Inferring spatiotemporal network patterns from intracranial EEG data

OBJECTIVE The characterization of spatial network dynamics is desirable for a better understanding of seizure physiology. The goal of this work is to develop a computational method for identifying transient spatial patterns from intracranial electroencephalographic (iEEG) data. METHODS Starting with bivariate synchrony measures, such as phase correlation, a two-step clustering procedure is used to identify statistically significant spatial network patterns, whose temporal evolution can be inferred. We refer to this as the composite synchrony profile (CSP) method. RESULTS The CSP method was verified with simulated data and evaluated using ictal and interictal recordings from three patients with intractable epilepsy. Application of the CSP method to these clinical iEEG datasets revealed a set of distinct CSPs with topographies consistent with medial temporal/limbic and superior parietal/medial frontal networks thought to be involved in the seizure generation process. CONCLUSIONS By combining relatively straightforward multivariate signal processing techniques, such as phase synchrony, with clustering and statistical hypothesis testing, the methods we describe may prove useful for network definition and identification. SIGNIFICANCE The network patterns we observe using the CSP method cannot be inferred from direct visual inspection of the raw time series data, nor are they apparent in voltage-based topographic map sequences.

[1]  Piotr J. Franaszczuk,et al.  Epileptic seizures are characterized by changing signal complexity , 2001, Clinical Neurophysiology.

[2]  V L Towle,et al.  Electrocorticographic coherence patterns. , 1999, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[3]  J. Wackermann,et al.  Distribution of Spatial Complexity of EEG in Idiopathic Generalized Epilepsy and Its Change After Chronic Valproate Therapy , 2005, Brain Topography.

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

[5]  K. Müller,et al.  Robustly estimating the flow direction of information in complex physical systems. , 2007, Physical review letters.

[6]  Michael L. Anderson,et al.  Brain Network Analysis of Seizure Evolution , 2008 .

[7]  Kaspar Anton Schindler,et al.  Assessing seizure dynamics by analysing the correlation structure of multichannel intracranial EEG. , 2006, Brain : a journal of neurology.

[8]  O. Sporns,et al.  Motifs in Brain Networks , 2004, PLoS biology.

[9]  R. Bracewell The Fourier Transform and Its Applications , 1966 .

[10]  Brian Litt,et al.  Epileptic seizure prediction using hybrid feature selection over multiple intracranial EEG electrode contacts: a report of four patients , 2003, IEEE Transactions on Biomedical Engineering.

[11]  G. Vachtsevanos,et al.  A multi-feature and multi-channel univariate selection process for seizure prediction , 2005, Clinical Neurophysiology.

[12]  S. Spencer Neural Networks in Human Epilepsy: Evidence of and Implications for Treatment , 2002, Epilepsia.

[13]  F. Mormann,et al.  Seizure prediction: the long and winding road. , 2007, Brain : a journal of neurology.

[14]  Carsten Allefeld,et al.  Detecting synchronization clusters in multivariate time series via coarse-graining of Markov chains. , 2007, Physical review. E, Statistical, nonlinear, and soft matter physics.

[15]  Brian Litt,et al.  Continuous energy variation during the seizure cycle: towards an on-line accumulated energy , 2005, Clinical Neurophysiology.

[16]  K. Lehnertz,et al.  Spatiotemporal Aspects of Synergetic Processes in the Auditory Cortex as Revealed by the Magnetoencephalogram , 1989 .

[17]  Michael C. Smith Multiple Subpial Transection in Patients with Extratemporal Epilepsy , 1998, Epilepsia.

[18]  Karl J. Friston Another Neural Code? , 1997, NeuroImage.

[19]  J. Martinerie,et al.  Preictal state identification by synchronization changes in long-term intracranial EEG recordings , 2005, Clinical Neurophysiology.

[20]  A. Kraskov,et al.  On the predictability of epileptic seizures , 2005, Clinical Neurophysiology.

[21]  H. Sugano,et al.  Hippocampal transection for treatment of left temporal lobe epilepsy with preservation of verbal memory , 2006, Journal of Clinical Neuroscience.

[22]  F. Mormann,et al.  Mean phase coherence as a measure for phase synchronization and its application to the EEG of epilepsy patients , 2000 .

[23]  D. Lowenstein,et al.  mechanisms of disease Epilepsy , 2003 .

[24]  Khaled H. Hamed,et al.  Time-frequency analysis , 2003 .

[25]  F. Mormann,et al.  Epileptic seizures are preceded by a decrease in synchronization , 2003, Epilepsy Research.

[26]  R. E. Greenblatt,et al.  Using Conditional Mutual Information to Approximate Causality for Multivariate Physiological Time Series , 2005 .

[27]  F. Wendling,et al.  Temporal lobe epilepsy , 2019, Radiopaedia.org.

[28]  Richard Wennberg,et al.  Preeminence of Extrahippocampal Structures in the Generation of Mesial Temporal Seizures: Evidence from Human Depth Electrode Recordings , 2002, Epilepsia.