Evaluation of dynamic scaling of growing interfaces in EEG fluctuations of seizures in animal model of temporal lobe epilepsy

Epileptic seizures, as a dynamic phenomenon in brain behavior, obey a scale-free behavior, frequently analyzed by electrical activity recording. This recording can be seen as a surface that roughens with time. Dynamic scaling studies roughening processes or growing interfaces. In this theory, a set of exponents -obtained from scale invariance properties- characterize rough interfaces growth. The aim of the present study was to investigate scaling behavior in EEG time series fluctuations of a chemical animal model of temporal lobe epilepsy, with dynamic scaling to detect changes on seizure onset. We analyzed local variables in different sampling intervals and estimated rough, scaling and dynamic exponents. Results exhibited long-range correlations in interictal activity. Results of renormalization and data collapsing confirmed that each epoch of EEG fluctuations for interictal, preictal and postictal collapse in a curve in different scales, each segment independently; remarkably, we found non-scaling behavior in seizures epochs. Data for the different sampling intervals for ictal period do not collapse in one curve, which implies that ictal activity does not exhibit the same scaling behavior than the other epochs. Statistical significant differences of growth exponent were found between interictal and ictal segment, while for scaling exponent, significant differences were found between interictal and postictal segment. These results confirm the potential of scaling exponents as characteristic parameters to detect changes on seizure onset, which suggests their use as inputs for analysis methods for seizure detection in long-term recordings, while changes in growth exponent are potentially useful for prediction purposes.

[1]  Biyu J. He,et al.  The Temporal Structures and Functional Significance of Scale-free Brain Activity , 2010, Neuron.

[2]  Cheryl Ann Zimmer,et al.  Dynamic Scaling in Chemical Ecology , 2008, Journal of Chemical Ecology.

[4]  Mark Frei Seizure detection , 2013, Scholarpedia.

[5]  G. Ódor Universality classes in nonequilibrium lattice systems , 2002, cond-mat/0205644.

[6]  Jiang Wang,et al.  Power spectral density and coherence analysis of Alzheimer’s EEG , 2014, Cognitive Neurodynamics.

[7]  A. Brú,et al.  The universal dynamics of tumor growth. , 2003, Biophysical journal.

[8]  Alexander S Balankin Dynamic scaling approach to study time series fluctuations. , 2007, Physical review. E, Statistical, nonlinear, and soft matter physics.

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

[10]  Mojtaba Bandarabadi,et al.  Epileptic seizure prediction using relative spectral power features , 2015, Clinical Neurophysiology.

[11]  Olga Sourina,et al.  ANALYSIS AND VISUALIZATION OF HUMAN ELECTROENCEPHALOGRAMS SEEN AS FRACTAL TIME SERIES , 2006 .

[12]  John B. Shoven,et al.  I , Edinburgh Medical and Surgical Journal.

[13]  M. Teplan FUNDAMENTALS OF EEG MEASUREMENT , 2002 .

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

[15]  G. G. Stokes "J." , 1890, The New Yale Book of Quotations.

[16]  Lopez,et al.  Generic dynamic scaling in kinetic roughening , 2000, Physical review letters.

[17]  V. Plerou,et al.  Scale invariance and universality: organizing principles in complex systems , 2000 .

[18]  I. Soltesz,et al.  Future of seizure prediction and intervention: closing the loop. , 2015, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[19]  J. Sprott Chaos and time-series analysis , 2001 .

[20]  W. Stacey,et al.  On the nature of seizure dynamics. , 2014, Brain : a journal of neurology.

[21]  Paul Meakin,et al.  Fractals, scaling, and growth far from equilibrium , 1998 .

[22]  F. Mormann,et al.  Seizure prediction for therapeutic devices: A review , 2016, Journal of Neuroscience Methods.

[23]  Alexander S. Balankin,et al.  Scaling dynamics of seismic activity fluctuations , 2009 .

