Automated Head Tissue Modelling Based on Structural Magnetic Resonance Images for Electroencephalographic Source Reconstruction

In the last years, technological advancements for the analysis of electroencephalography (EEG) recordings have permitted to investigate neural activity and connectivity in the human brain with unprecedented precision and reliability. A crucial element for accurate EEG source reconstruction is the construction of a realistic head model, incorporating information on electrode positions and head tissue distribution. In this paper, we introduce MR-TIM, a toolbox for head tissue modelling from structural magnetic resonance (MR) images. The toolbox consists of three modules: 1) image pre-processing – the raw MR image is denoised and prepared for further analyses; 2) tissue probability mapping – template tissue probability maps (TPMs) in individual space are generated from the MR image; 3) tissue segmentation – information from all the TPMs is integrated such that each voxel in the MR image is assigned to a specific tissue. MR-TIM generates highly realistic 3D masks, five of which are associated with brain structures (brain and cerebellar grey matter, brain and cerebellar white matter, and brainstem) and the remaining seven with other head tissues (cerebrospinal fluid, spongy and compact bones, eyes, muscle, fat and skin). Our validation, conducted on MR images collected in healthy volunteers and patients as well as an MR template image from an open-source repository, demonstrates that MR-TIM is more accurate than alternative approaches for whole-head tissue segmentation. We hope that MR-TIM, by yielding an increased precision in head modelling, will contribute to a more widespread use of EEG as a brain imaging technique. Supplementary Information The online version contains supplementary material available at 10.1007/s12021-020-09504-5.

[1]  Bruce Fischl,et al.  FreeSurfer , 2012, NeuroImage.

[2]  L. R. Dice Measures of the Amount of Ecologic Association Between Species , 1945 .

[3]  Richard M. Leahy,et al.  Brainstorm: A User-Friendly Application for MEG/EEG Analysis , 2011, Comput. Intell. Neurosci..

[4]  Federica Vatta,et al.  Solving the forward problem in EEG source analysis by spherical and fdm head modeling: a comparative analysis - biomed 2009. , 2009, Biomedical sciences instrumentation.

[5]  Niels Kuster,et al.  MIDA: A Multimodal Imaging-Based Detailed Anatomical Model of the Human Head and Neck , 2015, PloS one.

[6]  J. Ashburner,et al.  Nonlinear spatial normalization using basis functions , 1999, Human brain mapping.

[7]  Hans Hallez,et al.  Influence of Skull Modeling Approaches on EEG Source Localization , 2013, Brain Topography.

[8]  Dante Mantini,et al.  Hand, foot and lip representations in primary sensorimotor cortex: a high-density electroencephalography study , 2019, Scientific Reports.

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

[10]  P. Jaccard THE DISTRIBUTION OF THE FLORA IN THE ALPINE ZONE.1 , 1912 .

[11]  Kai Li,et al.  BrainK for Structural Image Processing: Creating Electrical Models of the Human Head , 2016, Comput. Intell. Neurosci..

[12]  Yu Huang,et al.  The New York Head—A precise standardized volume conductor model for EEG source localization and tES targeting , 2015, NeuroImage.

[13]  Dante Mantini,et al.  Shared and connection-specific intrinsic interactions in the default mode network , 2019, NeuroImage.

[14]  Jacob Cohen A Coefficient of Agreement for Nominal Scales , 1960 .

[15]  Mingni Sun,et al.  An efficient algorithm for computing multishell spherical volume conductor models in EEG dipole source localization. , 1997, IEEE transactions on bio-medical engineering.

[16]  Christopher R. Johnson,et al.  A High-Resolution Head and Brain Computer Model for Forward and Inverse EEG Simulation , 2019, bioRxiv.

[17]  Y. D'Asseler,et al.  A finite difference method with reciprocity used to incorporate anisotropy in electroencephalogram dipole source localization , 2005 .

[18]  Simon K. Warfield,et al.  EEG source analysis of epileptiform activity using a 1 mm anisotropic hexahedra finite element head model , 2009, NeuroImage.

[19]  N. Wenderoth,et al.  Detecting large‐scale networks in the human brain using high‐density electroencephalography , 2017, Human brain mapping.

[20]  David R. Wozny,et al.  The electrical conductivity of human cerebrospinal fluid at body temperature , 1997, IEEE Transactions on Biomedical Engineering.

