Intracortical mechanisms of single pulse electrical stimulation (SPES) evoked excitations and inhibitions in humans

Abstract Cortico-cortical evoked potentials (CCEPs) elicited by single-pulse electric stimulation (SPES) are widely used to assess effective connectivity between cortical areas and are also implemented in the presurgical evaluation of epileptic patients. Nevertheless, the cortical generators underly...

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Main Authors: Boglárka Hajnal, Johanna Petra Szabó, Emília Tóth, Corey J. Keller, Lucia Wittner, Ashesh D. Mehta, Loránd Erőss, István Ulbert, Dániel Fabó, László Entz
Format: Article
Language:English
Published: Nature Portfolio 2024-06-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-024-62433-0
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author Boglárka Hajnal
Johanna Petra Szabó
Emília Tóth
Corey J. Keller
Lucia Wittner
Ashesh D. Mehta
Loránd Erőss
István Ulbert
Dániel Fabó
László Entz
author_facet Boglárka Hajnal
Johanna Petra Szabó
Emília Tóth
Corey J. Keller
Lucia Wittner
Ashesh D. Mehta
Loránd Erőss
István Ulbert
Dániel Fabó
László Entz
author_sort Boglárka Hajnal
collection DOAJ
description Abstract Cortico-cortical evoked potentials (CCEPs) elicited by single-pulse electric stimulation (SPES) are widely used to assess effective connectivity between cortical areas and are also implemented in the presurgical evaluation of epileptic patients. Nevertheless, the cortical generators underlying the various components of CCEPs in humans have not yet been elucidated. Our aim was to describe the laminar pattern arising under SPES evoked CCEP components (P1, N1, P2, N2, P3) and to evaluate the similarities between N2 and the downstate of sleep slow waves. We used intra-cortical laminar microelectrodes (LMEs) to record CCEPs evoked by 10 mA bipolar 0.5 Hz electric pulses in seven patients with medically intractable epilepsy implanted with subdural grids. Based on the laminar profile of CCEPs, the latency of components is not layer-dependent, however their rate of appearance varies across cortical depth and stimulation distance, while the seizure onset zone does not seem to affect the emergence of components. Early neural excitation primarily engages middle and deep layers, propagating to the superficial layers, followed by mainly superficial inhibition, concluding in a sleep slow wave-like inhibition and excitation sequence.
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spelling doaj-art-675b29cbc830488cb999decfcf2537f42025-08-20T02:17:50ZengNature PortfolioScientific Reports2045-23222024-06-0114111710.1038/s41598-024-62433-0Intracortical mechanisms of single pulse electrical stimulation (SPES) evoked excitations and inhibitions in humansBoglárka Hajnal0Johanna Petra Szabó1Emília Tóth2Corey J. Keller3Lucia Wittner4Ashesh D. Mehta5Loránd Erőss6István Ulbert7Dániel Fabó8László Entz9Epilepsy Center, Clinic for Neurosurgery and Neurointervention, Semmelweis UniversityEpilepsy Center, Clinic for Neurosurgery and Neurointervention, Semmelweis UniversityEpilepsy and Cognitive Neurophysiology Laboratory, University of Alabama at BirminghamDepartment of Neuroscience, Albert Einstein College of MedicineInstitute of Cognitive Neuroscience and Psychology, Research Centre for Natural Sciences, HUN-RENDepartment of Neurosurgery, Hofstra North Shore LIJ School of Medicine and Feinstein Institute of Medical ResearchDepartment of Functional Neurosurgery, Clinic for Neurosurgery and Neurointervention, Semmelweis UniversityEpilepsy Center, Clinic for Neurosurgery and Neurointervention, Semmelweis UniversityEpilepsy Center, Clinic for Neurosurgery and Neurointervention, Semmelweis UniversityDepartment of Functional Neurosurgery, Clinic for Neurosurgery and Neurointervention, Semmelweis UniversityAbstract Cortico-cortical evoked potentials (CCEPs) elicited by single-pulse electric stimulation (SPES) are widely used to assess effective connectivity between cortical areas and are also implemented in the presurgical evaluation of epileptic patients. Nevertheless, the cortical generators underlying the various components of CCEPs in humans have not yet been elucidated. Our aim was to describe the laminar pattern arising under SPES evoked CCEP components (P1, N1, P2, N2, P3) and to evaluate the similarities between N2 and the downstate of sleep slow waves. We used intra-cortical laminar microelectrodes (LMEs) to record CCEPs evoked by 10 mA bipolar 0.5 Hz electric pulses in seven patients with medically intractable epilepsy implanted with subdural grids. Based on the laminar profile of CCEPs, the latency of components is not layer-dependent, however their rate of appearance varies across cortical depth and stimulation distance, while the seizure onset zone does not seem to affect the emergence of components. Early neural excitation primarily engages middle and deep layers, propagating to the superficial layers, followed by mainly superficial inhibition, concluding in a sleep slow wave-like inhibition and excitation sequence.https://doi.org/10.1038/s41598-024-62433-0
spellingShingle Boglárka Hajnal
Johanna Petra Szabó
Emília Tóth
Corey J. Keller
Lucia Wittner
Ashesh D. Mehta
Loránd Erőss
István Ulbert
Dániel Fabó
László Entz
Intracortical mechanisms of single pulse electrical stimulation (SPES) evoked excitations and inhibitions in humans
Scientific Reports
title Intracortical mechanisms of single pulse electrical stimulation (SPES) evoked excitations and inhibitions in humans
title_full Intracortical mechanisms of single pulse electrical stimulation (SPES) evoked excitations and inhibitions in humans
title_fullStr Intracortical mechanisms of single pulse electrical stimulation (SPES) evoked excitations and inhibitions in humans
title_full_unstemmed Intracortical mechanisms of single pulse electrical stimulation (SPES) evoked excitations and inhibitions in humans
title_short Intracortical mechanisms of single pulse electrical stimulation (SPES) evoked excitations and inhibitions in humans
title_sort intracortical mechanisms of single pulse electrical stimulation spes evoked excitations and inhibitions in humans
url https://doi.org/10.1038/s41598-024-62433-0
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