Spatial and temporal profile of high-frequency oscillations in posttraumatic epileptogenesis

We studied the role of temporal and spatial changes in high-frequency oscillation (HFO, 80–500 Hz) generation in epileptogenesis following traumatic brain injury (TBI).Experiments were conducted on adult male Sprague Dawley rats. For the TBI group, fluid percussion injury (FPI) on the left sensorimo...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Lin Li, Udaya Kumar, Jing You, Yufeng Zhou, Shennan A. Weiss, Jerome Engel, Anatol Bragin
Formato:	article
Lenguaje:	EN
Publicado:	Elsevier 2021
Materias:	Ripple Fast ripple Extrahippocampal HFO Posttraumatic epilepsy Epileptogenesis Neurosciences. Biological psychiatry. Neuropsychiatry RC321-571
Acceso en línea:	https://doaj.org/article/61b28fed7e9c42d7a60e6e73458282f4
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:61b28fed7e9c42d7a60e6e73458282f4
record_format	dspace
spelling	oai:doaj.org-article:61b28fed7e9c42d7a60e6e73458282f42021-12-04T04:33:10ZSpatial and temporal profile of high-frequency oscillations in posttraumatic epileptogenesis1095-953X10.1016/j.nbd.2021.105544https://doaj.org/article/61b28fed7e9c42d7a60e6e73458282f42021-12-01T00:00:00Zhttp://www.sciencedirect.com/science/article/pii/S096999612100293Xhttps://doaj.org/toc/1095-953XWe studied the role of temporal and spatial changes in high-frequency oscillation (HFO, 80–500 Hz) generation in epileptogenesis following traumatic brain injury (TBI).Experiments were conducted on adult male Sprague Dawley rats. For the TBI group, fluid percussion injury (FPI) on the left sensorimotor area was performed to induce posttraumatic epileptogenesis. For the sham control group, only the craniotomy was performed. After TBI, 8 bipolar micro-electrodes were implanted bilaterally in the prefrontal cortex, perilesional area and homotopic contralateral site, striatum, and hippocampus. Long-term video/local field potential (LFP) recordings were performed for up to 21 weeks to identify and characterize seizures and capture HFOs. The electrode tip locations and the volume of post TBI brain lesions were further estimated by ex-vivo MRI scans. HFOs were detected during slow-wave sleep and categorized as ripple (80–200 Hz) and fast ripple (FR, 250–500 Hz) events. HFO rates and the HFO peak frequencies were compared in the 8 recording locations and across 8-weeks following TBI.Data from 48 rats (8 sham controls and 40 TBI rats) were analyzed. Within the TBI group, 22 rats (55%) developed recurrent spontaneous seizures (E+ group), at an average of 62.2 (+17.1) days, while 18 rats (45%) did not (E- group). We observed that the HFOs in the E+ group had a higher mean peak frequency than the E- group and the sham group (P < 0.05). Furthermore, the FR rate of the E+ group showed a significant increase compared to the E-group (P < 0.01) and sham control group (P < 0.01), specifically in the perilesional area, homotopic contralateral site, bilateral hippocampus, and to a lesser degree bilateral striatum. When compared across time, the increased FR rate in the E+ group occurred immediately after the insult and remained stable across the duration of the experiment. In addition, lesion size was not statistically different in the E+ and E- group and was not correlated with HFO rates.Our results suggest that TBI results in the formation of a widespread epileptogenic network. FR rates serve as a biomarker of network formation and predict the future development of epilepsy, however FR are not a temporally specific biomarker of TBI sequelae responsible for epileptogenesis. These results suggest that in patients, future risk of post-TBI epilepsy can be predicted early using FR.Lin LiUdaya KumarJing YouYufeng ZhouShennan A. WeissJerome EngelAnatol BraginElsevierarticleRippleFast rippleExtrahippocampal HFOPosttraumatic epilepsyEpileptogenesisNeurosciences. Biological psychiatry. NeuropsychiatryRC321-571ENNeurobiology of Disease, Vol 161, Iss , Pp 105544- (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Ripple Fast ripple Extrahippocampal HFO Posttraumatic epilepsy Epileptogenesis Neurosciences. Biological psychiatry. Neuropsychiatry RC321-571
spellingShingle	Ripple Fast ripple Extrahippocampal HFO Posttraumatic epilepsy Epileptogenesis Neurosciences. Biological psychiatry. Neuropsychiatry RC321-571 Lin Li Udaya Kumar Jing You Yufeng Zhou Shennan A. Weiss Jerome Engel Anatol Bragin Spatial and temporal profile of high-frequency oscillations in posttraumatic epileptogenesis
