The effect of epoch length on estimated EEG functional connectivity and brain network organisation

OBJECTIVE Graph theory and network science tools have revealed fundamental mechanisms of functional brain organization in resting-state M/EEG analysis. Nevertheless, it is still not clearly understood how several methodological aspects may bias the topology of the reconstructed functional networks. In this context, the literature shows inconsistency in the chosen length of the selected epochs, impeding a meaningful comparison between results from different studies. APPROACH The aim of this study was to provide a network approach insensitive to the effects that epoch length has on functional connectivity and network reconstruction. Two different measures, the phase lag index (PLI) and the amplitude envelope correlation (AEC) were applied to EEG resting-state recordings for a group of 18 healthy volunteers using non-overlapping epochs with variable length (1, 2, 4, 6, 8, 10, 12, 14 and 16 s). Weighted clustering coefficient (CCw), weighted characteristic path length (L w) and minimum spanning tree (MST) parameters were computed to evaluate the network topology. The analysis was performed on both scalp and source-space data. MAIN RESULTS Results from scalp analysis show a decrease in both mean PLI and AEC values with an increase in epoch length, with a tendency to stabilize at a length of 12 s for PLI and 6 s for AEC. Moreover, CCw and L w show very similar behaviour, with metrics based on AEC more reliable in terms of stability. In general, MST parameters stabilize at short epoch lengths, particularly for MSTs based on PLI (1-6 s versus 4-8 s for AEC). At the source-level the results were even more reliable, with stability already at 1 s duration for PLI-based MSTs. SIGNIFICANCE The present work suggests that both PLI and AEC depend on epoch length and that this has an impact on the reconstructed network topology, particularly at the scalp-level. Source-level MST topology is less sensitive to differences in epoch length, therefore enabling the comparison of brain network topology between different studies.

[1]  J. Kruskal On the shortest spanning subtree of a graph and the traveling salesman problem , 1956 .

[2]  D. Louis Collins,et al.  Design and construction of a realistic digital brain phantom , 1998, IEEE Transactions on Medical Imaging.

[3]  Duncan J. Watts,et al.  Collective dynamics of ‘small-world’ networks , 1998, Nature.

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

[5]  Vinod Menon,et al.  Functional connectivity in the resting brain: A network analysis of the default mode hypothesis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

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

[7]  Anders M. Dale,et al.  Spectral spatiotemporal imaging of cortical oscillations and interactions in the human brain , 2004, NeuroImage.

[8]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[9]  Karl J. Friston,et al.  Evaluation of different measures of functional connectivity using a neural mass model , 2004, NeuroImage.

[10]  Krish D. Singh,et al.  A new approach to neuroimaging with magnetoencephalography , 2005, Human brain mapping.

[11]  Arjan Hillebrand,et al.  Beamformer analysis of MEG data. , 2005, International review of neurobiology.

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

[13]  Marianna D. Eddy,et al.  Masked repetition priming and event-related brain potentials: a new approach for tracking the time-course of object perception. , 2006, Psychophysiology.

[14]  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.

[15]  R. Ilmoniemi,et al.  Interpreting magnetic fields of the brain: minimum norm estimates , 2006, Medical and Biological Engineering and Computing.

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

[17]  Olaf Sporns,et al.  Network structure of cerebral cortex shapes functional connectivity on multiple time scales , 2007, Proceedings of the National Academy of Sciences.

[18]  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.

[19]  E. Whitham,et al.  Scalp electrical recording during paralysis: Quantitative evidence that EEG frequencies above 20Hz are contaminated by EMG , 2007, Clinical Neurophysiology.

[20]  M Valencia,et al.  Dynamic small-world behavior in functional brain networks unveiled by an event-related networks approach. , 2008, Physical review. E, Statistical, nonlinear, and soft matter physics.

[21]  Karl J. Friston,et al.  The Dynamic Brain: From Spiking Neurons to Neural Masses and Cortical Fields , 2008, PLoS Comput. Biol..

[22]  Kenneth J. Pope,et al.  Relation of Gamma Oscillations in Scalp Recordings to Muscular Activity , 2009, Brain Topography.

