Exploring MEG brain fingerprints: Evaluation, pitfalls, and interpretations

Individual characterization of subjects based on their functional connectome (FC), termed "FC fingerprinting", has become a highly sought-after goal in contemporary neuroscience research. Recent functional magnetic resonance imaging (fMRI) studies have demonstrated unique characterization and accurate identification of individuals as an accomplished task. However, FC fingerprinting in magnetoencephalography (MEG) data is still widely unexplored. Here, we study resting-state MEG data from the Human Connectome Project to assess the MEG FC fingerprinting and its relationship with several factors including amplitude- and phase-coupling functional connectivity measures, spatial leakage correction, frequency bands, and behavioral significance. To this end, we first employ two identification scoring methods, differential identifiability and success rate, to provide quantitative fingerprint scores for each FC measurement. Secondly, we explore the edgewise and nodal MEG fingerprinting patterns across the different frequency bands (delta, theta, alpha, beta, and gamma). Finally, we investigate the cross-modality fingerprinting patterns obtained from MEG and fMRI recordings from the same subjects. We assess the behavioral significance of FC across connectivity measures and imaging modalities using partial least square correlation analyses. Our results suggest that fingerprinting performance is heavily dependent on the functional connectivity measure, frequency band, identification scoring method, and spatial leakage correction. We report higher MEG fingerprints in phase-coupling methods, central frequency bands (alpha and beta), and in the visual, frontoparietal, dorsal-attention, and default-mode networks. Furthermore, cross-modality comparisons reveal a certain degree of spatial concordance in fingerprinting patterns between the MEG and fMRI data, especially in the visual system. Finally, the multivariate correlation analyses show that MEG connectomes have strong behavioral significance, which however depends on the considered connectivity measure and temporal scale. This comprehensive, albeit preliminary investigation of MEG connectome test-retest identification offers a first characterization of MEG fingerprinting in relation to different methodological and electrophysiological factors and contributes to the understanding of fingerprinting cross-modal relationships. We hope that this first investigation will contribute to setting the grounds for MEG connectome identification.

[1]  Gian Luca Marcialis,et al.  Robustness of functional connectivity metrics for EEG-based personal identification over task-induced intra-class and inter-class variations , 2019, Pattern Recognit. Lett..

[2]  Anthony Randal McIntosh,et al.  Partial Least Squares (PLS) methods for neuroimaging: A tutorial and review , 2011, NeuroImage.

[3]  Terry K Koo,et al.  A Guideline of Selecting and Reporting Intraclass Correlation Coefficients for Reliability Research. , 2016, Journal Chiropractic Medicine.

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

[5]  Fabio Baselice,et al.  An extension of Phase Linearity Measurement for revealing cross frequency coupling among brain areas , 2019, Journal of NeuroEngineering and Rehabilitation.

[6]  Matteo Fraschini,et al.  EEG fingerprinting: subject specific signature based on the aperiodic component of power spectrum , 2020, Comput. Biol. Medicine.

[7]  F. I. Karahanoğlu,et al.  Large-scale brain network dynamics provide a measure of psychosis and anxiety in 22q11.2 deletion syndrome , 2019, bioRxiv.

[8]  Andrew Zalesky,et al.  High-resolution connectomic fingerprints: Mapping neural identity and behavior , 2021, NeuroImage.

[9]  Edwin van Dellen,et al.  Structural degree predicts functional network connectivity: A multimodal resting-state fMRI and MEG study , 2014, NeuroImage.

[10]  R. Deriche,et al.  From Diffusion MRI to Brain Connectomics , 2013 .

[11]  Mark W. Woolrich,et al.  Measuring functional connectivity in MEG: A multivariate approach insensitive to linear source leakage , 2012, NeuroImage.

[12]  Pierpaolo Sorrentino,et al.  Phase Linearity Measurement: A Novel Index for Brain Functional Connectivity , 2019, IEEE Transactions on Medical Imaging.

[13]  Ben D. Fulcher,et al.  Bridging the Gap between Connectome and Transcriptome , 2019, Trends in Cognitive Sciences.

[14]  O. Sporns,et al.  Complex brain networks: graph theoretical analysis of structural and functional systems , 2009, Nature Reviews Neuroscience.

[15]  Xavier Bresson,et al.  Transient networks of spatio-temporal connectivity map communication pathways in brain functional systems , 2017, NeuroImage.

[16]  J. Palva,et al.  Discovering oscillatory interaction networks with M/EEG: challenges and breakthroughs , 2012, Trends in Cognitive Sciences.

[17]  M. Breakspear,et al.  The connectomics of brain disorders , 2015, Nature Reviews Neuroscience.

