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Sleep‐wake characteristics in a mouse model of severe traumatic brain injury: Relation to posttraumatic epilepsy

STUDY OBJECTIVES: Traumatic brain injury (TBI) results in sequelae that include posttraumatic epilepsy (PTE) and sleep‐wake disturbances. Here, we sought to determine whether sleep characteristics could predict development of PTE in a model of severe TBI. METHODS: Following controlled cortical impac...

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Autores principales: Konduru, Sai Sruthi, Wallace, Eli P., Pfammatter, Jesse A., Rodrigues, Paulo V., Jones, Mathew V., Maganti, Rama K.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7918302/
https://www.ncbi.nlm.nih.gov/pubmed/33681661
http://dx.doi.org/10.1002/epi4.12462
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author Konduru, Sai Sruthi
Wallace, Eli P.
Pfammatter, Jesse A.
Rodrigues, Paulo V.
Jones, Mathew V.
Maganti, Rama K.
author_facet Konduru, Sai Sruthi
Wallace, Eli P.
Pfammatter, Jesse A.
Rodrigues, Paulo V.
Jones, Mathew V.
Maganti, Rama K.
author_sort Konduru, Sai Sruthi
collection PubMed
description STUDY OBJECTIVES: Traumatic brain injury (TBI) results in sequelae that include posttraumatic epilepsy (PTE) and sleep‐wake disturbances. Here, we sought to determine whether sleep characteristics could predict development of PTE in a model of severe TBI. METHODS: Following controlled cortical impact (CCI) or sham injury (craniotomy only), CD‐1 mice were implanted with epidural electroencephalography (EEG) and nuchal electromyography (EMG) electrodes. Acute (1st week) and chronic (months 1, 2, or 3) 1‐week‐long video‐EEG recordings were performed after the injury to examine epileptiform activity. High‐amplitude interictal events were extracted from EEG using an automated method. After scoring sleep‐wake patterns, sleep spindles and EEG delta power were derived from nonrapid eye movement (NREM) sleep epochs. Brain CTs (computerized tomography) were performed in sham and CCI cohorts to quantify the brain lesions. We then employed a no craniotomy (NC) control to perform 1‐week‐long EEG recordings at week 1 and month 1 after surgery. RESULTS: Posttraumatic seizures were seen in the CCI group only, whereas interictal epileptiform activity was seen in CCI or sham. Sleep‐wake disruptions consisted of shorter wake or NREM bout lengths and shorter duration or lower power for spindles in CCI and sham. NREM EEG delta power increased in CCI and sham groups compared with NC though the CCI group with posttraumatic seizures had lower power at a chronic time point compared with those without. Follow‐up brain CTs showed a small lesion in the sham injury group suggesting a milder form of TBI that may account for their interictal activity and sleep changes. SIGNIFICANCE: In our TBI model, tracking changes in NREM delta power distinguishes between CCI acutely and animals that will eventually develop PTE, but further work is necessary to identify sleep biomarkers of PTE. Employing NC controls together with sham controls should be considered in future TBI studies.
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spelling pubmed-79183022021-03-05 Sleep‐wake characteristics in a mouse model of severe traumatic brain injury: Relation to posttraumatic epilepsy Konduru, Sai Sruthi Wallace, Eli P. Pfammatter, Jesse A. Rodrigues, Paulo V. Jones, Mathew V. Maganti, Rama K. Epilepsia Open Full‐length Original Research STUDY OBJECTIVES: Traumatic brain injury (TBI) results in sequelae that include posttraumatic epilepsy (PTE) and sleep‐wake disturbances. Here, we sought to determine whether sleep characteristics could predict development of PTE in a model of severe TBI. METHODS: Following controlled cortical impact (CCI) or sham injury (craniotomy only), CD‐1 mice were implanted with epidural electroencephalography (EEG) and nuchal electromyography (EMG) electrodes. Acute (1st week) and chronic (months 1, 2, or 3) 1‐week‐long video‐EEG recordings were performed after the injury to examine epileptiform activity. High‐amplitude interictal events were extracted from EEG using an automated method. After scoring sleep‐wake patterns, sleep spindles and EEG delta power were derived from nonrapid eye movement (NREM) sleep epochs. Brain CTs (computerized tomography) were performed in sham and CCI cohorts to quantify the brain lesions. We then employed a no craniotomy (NC) control to perform 1‐week‐long EEG recordings at week 1 and month 1 after surgery. RESULTS: Posttraumatic seizures were seen in the CCI group only, whereas interictal epileptiform activity was seen in CCI or sham. Sleep‐wake disruptions consisted of shorter wake or NREM bout lengths and shorter duration or lower power for spindles in CCI and sham. NREM EEG delta power increased in CCI and sham groups compared with NC though the CCI group with posttraumatic seizures had lower power at a chronic time point compared with those without. Follow‐up brain CTs showed a small lesion in the sham injury group suggesting a milder form of TBI that may account for their interictal activity and sleep changes. SIGNIFICANCE: In our TBI model, tracking changes in NREM delta power distinguishes between CCI acutely and animals that will eventually develop PTE, but further work is necessary to identify sleep biomarkers of PTE. Employing NC controls together with sham controls should be considered in future TBI studies. John Wiley and Sons Inc. 2021-01-15 /pmc/articles/PMC7918302/ /pubmed/33681661 http://dx.doi.org/10.1002/epi4.12462 Text en © 2020 The Authors. Epilepsia Open published by Wiley Periodicals LLC on behalf of International League Against Epilepsy This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Full‐length Original Research
Konduru, Sai Sruthi
Wallace, Eli P.
Pfammatter, Jesse A.
Rodrigues, Paulo V.
Jones, Mathew V.
Maganti, Rama K.
Sleep‐wake characteristics in a mouse model of severe traumatic brain injury: Relation to posttraumatic epilepsy
title Sleep‐wake characteristics in a mouse model of severe traumatic brain injury: Relation to posttraumatic epilepsy
title_full Sleep‐wake characteristics in a mouse model of severe traumatic brain injury: Relation to posttraumatic epilepsy
title_fullStr Sleep‐wake characteristics in a mouse model of severe traumatic brain injury: Relation to posttraumatic epilepsy
title_full_unstemmed Sleep‐wake characteristics in a mouse model of severe traumatic brain injury: Relation to posttraumatic epilepsy
title_short Sleep‐wake characteristics in a mouse model of severe traumatic brain injury: Relation to posttraumatic epilepsy
title_sort sleep‐wake characteristics in a mouse model of severe traumatic brain injury: relation to posttraumatic epilepsy
topic Full‐length Original Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7918302/
https://www.ncbi.nlm.nih.gov/pubmed/33681661
http://dx.doi.org/10.1002/epi4.12462
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