Information-theoretical analysis of resting state EEG microstate sequences - non-Markovianity, non-stationarity and periodicities

We present an information-theoretical analysis of temporal dependencies in EEG microstate sequences during wakeful rest. We interpret microstate sequences as discrete stochastic processes where each state corresponds to a representative scalp potential topography. Testing low-order Markovianity of these discrete sequences directly, we find that none of the recordings fulfils the Markov property of order 0, 1 or 2. Further analyses show that the microstate transition matrix is non-stationary over time in 80% (window size 10 s), 60% (window size 20 s) and 44% (window size 40 s) of the subjects, and that transition matrices are asymmetric in 14/20 (70%) subjects. To assess temporal dependencies globally, the time-lagged mutual information function (autoinformation function) of each sequence is compared to the first-order Markov model defined by the classical transition matrix approach. The autoinformation function for the Markovian case is derived analytically and numerically. For experimental data, we find non-Markovian behaviour in the range of the main EEG frequency bands where distinct periodicities related to the subject's EEG frequency spectrum appear. In particular, the microstate clustering algorithm induces frequency doubling with respect to the EEG power spectral density while the tail of the autoinformation function asymptotically reaches the first-order Markov confidence interval for time lags above 1000 ms. In summary, our results show that resting state microstate sequences are non-Markovian processes which inherit periodicities from the underlying EEG dynamics. Our results interpolate between two diverging models of microstate dynamics, memoryless Markov models on one side, and long-range correlated models on the other: microstate sequences display more complex temporal dependencies than captured by the transition matrix approach in the range of the main EEG frequency bands, but show finite memory content in the long run.

[1]  Christoph M. Michel,et al.  EEG microstates of wakefulness and NREM sleep , 2012, NeuroImage.

[2]  Enzo Tagliazucchi,et al.  Dynamic BOLD functional connectivity in humans and its electrophysiological correlates , 2012, Front. Hum. Neurosci..

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

[4]  K. Linkenkaer-Hansen,et al.  Long-Range Temporal Correlations and Scaling Behavior in Human Brain Oscillations , 2001, The Journal of Neuroscience.

[5]  Christoph M. Michel,et al.  Spatiotemporal Analysis of Multichannel EEG: CARTOOL , 2011, Comput. Intell. Neurosci..

[6]  D. Lehmann,et al.  Segmentation of brain electrical activity into microstates: model estimation and validation , 1995, IEEE Transactions on Biomedical Engineering.

[7]  J. McCauley,et al.  Markov processes, Hurst exponents, and nonlinear diffusion equations: With application to finance , 2006, cond-mat/0602316.

[8]  Bruce J. West,et al.  The dynamics of EEG entropy , 2009, Journal of biological physics.

[9]  Kevin E. Bassler,et al.  Hurst exponents, Markov processes, and fractional Brownian motion , 2006, cond-mat/0609671.

[10]  George E. P. Box,et al.  Time Series Analysis: Forecasting and Control , 1977 .

[11]  Enzo Tagliazucchi,et al.  Analytical and empirical fluctuation functions of the EEG microstate random walk - Short-range vs. long-range correlations , 2016, NeuroImage.

[12]  T. W. Anderson,et al.  Statistical Inference about Markov Chains , 1957 .

[13]  C. Peng,et al.  Long-range correlations in nucleotide sequences , 1992, Nature.

[14]  B. Mandelbrot,et al.  Fractional Brownian Motions, Fractional Noises and Applications , 1968 .

[15]  P. Robinson,et al.  Prediction of electroencephalographic spectra from neurophysiology. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[16]  P. Billingsley,et al.  Statistical Methods in Markov Chains , 1961 .

[17]  Eduardo Ríos,et al.  Intracellular Ca(2+) release as irreversible Markov process. , 2002, Biophysical journal.

[18]  Solomon Kullback,et al.  Information Theory and Statistics , 1960 .

[19]  D Lehmann,et al.  EEG alpha map series: brain micro-states by space-oriented adaptive segmentation. , 1987, Electroencephalography and clinical neurophysiology.

[20]  Han Yuan,et al.  Spatiotemporal dynamics of the brain at rest — Exploring EEG microstates as electrophysiological signatures of BOLD resting state networks , 2012, NeuroImage.

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

[22]  S. Kullback,et al.  Tests for Contingency Tables and Marltov Chains , 1962 .

[23]  Denis Brunet,et al.  Topographic ERP Analyses: A Step-by-Step Tutorial Review , 2008, Brain Topography.

[24]  Jianbo Gao,et al.  A tutorial introduction to adaptive fractal analysis , 2012, Front. Physio..

[25]  Olle Häggström Finite Markov Chains and Algorithmic Applications , 2002 .

[26]  Feller William,et al.  An Introduction To Probability Theory And Its Applications , 1950 .

[27]  Ernst Fernando Lopes Da Silva Niedermeyer,et al.  Electroencephalography, basic principles, clinical applications, and related fields , 1982 .

[28]  Dietrich Lehmann,et al.  A deviant EEG brain microstate in acute, neuroleptic-naive schizophrenics at rest , 1999, European Archives of Psychiatry and Clinical Neuroscience.

[29]  Dimitri Van De Ville,et al.  Long-range dependencies make the difference—Comment on “A stochastic model for EEG microstate sequence analysis” , 2015, NeuroImage.

[30]  Juliane Britz,et al.  EEG microstate sequences in healthy humans at rest reveal scale-free dynamics , 2010, Proceedings of the National Academy of Sciences.

[31]  Enzo Tagliazucchi,et al.  Narcoleptic Patients Show Fragmented EEG-Microstructure During Early NREM Sleep , 2014, Brain Topography.

[32]  Bruce J. West,et al.  Dynamics of electroencephalogram entropy and pitfalls of scaling detection. , 2010, Physical review. E, Statistical, nonlinear, and soft matter physics.

[33]  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.

[34]  Helmut Laufs,et al.  A stochastic model for EEG microstate sequence analysis , 2015, NeuroImage.