[24]  Stiliyan Kalitzin,et al.  Dynamical diseases of brain systems: different routes to epileptic seizures , 2003, IEEE Transactions on Biomedical Engineering.

[25]  J. Parra,et al.  Epilepsies as Dynamical Diseases of Brain Systems: Basic Models of the Transition Between Normal and Epileptic Activity , 2003, Epilepsia.

[26]  D. Nair,et al.  Management of Drug-Resistant Epilepsy , 2016, Continuum.

[27]  J. Manjarrez,et al.  Differential effects of NMDA antagonists microinjections into the nucleus reticularis pontis caudalis on seizures induced by pentylenetetrazol in the rat , 2001, Epilepsy Research.

[28]  Abigail R. Colson,et al.  Health and economic benefits of public financing of epilepsy treatment in India: An agent‐based simulation model , 2016, Epilepsia.

[29]  F. D. A. Aarao Reis,et al.  Dynamic scaling and temperature effects in thin film roughening , 2015 .

[30]  Tobias Loddenkemper,et al.  Seizure detection, seizure prediction, and closed-loop warning systems in epilepsy , 2014, Epilepsy & Behavior.

[31]  M. E. J. Newman,et al.  Power laws, Pareto distributions and Zipf's law , 2005 .

[32]  Mark E. J. Newman,et al.  Power-Law Distributions in Empirical Data , 2007, SIAM Rev..

[33]  P. Pardalos,et al.  An investigation of EEG dynamics in an animal model of temporal lobe epilepsy using the maximum Lyapunov exponent , 2009, Experimental Neurology.

[34]  Wolfgang Löscher,et al.  Critical review of current animal models of seizures and epilepsy used in the discovery and development of new antiepileptic drugs , 2011, Seizure.

[35]  Annika Lüttjohann,et al.  A revised Racine's scale for PTZ-induced seizures in rats , 2009, Physiology & Behavior.

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

[37]  Petr Bob The Chaotic Brain, Dissociative States, and Dream Function , 2007 .

[38]  Lamberto Rondoni,et al.  Applications of chaos and nonlinear dynamics in engineering , 2011 .

[39]  J. Milton,et al.  Epilepsy as a Dynamic Disease , 2003 .

[40]  Stiliyan Kalitzin,et al.  Predicting the unpredictable: The challenge or mirage of seizure prediction? , 2014, Clinical Neurophysiology.

[41]  S. Foss,et al.  An Introduction to Heavy-Tailed and Subexponential Distributions , 2011 .

[42]  Tamás Vicsek,et al.  Dynamic scaling of the interface in two-phase viscous flows in porous media , 1991 .

[43]  John Stonham,et al.  Dynamics of regional brain activity in epilepsy: a cross-disciplinary study on both intracranial and scalp-recorded epileptic seizures , 2014, Journal of neural engineering.

[44]  Geoffrey B. West,et al.  Life's Universal Scaling Laws , 2004 .

[45]  John Milton,et al.  Dynamic diseases in neurology and psychiatry. , 1995, Chaos.

[46]  Wolfgang Löscher,et al.  Animal models of seizures and epilepsy , 2011 .

[47]  S. Huffel,et al.  Non-EEG seizure-detection systems and potential SUDEP prevention: State of the art , 2013, Seizure.

[48]  Rudolph C. Hwa,et al.  Power-law scaling in human EEG: relation to Fourier power spectrum , 2003, Neurocomputing.

[49]  Alexei Sourin,et al.  Human electroencephalograms seen as fractal time series: Mathematical analysis and visualization , 2006, Comput. Biol. Medicine.

[50]  Tamás Roska,et al.  Long-range dependence of long-term continuous intracranial electroencephalograms for detection and prediction of epileptic seizures , 2008 .

[51]  P ? ? ? ? ? ? ? % ? ? ? ? , 1991 .