[18]  Thomas E. Nichols,et al.  A positive-negative mode of population covariation links brain connectivity, demographics and behavior , 2015, Nature Neuroscience.

[19]  M. Chun,et al.  Functional connectome fingerprinting: Identifying individuals based on patterns of brain connectivity , 2015, Nature Neuroscience.

[20]  Joaquín Goñi,et al.  Uncovering multi-site identifiability based on resting-state functional connectomes , 2018, NeuroImage.

[21]  Matthew J. Brookes,et al.  Measuring functional connectivity using MEG: Methodology and comparison with fcMRI , 2011, NeuroImage.

[22]  Thomas J. Wills,et al.  Reconciling the different faces of hippocampal theta: The role of theta oscillations in cognitive, emotional and innate behaviors , 2018, Neuroscience & Biobehavioral Reviews.

[23]  Suresh C. Mehrotra,et al.  Introduction to EEG- and Speech-Based Emotion Recognition , 2016 .

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

[25]  B. W. van Dijk,et al.  Opportunities and methodological challenges in EEG and MEG resting state functional brain network research , 2015, Clinical Neurophysiology.

[26]  C. Stam,et al.  Phase lag index: Assessment of functional connectivity from multi channel EEG and MEG with diminished bias from common sources , 2007, Human brain mapping.

[27]  Enrico Amico,et al.  Multi-timescale hybrid components of the functional brain connectome: A bimodal EEG-fMRI decomposition , 2019, bioRxiv.

[28]  Mark Jenkinson,et al.  The minimal preprocessing pipelines for the Human Connectome Project , 2013, NeuroImage.

[29]  Essa Yacoub,et al.  The WU-Minn Human Connectome Project: An overview , 2013, NeuroImage.

[30]  Jonathan D. Power,et al.  Evidence for Hubs in Human Functional Brain Networks , 2013, Neuron.

[31]  W. Klimesch Alpha-band oscillations, attention, and controlled access to stored information , 2012, Trends in Cognitive Sciences.

[32]  O. Sporns,et al.  Network neuroscience , 2017, Nature Neuroscience.

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

[34]  H H Donaldson,et al.  LOCALIZATION IN THE BRAIN. , 1884, Science.

[35]  Sylvain Baillet,et al.  MEG, myself, and I: individual identification from neurophysiological brain activity , 2021, bioRxiv.

[36]  Edward T. Bullmore,et al.  Connectomics: A new paradigm for understanding brain disease , 2015, European Neuropsychopharmacology.

[37]  Anders M. Dale,et al.  An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest , 2006, NeuroImage.

[38]  F. I. Karahanoğlu,et al.  Large-Scale Brain Network Dynamics Provide a Measure of Psychosis and Anxiety in 22q11.2 Deletion Syndrome. , 2019, Biological psychiatry. Cognitive neuroscience and neuroimaging.

[39]  C. Stam Modern network science of neurological disorders , 2014, Nature Reviews Neuroscience.

[40]  Karl J. Friston Functional and effective connectivity in neuroimaging: A synthesis , 1994 .

[41]  C. Stam,et al.  The organization of physiological brain networks , 2012, Clinical Neurophysiology.

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

[43]  Robert Oostenveld,et al.  An improved index of phase-synchronization for electrophysiological data in the presence of volume-conduction, noise and sample-size bias , 2011, NeuroImage.

[44]  João Ricardo Sato,et al.  Identifying individuals using fNIRS-based cortical connectomes. , 2019, Biomedical optics express.

[45]  Mark W. Woolrich,et al.  MEG beamforming using Bayesian PCA for adaptive data covariance matrix regularization , 2011, NeuroImage.

[46]  G. Buzsáki,et al.  Neuronal Oscillations in Cortical Networks , 2004, Science.

[47]  Enrico Amico,et al.  GEFF: Graph embedding for functional fingerprinting , 2020, NeuroImage.

[48]  Gian Luca Marcialis,et al.  An EEG-Based Biometric System Using Eigenvector Centrality in Resting State Brain Networks , 2015, IEEE Signal Processing Letters.

[49]  A. Engel,et al.  Beta-band oscillations—signalling the status quo? , 2010, Current Opinion in Neurobiology.

[50]  Dustin Scheinost,et al.  Influences on the Test–Retest Reliability of Functional Connectivity MRI and its Relationship with Behavioral Utility , 2017, Cerebral cortex.

[51]  Martijn P. van den Heuvel,et al.  The parcellation-based connectome: Limitations and extensions , 2013, NeuroImage.

[52]  K. McGraw,et al.  Forming inferences about some intraclass correlation coefficients. , 1996 .

[53]  Priya Aggarwal,et al.  Multivariate brain network graph identification in functional MRI , 2017, Medical Image Anal..

