{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,9,2]],"date-time":"2025-09-02T10:57:03Z","timestamp":1756810623485,"version":"3.41.2"},"reference-count":50,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2021,6,14]],"date-time":"2021-06-14T00:00:00Z","timestamp":1623628800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["31771255","32020103009"],"award-info":[{"award-number":["31771255","32020103009"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Neurosci."],"abstract":"<jats:sec><jats:title>Propose<\/jats:title><jats:p>Directed cortical responses to intracranial electrical stimulation are a good standard for mapping inter-regional direct connectivity. Cortico-cortical evoked potential (CCEP), elicited by single pulse electrical stimulation (SPES), has been widely used to map the normal and abnormal brain effective network. However, automated processing of CCEP datasets and visualization of connectivity results remain challenging for researchers and clinicians. In this study, we develop a Matlab toolbox named MRIES (Mapping the Responses to Intracranial Electrical Stimulation) to automatically process CCEP data and visualize the connectivity results.<\/jats:p><\/jats:sec><jats:sec><jats:title>Method<\/jats:title><jats:p>The MRIES integrates the processing pipeline of the CCEP datasets and various methods for connectivity calculation based on low- and high-frequency signals with stimulation artifacts removed. The connectivity matrices are saved in different folders for visualization. Different visualization patterns (connectivity matrix, circle map, surface map, and volume map) are also integrated to the graphical user interface (GUI), which makes it easy to intuitively display and compare different connectivity measurements. Furthermore, one sample CCEP data set collected from eight epilepsy patients is used to validate the MRIES toolbox.<\/jats:p><\/jats:sec><jats:sec><jats:title>Result<\/jats:title><jats:p>We show the GUI and visualization functions of MRIES using one example CCEP data that has been described in a complete tutorial. We applied this toolbox to the sample CCEP data set to investigate the direct connectivity between the medial temporal lobe and the insular cortex. We find bidirectional connectivity between MTL and insular that are consistent with the findings of previous studies.<\/jats:p><\/jats:sec><jats:sec><jats:title>Conclusion<\/jats:title><jats:p>MRIES has a friendly GUI and integrates the full processing pipeline of CCEP data and various visualization methods. The MRIES toolbox, tutorial, and example data can be freely downloaded. As an open-source package, MRIES is expected to improve the reproducibility of CCEP findings and facilitate clinical translation.<\/jats:p><\/jats:sec>","DOI":"10.3389\/fnins.2021.652841","type":"journal-article","created":{"date-parts":[[2021,6,14]],"date-time":"2021-06-14T09:23:23Z","timestamp":1623662603000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":3,"title":["MRIES: A Matlab Toolbox for Mapping the Responses to Intracranial Electrical Stimulation"],"prefix":"10.3389","volume":"15","author":[{"given":"Kaijia","family":"Sun","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Haixiang","family":"Wang","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yunxian","family":"Bai","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Wenjing","family":"Zhou","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Liang","family":"Wang","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1965","published-online":{"date-parts":[[2021,6,14]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"2779","DOI":"10.1002\/hbm.22366","article-title":"Intrainsular functional connectivity in human: human intrainsular connectivity.","volume":"35","author":"Almashaikhi","year":"2014","journal-title":"Hum. Brain Mapp."},{"key":"B2","doi-asserted-by":"publisher","first-page":"129","DOI":"10.1111\/acps.12724","article-title":"Insula and amygdala resting-state functional connectivity differentiate bipolar from unipolar depression.","volume":"136","author":"Ambrosi","year":"2017","journal-title":"Acta Psychiatr. Scand."},{"key":"B3","doi-asserted-by":"publisher","first-page":"1131","DOI":"10.1111\/epi.13791","article-title":"Defining epileptogenic networks: contribution of SEEG and signal analysis.","volume":"58","author":"Bartolomei","year":"2017","journal-title":"Epilepsia"},{"key":"B4","doi-asserted-by":"publisher","first-page":"4267","DOI":"10.1002\/hbm.22516","article-title":"Stimulus-evoked potentials contribute to map the epileptogenic zone during stereo-EEG presurgical monitoring: stimulus-evoked potentials.","volume":"35","author":"Boido","year":"2014","journal-title":"Hum. Brain Mapp."