[21]  M. Hämäläinen,et al.  Realistic conductivity geometry model of the human head for interpretation of neuromagnetic data , 1989, IEEE Transactions on Biomedical Engineering.

[22]  D. Mantini,et al.  Hemodynamic Correlates of Electrophysiological Activity in the Default Mode Network , 2019, Front. Neurosci..

[23]  Mingni Sun,et al.  An efficient algorithm for computing multishell spherical volume conductor models in EEG dipole source localization , 1997, IEEE Transactions on Biomedical Engineering.

[24]  D. Mantini,et al.  Functional connectivity and oscillatory neuronal activity in the resting human brain , 2013, Neuroscience.

[25]  Ron Kikinis,et al.  Forward and inverse electroencephalographic modeling in health and in acute traumatic brain injury , 2013, Clinical Neurophysiology.

[26]  Meritxell Bach Cuadra,et al.  A multidimensional segmentation evaluation for medical image data , 2009, Comput. Methods Programs Biomed..

[27]  Kirby G. Vosburgh,et al.  3D Slicer: A Platform for Subject-Specific Image Analysis, Visualization, and Clinical Support , 2014 .

[28]  J. Haueisen,et al.  Influence of head models on neuromagnetic fields and inverse source localizations , 2006, Biomedical engineering online.

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

[30]  F. Briend,et al.  GeodesicSlicer: a Slicer Toolbox for Targeting Brain Stimulation , 2020, Neuroinformatics.

[31]  S. Makeig,et al.  Improved EEG source analysis using low‐resolution conductivity estimation in a four‐compartment finite element head model , 2009, Human brain mapping.

[32]  J. Haueisen,et al.  Influence of tissue resistivities on neuromagnetic fields and electric potentials studied with a finite element model of the head , 1997, IEEE Transactions on Biomedical Engineering.

[33]  Christoph M. Michel,et al.  Towards the utilization of EEG as a brain imaging tool , 2012, NeuroImage.

[34]  U Moström,et al.  Location of electric current sources in the human brain estimated by the dipole tracing method of the scalp-skull-brain (SSB) head model. , 1994, Electroencephalography and clinical neurophysiology.

[35]  Giampaolo Pisano,et al.  Variation in Reported Human Head Tissue Electrical Conductivity Values , 2019, Brain Topography.

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

[37]  N. G. Gencer,et al.  An advanced boundary element method (BEM) implementation for the forward problem of electromagnetic source imaging. , 2004, Physics in medicine and biology.

[38]  H. I. Saleheen,et al.  New finite difference formulations for general inhomogeneous anisotropic bioelectric problems , 1997, IEEE Transactions on Biomedical Engineering.

[39]  W. Sutherling,et al.  Conductivities of Three-Layer Live Human Skull , 2004, Brain Topography.

[40]  M. Murray,et al.  EEG source imaging , 2004, Clinical Neurophysiology.

[41]  D. Stegeman,et al.  Investigation of tDCS volume conduction effects in a highly realistic head model , 2014, Journal of neural engineering.

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

[43]  P. Berg,et al.  A fast method for forward computation of multiple-shell spherical head models. , 1994, Electroencephalography and clinical neurophysiology.

[44]  Eduard T. Klapwijk,et al.  Qoala-T: A supervised-learning tool for quality control of FreeSurfer segmented MRI data , 2019, NeuroImage.

[45]  R. Sadleir,et al.  Predicted current densities in the brain during transcranial electrical stimulation , 2006, Clinical Neurophysiology.

[46]  Dante Mantini,et al.  A Finite-Difference Solution for the EEG Forward Problem in Inhomogeneous Anisotropic Media , 2018, Brain Topography.

[47]  Giampaolo Pisano,et al.  Variation in Reported Human Head Tissue Electrical Conductivity Values , 2019, Brain Topography.

[48]  Christoph M. Michel,et al.  Subcortical electrophysiological activity is detectable with high-density EEG source imaging , 2019, Nature Communications.

[49]  Marco Ganzetti,et al.  Detecting Large-Scale Brain Networks Using EEG: Impact of Electrode Density, Head Modeling and Source Localization , 2018, Front. Neuroinform..

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

[51]  Carsten H. Wolters,et al.  Geometry-Adapted Hexahedral Meshes Improve Accuracy of Finite-Element-Method-Based EEG Source Analysis , 2007, IEEE Transactions on Biomedical Engineering.

[52]  Mark W. Woolrich,et al.  FSL , 2012, NeuroImage.