Document Type : Full Research Paper

Authors

1 PHD Candidate of Biomedical Engineering, Control and Intelligent Processing Center of Excellence, School of Electrical and Computer Engineering, College of Engineering, University of Tehran

2 Associate Professor of Biomedical Engineering, Control and Intelligent Processing Center of Excellence, School of Electrical and Computer Engineering, College of Engineering, University of Tehran - School of Cognitive Sciences, Institute for Research in Fundamental Sciences (IPM)

10.22041/ijbme.2014.13050

Abstract

In EEG/MEG datasets, the Volume Conduction (VC) artifact appears as instantaneous linear mixing of brain source activities on the channel measurements. A desired characteristic of an ideal EEG/MEG connectivity estimator (on sensor-space) is its robustness to VC artifact. This means that the VC of independent brain sources must never lead to detection of significant connectivity among EEG/MEG channels. There has been no criterion in the literature so far that can compare the robustness levels of different (sensor-space) connectivity estimators against VC artifact. In this paper, a criterion called Robustness Index (RI) is proposed to compare the robustness levels of connectivity estimators to channel couplings which are modeled by instantaneous linear mixing of quasi-independent components. Since the VC effects have instantaneous linear mixing nature, we expect RI to rank the connectivity estimators according to their robustness levels to VC artifact. RI is used to rank seven functional connectivity estimators: the absolute value of Pearson Correlation Coefficient (CC), Mutual Information (MI), Magnitude Squared Coherence (Coh), (1:1) Phase Locking Value ((1:1)PLV), the absolute value of Imaginary part of Coherency (ImC), Phase Lag Index (PLI) and Weighted Phase Lag Index (WPLI). The results for simulated data and a real EEG dataset show the connectivity estimators that are theoretically robust to VC artifact (ImC, PLI and WPLI) yield RI values near %100 and have the highest ranks, as expected. Also, for the simulated models in which the true VC effects and brain sources are known, ranking the connectivity estimators by RI is consistent with their robustness levels against VC artifact. This supports the possibility of using RI as a tool for ranking the robustness levels of connectivity estimators against VC artifact for real EEG/MEG datasets.