},{"key":"B5","doi-asserted-by":"publisher","first-page":"343","DOI":"10.1016\/j.neuroimage.2012.04.012","article-title":"Meta-analytic clustering of the insular cortex: characterizing the meta-analytic connectivity of the insula when involved in active tasks.","volume":"62","author":"Cauda","year":"2012","journal-title":"NeuroImage"},{"key":"B6","doi-asserted-by":"publisher","first-page":"1100","DOI":"10.1016\/j.compbiomed.2011.07.008","article-title":"Anatomic and electro-physiologic connectivity of the language system: a combined DTI-CCEP study.","volume":"41","author":"Conner","year":"2011","journal-title":"Comput. Biol. Med."},{"key":"B7","doi-asserted-by":"publisher","first-page":"565","DOI":"10.1016\/S1388-2457(00)00545-9","article-title":"Induced electrocorticographic gamma activity during auditory perception.","volume":"112","author":"Crone","year":"2001","journal-title":"Clin. Neurophysiol."},{"key":"B8","doi-asserted-by":"publisher","first-page":"67","DOI":"10.1016\/j.jneumeth.2018.09.034","article-title":"A quantitative method for evaluating cortical responses to electrical stimulation.","volume":"311","author":"Crowther","year":"2019","journal-title":"J. Neurosci. Methods"},{"key":"B9","doi-asserted-by":"publisher","first-page":"2898","DOI":"10.1093\/brain\/awr238","article-title":"Imaging the seizure onset zone with stereo-electroencephalography.","volume":"134","author":"David","year":"2011","journal-title":"Brain"},{"key":"B10","doi-asserted-by":"publisher","first-page":"2466","DOI":"10.1016\/j.clinph.2018.06.021","article-title":"Delayed high-frequency suppression after automated single-pulse electrical stimulation identifies the seizure onset zone in patients with refractory epilepsy.","volume":"129","author":"Davis","year":"2018","journal-title":"Clin. Neurophysiol."},{"key":"B11","doi-asserted-by":"publisher","first-page":"9","DOI":"10.1016\/j.jneumeth.2003.10.009","article-title":"EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis.","volume":"134","author":"Delorme","year":"2004","journal-title":"J. Neurosci. Methods"},{"key":"B12","doi-asserted-by":"publisher","first-page":"419","DOI":"10.1016\/j.cortex.2019.05.019","article-title":"Connectivity of the human insula: a cortico-cortical evoked potential (CCEP) study.","volume":"120","author":"Dionisio","year":"2019","journal-title":"Cortex"},{"key":"B13","doi-asserted-by":"publisher","first-page":"20","DOI":"10.1016\/j.cortex.2014.06.018","article-title":"Connections of the limbic network: a corticocortical evoked potentials study.","volume":"62","author":"Enatsu","year":"2015","journal-title":"Cortex"},{"key":"B14","doi-asserted-by":"publisher","first-page":"90","DOI":"10.3171\/2015.6.JNS15622","article-title":"Connectivity of the frontal and anterior insular network: a cortico-cortical evoked potential study.","volume":"125","author":"Enatsu","year":"2016","journal-title":"JNS"},{"key":"B15","doi-asserted-by":"publisher","first-page":"2080","DOI":"10.1016\/j.cortex.2012.08.026","article-title":"Cortical negative motor network in comparison with sensorimotor network: a cortico-cortical evoked potential study.","volume":"49","author":"Enatsu","year":"2013","journal-title":"Cortex"},{"key":"B16","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-018-26995-0","article-title":"Subcortical structural connectivity of insular subregions.","volume":"8","author":"Ghaziri","year":"2018","journal-title":"Sci. Rep."},{"key":"B17","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuroimage.2020.116734","article-title":"Comparing dynamic causal models of neurovascular coupling with fMRI and EEG\/MEG.","volume":"216","author":"Jafarian","year":"2020","journal-title":"NeuroImage"},{"key":"B18","doi-asserted-by":"publisher","first-page":"208","DOI":"10.1016\/j.cortex.2015.01.011","article-title":"Incidence of functional bi-temporal connections in the human brain in vivo and their relevance to epilepsy surgery.","volume":"65","author":"Jim\u00e9nez-Jim\u00e9nez","year":"2015","journal-title":"Cortex"},{"key":"B19","doi-asserted-by":"publisher","first-page":"10308","DOI":"10.1073\/pnas.1019750108","article-title":"Intrinsic functional architecture predicts electrically evoked responses in the human brain.","volume":"108","author":"Keller","year":"2011","journal-title":"PNAS"},{"key":"B20","doi-asserted-by":"publisher","first-page":"5384","DOI":"10.1523\/JNEUROSCI.1088-17.2018","article-title":"Induction and quantification of excitability changes in human cortical networks.","volume":"38","author":"Keller","year":"2018","journal-title":"J. Neurosci."