Mutual Information of Multiple Rhythms for EEG Signals

Electroencephalograms (EEG) are one of the most commonly used measures to study brain functioning at a macroscopic level. The structure of the EEG time series is composed of many neural rhythms interacting at different spatiotemporal scales. This interaction is often named as cross frequency coupling, and consists of transient couplings between various parameters of different rhythms. This coupling has been hypothesized to be a basic mechanism involved in cognitive functions. There are several methods to measure cross frequency coupling between two rhythms but no single method has been selected as the gold standard. Current methods only serve to explore two rhythms at a time, are computationally demanding, and impose assumptions about the nature of the signal. Here we present a new approach based on Information Theory in which we can characterize the interaction of more than two rhythms in a given EEG time series. It estimates the mutual information of multiple rhythms (MIMR) extracted from the original signal. We tested this measure using simulated and real empirical data. We simulated signals composed of three frequencies and background noise. When the coupling between each frequency component was manipulated, we found a significant variation in the MIMR. In addition, we found that MIMR was sensitive to real EEG time series collected with open vs. closed eyes, and intra-cortical recordings from epileptic and non-epileptic signals registered at different regions of the brain. MIMR is presented as a tool to explore multiple rhythms, easy to compute and without a priori assumptions.

[1]  C. Piccardi On the control of chaotic systems via symbolic time series analysis. , 2004, Chaos.

[2]  Josef Parvizi,et al.  Dynamic Changes in Phase-Amplitude Coupling Facilitate Spatial Attention Control in Fronto-Parietal Cortex , 2014, PLoS biology.

[3]  C. Finney,et al.  A review of symbolic analysis of experimental data , 2003 .

[4]  Viktor K. Jirsa,et al.  Cross-frequency coupling in real and virtual brain networks , 2013, Front. Comput. Neurosci..

[5]  M. Wibral,et al.  Untangling cross-frequency coupling in neuroscience , 2014, Current Opinion in Neurobiology.

[6]  Tao Zhang,et al.  A Precise Annotation of Phase-Amplitude Coupling Intensity , 2016, PloS one.

[7]  J. D. Saddy,et al.  Symbolic dynamics of event-related brain potentials. , 2000, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[8]  F. Wendling,et al.  Extraction of spatio-temporal signatures from depth EEG seizure signals based on objective matching in warped vectorial observations , 1996, IEEE Transactions on Biomedical Engineering.

[9]  R. Barry,et al.  EEG differences between eyes-closed and eyes-open resting conditions , 2007, Clinical Neurophysiology.

[10]  P. Graben,et al.  Estimating and improving the signal-to-noise ratio of time series by symbolic dynamics. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[11]  Dezhong Yao,et al.  EEG Scaling Difference Between Eyes-Closed and Eyes-Open Conditions by Detrended Fluctuation Analysis , 2008 .

[12]  J. Lisman,et al.  The Theta-Gamma Neural Code , 2013, Neuron.

[13]  B. Singer,et al.  Controlling the False Discovery Rate: A New Application to Account for Multiple and Dependent Tests in Local Statistics of Spatial Association , 2006 .

[14]  Guy M McKhann,et al.  Ictal high frequency oscillations distinguish two types of seizure territories in humans. , 2013, Brain : a journal of neurology.

[15]  Tao Zhang,et al.  Reduction in LFP cross-frequency coupling between theta and gamma rhythms associated with impaired STP and LTP in a rat model of brain ischemia , 2013, Front. Comput. Neurosci..

[16]  Ling Li,et al.  The Difference of Brain Functional Connectivity between Eyes-Closed and Eyes-Open Using Graph Theoretical Analysis , 2013, Comput. Math. Methods Medicine.

[17]  J. Fell,et al.  The role of phase synchronization in memory processes , 2011, Nature Reviews Neuroscience.

[18]  W. Pennya,et al.  Testing for nested oscillation , 2008 .

[19]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[20]  R. Knight,et al.  Shifts in Gamma Phase–Amplitude Coupling Frequency from Theta to Alpha Over Posterior Cortex During Visual Tasks , 2010, Front. Hum. Neurosci..

[21]  Haruhiko Kishima,et al.  Detection of Epileptic Seizures Using Phase–Amplitude Coupling in Intracranial Electroencephalography , 2016, Scientific Reports.

