage.

[21]  Olivier D. Faugeras,et al.  A common formalism for the Integral formulations of the forward EEG problem , 2005, IEEE Transactions on Medical Imaging.

[22]  Karl J. Friston,et al.  EEG-fMRI integration: a critical review of biophysical modeling and data analysis approaches. , 2010, Journal of integrative neuroscience.

[23]  Jean Gotman,et al.  Analysis of the EEG–fMRI response to prolonged bursts of interictal epileptiform activity , 2005, NeuroImage.

[24]  F. Babiloni,et al.  Estimation of the cortical functional connectivity with the multimodal integration of high-resolution EEG and fMRI data by directed transfer function , 2005, NeuroImage.

[25]  A K Liu,et al.  Spatiotemporal imaging of human brain activity using functional MRI constrained magnetoencephalography data: Monte Carlo simulations. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[26]  S.N. Erné,et al.  A NEW METHOD FOR THE ANALYSIS OF FUNCTIONAL MAGNETIC RESONANCE IMAGING DATA: MUTUAL INFORMATION TESTS , 2003 .

[27]  D. Nair About being BOLD , 2005, Brain Research Reviews.

[28]  Marnie E. Shaw,et al.  How reliable are fMRI–EEG studies of epilepsy? A nonparametric approach to analysis validation and optimization , 2005, NeuroImage.

[29]  R. Buxton,et al.  Dynamics of blood flow and oxygenation changes during brain activation: The balloon model , 1998, Magnetic resonance in medicine.

[30]  Jeffrey K. Uhlmann,et al.  New extension of the Kalman filter to nonlinear systems , 1997, Defense, Security, and Sensing.

[31]  Anders M. Dale,et al.  Improved Localization of Cortical Activity By Combining EEG and MEG with MRI Cortical Surface Reconstruction , 2002 .

[32]  Seppo P. Ahlfors,et al.  Geometrical interpretation of fMRI-guided MEG/EEG inverse estimates , 2004, NeuroImage.

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

[34]  A. Engel,et al.  Opinion TRENDS in Cognitive Sciences Vol.10 No.12 Single-trial EEG–fMRI reveals the dynamics of cognitive function , 2022 .

[35]  T. Başar,et al.  A New Approach to Linear Filtering and Prediction Problems , 2001 .

[36]  Stephen A. Billings,et al.  A three-compartment model of the hemodynamic response and oxygen delivery to brain , 2005, NeuroImage.

[37]  Diego Clonda,et al.  Bayesian spatio-temporal approach for EEG source reconstruction: conciliating ECD and distributed models , 2006, IEEE Transactions on Biomedical Engineering.

[38]  Barak A. Pearlmutter,et al.  Fusion of Functional Brain Imaging Modalities via Linear Programming , .

[39]  Sylvain Baillet,et al.  A Bayesian approach to introducing anatomo-functional priors in the EEG/MEG inverse problem , 1997, IEEE Transactions on Biomedical Engineering.

[40]  Nelson J. Trujillo-Barreto,et al.  Biophysical model for integrating neuronal activity, EEG, fMRI and metabolism , 2008, NeuroImage.

[41]  G. Aubert,et al.  Mathematical Problems in Image Processing: Partial Differential Equations and the Calculus of Variations (Applied Mathematical Sciences) , 2006 .

[42]  Karl J. Friston,et al.  Statistical parametric mapping for event-related potentials (II): a hierarchical temporal model , 2004, NeuroImage.

[43]  G. Glover Deconvolution of Impulse Response in Event-Related BOLD fMRI1 , 1999, NeuroImage.

[44]  Cornelius Weiller,et al.  Joint EEG/fMRI state space model for the detection of directed interactions in human brains--a simulation study. , 2011, Physiological measurement.

[45]  R. Keriven,et al.  Imaging Methods for MEG/EEG Inverse Problem , 2005 .

[46]  Jérémie Mattout,et al.  Symmetrical event-related EEG/fMRI information fusion in a variational Bayesian framework , 2007, NeuroImage.

[47]  David M. Rector,et al.  Dynamic functional neuroimaging integrating multiple modalities , 2001 .

[48]  Seong-Gi Kim,et al.  Neural Interpretation of Blood Oxygenation Level-Dependent fMRI Maps at Submillimeter Columnar Resolution , 2007, The Journal of Neuroscience.

[49]  R. Buxton,et al.  Modeling the hemodynamic response to brain activation , 2004, NeuroImage.

[50]  C. Petersen,et al.  Visualizing the Cortical Representation of Whisker Touch: Voltage-Sensitive Dye Imaging in Freely Moving Mice , 2006, Neuron.

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

[52]  Karl J. Friston,et al.  Bayesian Estimation of Dynamical Systems: An Application to fMRI , 2002, NeuroImage.

[53]  Fumikazu Miwakeichi,et al.  Concurrent EEG/fMRI analysis by multiway Partial Least Squares , 2004, NeuroImage.

[54]  P. Nunez,et al.  On the Relationship of Synaptic Activity to Macroscopic Measurements: Does Co-Registration of EEG with fMRI Make Sense? , 2004, Brain Topography.

[55]  Karl J. Friston,et al.  Hemodynamic correlates of EEG: A heuristic , 2005, NeuroImage.