},{"key":"B21","doi-asserted-by":"publisher","first-page":"1673","DOI":"10.1016\/j.clinph.2017.06.249","article-title":"High frequency activity overriding cortico-cortical evoked potentials reflects altered excitability in the human epileptic focus.","volume":"128","author":"Kobayashi","year":"2017","journal-title":"Clin. Neurophysiol."},{"key":"B22","doi-asserted-by":"publisher","first-page":"918","DOI":"10.1093\/cercor\/bhr163","article-title":"Connectivity between perisylvian and bilateral basal temporal cortices.","volume":"22","author":"Koubeissi","year":"2012","journal-title":"Cereb. Cortex"},{"key":"B23","doi-asserted-by":"publisher","first-page":"2966","DOI":"10.1093\/brain\/awy214","article-title":"Interictal stereotactic-EEG functional connectivity in refractory focal epilepsies.","volume":"141","author":"Lagarde","year":"2018","journal-title":"Brain"},{"key":"B24","doi-asserted-by":"publisher","first-page":"27","DOI":"10.1016\/j.seizure.2016.11.003","article-title":"Single pulse electrical stimulation to probe functional and pathological connectivity in epilepsy.","volume":"44","author":"Matsumoto","year":"2017","journal-title":"Seizure"},{"key":"B25","doi-asserted-by":"publisher","first-page":"181","DOI":"10.1093\/brain\/awl257","article-title":"Functional connectivity in human cortical motor system: a cortico-cortical evoked potential study.","volume":"130","author":"Matsumoto","year":"2006","journal-title":"Brain"},{"key":"B26","doi-asserted-by":"publisher","first-page":"2316","DOI":"10.1093\/brain\/awh246","article-title":"Functional connectivity in the human language system: a cortico-cortical evoked potential study.","volume":"127","author":"Matsumoto","year":"2004","journal-title":"Brain"},{"key":"B27","doi-asserted-by":"publisher","first-page":"3445","DOI":"10.1093\/cercor\/bhx211","article-title":"Structural connections of functionally defined human insular subdivisions.","volume":"28","author":"Nomi","year":"2018","journal-title":"Cereb. Cortex"},{"key":"B28","doi-asserted-by":"publisher","DOI":"10.1155\/2011\/156869","article-title":"FieldTrip: open source software for advanced analysis of meg, eeg, and invasive electrophysiological data.","volume":"2011","author":"Oostenveld","year":"2010","journal-title":"Comput. Intell. Neurosci."},{"key":"B29","doi-asserted-by":"publisher","first-page":"943","DOI":"10.1016\/j.nicl.2017.12.020","article-title":"Structural and effective connectivity in focal epilepsy.","volume":"17","author":"Parker","year":"2018","journal-title":"NeuroImage Clinical"},{"key":"B30","doi-asserted-by":"publisher","DOI":"10.1016\/j.jneumeth.2020.108639","article-title":"Quantifying volume conducted potential using stimulation artefact in cortico-cortical evoked potentials.","volume":"337","author":"Prime","year":"2020","journal-title":"J. Neurosci. Methods"},{"key":"B31","doi-asserted-by":"publisher","DOI":"10.3389\/fninf.2017.00010","article-title":"Automatic and precise localization and cortical labeling of subdural and depth intracranial electrodes.","volume":"11","author":"Qin","year":"2017","journal-title":"Front. Neuroinform."},{"key":"B32","doi-asserted-by":"publisher","first-page":"1751","DOI":"10.1038\/s41593-019-0510-4","article-title":"Advancing functional connectivity research from association to causation.","volume":"22","author":"Reid","year":"2019","journal-title":"Nat. Neurosci."},{"key":"B33","doi-asserted-by":"publisher","first-page":"827","DOI":"10.3171\/2014.4.JNS131195","article-title":"Intraoperative cortico-cortical evoked potentials for the evaluation of language function during brain tumor resection: initial experience with 13 cases: clinical article.","volume":"121","author":"Saito","year":"2014","journal-title":"J. Neurosurg."},{"key":"B34","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-017-01763-2","article-title":"Widespread theta synchrony and high-frequency desynchronization underlies enhanced cognition.","volume":"8","author":"Solomon","year":"2017","journal-title":"Nat. Commun."},{"key":"B35","doi-asserted-by":"publisher","first-page":"1100","DOI":"10.1016\/j.cub.2019.02.020","article-title":"Dynamic theta networks in the human medial temporal lobe support episodic memory.","volume":"29","author":"Solomon","year":"2019","journal-title":"Curr. Biol."},{"key":"B36","doi-asserted-by":"publisher","first-page":"2860","DOI":"10.1016\/j.neuroimage.2011.09.049","article-title":"Roles for the pre-supplementary motor area and the right inferior frontal gyrus in stopping action: electrophysiological responses and functional and structural connectivity.","volume":"59","author":"Swann","year":"2012","journal-title":"NeuroImage"},{"key":"B37","doi-asserted-by":"publisher","first-page":"1580","DOI":"10.3171\/2015.4.JNS15193","article-title":"Passive language mapping combining real-time oscillation analysis with cortico-cortical evoked potentials for awake craniotomy.","volume":"125","author":"Tamura","year":"2016","journal-title":"J. Neurosurg."