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

[24]  Michael Vourkas,et al.  Tracking brain dynamics via time-dependent network analysis , 2010, Journal of Neuroscience Methods.

[25]  Théodore Papadopoulo,et al.  OpenMEEG: opensource software for quasistatic bioelectromagnetics , 2010, Biomedical engineering online.

[26]  Olaf Sporns,et al.  Complex network measures of brain connectivity: Uses and interpretations , 2010, NeuroImage.

[27]  Martin Vinck,et al.  The pairwise phase consistency: A bias-free measure of rhythmic neuronal synchronization , 2010, NeuroImage.

[28]  Andreas Daffertshofer,et al.  Comparing Brain Networks of Different Size and Connectivity Density Using Graph Theory , 2010, PloS one.

[29]  Selin Aviyente,et al.  A phase synchrony measure for quantifying dynamic functional integration in the brain , 2011, Human brain mapping.

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

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

[32]  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.

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

[34]  Ali Yener Mutlu,et al.  A Signal-Processing-Based Approach to Time-Varying Graph Analysis for Dynamic Brain Network Identification , 2012, Comput. Math. Methods Medicine.

[35]  Gareth R. Barnes,et al.  Frequency-dependent functional connectivity within resting-state networks: An atlas-based MEG beamformer solution , 2012, NeuroImage.

[36]  Olaf Sporns,et al.  Synchronization dynamics and evidence for a repertoire of network states in resting EEG , 2012, Front. Comput. Neurosci..

[37]  M. Kramer,et al.  Emergence of Stable Functional Networks in Long-Term Human Electroencephalography , 2012, The Journal of Neuroscience.

[38]  Matteo Fraschini,et al.  Brain network analysis of EEG functional connectivity during imagery hand movements. , 2013, Journal of integrative neuroscience.

[39]  Richard M. Leahy,et al.  A note on the phase locking value and its properties , 2013, NeuroImage.

[40]  A. Engel,et al.  Intrinsic Coupling Modes: Multiscale Interactions in Ongoing Brain Activity , 2013, Neuron.

[41]  Cornelis J. Stam,et al.  Growing Trees in Child Brains: Graph Theoretical Analysis of Electroencephalography-Derived Minimum Spanning Tree in 5- and 7-Year-Old Children Reflects Brain Maturation , 2013, Brain Connect..

[42]  S. Muthukumaraswamy High-frequency brain activity and muscle artifacts in MEG/EEG: a review and recommendations , 2013, Front. Hum. Neurosci..

[43]  Michael Breakspear,et al.  Low-Dimensional Dynamics of Resting-State Cortical Activity , 2013, Brain Topography.

[44]  Olaf Sporns,et al.  Network attributes for segregation and integration in the human brain , 2013, Current Opinion in Neurobiology.

[45]  David A. Leopold,et al.  Dynamic functional connectivity: Promise, issues, and interpretations , 2013, NeuroImage.

[46]  P. Rapp,et al.  Time domain measures of inter-channel EEG correlations: a comparison of linear, nonparametric and nonlinear measures , 2013, Cognitive Neurodynamics.

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

[48]  Mahmoud Hassan,et al.  EEG Source Connectivity Analysis: From Dense Array Recordings to Brain Networks , 2014, PloS one.

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

[50]  C J Stam,et al.  The trees and the forest: Characterization of complex brain networks with minimum spanning trees. , 2014, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[51]  Karl-Olof Lovblad,et al.  Two Intrinsic Coupling Types for Resting-State Integration in the Human Brain , 2015, Brain Topography.

[52]  Á. Pascual-Leone,et al.  Microstates in resting-state EEG: Current status and future directions , 2015, Neuroscience & Biobehavioral Reviews.

[53]  Jaroslav Hlinka,et al.  On the danger of detecting network states in white noise , 2015, Front. Comput. Neurosci..

[54]  Edwin van Dellen,et al.  The minimum spanning tree: An unbiased method for brain network analysis , 2015, NeuroImage.

[55]  Russell A. Poldrack,et al.  Estimation of dynamic functional connectivity using Multiplication of Temporal Derivatives , 2015, NeuroImage.

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