The impact of pathological high-frequency oscillations on hippocampal network activity in rats with chronic epilepsy

In epilepsy, brain networks generate pathological high-frequency oscillations (pHFOs) during interictal periods. To understand how pHFOs differ from normal oscillations in overlapping frequency bands and potentially perturb hippocampal processing, we performed high-density single unit and local fiel...

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Main Authors: Laura A Ewell, Kyle B Fischer, Christian Leibold, Stefan Leutgeb, Jill K Leutgeb
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2019-02-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/42148
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author Laura A Ewell
Kyle B Fischer
Christian Leibold
Stefan Leutgeb
Jill K Leutgeb
author_facet Laura A Ewell
Kyle B Fischer
Christian Leibold
Stefan Leutgeb
Jill K Leutgeb
author_sort Laura A Ewell
collection DOAJ
description In epilepsy, brain networks generate pathological high-frequency oscillations (pHFOs) during interictal periods. To understand how pHFOs differ from normal oscillations in overlapping frequency bands and potentially perturb hippocampal processing, we performed high-density single unit and local field potential recordings from hippocampi of behaving rats with and without chronic epilepsy. In epileptic animals, we observed two types of co-occurring fast oscillations, which by comparison to control animals we could classify as ‘ripple-like’ or ‘pHFO’. We compared their spectral characteristics, brain state dependence, and cellular participants. Strikingly, pHFO occurred irrespective of brain state, were associated with interictal spikes, engaged distinct subnetworks of principal neurons compared to ripple-like events, increased the sparsity of network activity, and initiated both general and immediate disruptions in spatial information coding. Taken together, our findings suggest that events that result in pHFOs have an immediate impact on memory processes, corroborating the need for proper classification of pHFOs to facilitate therapeutic interventions that selectively target pathological activity.
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spelling doaj.art-1329ee9b43ae40a0bbb541ae33f46b792022-12-22T03:51:13ZengeLife Sciences Publications LtdeLife2050-084X2019-02-01810.7554/eLife.42148The impact of pathological high-frequency oscillations on hippocampal network activity in rats with chronic epilepsyLaura A Ewell0https://orcid.org/0000-0002-1638-426XKyle B Fischer1Christian Leibold2https://orcid.org/0000-0002-4859-8000Stefan Leutgeb3https://orcid.org/0000-0003-3367-6536Jill K Leutgeb4https://orcid.org/0000-0002-2014-842XNeurobiology Section and Center for Neural Circuits and Behavior, Division of Biological Sciences, University of California, San Diego, La Jolla, United States; Institute of Experimental Epileptology and Cognition Research, University of Bonn Medical Center, Bonn, GermanyNeurobiology Section and Center for Neural Circuits and Behavior, Division of Biological Sciences, University of California, San Diego, La Jolla, United States; Neuroscience Graduate Program, University of California, San Diego, La Jolla, United StatesDepartment Biologie II, Ludwig-Maximilians-Universität München, Martinsried, Germany; Berstein Center for Computational Neuroscience Munich, Martinried, GermanyNeurobiology Section and Center for Neural Circuits and Behavior, Division of Biological Sciences, University of California, San Diego, La Jolla, United States; Kavli Institute for Brain and Mind, University of California, San Diego, La Jolla, United StatesNeurobiology Section and Center for Neural Circuits and Behavior, Division of Biological Sciences, University of California, San Diego, La Jolla, United StatesIn epilepsy, brain networks generate pathological high-frequency oscillations (pHFOs) during interictal periods. To understand how pHFOs differ from normal oscillations in overlapping frequency bands and potentially perturb hippocampal processing, we performed high-density single unit and local field potential recordings from hippocampi of behaving rats with and without chronic epilepsy. In epileptic animals, we observed two types of co-occurring fast oscillations, which by comparison to control animals we could classify as ‘ripple-like’ or ‘pHFO’. We compared their spectral characteristics, brain state dependence, and cellular participants. Strikingly, pHFO occurred irrespective of brain state, were associated with interictal spikes, engaged distinct subnetworks of principal neurons compared to ripple-like events, increased the sparsity of network activity, and initiated both general and immediate disruptions in spatial information coding. Taken together, our findings suggest that events that result in pHFOs have an immediate impact on memory processes, corroborating the need for proper classification of pHFOs to facilitate therapeutic interventions that selectively target pathological activity.https://elifesciences.org/articles/42148epilepsyhippocampusplace fieldpathological high frequency oscillationsmemory
spellingShingle Laura A Ewell
Kyle B Fischer
Christian Leibold
Stefan Leutgeb
Jill K Leutgeb
The impact of pathological high-frequency oscillations on hippocampal network activity in rats with chronic epilepsy
eLife
epilepsy
hippocampus
place field
pathological high frequency oscillations
memory
title The impact of pathological high-frequency oscillations on hippocampal network activity in rats with chronic epilepsy
title_full The impact of pathological high-frequency oscillations on hippocampal network activity in rats with chronic epilepsy
title_fullStr The impact of pathological high-frequency oscillations on hippocampal network activity in rats with chronic epilepsy
title_full_unstemmed The impact of pathological high-frequency oscillations on hippocampal network activity in rats with chronic epilepsy
title_short The impact of pathological high-frequency oscillations on hippocampal network activity in rats with chronic epilepsy
title_sort impact of pathological high frequency oscillations on hippocampal network activity in rats with chronic epilepsy
topic epilepsy
hippocampus
place field
pathological high frequency oscillations
memory
url https://elifesciences.org/articles/42148
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