Keywords

Main Subjects

[1]     O. Sporns, and G. Tononi, “Structural determinants of functional brain dynamics” in Handbook of Brain Connectivity, V. K. Jirsa and A. R. McIntosh, Eds. Berlin Heidelberg: Springer-Verlag, 2007, pp. 117–119.
[2]     G. Rippon, J. Brock, C. Brown, and J. Boucher, “Disordered connectivity in the autistic brain: Challenges for the ‘new psychophysiology’,” Int. J. Psychophysiol., 2007, 63:164–172.
[3]     J. R. Hughes, “Autism: The first firm finding = underconnectivity?,” Epilepsy & Behavior, 2007, 11:20–24.
[5]     Y. He, Z. Chen, G. Gong, and A. Evans, “Neuronal Networks in Alzheimer’s Disease,” Neuroscientist, 2009, 15(4):333-350.
[6]     C. J. Stam, “Use of magnetoencephalography (MEG) to study functional brain networks in neurodegenerative disorders,” J. Neurol. Sci., 2010, 289(1-2):128-134.
[7]     M. Jalili, and M. G. Knyazeva, “EEG-based functional networks in schizophrenia,” Comput. Biol. Med., 2011, 41(12):1178–1186.
[8]     M. E. Lynall, D. S. Bassett, R. KerwinP. J. McKenna, M. Kitzbichler, U. Muller, and E. Bullmore, “Functional connectivity and brain networks in schizophrenia,” J. Neurosci., 2010, 30(28):9477-9487.
[9]     L. Amini, C. Jutten, S. Achard, O. David, P. Kahane, L. Vercueil, L. Minotti, G. A. Hossein-Zadeh, and H. Soltanian-Zadeh, “Comparison of five directed graph measures for identification of leading interictal epileptic regions,” Physiol. Meas., 2010, 31:1529–1546.
[10] L. Amini, C. Jutten, S. Achard, O. David, H. Soltanian-Zadeh, G. A. Hossein-Zadeh, P. Kahne, L. Minotti, L. Vercueil, “Directed differential connectivity graph of interictal epileptiform discharges,” IEEE Trans. Biomed. Eng., 2010,58(4):884-893.
[11] B. He, L. Yang, C. Wilke, and H. Yuan, “Electrophysiological imaging of brain activity and connectivity—challenges and opportunities,” IEEE Trans. Biomed. Eng., 2011, 58(7):1918-1931.
[12] P. L. Nunez, and R. Srinivasan, Electric fields in the brain: the neurophysics of EEG, Oxford University Press., 2005.
[13] P. L. Nunez, R. Srinivasan, A. F. Westdorp, R. S. Wijesinghe, D. M. Tucker, R. B. Silberstein, and P. J. Cadusch, “EEG coherency. I. Statistics, reference electrode, volume conduction, Laplacians, cortical imaging, and interpretation at multiple scales,” Electroencephalogr. Clin. Neurophysiol., 1997, 103:499–515.
[14] Schoffelen J. M., and Gross J., “Source connectivity analysis with MEG and MEG,” Hum. Brain Mapp., 2009, 30:1857–1865.
[15] C. Cao, and S. Slobounov, “Alteration of cortical functional connectivity as a result of traumatic brain injury Revealed by graph theory, ICA, and sLORETA Analyses of EEG signals,” IEEE Trans. Neural Syst. Rehabil. Eng., 2010, 18(1):11-19.
[16] G. Nolte, O. Bai, L. Wheaton, Z. Mari, S. Vorbach, and M. Hallett,  “Identifying true brain interaction from EEG data using the imaginary part of coherency,” Clin. Neurophysiol., 2004, 115:2292–2307.
[17] A. Ewald, L. Marzetti, F. Zappasodi, F. C. Meinecke, and G. Nolte, “Estimating true brain connectivity from EEG/MEG data invariant to linear and static transformations in sensor space,” NeuroImage, 2012, 60:476–488.
[18] C. J. Stam, G. Nolte, and A. Daffertshofer, “Phase lag index: assessment of functional connectivity from multi channel EEG and MEG with diminished bias from common sources,” Hum. Brain Mapp., 2007, 28:1178–1193.
[19] M. Vinck, R. Oostenveld, M. van Wingerden, F. Battaglia, and C. M. A. Pennartz, “An improved index of phase-synchronization for electrophysiological data in the presence of volume-conduction, noise and sample-size bias,” NeuroImage, 2011, 55:1548–1565.
[20] C. J. Stam, and E. C. W. van Straaten, “Go with the flow: Use of a directed phase lag index (dPLI) to characterize patterns of phase relations in a large-scale model of brain dynamics,” NeuroImage, 2012, 62:1415–1428.
[21] Cover T. M. and Thomas J. M., Elements of information theory, Second edition, John Wiley & Sons, 2006.
[22] J. S. Bandat and A. G. Piersol, Random Data, Whily-Interscience, 1986.
[23] J. P. Lachaux, E. Rodriguez, J. Martinerie, and F. J. Varela, “Measuring phase synchrony in brain signals,” Hum. Brain Mapp., 1999, 8:194–208.
[24] L. Faes, G. Nollo, and A. Porta, “Information-based detection of nonlinear Granger causality in multivariate processes via a non uniform embedding technique,” Phys. Rev. E., 2011, 83(5):051112.
[25] L. Faes, A. Porta, and G. Nollo, “Mutual nonlinear prediction as a tool to evaluate coupling strength and directionality in bivariate time series: Comparison among different strategies based on k nearest neighbors,” Phys. Rev. E., 2008, 78(2):026201.
[26] R. Q. Quiroga, A. Kraskov, T. Kreuz, and P. Grassberger, “Performance of different synchronization measures in real data: A case study on electroencephalographic signals,” Phys. Rev. E., 2002, 65(4):041903.
[27] I. Vlachos, and D. Kugiumtzis, “Nonuniform state-space reconstruction and coupling detection,” Phys. Rev. E., 2010, 82(1):016207.
[28] F. Shahbazi, A. Ewald, A. Ziehe, and G. Nolte, “Constructing surrogate data to control for artifacts of volume conduction for functional connectivity measures,” in Proc. Biomag2010 IFMBE, Dubrovnik, Croatia, 2010, pp. 207–210.
[29] Rutanen K., TIM C++ library, Available online: http://www.tut.fi/tim.
[30] Gomez-Herrero G., “Brain connectivity analysis with EEG,” PHD Dissertation, Tamper university of technology, 2010.
[31] F. Mormann, K. Lehnertz, P. David, and C. E. Elger, “Mean phase coherence as a measure for phase synchronization and its application to the EEG of epilepsy patients,” Physica. D, 2000, 144:358–369.
[32] David O., Cosmelli D. and Friston K. J., “Evaluation of different measures of functional connectivity using a neural mass model,” NeuroImage, 2004, 21:659–673.
[33] Delorme A. and Makeig S., “EEGLAB: an open source toolbox for analysis of single trial EEG dynamics including independent component analysis,” J. Neurosci. Methods, 2004, 134(1):9–21.
[34] EEGLAB freeware,  Available online: sccn.ucsd.edu/eeglab
[35] Lee T. W., Girolami M., Bell A. J. and Sejnowski T. J., “A unifying information theoretic framework for independent component analysis,” Comput. Math. Appl., 2000, 31:1–21.
[36] P. Sauseng, and W. Klimesch, “What does phase information of oscillatory brain activity tell us about cognitive processes?,” Neurosci. Biobehav. Rev., 2008, 32:1001–1013.   
[37] A. Delorme, J. Palmer, J. Onton, R. Oostenveld, S. Makeig, “Independent EEG sources are dipolar,” Plos One, 2012, 7(2):e30135.