Anti-seizure effect and neuronal activity change in the genetic-epileptic model rat with acute and chronic vagus nerve stimulation.


Journal

Epilepsy research
ISSN: 1872-6844
Titre abrégé: Epilepsy Res
Pays: Netherlands
ID NLM: 8703089

Informations de publication

Date de publication:
09 2019
Historique:
received: 10 03 2019
revised: 14 06 2019
accepted: 24 06 2019
pubmed: 6 7 2019
medline: 27 5 2020
entrez: 6 7 2019
Statut: ppublish

Résumé

VNS showed time-dependent anti-seizure effect. However, the precise mechanism of VNS in acute and chronic anti-seizure effect has not been fully elucidated. Noda epileptic rat (NER) is genetic epilepsy model rat which exhibits spontaneous generalized tonic-clonic seizure (GTC) approximately once per 30 h and frequent dialeptic seizure (DS). We performed acute and chronic VNS on NER to focus on the acute and chronic anti-epileptic effect and neuronal activity change by VNS. We performed acute VNS (2 h) on 22 NERs (VNS, n = 11, control, n = 11), then subsequently administered chronic (4 weeks) VNS on 10 of 22 NERs (VNS n = 5, control n = 5). We evaluated the acute and chronic anti-seizure effects of VNS on GTC and DS by behavioral and electroencephalographical observation (2 h every week). We carried out double immunofluorescence for biomarkers of short-term (c-Fos) and long-term (ΔFosB) neuronal activation to map regions in the brain that were activated by acute (VNS n = 6, control n = 6) or chronic VNS (VNS n = 5, control n = 5). Furthermore, we performed chronic VNS (4 w) on 12 NERs (VNS n = 6, control n = 6) with long-term observation (8 h a day, 5d per week) to obtain an adequate number of GTCs to elucidate the time dependent anti-epileptic effect on GTC. Acute VNS treatment reduced GTC seizure frequency and total duration of the DS. Chronic VNS resulted in a time-dependent reduction of DS frequency and duration. However, chronic VNS did not show time-dependent reduction of GTC frequency. There were significant c-Fos expressions in the central medial nucleus (CM), mediodorsal thalamic nucleus (MDM), locus coeruleus (LC), and nucleus of solitary tract (NTS) after acute VNS. And there were significant ΔFosB expressions in the lateral septal nucleus (LSV), medial septal nucleus (MSV), MDM, and pontine reticular nucleus caudal (PnC) after chronic VNS. Any decrease in frequency of GTCs by chronic VNS could not be confirmed even with long-term observation. We confirmed acute VNS significantly reduced the frequency of GTC and duration of DS. Chronic VNS decreased the frequency and duration of DS in a time-dependent manner. The brainstem and midline thalamus were activated after acute and chronic VNS. The forebrain was activated only after chronic VNS.

Sections du résumé

BACKGROUND
VNS showed time-dependent anti-seizure effect. However, the precise mechanism of VNS in acute and chronic anti-seizure effect has not been fully elucidated. Noda epileptic rat (NER) is genetic epilepsy model rat which exhibits spontaneous generalized tonic-clonic seizure (GTC) approximately once per 30 h and frequent dialeptic seizure (DS). We performed acute and chronic VNS on NER to focus on the acute and chronic anti-epileptic effect and neuronal activity change by VNS.
METHODS
We performed acute VNS (2 h) on 22 NERs (VNS, n = 11, control, n = 11), then subsequently administered chronic (4 weeks) VNS on 10 of 22 NERs (VNS n = 5, control n = 5). We evaluated the acute and chronic anti-seizure effects of VNS on GTC and DS by behavioral and electroencephalographical observation (2 h every week). We carried out double immunofluorescence for biomarkers of short-term (c-Fos) and long-term (ΔFosB) neuronal activation to map regions in the brain that were activated by acute (VNS n = 6, control n = 6) or chronic VNS (VNS n = 5, control n = 5). Furthermore, we performed chronic VNS (4 w) on 12 NERs (VNS n = 6, control n = 6) with long-term observation (8 h a day, 5d per week) to obtain an adequate number of GTCs to elucidate the time dependent anti-epileptic effect on GTC.
RESULTS
Acute VNS treatment reduced GTC seizure frequency and total duration of the DS. Chronic VNS resulted in a time-dependent reduction of DS frequency and duration. However, chronic VNS did not show time-dependent reduction of GTC frequency. There were significant c-Fos expressions in the central medial nucleus (CM), mediodorsal thalamic nucleus (MDM), locus coeruleus (LC), and nucleus of solitary tract (NTS) after acute VNS. And there were significant ΔFosB expressions in the lateral septal nucleus (LSV), medial septal nucleus (MSV), MDM, and pontine reticular nucleus caudal (PnC) after chronic VNS. Any decrease in frequency of GTCs by chronic VNS could not be confirmed even with long-term observation.
CONCLUSION
We confirmed acute VNS significantly reduced the frequency of GTC and duration of DS. Chronic VNS decreased the frequency and duration of DS in a time-dependent manner. The brainstem and midline thalamus were activated after acute and chronic VNS. The forebrain was activated only after chronic VNS.