[22]  Klaus Lehnertz,et al.  Evolving networks in the human epileptic brain , 2013, 1309.4039.

[23]  G. Knyazev,et al.  Cross-Frequency Coupling in Developmental Perspective , 2019, Front. Hum. Neurosci..

[24]  Roberto Hornero,et al.  Interpretation of the auto-mutual information rate of decrease in the context of biomedical signal analysis. Application to electroencephalogram recordings , 2009, Physiological measurement.

[25]  V. Litvak,et al.  Parametric estimation of cross-frequency coupling , 2015, Journal of Neuroscience Methods.

[26]  J. Fell,et al.  Cross-frequency coupling supports multi-item working memory in the human hippocampus , 2010, Proceedings of the National Academy of Sciences.

[27]  Nitin Tandon,et al.  Mutual Information in Frequency and Its Application to Measure Cross-Frequency Coupling in Epilepsy , 2017, IEEE Transactions on Signal Processing.

[28]  José Manuel Pastor,et al.  Symbolic Analysis of Brain Dynamics Detects Negative Stress , 2017, Entropy.

[29]  Adriano B. L. Tort,et al.  Dynamic cross-frequency couplings of local field potential oscillations in rat striatum and hippocampus during performance of a T-maze task , 2008, Proceedings of the National Academy of Sciences.

[30]  Raúl Alcaraz Symbolic Entropy Analysis and Its Applications , 2018, Entropy.

[31]  K Lehnertz,et al.  Indications of nonlinear deterministic and finite-dimensional structures in time series of brain electrical activity: dependence on recording region and brain state. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[32]  R. Knight,et al.  The functional role of cross-frequency coupling , 2010, Trends in Cognitive Sciences.

[33]  C. van Vreeswijk,et al.  What Is the Neural Code , 2006 .

[34]  Barbara F. Händel,et al.  Cross-frequency coupling of brain oscillations indicates the success in visual motion discrimination , 2009, NeuroImage.

[35]  Nicholas M. Timme,et al.  A Tutorial for Information Theory in Neuroscience , 2018, eNeuro.

[36]  Adriano B. L. Tort,et al.  Hippocampal theta rhythm and its coupling with gamma oscillations require fast inhibition onto parvalbumin-positive interneurons , 2009, Proceedings of the National Academy of Sciences.

[37]  E. Novikov,et al.  Scale-similar activity in the brain , 1997 .

[38]  S. Charpier,et al.  Slow modulations of high-frequency activity (40–140 Hz) discriminate preictal changes in human focal epilepsy , 2014, Scientific Reports.

[39]  V. Protopopescu,et al.  Timely detection of dynamical change in scalp EEG signals. , 2000, Chaos.

[40]  N. Logothetis,et al.  Scaling Brain Size, Keeping Timing: Evolutionary Preservation of Brain Rhythms , 2013, Neuron.

[41]  Ankoor S. Shah,et al.  An oscillatory hierarchy controlling neuronal excitability and stimulus processing in the auditory cortex. , 2005, Journal of neurophysiology.

[42]  Biyu J. He Scale-free brain activity: past, present, and future , 2014, Trends in Cognitive Sciences.

[43]  Scott Makeig,et al.  Measuring transient phase-amplitude coupling using local mutual information , 2019, NeuroImage.

[44]  H. Eichenbaum,et al.  Measuring phase-amplitude coupling between neuronal oscillations of different frequencies. , 2010, Journal of neurophysiology.

[45]  M. Berger,et al.  High Gamma Power Is Phase-Locked to Theta Oscillations in Human Neocortex , 2006, Science.

[46]  C. Schroeder,et al.  Low-frequency neuronal oscillations as instruments of sensory selection , 2009, Trends in Neurosciences.

[47]  Yves Grenier,et al.  Non-linear auto-regressive models for cross-frequency coupling in neural time series , 2017, bioRxiv.

[48]  D. Bates,et al.  Fitting Linear Mixed-Effects Models Using lme4 , 2014, 1406.5823.

[49]  Michael X Cohen,et al.  Assessing transient cross-frequency coupling in EEG data , 2008, Journal of Neuroscience Methods.

[50]  Reducing noise in discretized time series. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.