Human entorhinal cortex electrical stimulation evoked short‐latency potentials in the broad neocortical regions: Evidence from cortico‐cortical evoked potential recordings

Abstract Objective We aimed at clarifying the clinical significance of the responses evoked by human entorhinal cortex (EC) electrical stimulation by means of cortico‐cortical evoked potentials (CCEPs). Methods We enrolled nine patients with medically intractable medial temporal lobe epilepsy who un...

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Main Authors: Hirofumi Takeyama, Riki Matsumoto, Kiyohide Usami, Takuro Nakae, Katsuya Kobayashi, Akihiro Shimotake, Takayuki Kikuchi, Kazumichi Yoshida, Takeharu Kunieda, Susumu Miyamoto, Ryosuke Takahashi, Akio Ikeda
Format: Article
Language:English
Published: Wiley 2019-09-01
Series:Brain and Behavior
Subjects:
Online Access:https://doi.org/10.1002/brb3.1366
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author Hirofumi Takeyama
Riki Matsumoto
Kiyohide Usami
Takuro Nakae
Katsuya Kobayashi
Akihiro Shimotake
Takayuki Kikuchi
Kazumichi Yoshida
Takeharu Kunieda
Susumu Miyamoto
Ryosuke Takahashi
Akio Ikeda
author_facet Hirofumi Takeyama
Riki Matsumoto
Kiyohide Usami
Takuro Nakae
Katsuya Kobayashi
Akihiro Shimotake
Takayuki Kikuchi
Kazumichi Yoshida
Takeharu Kunieda
Susumu Miyamoto
Ryosuke Takahashi
Akio Ikeda
author_sort Hirofumi Takeyama
collection DOAJ
description Abstract Objective We aimed at clarifying the clinical significance of the responses evoked by human entorhinal cortex (EC) electrical stimulation by means of cortico‐cortical evoked potentials (CCEPs). Methods We enrolled nine patients with medically intractable medial temporal lobe epilepsy who underwent invasive presurgical evaluations with subdural or depth electrodes. Single‐pulse electrical stimulation was delivered to the EC and fusiform gyrus (FG), and their evoked potentials were compared. The correlation between the evoked potentials and Wechsler Memory Scale‐Revised (WMS‐R) score was analyzed to investigate whether memory circuit was involved in the generation of the evoked potentials. Results In most electrodes placed on the neocortex, EC stimulation induced unique evoked potentials with positive polarity, termed as “widespread P1” (P1w). Compared with FG stimulation, P1w induced by EC stimulation were distinguished by their high occurrence rate, short peak latency (mean: 20.1 ms), small peak amplitude, and waveform uniformity among different recording sites. A stimulation of more posterior parts of the EC induced P1w with shorter latency and larger amplitude. P1w peak amplitude had a positive correlation (r = .69) with the visual memory score of the WMS‐R. In one patient, with depth electrode implanted into the hippocampus, the giant evoked potentials were recorded in the electrodes of the anterior hippocampus and EC near the stimulus site. Conclusions The human EC electrical stimulation evoked the short‐latency potentials in the broad neocortical regions. The origin of P1w remains unclear, although the limited evidence suggests that P1w is the far‐field potential by the volume conduction of giant evoked potential from the EC itself and hippocampus. The significance of the present study is that those evoked potentials may be a potential biomarker of memory impairment in various neurological diseases, and we provided direct evidence for the functional subdivisions along the anterior–posterior axis in the human EC.
