Multivariate autoregressive models with exogenous inputs for intracerebral responses to direct electrical stimulation of the human brain

A multivariate autoregressive (MVAR) model with exogenous inputs (MVARX) is developed for describing the cortical interactions excited by direct electrical current stimulation of the cortex. Current stimulation is challenging to model because it excites neurons in multiple locations both near and distant to the stimulation site. The approach presented here models these effects using an exogenous input that is passed through a bank of filters, one for each channel. The filtered input and a random input excite a MVAR system describing the interactions between cortical activity at the recording sites. The exogenous input filter coefficients, the autoregressive coefficients, and random input characteristics are estimated from the measured activity due to current stimulation. The effectiveness of the approach is demonstrated using intracranial recordings from three surgical epilepsy patients. We evaluate models for wakefulness and NREM sleep in these patients with two stimulation levels in one patient and two stimulation sites in another resulting in a total of 10 datasets. Excellent agreement between measured and model-predicted evoked responses is obtained across all datasets. Furthermore, one-step prediction is used to show that the model also describes dynamics in pre-stimulus and evoked recordings. We also compare integrated information—a measure of intracortical communication thought to reflect the capacity for consciousness—associated with the network model in wakefulness and sleep. As predicted, higher information integration is found in wakefulness than in sleep for all five cases.

[1]  Peter König,et al.  On the directionality of cortical interactions studied by structural analysis of electrophysiological recordings , 1999, Biological Cybernetics.

[2]  A. Rechtschaffen A manual of Standardized Terminology , 1968 .

[3]  C. Chatfield,et al.  Fourier Analysis of Time Series: An Introduction , 1977, IEEE Transactions on Systems, Man, and Cybernetics.

[4]  J. B. Ranck,et al.  Which elements are excited in electrical stimulation of mammalian central nervous system: A review , 1975, Brain Research.

[5]  Karin Schwab,et al.  Comparison of linear signal processing techniques to infer directed interactions in multivariate neural systems , 2005, Signal Process..

[6]  Thomas M. Cover,et al.  Elements of Information Theory , 2005 .

[7]  H. Lüders,et al.  Functional connectivity in human cortical motor system: a cortico-cortical evoked potential study. , 2006, Brain : a journal of neurology.

[8]  A. Seth,et al.  Behaviour of Granger causality under filtering: Theoretical invariance and practical application , 2011, Journal of Neuroscience Methods.

[9]  G. Tononi Consciousness as Integrated Information: a Provisional Manifesto , 2008, The Biological Bulletin.

[10]  A. McQuarrie,et al.  Regression and Time Series Model Selection , 1998 .

[11]  Luiz A. Baccalá,et al.  Partial directed coherence: a new concept in neural structure determination , 2001, Biological Cybernetics.

[12]  S. Sarasso,et al.  Local aspects of sleep: observations from intracerebral recordings in humans. , 2012, Progress in brain research.

[13]  G. Tononi An information integration theory of consciousness , 2004, BMC Neuroscience.

[14]  A. Rechtschaffen A manual of standardized terminology, techniques and scoring system for sleep of human subjects , 1968 .

[15]  Robert D. Nowak,et al.  Cross Validation for Selection of Cortical Interaction Models From Scalp EEG or MEG , 2012, IEEE Transactions on Biomedical Engineering.

[16]  Ciprian M Crainiceanu,et al.  Dynamics of event‐related causality in brain electrical activity , 2008, Human brain mapping.

[17]  F. Babiloni,et al.  Estimation of the cortical functional connectivity with the multimodal integration of high-resolution EEG and fMRI data by directed transfer function , 2005, NeuroImage.

[18]  Gonzalo Alarcón,et al.  Single pulse electrical stimulation for identification of structural abnormalities and prediction of seizure outcome after epilepsy surgery: a prospective study , 2005, The Lancet Neurology.

[19]  Lino Nobili,et al.  Dissociated wake-like and sleep-like electro-cortical activity during sleep , 2011, NeuroImage.