[52]  Mohammad B. Shamsollahi,et al.  Seizure Detection in EEG signals: A Comparison of Different approaches , 2006, 2006 International Conference of the IEEE Engineering in Medicine and Biology Society.

[53]  Mike Mannion,et al.  Complex systems , 1997, Proceedings International Conference and Workshop on Engineering of Computer-Based Systems.

[54]  D. Sornette,et al.  Epileptic seizures: Quakes of the brain? , 2007, Physical review. E, Statistical, nonlinear, and soft matter physics.

[55]  A. Barabasi,et al.  Fractal concepts in surface growth , 1995 .

[56]  Ivan Osorio,et al.  Hurst parameter estimation for epleptic seizure detection , 2007, Commun. Inf. Syst..

[57]  Colleen A Brenner,et al.  Resting state EEG power and coherence abnormalities in bipolar disorder and schizophrenia. , 2013, Journal of psychiatric research.

[58]  Maxence Bigerelle,et al.  Dynamic evolution of interface roughness during friction and wear processes. , 2014, Scanning.

[59]  Bahador Bahrami,et al.  Brain complexity increases in mania , 2005, Neuroreport.

[60]  Albert-László Barabási,et al.  Roughening of growing surfaces: Kinetic models and continuum theories , 1996 .

[61]  P. Chantrenne,et al.  Cross-plane thermal conductivity of superlattices with rough interfaces using equilibrium and non-equilibrium molecular dynamics , 2011 .

[62]  Juan Bory-Reyes,et al.  The crude oil price bubbling and universal scaling dynamics of price volatility , 2016 .

[63]  Aboul Ella Hassanien,et al.  Brain-Computer Interfaces - Current Trends and Applications , 2014, rain-Computer Interfaces.

[64]  Luis Vazquez,et al.  Universality issues in surface kinetic roughening of thin solid films , 2004 .

[65]  Joaquín Manjarrez-Marmolejo,et al.  Anticonvulsant effects of mefloquine on generalized tonic-clonic seizures induced by two acute models in rats , 2015, BMC Neuroscience.

[66]  Frederico A. C. Azevedo,et al.  Equal numbers of neuronal and nonneuronal cells make the human brain an isometrically scaled‐up primate brain , 2009, The Journal of comparative neurology.

[67]  J. M. Pastor,et al.  Super-rough dynamics on tumor growth , 1998 .

[68]  George Minadakis,et al.  Dynamical analogy between epileptic seizures and seismogenic electromagnetic emissions by means of nonextensive statistical mechanics , 2012, 1209.3803.

[69]  Jean Gotman,et al.  Scale Invariance Properties of Intracerebral EEG Improve Seizure Prediction in Mesial Temporal Lobe Epilepsy , 2015, PloS one.

[70]  A. Brú,et al.  Fractal analysis and tumour growth , 2008, Math. Comput. Model..

[71]  Margaret Fahnestock,et al.  Kindling and status epilepticus models of epilepsy: rewiring the brain , 2004, Progress in Neurobiology.

[72]  J Gotman,et al.  Interhemispheric Relations During Bilateral Spike‐and‐Wave Activity , 1981, Epilepsia.

[73]  C. L. Martínez-González,et al.  Fractal Analysis of EEG Signals in the Brain of Epileptic Rats, with and without Biocompatible Implanted Neuroreservoirs , 2009 .

[74]  David M. Himes,et al.  Prediction of seizure likelihood with a long-term, implanted seizure advisory system in patients with drug-resistant epilepsy: a first-in-man study , 2013, The Lancet Neurology.

[75]  Joachim P. Sturmberg,et al.  Complexity in Health: An Introduction , 2013 .

[76]  Jeffrey G. Ojemann,et al.  Power-Law Scaling in the Brain Surface Electric Potential , 2009, PLoS Comput. Biol..

[77]  Dongkyoo Shin,et al.  Mental State Measurement System Using EEG Analysis , 2014 .