Quantifying the performance of MEG source reconstruction using resting state data

Resting state networks measured with magnetoencephalography (MEG) form transiently stable spatio-temporal patterns in the subsecond range, and therefore fluctuate more rapidly than previously appreciated. These states populate and interact across the whole brain, are simple to record, and possess the same dynamic structure of task related changes. They therefore provide a generic, heterogeneous, and plentiful functional substrate against which to test different MEG recording and reconstruction approaches. Here we validate a non-invasive method for quantifying the resolution of different inversion assumptions under different recording regimes (with and without head-casts) based on resting state MEG. Spatio-temporally partitioning of data into self-similar periods confirmed a rich and rapidly dynamic temporal structure with a small number of regularly reoccurring states. To test the anatomical precision that could be resolved through these transient states we then inverted these data onto libraries of systematically distorted, subject specific, cortical meshes and compared the quality of the fit using Cross Validation and a Free Energy metric. This revealed which inversion scheme was able to best support the least distorted (most accurate) anatomical models. Both datasets showed an increase in model fit as anatomical models moved towards the true cortical surface. In the head-cast MEG data, the Empirical Bayesian Beamformer (EBB) algorithm showed the best mean anatomical discrimination (3.7 mm) compared with Minimum Norm / LORETA (6.0 mm) and Multiple Sparse priors (9.4 mm). This pattern was replicated in the second (conventional dataset) although with a marginally poorer prediction of the missing (cross-validated) data. Our findings suggest that the abundant resting state data now commonly available could be used to refine and validate MEG source reconstruction methods or recording paradigms.

[1]  Yu-Feng Zang,et al.  Resting-state fMRI studies in epilepsy , 2012, Neuroscience Bulletin.

[2]  David P. Wipf,et al.  A unified Bayesian framework for MEG/EEG source imaging , 2009, NeuroImage.

[3]  M. T. Pellecchia,et al.  Resting-state brain connectivity in patients with Parkinson's disease and freezing of gait. , 2012, Parkinsonism & related disorders.

[4]  Mark W. Woolrich,et al.  Spectrally resolved fast transient brain states in electrophysiological data , 2016, NeuroImage.

[5]  Karl J. Friston,et al.  Canonical Microcircuits for Predictive Coding , 2012, Neuron.

[6]  Antoine Lutti,et al.  High precision anatomy for MEG , 2014, NeuroImage.

[7]  Matthew J. Brookes,et al.  Does function fit structure? A ground truth for non-invasive neuroimaging , 2014, NeuroImage.

[8]  D. Lehmann,et al.  Functional imaging with low-resolution brain electromagnetic tomography (LORETA): a review. , 2002, Methods and findings in experimental and clinical pharmacology.

[9]  Antoine Lutti,et al.  Discrimination of cortical laminae using MEG , 2014, NeuroImage.

[10]  S. Nagarajan,et al.  Clinical Symptoms and Alpha Band Resting-State Functional Connectivity Imaging in Patients With Schizophrenia: Implications for Novel Approaches to Treatment , 2011, Biological Psychiatry.

[11]  Richard M. Leahy,et al.  Electromagnetic brain mapping , 2001, IEEE Signal Process. Mag..

[12]  P. Golland,et al.  Whole brain resting state functional connectivity abnormalities in schizophrenia , 2012, Schizophrenia Research.

[13]  Sylvain Baillet,et al.  Forward and Inverse Problems of MEG/EEG , 2014, Encyclopedia of Computational Neuroscience.

[14]  Gareth R. Barnes,et al.  Practical constraints on estimation of source extent with MEG beamformers , 2011, NeuroImage.

[15]  M. Sigman,et al.  Signature of consciousness in the dynamics of resting-state brain activity , 2015, Proceedings of the National Academy of Sciences.

[16]  Nikolaus Weiskopf,et al.  Quantitative multi-parameter mapping of R1, PD*, MT, and R2* at 3T: a multi-center validation , 2013, Front. Neurosci..

[17]  M. Corbetta,et al.  Learning sculpts the spontaneous activity of the resting human brain , 2009, Proceedings of the National Academy of Sciences.

[18]  Joseph Newman,et al.  Altered Resting-State Functional Connectivity in Cortical Networks in Psychopathy , 2015, The Journal of Neuroscience.

[19]  J. Han,et al.  The transcription factor Pou3f1 promotes neural fate commitment via activation of neural lineage genes and inhibition of external signaling pathways , 2014, eLife.

[20]  Angela R. Laird,et al.  ICA model order selection of task co-activation networks , 2013, Front. Neurosci..