[54]  Fabio Babiloni,et al.  Human Brain Distinctiveness Based on EEG Spectral Coherence Connectivity , 2014, IEEE Transactions on Biomedical Engineering.

[55]  Steen Moeller,et al.  The Human Connectome Project: A data acquisition perspective , 2012, NeuroImage.

[56]  R. Malenka,et al.  Closing the loop on impulsivity via nucleus accumbens delta-band activity in mice and man , 2017, Proceedings of the National Academy of Sciences.

[57]  Edward T. Bullmore,et al.  Fundamentals of Brain Network Analysis , 2016 .

[58]  Joerg F. Hipp,et al.  BOLD fMRI Correlation Reflects Frequency-Specific Neuronal Correlation , 2015, Current Biology.

[59]  Bernard Ng,et al.  Optimization of rs-fMRI Pre-processing for Enhanced Signal-Noise Separation, Test-Retest Reliability, and Group Discrimination , 2015, NeuroImage.

[60]  Thomas E. Nichols,et al.  Nonparametric permutation tests for functional neuroimaging: A primer with examples , 2002, Human brain mapping.

[61]  Fernando Maestú,et al.  Multimodal description of whole brain connectivity: A comparison of resting state MEG, fMRI, and DWI , 2015, Human brain mapping.

[62]  Damien A. Fair,et al.  Connectotyping: Model Based Fingerprinting of the Functional Connectome , 2014, PloS one.

[63]  Monica D. Rosenberg,et al.  Beyond fingerprinting: Choosing predictive connectomes over reliable connectomes , 2021, NeuroImage.

[64]  R. Cameron Craddock,et al.  Clinical applications of the functional connectome , 2013, NeuroImage.

[65]  M Corbetta,et al.  A Dynamic Core Network and Global Efficiency in the Resting Human Brain. , 2016, Cerebral cortex.

[66]  Mia Liljeström,et al.  Task- and stimulus-related cortical networks in language production: Exploring similarity of MEG- and fMRI-derived functional connectivity , 2015, NeuroImage.

[67]  Joaquín Goñi,et al.  The quest for identifiability in human functional connectomes , 2017, Scientific Reports.

[68]  Morten L. Kringelbach,et al.  Functional connectivity dynamically evolves on multiple time-scales over a static structural connectome: Models and mechanisms , 2017, NeuroImage.

[69]  C. J. Stam,et al.  Alzheimer’s disease: The state of the art in resting-state magnetoencephalography , 2017, Clinical Neurophysiology.

[70]  Blessin Varkey,et al.  Functional Brain Connectivity Analysis in Intellectual Developmental Disorder During Music Perception , 2020, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[71]  Anders M. Dale,et al.  Automatic parcellation of human cortical gyri and sulci using standard anatomical nomenclature , 2010, NeuroImage.

[72]  Joachim Gross,et al.  Good practice for conducting and reporting MEG research , 2013, NeuroImage.

[73]  F. Varela,et al.  Measuring phase synchrony in brain signals , 1999, Human brain mapping.

[74]  Pia Tikka,et al.  Consistency and similarity of MEG- and fMRI-signal time courses during movie viewing , 2018, NeuroImage.

[75]  Marisa O. Hollinshead,et al.  The organization of the human cerebral cortex estimated by intrinsic functional connectivity. , 2011, Journal of neurophysiology.

[76]  Mark W. Woolrich,et al.  Adding dynamics to the Human Connectome Project with MEG , 2013, NeuroImage.

[77]  M. Corbetta,et al.  Temporal dynamics of spontaneous MEG activity in brain networks , 2010, Proceedings of the National Academy of Sciences.

[78]  Olaf Sporns,et al.  The Human Connectome: A Structural Description of the Human Brain , 2005, PLoS Comput. Biol..

[79]  G. Knyazev,et al.  Neuroscience and Biobehavioral Reviews , 2012 .

[80]  C. Stam,et al.  The effect of epoch length on estimated EEG functional connectivity and brain network organisation , 2016, Journal of neural engineering.

[81]  G. Nolte The magnetic lead field theorem in the quasi-static approximation and its use for magnetoencephalography forward calculation in realistic volume conductors. , 2003, Physics in medicine and biology.

[82]  Abraham Z. Snyder,et al.  Function in the human connectome: Task-fMRI and individual differences in behavior , 2013, NeuroImage.

[83]  D I Boomsma,et al.  Functional and effective whole brain connectivity using magnetoencephalography to identify monozygotic twin pairs , 2017, Scientific Reports.

[84]  J. Bartko The Intraclass Correlation Coefficient as a Measure of Reliability , 1966, Psychological reports.

[85]  Michael Berk,et al.  The new field of ‘precision psychiatry’ , 2017, BMC Medicine.