Cortico-cortical evoked potentials for sites of early versus late seizure spread in stereoelectroencephalography

Cortico-cortical evoked potentials offer the possibility of understanding connectivity within seizure networks to improve diagnosis and more accurately identify candidates for seizure surgery. We sought to determine if cortico-cortical evoked potentials and post-stimulation oscillatory changes differ for sites of EARLY versus LATE ictal spread. 37 patients undergoing stereoelectroencephalography were tested using a cortico-cortical evoked potential paradigm. All electrodes were classified according to the speed of ictal spread. EARLY spread sites were matched to a LATE spread site equidistant from the onset zone. Root-mean-square was used to quantify evoked responses and post-stimulation gamma band power and coherence were extracted and compared. Sites of EARLY spread exhibited significantly greater evoked responses after stimulation across all patients (t(36)=2.973, p=0.004). Stimulation elicited enhanced gamma band activity at EARLY spread sites (t(36)=2.61, p=0.03, FDR corrected); this gamma band oscillation was highly coherent with the onset zone. Cortico-cortical evoked potentials and post-stimulation changes in gamma band activity differ between sites of EARLY versus LATE ictal spread. The oscillatory changes can help visualize connectivity within the seizure network.

[1]  R. Burgess,et al.  In vivo human hippocampal cingulate connectivity: A corticocortical evoked potentials (CCEPs) study , 2013, Clinical Neurophysiology.

[2]  Chun Kee Chung,et al.  Extent of neocortical resection and surgical outcome of epilepsy: Intracranial EEG analysis , 2010, Epilepsia.

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

[4]  C D Binnie,et al.  Single-pulse electrical stimulation identifies epileptogenic frontal cortex in the human brain , 2005, Neurology.

[5]  M. Kahana,et al.  Comparison of spectral analysis methods for characterizing brain oscillations , 2007, Journal of Neuroscience Methods.

[6]  H. Berendse,et al.  The application of graph theoretical analysis to complex networks in the brain , 2007, Clinical Neurophysiology.

[7]  Fabrice Wendling,et al.  Rhinal–hippocampal interactions during déjà vu , 2012, Clinical Neurophysiology.

[8]  Philippe Kahane,et al.  Preictal short-term plasticity induced by intracerebral 1 Hz stimulation , 2008, NeuroImage.

[9]  Richard Burgess,et al.  Cortical excitability varies upon ictal onset patterns in neocortical epilepsy: A cortico-cortical evoked potential study , 2012, Clinical Neurophysiology.

[10]  J. Gotman,et al.  Patterns of altered functional connectivity in mesial temporal lobe epilepsy , 2012, Epilepsia.

[11]  Marc W Howard,et al.  Theta and Gamma Oscillations during Encoding Predict Subsequent Recall , 2003, The Journal of Neuroscience.

[12]  D. Spencer,et al.  Prediction of Surgical Outcome by Interictal Epileptiform Abnormalities During Intracranial EEG Monitoring in Patients with Extrahippocampal Seizures , 1999, Epilepsia.

[13]  Gonzalo Alarcón,et al.  Role of single pulse electrical stimulation (SPES) to guide electrode implantation under general anaesthesia in presurgical assessment of epilepsy , 2013, Seizure.

[14]  M. Kramer,et al.  Epilepsy as a Disorder of Cortical Network Organization , 2012, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[15]  Fabrice Wendling,et al.  Impaired consciousness during temporal lobe seizures is related to increased long-distance cortical-subcortical synchronization. , 2009, Brain : a journal of neurology.

[16]  J. Martinerie,et al.  Comparison of Hilbert transform and wavelet methods for the analysis of neuronal synchrony , 2001, Journal of Neuroscience Methods.

[17]  William Sutherling,et al.  Current source-density and neuromagnetic analysis of the direct cortical response in rat cortex , 1988, Brain Research.

[18]  I. Módy,et al.  High-frequency oscillations : What is normal and what is not ? , 2008 .

[19]  Christoph Baumgartner,et al.  Laminar cortical interactions during epileptic spikes studied with principal component analysis and physiological modeling , 1989, Brain Research.

[20]  J. Régis,et al.  Acute alteration of emotional behaviour in epileptic seizures is related to transient desynchrony in emotion-regulation networks , 2005, Clinical Neurophysiology.

[21]  Patrick Chauvel,et al.  Emergence of semiology in epileptic seizures , 2014, Epilepsy & Behavior.

[22]  Richard C. Burgess,et al.  Correlations between ictal propagation and response to electrical cortical stimulation: A cortico-cortical evoked potential study , 2012, Epilepsy Research.

