Stimulus‐evoked potentials contribute to map the epileptogenic zone during stereo‐EEG presurgical monitoring

Presurgical monitoring with intracerebral electrodes in patients with drug‐resistant focal epilepsy represents a standard invasive procedure to localize the sites of seizures origin, defined as the epileptogenic zone (EZ). During presurgical evaluation, intracerebral single‐pulse electrical stimulation (SPES) is performed to define the boundaries of eloquent areas and to evoke seizure‐associated symptoms. Extensive intracranial exploration and stimulation generate a large dataset on brain connectivity that can be used to improve EZ detection and to understand the organization of the human epileptic brain. We developed a protocol to analyse field responses evoked by intracranial stimulation. Intracerebral recordings were performed with 105–162 recording sites positioned in fronto‐temporal regions in 12 patients with pharmacoresistant focal epilepsy. Recording sites were used for bipolar SPES at 1 Hz. Reproducible early and late phases (<60 ms and 60–500 ms from stimulus artefact, respectively) were identified on averaged evoked responses. Phase 1 and 2 responses recorded at all and each recording sites were plotted on a 3D brain reconstructions. Based on connectivity properties, electrode contacts were primarily identified as receivers, mainly activators or bidirectional. We used connectivity patterns to construct networks and applied cluster partitioning to study the proprieties between potentials evoked/stimulated in different regions. We demonstrate that bidirectional connectivity during phase 1 is a prevalent feature that characterize contacts included in the EZ. This study shows that the application of an analytical protocol on intracerebral stimulus‐evoked recordings provides useful information that may contribute to EZ detection and to the management of surgical‐remediable epilepsies. Hum Brain Mapp 35:4267–4281, 2014. © 2014 Wiley Periodicals, Inc.

[1]  T L Babb,et al.  Functional connections in the human temporal lobe , 2004, Experimental Brain Research.

[2]  Philippe Kahane,et al.  Imaging the seizure onset zone with stereo-electroencephalography. , 2011, Brain : a journal of neurology.

[3]  Haiyuan Yu,et al.  Detecting overlapping protein complexes in protein-protein interaction networks , 2012, Nature Methods.

[4]  J. Engel Progress in the field of epilepsy. , 2013, Current opinion in neurology.

[5]  C. Wilson,et al.  Paired pulse suppression and facilitation in human epileptogenic hippocampal formation , 1998, Epilepsy Research.

[6]  Gonzalo Alarcón,et al.  Single‐pulse electrical stimulation helps to identify epileptogenic cortex in children , 2009, Epilepsia.

[7]  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.

[8]  H. Markram,et al.  Disynaptic Inhibition between Neocortical Pyramidal Cells Mediated by Martinotti Cells , 2007, Neuron.

[9]  G. Ojemann,et al.  Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. , 1989, Journal of neurosurgery.

[10]  Gabriele Arnulfo,et al.  Stereoelectroencephalography: surgical methodology, safety, and stereotactic application accuracy in 500 procedures. , 2013, Neurosurgery.

[11]  R. Yuste,et al.  The Brain Activity Map Project and the Challenge of Functional Connectomics , 2012, Neuron.

[12]  Giulio Tononi,et al.  Human brain connectivity during single and paired pulse transcranial magnetic stimulation , 2011, NeuroImage.

[13]  J. Lambert,et al.  Depression of the fast IPSP underlies paired-pulse facilitation in area CA1 of the rat hippocampus. , 1991, Journal of neurophysiology.

[14]  Nathalie Jette,et al.  Pharmacoresistance and the role of surgery in difficult to treat epilepsy , 2012, Nature Reviews Neurology.

[15]  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.

[16]  J R Huguenard,et al.  Properties of excitatory synaptic connections mediated by the corpus callosum in the developing rat neocortex. , 2001, Journal of neurophysiology.

[17]  Edward M. Reingold,et al.  Graph drawing by force‐directed placement , 1991, Softw. Pract. Exp..

[18]  M. Curtis,et al.  Interactions between Associative Synaptic Potentials in the Piriform Cortex of the In Vitro Isolated Guinea Pig Brain , 1996, The European journal of neuroscience.

