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Effects of Spatial Memory Processing on Hippocampal Ripples

Human High-Frequency-Oscillations (HFO) in the ripple band are oscillatory brain activity in the frequency range between 80 and 250 Hz. HFOs may comprise different subgroups that either play a role in physiologic or pathologic brain functions. An exact differentiation between physiologic and patholo...

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Autores principales: Lachner-Piza, Daniel, Kunz, Lukas, Brandt, Armin, Dümpelmann, Matthias, Thomschewski, Aljoscha, Schulze-Bonhage, Andreas
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7973270/
https://www.ncbi.nlm.nih.gov/pubmed/33746877
http://dx.doi.org/10.3389/fneur.2021.620670
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author Lachner-Piza, Daniel
Kunz, Lukas
Brandt, Armin
Dümpelmann, Matthias
Thomschewski, Aljoscha
Schulze-Bonhage, Andreas
author_facet Lachner-Piza, Daniel
Kunz, Lukas
Brandt, Armin
Dümpelmann, Matthias
Thomschewski, Aljoscha
Schulze-Bonhage, Andreas
author_sort Lachner-Piza, Daniel
collection PubMed
description Human High-Frequency-Oscillations (HFO) in the ripple band are oscillatory brain activity in the frequency range between 80 and 250 Hz. HFOs may comprise different subgroups that either play a role in physiologic or pathologic brain functions. An exact differentiation between physiologic and pathologic HFOs would help elucidate their relevance for cognitive and epileptogenic brain mechanisms, but the criteria for differentiating between physiologic and pathologic HFOs remain controversial. In particular, the separation of pathologic HFOs from physiologic HFOs could improve the identification of epileptogenic brain regions during the pre-surgical evaluation of epilepsy patients. In this study, we performed intracranial electroencephalography recordings from the hippocampus of epilepsy patients before, during, and after the patients completed a spatial navigation task. We isolated hippocampal ripples from the recordings and categorized the ripples into the putative pathologic group iesRipples, when they coincided with interictal spikes, and the putative physiologic group isolRipples, when they did not coincide with interictal spikes. We found that the occurrence of isolRipples significantly decreased during the task as compared to periods before and after the task. The rate of iesRipples was not modulated by the task. In patients who completed the spatial navigation task on two consecutive days, we furthermore examined the occurrence of ripples in the intervening night. We found that the rate of ripples that coincided with sleep spindles and were therefore putatively physiologic correlated with the performance improvement on the spatial navigation task, whereas the rate of all ripples did not show this relationship. Together, our results suggest that the differentiation of HFOs into putative physiologic and pathologic subgroups may help identify their role for spatial memory and memory consolidation processes. Conversely, excluding putative physiologic HFOs from putative pathologic HFOs may improve the HFO-based identification of epileptogenic brain regions in future studies.
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spelling pubmed-79732702021-03-20 Effects of Spatial Memory Processing on Hippocampal Ripples Lachner-Piza, Daniel Kunz, Lukas Brandt, Armin Dümpelmann, Matthias Thomschewski, Aljoscha Schulze-Bonhage, Andreas Front Neurol Neurology Human High-Frequency-Oscillations (HFO) in the ripple band are oscillatory brain activity in the frequency range between 80 and 250 Hz. HFOs may comprise different subgroups that either play a role in physiologic or pathologic brain functions. An exact differentiation between physiologic and pathologic HFOs would help elucidate their relevance for cognitive and epileptogenic brain mechanisms, but the criteria for differentiating between physiologic and pathologic HFOs remain controversial. In particular, the separation of pathologic HFOs from physiologic HFOs could improve the identification of epileptogenic brain regions during the pre-surgical evaluation of epilepsy patients. In this study, we performed intracranial electroencephalography recordings from the hippocampus of epilepsy patients before, during, and after the patients completed a spatial navigation task. We isolated hippocampal ripples from the recordings and categorized the ripples into the putative pathologic group iesRipples, when they coincided with interictal spikes, and the putative physiologic group isolRipples, when they did not coincide with interictal spikes. We found that the occurrence of isolRipples significantly decreased during the task as compared to periods before and after the task. The rate of iesRipples was not modulated by the task. In patients who completed the spatial navigation task on two consecutive days, we furthermore examined the occurrence of ripples in the intervening night. We found that the rate of ripples that coincided with sleep spindles and were therefore putatively physiologic correlated with the performance improvement on the spatial navigation task, whereas the rate of all ripples did not show this relationship. Together, our results suggest that the differentiation of HFOs into putative physiologic and pathologic subgroups may help identify their role for spatial memory and memory consolidation processes. Conversely, excluding putative physiologic HFOs from putative pathologic HFOs may improve the HFO-based identification of epileptogenic brain regions in future studies. Frontiers Media S.A. 2021-03-05 /pmc/articles/PMC7973270/ /pubmed/33746877 http://dx.doi.org/10.3389/fneur.2021.620670 Text en Copyright © 2021 Lachner-Piza, Kunz, Brandt, Dümpelmann, Thomschewski and Schulze-Bonhage. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neurology
Lachner-Piza, Daniel
Kunz, Lukas
Brandt, Armin
Dümpelmann, Matthias
Thomschewski, Aljoscha
Schulze-Bonhage, Andreas
Effects of Spatial Memory Processing on Hippocampal Ripples
title Effects of Spatial Memory Processing on Hippocampal Ripples
title_full Effects of Spatial Memory Processing on Hippocampal Ripples
title_fullStr Effects of Spatial Memory Processing on Hippocampal Ripples
title_full_unstemmed Effects of Spatial Memory Processing on Hippocampal Ripples
title_short Effects of Spatial Memory Processing on Hippocampal Ripples
title_sort effects of spatial memory processing on hippocampal ripples
topic Neurology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7973270/
https://www.ncbi.nlm.nih.gov/pubmed/33746877
http://dx.doi.org/10.3389/fneur.2021.620670
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