[20]  H. Lüders,et al.  Functional connectivity in the human language system: a cortico-cortical evoked potential study. , 2004, Brain : a journal of neurology.

[21]  G. Tononi,et al.  Breakdown of Cortical Effective Connectivity During Sleep , 2005, Science.

[22]  Larry A. Kramer,et al.  Interhemispheric Effective and Functional Cortical Connectivity Signatures of Spina Bifida Are Consistent with Callosal Anomaly , 2012, Brain Connect..

[23]  J. Changeux,et al.  Opinion TRENDS in Cognitive Sciences Vol.10 No.5 May 2006 Conscious, preconscious, and subliminal processing: a testable taxonomy , 2022 .

[24]  Helmut Ltkepohl,et al.  New Introduction to Multiple Time Series Analysis , 2007 .

[25]  H. Lüders,et al.  Parieto‐frontal network in humans studied by cortico‐cortical evoked potential , 2012, Human brain mapping.

[26]  Laura Astolfi,et al.  Tracking the Time-Varying Cortical Connectivity Patterns by Adaptive Multivariate Estimators , 2008, IEEE Transactions on Biomedical Engineering.

[27]  C D Binnie,et al.  Responses to single pulse electrical stimulation identify epileptogenesis in the human brain in vivo. , 2002, Brain : a journal of neurology.

[28]  J. Geweke,et al.  Measures of Conditional Linear Dependence and Feedback between Time Series , 1984 .

[29]  G. Tononi Information integration: its relevance to brain function and consciousness. , 2010, Archives italiennes de biologie.

[30]  Pierre Duchesne,et al.  On consistent testing for serial correlation of unknown form in vector time series models , 2004 .

[31]  C. Munari,et al.  Stereo‐electroencephalography methodology: advantages and limits , 1994, Acta neurologica Scandinavica. Supplementum.

[32]  Steven Laureys The neural correlate of (un)awareness: lessons from the vegetative state , 2005, Trends in Cognitive Sciences.

[33]  Francesco Cardinale,et al.  Stereoelectroencephalography in the Presurgical Evaluation of Focal Epilepsy: A Retrospective Analysis of 215 Procedures , 2005, Neurosurgery.

[34]  Axel Cleeremans,et al.  Measuring consciousness: relating behavioural and neurophysiological approaches , 2008, Trends in Cognitive Sciences.

[35]  K. Penny Appropriate Critical Values When Testing for a Single Multivariate Outlier by Using the Mahalanobis Distance , 1996 .

[36]  Katarzyna J. Blinowska,et al.  A new method of the description of the information flow in the brain structures , 1991, Biological Cybernetics.

[37]  M. Arnold,et al.  Instantaneous multivariate EEG coherence analysis by means of adaptive high-dimensional autoregressive models , 2001, Journal of Neuroscience Methods.

[38]  Giulio Tononi,et al.  Integrated Information in Discrete Dynamical Systems: Motivation and Theoretical Framework , 2008, PLoS Comput. Biol..

[39]  S. Bressler,et al.  Beta oscillations in a large-scale sensorimotor cortical network: directional influences revealed by Granger causality. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[40]  Yongmiao Hong,et al.  Consistent Testing for Serial Correlation of Unknown Form , 1996 .

[41]  E. Wolpert A Manual of Standardized Terminology, Techniques and Scoring System for Sleep Stages of Human Subjects. , 1969 .

[42]  Anil K. Seth,et al.  Practical Measures of Integrated Information for Time-Series Data , 2011, PLoS Comput. Biol..

[43]  Hualou Liang,et al.  Short-window spectral analysis of cortical event-related potentials by adaptive multivariate autoregressive modeling: data preprocessing, model validation, and variability assessment , 2000, Biological Cybernetics.

[44]  S. Bressler,et al.  Granger Causality: Basic Theory and Application to Neuroscience , 2006, q-bio/0608035.