description	We studied the role of temporal and spatial changes in high-frequency oscillation (HFO, 80–500 Hz) generation in epileptogenesis following traumatic brain injury (TBI).Experiments were conducted on adult male Sprague Dawley rats. For the TBI group, fluid percussion injury (FPI) on the left sensorimotor area was performed to induce posttraumatic epileptogenesis. For the sham control group, only the craniotomy was performed. After TBI, 8 bipolar micro-electrodes were implanted bilaterally in the prefrontal cortex, perilesional area and homotopic contralateral site, striatum, and hippocampus. Long-term video/local field potential (LFP) recordings were performed for up to 21 weeks to identify and characterize seizures and capture HFOs. The electrode tip locations and the volume of post TBI brain lesions were further estimated by ex-vivo MRI scans. HFOs were detected during slow-wave sleep and categorized as ripple (80–200 Hz) and fast ripple (FR, 250–500 Hz) events. HFO rates and the HFO peak frequencies were compared in the 8 recording locations and across 8-weeks following TBI.Data from 48 rats (8 sham controls and 40 TBI rats) were analyzed. Within the TBI group, 22 rats (55%) developed recurrent spontaneous seizures (E+ group), at an average of 62.2 (+17.1) days, while 18 rats (45%) did not (E- group). We observed that the HFOs in the E+ group had a higher mean peak frequency than the E- group and the sham group (P < 0.05). Furthermore, the FR rate of the E+ group showed a significant increase compared to the E-group (P < 0.01) and sham control group (P < 0.01), specifically in the perilesional area, homotopic contralateral site, bilateral hippocampus, and to a lesser degree bilateral striatum. When compared across time, the increased FR rate in the E+ group occurred immediately after the insult and remained stable across the duration of the experiment. In addition, lesion size was not statistically different in the E+ and E- group and was not correlated with HFO rates.Our results suggest that TBI results in the formation of a widespread epileptogenic network. FR rates serve as a biomarker of network formation and predict the future development of epilepsy, however FR are not a temporally specific biomarker of TBI sequelae responsible for epileptogenesis. These results suggest that in patients, future risk of post-TBI epilepsy can be predicted early using FR.
format	article
author	Lin Li Udaya Kumar Jing You Yufeng Zhou Shennan A. Weiss Jerome Engel Anatol Bragin
author_facet	Lin Li Udaya Kumar Jing You Yufeng Zhou Shennan A. Weiss Jerome Engel Anatol Bragin
author_sort	Lin Li
title	Spatial and temporal profile of high-frequency oscillations in posttraumatic epileptogenesis
title_short	Spatial and temporal profile of high-frequency oscillations in posttraumatic epileptogenesis
title_full	Spatial and temporal profile of high-frequency oscillations in posttraumatic epileptogenesis
title_fullStr	Spatial and temporal profile of high-frequency oscillations in posttraumatic epileptogenesis
title_full_unstemmed	Spatial and temporal profile of high-frequency oscillations in posttraumatic epileptogenesis
title_sort	spatial and temporal profile of high-frequency oscillations in posttraumatic epileptogenesis
publisher	Elsevier
publishDate	2021
url	https://doaj.org/article/61b28fed7e9c42d7a60e6e73458282f4
work_keys_str_mv	AT linli spatialandtemporalprofileofhighfrequencyoscillationsinposttraumaticepileptogenesis AT udayakumar spatialandtemporalprofileofhighfrequencyoscillationsinposttraumaticepileptogenesis AT jingyou spatialandtemporalprofileofhighfrequencyoscillationsinposttraumaticepileptogenesis AT yufengzhou spatialandtemporalprofileofhighfrequencyoscillationsinposttraumaticepileptogenesis AT shennanaweiss spatialandtemporalprofileofhighfrequencyoscillationsinposttraumaticepileptogenesis AT jeromeengel spatialandtemporalprofileofhighfrequencyoscillationsinposttraumaticepileptogenesis AT anatolbragin spatialandtemporalprofileofhighfrequencyoscillationsinposttraumaticepileptogenesis
_version_	1718373033799843840

Spatial and temporal profile of high-frequency oscillations in posttraumatic epileptogenesis

Ejemplares similares