Multiscale entropy analysis of resting-state magnetoencephalogram with tensor factorisations in Alzheimer's disease

Tensor factorisations have proven useful to model amplitude and spectral information of brain recordings. Here, we assess the usefulness of tensor factorisations in the multiway analysis of other brain signal features in the context of complexity measures recently proposed to inspect multiscale dynamics. We consider the "refined composite multiscale entropy" (rcMSE), which computes entropy "profiles" showing levels of physiological complexity over temporal scales for individual signals. We compute the rcMSE of resting-state magnetoencephalogram (MEG) recordings from 36 patients with Alzheimer's disease and 26 control subjects. Instead of traditional simple visual examinations, we organise the entropy profiles as a three-way tensor to inspect relationships across temporal and spatial scales and subjects with multiway data analysis techniques based on PARAFAC and PARAFAC2 factorisations. A PARAFAC2 model with two factors was appropriate to account for the interactions in the entropy tensor between temporal scales and MEG channels for all subjects. Moreover, the PARAFAC2 factors had information related to the subjects' diagnosis, achieving a cross-validated area under the ROC curve of 0.77. This confirms the suitability of tensor factorisations to represent electrophysiological brain data efficiently despite the unsupervised nature of these techniques. This article is part of a Special Issue entitled 'Neural data analysis'.

[1]  Jeffrey M. Hausdorff,et al.  Fractal dynamics in physiology: Alterations with disease and aging , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[2]  F. D. Silva,et al.  EEG and MEG: Relevance to Neuroscience , 2013, Neuron.

[3]  Francesco Carlo Morabito,et al.  Multivariate Multi-Scale Permutation Entropy for Complexity Analysis of Alzheimer's Disease EEG , 2012, Entropy.

[4]  Fumikazu Miwakeichi,et al.  Decomposing EEG data into space–time–frequency components using Parallel Factor Analysis , 2004, NeuroImage.

[5]  Roberto Hornero,et al.  Analysis of electroencephalograms in Alzheimer's disease patients with multiscale entropy. , 2006 .

[6]  G. Edelman,et al.  Consciousness and Complexity , 1998 .

[7]  Tamara G. Kolda,et al.  Tensor Decompositions and Applications , 2009, SIAM Rev..

[8]  Andrzej Cichocki,et al.  Multiway array decomposition analysis of EEGs in Alzheimer's disease , 2012, Journal of Neuroscience Methods.

[9]  Andrzej Cichocki,et al.  Tensor Decompositions for Signal Processing Applications: From two-way to multiway component analysis , 2014, IEEE Signal Processing Magazine.

[10]  S. Tsai,et al.  Is mental illness complex? From behavior to brain , 2013, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[11]  J. Chang,et al.  Analysis of individual differences in multidimensional scaling via an n-way generalization of “Eckart-Young” decomposition , 1970 .

[12]  A. McIntosh,et al.  Applications of EEG Neuroimaging Data: Event-related Potentials, Spectral Power, and Multiscale Entropy , 2013, Journal of visualized experiments : JoVE.

[13]  Bülent Yener,et al.  Unsupervised Multiway Data Analysis: A Literature Survey , 2009, IEEE Transactions on Knowledge and Data Engineering.

[14]  Chun-Chieh Wang,et al.  Time Series Analysis Using Composite Multiscale Entropy , 2013, Entropy.

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

[16]  K. Davis,et al.  A new rating scale for Alzheimer's disease. , 1984, The American journal of psychiatry.

[17]  Rasmus Bro,et al.  Multiway analysis of epilepsy tensors , 2007, ISMB/ECCB.

[18]  Lars Kai Hansen,et al.  Shift-invariant multilinear decomposition of neuroimaging data , 2008, NeuroImage.

[19]  R. Bro,et al.  Core consistency diagnostic in PARAFAC2 , 2013 .

[20]  C. Stam,et al.  Nonlinear dynamical analysis of EEG and MEG: Review of an emerging field , 2005, Clinical Neurophysiology.

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

[22]  J. Morris,et al.  The diagnosis of dementia due to Alzheimer’s disease: Recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer's disease , 2011, Alzheimer's & Dementia.

[23]  Javier Escudero,et al.  Inspecting temporal scales with non-linear signal features: A way to extract more information from brain activity? , 2015, Clinical Neurophysiology.

[24]  Richard A. Harshman,et al.  Foundations of the PARAFAC procedure: Models and conditions for an "explanatory" multi-model factor analysis , 1970 .

[25]  C. Nelson,et al.  EEG complexity as a biomarker for autism spectrum disorder risk , 2011, BMC medicine.

[26]  Lars Kai Hansen,et al.  Parallel Factor Analysis as an exploratory tool for wavelet transformed event-related EEG , 2006, NeuroImage.

[27]  S. Folstein,et al.  "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. , 1975, Journal of psychiatric research.

[28]  Chaur-Jong Hu,et al.  Multiscale Entropy Analysis of Electroencephalography During Sleep in Patients With Parkinson Disease , 2013, Clinical EEG and neuroscience.

[29]  M. Folstein,et al.  Clinical diagnosis of Alzheimer's disease , 1984, Neurology.

[30]  Joachim Möcks,et al.  Decomposing event-related potentials: A new topographic components model , 1988, Biological Psychology.

[31]  Roberto Hornero,et al.  Changes in the MEG background activity in patients with positive symptoms of schizophrenia: spectral analysis and impact of age , 2013, Physiological measurement.

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

[33]  S. Sanei,et al.  Regional coherence evaluation in mild cognitive impairment and Alzheimer's disease based on adaptively extracted magnetoencephalogram rhythms , 2011, Physiological measurement.

[34]  W. Ray,et al.  EEG correlates of emotional tasks related to attentional demands. , 1985, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[35]  C. Peng,et al.  Analysis of complex time series using refined composite multiscale entropy , 2014 .

[36]  C. Peng,et al.  Cognitive and neuropsychiatric correlates of EEG dynamic complexity in patients with Alzheimer's disease , 2013, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[37]  Ian M. McDonough,et al.  Network complexity as a measure of information processing across resting-state networks: evidence from the Human Connectome Project , 2014, Front. Hum. Neurosci..

[38]  Danilo P Mandic,et al.  Multivariate multiscale entropy: a tool for complexity analysis of multichannel data. , 2011, Physical review. E, Statistical, nonlinear, and soft matter physics.

[39]  Morten Mørup,et al.  Applications of tensor (multiway array) factorizations and decompositions in data mining , 2011, WIREs Data Mining Knowl. Discov..

[40]  Koichi Takahashi,et al.  Antipsychotics reverse abnormal EEG complexity in drug-naive schizophrenia: A multiscale entropy analysis , 2010, NeuroImage.

[41]  S. Baron-Cohen,et al.  Atypical EEG complexity in autism spectrum conditions: A multiscale entropy analysis , 2011, Clinical Neurophysiology.

[42]  Jaeseung Jeong EEG dynamics in patients with Alzheimer's disease , 2004, Clinical Neurophysiology.

[43]  Roberto Hornero,et al.  Nonlinear analysis of electroencephalogram and magnetoencephalogram recordings in patients with Alzheimer's disease , 2009, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[44]  Patrick Dupont,et al.  Canonical decomposition of ictal scalp EEG reliably detects the seizure onset zone , 2007, NeuroImage.