[19]  A L Benabid,et al.  Intracerebral low frequency electrical stimulation: a new tool for the definition of the "epileptogenic area"? , 1993, Acta neurochirurgica. Supplementum.

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

[21]  R.N.Dej.,et al.  Epilepsy and the Functional Anatomy of the Human Brain , 1954, Neurology.

[22]  I. S. Gousias,et al.  Whole-brain mapping of structural connectivity in infants reveals altered connection strength associated with growth and preterm birth. , 2014, Cerebral cortex.

[23]  P J Franaszczuk,et al.  Analysis of mesial temporal seizure onset and propagation using the directed transfer function method. , 1994, Electroencephalography and clinical neurophysiology.

[24]  S. Strogatz Exploring complex networks , 2001, Nature.

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

[26]  P. Shannon,et al.  Cytoscape: a software environment for integrated models of biomolecular interaction networks. , 2003, Genome research.

[27]  G. Klem,et al.  Extraoperative Cortical Functional Localization in Patients with Epilepsy , 1987, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

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

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

[30]  R. Metherate,et al.  Facilitation of an NMDA receptor‐mediated EPSP by paired‐pulse stimulation in rat neocortex via depression of GABAergic IPSPs. , 1994, The Journal of physiology.

[31]  R P Lesser,et al.  Basal temporal language area demonstrated by electrical stimulation , 1986, Neurology.

[32]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[33]  Philippe Kahane,et al.  Reappraisal of the human vestibular cortex by cortical electrical stimulation study , 2003, Annals of neurology.

[34]  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.

[35]  W T Blume,et al.  A randomized, controlled trial of surgery for temporal-lobe epilepsy. , 2001, The New England journal of medicine.

[36]  J. Talairach,et al.  [Current indications of stereotaxic interstitial irradiation in acromegaly. Ophthalmologic and neuroendocrinologic correlations in relation to prolonged time]. , 1974, Neuro-Chirurgie.

[37]  N. Thakor,et al.  Determination of current density distributions generated by electrical stimulation of the human cerebral cortex. , 1993, Electroencephalography and clinical neurophysiology.

[38]  J. Martinerie,et al.  Mapping interictal oscillations greater than 200 Hz recorded with intracranial macroelectrodes in human epilepsy. , 2010, Brain : a journal of neurology.

[39]  S. Goldring,et al.  INTRACELLULAR POTENTIALS ASSOCIATED WITH DIRECT CORTICAL RESPONSE AND SEIZURE DISCHARGE IN CAT. , 1964, Electroencephalography and clinical neurophysiology.

[40]  P. Ryvlin,et al.  Evoked potential study of hippocampal efferent projections in the human brain , 2011, Clinical Neurophysiology.

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

[42]  I. Scheffer,et al.  Epilepsy in 2012: Advances in epilepsy shed light on key questions , 2013, Nature Reviews Neurology.

[43]  O. Bertrand,et al.  Relationship between task‐related gamma oscillations and BOLD signal: New insights from combined fMRI and intracranial EEG , 2007, Human brain mapping.

[44]  Francesco Cardinale,et al.  Identification of reproducible ictal patterns based on quantified frequency analysis of intracranial EEG signals , 2011, Epilepsia.

[45]  Bin He,et al.  Graph analysis of epileptogenic networks in human partial epilepsy , 2011, Epilepsia.

[46]  Laura Tassi,et al.  Epileptogenic networks of type II focal cortical dysplasia: A stereo-EEG study , 2012, NeuroImage.

[47]  C. Koch,et al.  Recurrent excitation in neocortical circuits , 1995, Science.

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

[49]  J. Engel,et al.  Intracerebral recordings: organization of the human epileptogenic region. , 1993, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[50]  F. Mormann,et al.  Improved spatial characterization of the epileptic brain by focusing on nonlinearity , 2006, Epilepsy Research.

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

[52]  Alex M Thomson,et al.  Excitatory connections made by presynaptic cortico-cortical pyramidal cells in layer 6 of the neocortex. , 2005, Cerebral cortex.

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