},{"key":"B38","doi-asserted-by":"publisher","DOI":"10.1016\/j.eplepsyres.2020.106264","article-title":"The FAST graph: a novel framework for the anatomically-guided visualization and analysis of cortico-cortical evoked potentials.","volume":"161","author":"Taylor","year":"2020","journal-title":"Epilepsy Res."},{"key":"B39","doi-asserted-by":"publisher","first-page":"14","DOI":"10.1002\/hbm.21189","article-title":"Uneven interhemispheric connections between left and right primary sensori-motor areas.","volume":"33","author":"Terada","year":"2012","journal-title":"Hum. Brain Mapp."},{"key":"B40","doi-asserted-by":"publisher","first-page":"1872","DOI":"10.1093\/brain\/awx123","article-title":"Connectivity in ictal single photon emission computed tomography perfusion: a cortico-cortical evoked potential study.","volume":"140","author":"Tousseyn","year":"2017","journal-title":"Brain"},{"key":"B41","doi-asserted-by":"publisher","first-page":"777","DOI":"10.1093\/cercor\/bhx361","article-title":"Cortical responses to input from distant areas are modulated by local spontaneous alpha\/beta oscillations.","volume":"29","author":"Usami","year":"2018","journal-title":"Cereb. Cortex"},{"key":"B42","doi-asserted-by":"publisher","first-page":"1855","DOI":"10.1111\/epi.12350","article-title":"Functional and structural brain networks in epilepsy: what have we learned?","volume":"54","author":"van Diessen","year":"2013","journal-title":"Epilepsia"},{"key":"B43","doi-asserted-by":"publisher","first-page":"858","DOI":"10.1016\/j.clinph.2017.01.017","article-title":"Evoked versus spontaneous high frequency oscillations in the chronic electrocorticogram in focal epilepsy.","volume":"128","author":"van \u2019t Klooster","year":"2017","journal-title":"Clin. Neurophysiol."},{"key":"B44","doi-asserted-by":"publisher","first-page":"2855","DOI":"10.1093\/brain\/awr211","article-title":"Time\u2013frequency analysis of single pulse electrical stimulation to assist delineation of epileptogenic cortex.","volume":"134","author":"van \u2019t Klooster","year":"2011","journal-title":"Brain"},{"key":"B45","doi-asserted-by":"publisher","first-page":"2491","DOI":"10.1162\/jocn.2009.21384","article-title":"Hemicraniectomy: a new model for human electrophysiology with high spatio-temporal resolution.","volume":"22","author":"Voytek","year":"2009","journal-title":"J. Cogn. Neurosci."},{"key":"B46","doi-asserted-by":"publisher","first-page":"157","DOI":"10.1016\/j.pmr.2009.07.003","article-title":"Neural interface technology for rehabilitation: exploiting and promoting neuroplasticity.","volume":"21","author":"Wang","year":"2010","journal-title":"Phys. Med. Rehab. Clin. North Am."},{"key":"B47","doi-asserted-by":"publisher","first-page":"349","DOI":"10.1038\/nn.3315","article-title":"Frequency\u2013specific network connectivity increases underlie accurate spatiotemporal memory retrieval.","volume":"16","author":"Watrous","year":"2013","journal-title":"Nat. Neurosci."},{"key":"B48","doi-asserted-by":"publisher","first-page":"279","DOI":"10.1007\/BF00231248","article-title":"Functional connections in the human temporal lobe - I. Analysis of limbic system pathways using neuronal responses evoked by electrical stimulation.","volume":"82","author":"Wilson","year":"1990","journal-title":"Exp. Brain Res."},{"key":"B49","doi-asserted-by":"publisher","first-page":"174","DOI":"10.1007\/BF00229999","article-title":"Functional connections in the human temporal lobe.","volume":"85","author":"Wilson","year":"1991","journal-title":"Exp. Brain Res."},{"key":"B50","doi-asserted-by":"publisher","DOI":"10.3389\/fninf.2019.00031","article-title":"Localization of Epileptogenic Zone Based on Cortico-Cortical Evoked Potential (CCEP): a feature extraction and graph theory approach.","volume":"13","author":"Zhao","year":"2019","journal-title":"Front. Neuroinform."}],"container-title":["Frontiers in Neuroscience"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fnins.2021.652841\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,6,14]],"date-time":"2021-06-14T09:23:27Z","timestamp":1623662607000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fnins.2021.652841\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,6,14]]},"references-count":50,"alternative-id":["10.3389\/fnins.2021.652841"],"URL":"https:\/\/doi.org\/10.3389\/fnins.2021.652841","relation":{},"ISSN":["1662-453X"],"issn-type":[{"type":"electronic","value":"1662-453X"}],"subject":[],"published":{"date-parts":[[2021,6,14]]},"article-number":"652841"}}