Multichannel Time–Frequency Complexity Measures for the Analysis of Age-Related Changes in Neuromagnetic Resting-State Activity

We propose new multichannel time–frequency complexity measures to evaluate differences on magnetoencephalograpy (MEG) recordings between healthy young and old subjects at rest at different spatial scales. After reviewing the Rényi and singular value decomposition entropies based on time–frequency representations, we introduce multichannel generalizations, using multilinear singular value decomposition for one of them. We test these quantities on synthetic data, illustrating how the introduced complexity measures focus on number of components, nonstationarity, and similarity across channels. Friedman tests are used to confirm the differences between young and old groups, and heterogeneity within groups. Experimental results show a consistent increase in complexity measures for the old group. When analyzing the topographical distribution of complexity values, we found clusters in the frontal sensors. The complexity measures here introduced seem to be a better indicator of the neurophysiologic changes of aging than power envelope connectivity. Here, we applied new multichannel time–frequency complexity measures to resting-state MEG recordings from healthy young and old subjects. We showed that these features are able to reveal regional clusters. The multichannel time–frequency complexities can be used to monitor the aging of subjects. They also allow a mutual information approach, and could be applied to a wider range of problems.

[1]  Darren Price,et al.  Investigating the electrophysiological basis of resting state networks using magnetoencephalography , 2011, Proceedings of the National Academy of Sciences.

[2]  I. Percival,et al.  A spectral entropy method for distinguishing regular and irregular motion of Hamiltonian systems , 1979 .

[3]  D. Abásolo,et al.  Brain oscillatory complexity across the life span , 2012, Clinical Neurophysiology.

[4]  Wens Vincent,et al.  The electrophysiological connectome is maintained in healthy elders: a power envelope correlation MEG study , 2016 .

[5]  David Bartrés-Faz,et al.  Reorganization of brain networks in aging: a review of functional connectivity studies , 2015, Front. Psychol..

[6]  Wu Hau-Tieng,et al.  Using synchrosqueezing transform to discover breathing dynamics from ECG signals , 2011 .

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

[8]  J. Schoffelen,et al.  Source connectivity analysis with MEG and EEG , 2009, Human brain mapping.

[9]  Sylvain Meignen,et al.  Second-Order Synchrosqueezing Transform or Invertible Reassignment? Towards Ideal Time-Frequency Representations , 2015, IEEE Transactions on Signal Processing.

[10]  Bruno Torrésani,et al.  Multiridge detection and time-frequency reconstruction , 1999, IEEE Trans. Signal Process..

[11]  S. Rossi,et al.  Clinical neurophysiology of aging brain: From normal aging to neurodegeneration , 2007, Progress in Neurobiology.

[12]  S. Taulu,et al.  Applications of the signal space separation method , 2005, IEEE Transactions on Signal Processing.

[13]  J. Obleser,et al.  States and traits of neural irregularity in the age-varying human brain , 2017, Scientific Reports.

[14]  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.

[15]  Mathieu Bourguignon,et al.  About the electrophysiological basis of resting state networks , 2014, Clinical Neurophysiology.

[16]  Tony Lindeberg,et al.  Scale-space theory : A framework for handling image structures at multiple scales , 1996 .

[17]  Matthew J. Brookes,et al.  How do spatially distinct frequency specific MEG networks emerge from one underlying structural connectome? The role of the structural eigenmodes , 2019, NeuroImage.

[18]  John M. O'Toole,et al.  Time-Frequency Processing of Nonstationary Signals: Advanced TFD Design to Aid Diagnosis with Highlights from Medical Applications , 2013, IEEE Signal Processing Magazine.

[19]  William J. Williams,et al.  Uncertainty, information, and time-frequency distributions , 1991, Optics & Photonics.

[20]  Olivier J. J. Michel,et al.  Measuring time-Frequency information content using the Rényi entropies , 2001, IEEE Trans. Inf. Theory.

[21]  Victor Sucic,et al.  Instantaneous counting of components in nonstationary signals , 2013, 21st European Signal Processing Conference (EUSIPCO 2013).

[22]  J. Martinerie,et al.  The brainweb: Phase synchronization and large-scale integration , 2001, Nature Reviews Neuroscience.

[23]  D. Botstein,et al.  Singular value decomposition for genome-wide expression data processing and modeling. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[24]  Daniel Abásolo,et al.  Complexity Changes in Brain Activity in Healthy Ageing: A Permutation Lempel-Ziv Complexity Study of Magnetoencephalograms , 2018, Entropy.

[25]  P. Nunez Toward a quantitative description of large-scale neocortical dynamic function and EEG , 2000, Behavioral and Brain Sciences.

[26]  Tony Lindeberg Kth Scale-space: A framework for handling image structures at multiple scales , 1996 .

[27]  E. Pekkonen Mismatch Negativity in Aging and in Alzheimer’s and Parkinson’s Diseases , 2000, Audiology and Neurotology.

[28]  Daniel Abásolo,et al.  Permutation Entropy for the Characterisation of Brain Activity Recorded with Magnetoencephalograms in Healthy Ageing , 2017, Entropy.

[29]  Joos Vandewalle,et al.  A Multilinear Singular Value Decomposition , 2000, SIAM J. Matrix Anal. Appl..

[30]  P. Rossini,et al.  Sources of cortical rhythms in adults during physiological aging: A multicentric EEG study , 2006, Human brain mapping.

[31]  Bruno Torrésani,et al.  Characterization of signals by the ridges of their wavelet transforms , 1997, IEEE Trans. Signal Process..

[32]  F. L. D. Silva,et al.  Dynamics of the human alpha rhythm: evidence for non-linearity? , 1999, Clinical Neurophysiology.

[33]  Stéphane Mallat,et al.  A Wavelet Tour of Signal Processing - The Sparse Way, 3rd Edition , 2008 .

[34]  R. Ilmoniemi,et al.  Magnetoencephalography-theory, instrumentation, and applications to noninvasive studies of the working human brain , 1993 .

[35]  Anne Humeau-Heurtier,et al.  Time-Varying Time–Frequency Complexity Measures for Epileptic EEG Data Analysis , 2018, IEEE Transactions on Biomedical Engineering.

[36]  K. Lai,et al.  A new approach for crude oil price analysis based on Empirical Mode Decomposition , 2008 .

[37]  Madalena Costa,et al.  Multiscale entropy analysis of complex physiologic time series. , 2002, Physical review letters.

[38]  A. Engel,et al.  Spectral fingerprints of large-scale neuronal interactions , 2012, Nature Reviews Neuroscience.

[39]  Vasily A. Vakorin,et al.  Spatiotemporal Dependency of Age-Related Changes in Brain Signal Variability , 2013, Cerebral cortex.

[40]  Winfried Schlee,et al.  Resting-state slow wave power, healthy aging and cognitive performance , 2014, Scientific Reports.

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

[42]  Madalena Costa,et al.  Multiscale entropy analysis of biological signals. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.