Identifiants

pubmed: 31277035
pii: S0920-1211(19)30163-9
doi: 10.1016/j.eplepsyres.2019.106159
pii:
doi:

Substances chimiques

Proto-Oncogene Proteins c-fos 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

106159

Informations de copyright

Copyright © 2019 Elsevier B.V. All rights reserved.

Auteurs

Masaya Katagiri (M)

Department of Neurosurgery, Graduate School of Biomedical and Health Sciences, Hiroshima University, 1-2-3, Kasumi, Minami-ku, Hiroshima, 734-8551, Japan; Epilepsy Center, Hiroshima University Hospital, 1-2-3, Kasumi, Minami-ku, Hiroshima, 734-8551, Japan; Epilepsy Center, Cleveland Clinic Foundation, 9500 Euclid Avenue, Cleveland, OH, 44195, USA. Electronic address: katagim@hiroshima-u.ac.jp.

Koji Iida (K)

Department of Neurosurgery, Graduate School of Biomedical and Health Sciences, Hiroshima University, 1-2-3, Kasumi, Minami-ku, Hiroshima, 734-8551, Japan; Epilepsy Center, Hiroshima University Hospital, 1-2-3, Kasumi, Minami-ku, Hiroshima, 734-8551, Japan. Electronic address: iidak@hiroshima-u.ac.jp.

Kumatoshi Ishihara (K)

Laboratory of Neuropharmacology, Faculty of Pharmaceutical Sciences, Hiroshima International University, 5-1-1, Hirokoshingai, Kure, 737-0112, Japan. Electronic address: ishihara@hirokoku-u.ac.jp.

Dileep Nair (D)

Epilepsy Center, Cleveland Clinic Foundation, 9500 Euclid Avenue, Cleveland, OH, 44195, USA. Electronic address: naird@ccf.org.

Kana Harada (K)

Laboratory of Neuropharmacology, Faculty of Pharmaceutical Sciences, Hiroshima International University, 5-1-1, Hirokoshingai, Kure, 737-0112, Japan. Electronic address: haradak@hiroshima-u.ac.jp.

Kota Kagawa (K)

Department of Neurosurgery, Graduate School of Biomedical and Health Sciences, Hiroshima University, 1-2-3, Kasumi, Minami-ku, Hiroshima, 734-8551, Japan; Epilepsy Center, Hiroshima University Hospital, 1-2-3, Kasumi, Minami-ku, Hiroshima, 734-8551, Japan. Electronic address: kotak.0801@miracle.ocn.ne.jp.

Go Seyama (G)

Department of Neurosurgery, Graduate School of Biomedical and Health Sciences, Hiroshima University, 1-2-3, Kasumi, Minami-ku, Hiroshima, 734-8551, Japan; Epilepsy Center, Hiroshima University Hospital, 1-2-3, Kasumi, Minami-ku, Hiroshima, 734-8551, Japan. Electronic address: goseyama@hiroshima-u.ac.jp.

Akira Hashizume (A)

Department of Neurosurgery, Graduate School of Biomedical and Health Sciences, Hiroshima University, 1-2-3, Kasumi, Minami-ku, Hiroshima, 734-8551, Japan; Epilepsy Center, Hiroshima University Hospital, 1-2-3, Kasumi, Minami-ku, Hiroshima, 734-8551, Japan. Electronic address: hashizume@jinyoukai.or.jp.

Takashi Kuramoto (T)

Institute of Laboratory Animals, Graduate School of Medicine, Kyoto University, Yoshida-Konoe cho, 606-8501, Kyoto, Japan. Electronic address: tkuramot@anim.med.kyoto-u.ac.jp.

Ryosuke Hanaya (R)

Department of Neurosurgery, Graduate School of Medical and Dental Sciences, Kagoshima University, 8-35-1, Sakuragaoka, Kagoshima, 890-8520, Japan. Electronic address: hanaya@m2.kufm.kagoshima-u.ac.jp.

Kazunori Arita (K)

Department of Neurosurgery, Graduate School of Medical and Dental Sciences, Kagoshima University, 8-35-1, Sakuragaoka, Kagoshima, 890-8520, Japan. Electronic address: karita@m2.kufm.kagoshima-u.ac.jp.

Kaoru Kurisu (K)

Department of Neurosurgery, Graduate School of Biomedical and Health Sciences, Hiroshima University, 1-2-3, Kasumi, Minami-ku, Hiroshima, 734-8551, Japan. Electronic address: kuka422@hiroshima-u.ac.jp.

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