[23]  J Bancaud,et al.  Unilateral connections between amygdala and hippocampus in man. A study of epileptic patients with depth electrodes. , 1983, Electroencephalography and clinical neurophysiology.

[24]  Philippe Kahane,et al.  Definition and localization of the epileptogenic zone The Bancaud and Talairach view on the epileptogenic zone : a working hypothesis , 2006 .

[25]  Andreas Schulze-Bonhage,et al.  Spread of ictal activity in focal epilepsy , 2008, Epilepsia.

[26]  J. Gotman,et al.  High frequency oscillations (80–500 Hz) in the preictal period in patients with focal seizures , 2009, Epilepsia.

[27]  Jeremy R. Manning,et al.  Broadband Shifts in Local Field Potential Power Spectra Are Correlated with Single-Neuron Spiking in Humans , 2009, The Journal of Neuroscience.

[28]  P. Chauvel,et al.  Epileptogenicity of brain structures in human temporal lobe epilepsy: a quantified study from intracerebral EEG. , 2008, Brain : a journal of neurology.

[29]  Fabrice Wendling,et al.  Seizures of temporal lobe epilepsy: identification of subtypes by coherence analysis using stereo-electro-encephalography , 1999, Clinical Neurophysiology.

[30]  Y. Benjamini,et al.  THE CONTROL OF THE FALSE DISCOVERY RATE IN MULTIPLE TESTING UNDER DEPENDENCY , 2001 .

[31]  J. Hahn,et al.  Complications of invasive video-EEG monitoring with subdural grid electrodes , 2002, Neurology.

[32]  N. Ebrahimi,et al.  Initial outcomes in the Multicenter Study of Epilepsy Surgery , 2003, Neurology.

[33]  Fabrice Wendling,et al.  Abnormal binding and disruption in large scale networks involved in human partial seizures , 2013 .

[34]  Philippe Kahane,et al.  Probabilistic functional tractography of the human cortex , 2013, NeuroImage.

[35]  G. Sandini,et al.  Graph theoretical analysis of magnetoencephalographic functional connectivity in Alzheimer's disease. , 2009, Brain : a journal of neurology.

[36]  L. Senhadji,et al.  From EEG signals to brain connectivity: A model-based evaluation of interdependence measures , 2009, Journal of Neuroscience Methods.

[37]  Jorge Gonzalez-Martinez,et al.  Stereoelectroencephalography in the “difficult to localize” refractory focal epilepsy: Early experience from a North American epilepsy center , 2013, Epilepsia.

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

[39]  B. Litt,et al.  High-frequency oscillations in human temporal lobe: simultaneous microwire and clinical macroelectrode recordings. , 2008, Brain : a journal of neurology.

[40]  Maeike Zijlmans,et al.  Time-frequency analysis of single pulse electrical stimulation to assist delineation of epileptogenic cortex. , 2011, Brain : a journal of neurology.

[41]  Riki Matsumoto,et al.  Accentuated cortico-cortical evoked potentials in neocortical epilepsy in areas of ictal onset , 2010, Epileptic disorders : international epilepsy journal with videotape.

[42]  F. Bartolomei,et al.  Alteration of global workspace during loss of consciousness: A study of parietal seizures , 2012, Epilepsia.

[43]  J. Csicsvari,et al.  Mechanisms of Gamma Oscillations in the Hippocampus of the Behaving Rat , 2003, Neuron.

[44]  Lotfi Senhadji,et al.  Spatial analysis of intracerebral electroencephalographic signals in the time and frequency domain: identification of epileptogenic networks in partial epilepsy , 2008, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[45]  M. Serruya,et al.  Brain-machine interfaces: electrophysiological challenges and limitations. , 2011, Critical reviews in biomedical engineering.

[46]  Rajesh P. N. Rao,et al.  Real-time functional brain mapping using electrocorticography , 2007, NeuroImage.

[47]  Partha P. Mitra,et al.  Chronux: A platform for analyzing neural signals , 2010, Journal of Neuroscience Methods.

[48]  P. Chauvel,et al.  CLINICAL AND ANATOMIC CHARACTERISTICS OF HUMMING AND SINGING IN PARTIAL SEIZURES , 2007, Neurology.

[49]  Jean Gotman,et al.  High frequency oscillations: The new EEG frontier? , 2010, Epilepsia.

[50]  J. Gotman,et al.  High-frequency oscillations during human focal seizures. , 2006, Brain : a journal of neurology.

[51]  J. Dostrovsky,et al.  Microstimulation-induced inhibition of neuronal firing in human globus pallidus. , 2000, Journal of neurophysiology.