[21]  Mark W. Woolrich,et al.  How reliable are MEG resting-state connectivity metrics? , 2016, NeuroImage.

[22]  Mark W. Woolrich,et al.  Using generative models to make probabilistic statements about hippocampal engagement in MEG , 2017, NeuroImage.

[23]  W. Penny,et al.  Reconstructing anatomy from electro-physiological data , 2017, NeuroImage.

[24]  Dietrich Lehmann,et al.  Millisecond by Millisecond, Year by Year: Normative EEG Microstates and Developmental Stages , 2002, NeuroImage.

[25]  Gareth R. Barnes,et al.  Laminar-specific cortical dynamics in human visual and sensorimotor cortices , 2017, bioRxiv.

[26]  E. Somersalo,et al.  Visualization of Magnetoencephalographic Data Using Minimum Current Estimates , 1999, NeuroImage.

[27]  B. W. van Dijk,et al.  Resting state oscillatory brain dynamics in Parkinson’s disease: An MEG study , 2006, Clinical Neurophysiology.

[28]  Karl J. Friston,et al.  Variational free energy and the Laplace approximation , 2007, NeuroImage.

[29]  Steven C. Cramer,et al.  Resting-state cortical connectivity predicts motor skill acquisition , 2014, NeuroImage.

[30]  Karl J. Friston,et al.  Selecting forward models for MEG source-reconstruction using model-evidence , 2009, NeuroImage.

[31]  Marie T. Banich,et al.  Resting-state networks predict individual differences in common and specific aspects of executive function , 2015, NeuroImage.

[32]  M. Raichle,et al.  Resting State Functional Connectivity in Preclinical Alzheimer’s Disease , 2013, Biological Psychiatry.

[33]  Nikolaus Weiskopf,et al.  Using high-resolution quantitative mapping of R1 as an index of cortical myelination , 2014, NeuroImage.

[34]  J. Andrews-Hanna,et al.  Large-Scale Network Dysfunction in Major Depressive Disorder: A Meta-analysis of Resting-State Functional Connectivity. , 2015, JAMA psychiatry.

[35]  Stephen M Smith,et al.  Fast transient networks in spontaneous human brain activity , 2014, eLife.

[36]  Linda Douw,et al.  Disturbed functional brain networks and neurocognitive function in low-grade glioma patients: a graph theoretical analysis of resting-state MEG , 2009, Nonlinear biomedical physics.

[37]  Hamid Reza Mohseni,et al.  Dynamic state allocation for MEG source reconstruction , 2013, NeuroImage.

[38]  Karl J. Friston,et al.  Multiple sparse priors for the M/EEG inverse problem , 2008, NeuroImage.

[39]  William D. Penny,et al.  A general Bayesian treatment for MEG source reconstruction incorporating lead field uncertainty , 2012, NeuroImage.

[40]  Moo K. Chung,et al.  Weighted Fourier Series Representation and Its Application to Quantifying the Amount of Gray Matter , 2007, IEEE Transactions on Medical Imaging.

[41]  Matthew J. Brookes,et al.  Optimising experimental design for MEG resting state functional connectivity measurement , 2017, NeuroImage.

[42]  Karl J. Friston,et al.  Algorithmic procedures for Bayesian MEG/EEG source reconstruction in SPM , 2014, NeuroImage.

[43]  Hubert Preissl,et al.  Source Reconstruction Accuracy of MEG and EEG Bayesian Inversion Approaches , 2012, PloS one.

[44]  Gareth R. Barnes,et al.  Non-invasive laminar inference with MEG: Comparison of methods and source inversion algorithms , 2017, NeuroImage.

[45]  Ping Li,et al.  Altered resting state functional connectivity patterns of the anterior prefrontal cortex in obsessive-compulsive disorder , 2012, Neuroreport.

[46]  Luc H. Arnal,et al.  Cortical oscillations and sensory predictions , 2012, Trends in Cognitive Sciences.

[47]  Nikolaus Weiskopf,et al.  Flexible head-casts for high spatial precision MEG , 2017, Journal of Neuroscience Methods.

[48]  Mark W. Woolrich,et al.  Measurement of dynamic task related functional networks using MEG , 2017, NeuroImage.

[49]  D. Lehmann,et al.  Adaptive segmentation of spontaneous EEG map series into spatially defined microstates. , 1993, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[50]  R. Lanius,et al.  Resting-State Neuroimaging Studies: A New Way of Identifying Differences and Similarities among the Anxiety Disorders? , 2014, Canadian journal of psychiatry. Revue canadienne de psychiatrie.