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spelling doaj.art-be56261f50574bffbcc3e4f0b522e7b72022-12-21T19:04:35ZengWileyBrain and Behavior2162-32792019-09-0199n/an/a10.1002/brb3.1366Human entorhinal cortex electrical stimulation evoked short‐latency potentials in the broad neocortical regions: Evidence from cortico‐cortical evoked potential recordingsHirofumi Takeyama0Riki Matsumoto1Kiyohide Usami2Takuro Nakae3Katsuya Kobayashi4Akihiro Shimotake5Takayuki Kikuchi6Kazumichi Yoshida7Takeharu Kunieda8Susumu Miyamoto9Ryosuke Takahashi10Akio Ikeda11Department of Respiratory Care and Sleep Control Medicine Kyoto University Kyoto JapanDepartment of Neurology Kyoto University Kyoto JapanDepartment of Epilepsy, Movement Disorders and Physiology Kyoto University Kyoto JapanDepartment of Neurosurgery Shiga Medical Center for Adults Moriyama JapanDepartment of Neurology Kyoto University Kyoto JapanDepartment of Epilepsy, Movement Disorders and Physiology Kyoto University Kyoto JapanDepartment of Neurosurgery Kyoto University Kyoto JapanDepartment of Neurosurgery Kyoto University Kyoto JapanDepartment of Neurosurgery Ehime University Matsuyama JapanDepartment of Neurosurgery Kyoto University Kyoto JapanDepartment of Neurology Kyoto University Kyoto JapanDepartment of Epilepsy, Movement Disorders and Physiology Kyoto University Kyoto JapanAbstract Objective We aimed at clarifying the clinical significance of the responses evoked by human entorhinal cortex (EC) electrical stimulation by means of cortico‐cortical evoked potentials (CCEPs). Methods We enrolled nine patients with medically intractable medial temporal lobe epilepsy who underwent invasive presurgical evaluations with subdural or depth electrodes. Single‐pulse electrical stimulation was delivered to the EC and fusiform gyrus (FG), and their evoked potentials were compared. The correlation between the evoked potentials and Wechsler Memory Scale‐Revised (WMS‐R) score was analyzed to investigate whether memory circuit was involved in the generation of the evoked potentials. Results In most electrodes placed on the neocortex, EC stimulation induced unique evoked potentials with positive polarity, termed as “widespread P1” (P1w). Compared with FG stimulation, P1w induced by EC stimulation were distinguished by their high occurrence rate, short peak latency (mean: 20.1 ms), small peak amplitude, and waveform uniformity among different recording sites. A stimulation of more posterior parts of the EC induced P1w with shorter latency and larger amplitude. P1w peak amplitude had a positive correlation (r = .69) with the visual memory score of the WMS‐R. In one patient, with depth electrode implanted into the hippocampus, the giant evoked potentials were recorded in the electrodes of the anterior hippocampus and EC near the stimulus site. Conclusions The human EC electrical stimulation evoked the short‐latency potentials in the broad neocortical regions. The origin of P1w remains unclear, although the limited evidence suggests that P1w is the far‐field potential by the volume conduction of giant evoked potential from the EC itself and hippocampus. The significance of the present study is that those evoked potentials may be a potential biomarker of memory impairment in various neurological diseases, and we provided direct evidence for the functional subdivisions along the anterior–posterior axis in the human EC.https://doi.org/10.1002/brb3.1366cortico‐cortical evoked potentialelectrical stimulationentorhinal cortexhippocampusmemory
spellingShingle Hirofumi Takeyama
Riki Matsumoto
Kiyohide Usami
Takuro Nakae
Katsuya Kobayashi
Akihiro Shimotake
Takayuki Kikuchi
Kazumichi Yoshida
Takeharu Kunieda
Susumu Miyamoto
Ryosuke Takahashi
Akio Ikeda
Human entorhinal cortex electrical stimulation evoked short‐latency potentials in the broad neocortical regions: Evidence from cortico‐cortical evoked potential recordings
Brain and Behavior
cortico‐cortical evoked potential
electrical stimulation
entorhinal cortex
hippocampus
memory
title Human entorhinal cortex electrical stimulation evoked short‐latency potentials in the broad neocortical regions: Evidence from cortico‐cortical evoked potential recordings
title_full Human entorhinal cortex electrical stimulation evoked short‐latency potentials in the broad neocortical regions: Evidence from cortico‐cortical evoked potential recordings
title_fullStr Human entorhinal cortex electrical stimulation evoked short‐latency potentials in the broad neocortical regions: Evidence from cortico‐cortical evoked potential recordings
title_full_unstemmed Human entorhinal cortex electrical stimulation evoked short‐latency potentials in the broad neocortical regions: Evidence from cortico‐cortical evoked potential recordings
title_short Human entorhinal cortex electrical stimulation evoked short‐latency potentials in the broad neocortical regions: Evidence from cortico‐cortical evoked potential recordings
title_sort human entorhinal cortex electrical stimulation evoked short latency potentials in the broad neocortical regions evidence from cortico cortical evoked potential recordings
topic cortico‐cortical evoked potential
electrical stimulation
entorhinal cortex
hippocampus
memory
url https://doi.org/10.1002/brb3.1366
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