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Optogenetically Blocking Sharp Wave Ripple Events in Sleep Does Not Interfere with the Formation of Stable Spatial Representation in the CA1 Area of the Hippocampus

During hippocampal sharp wave/ripple (SWR) events, previously occurring, sensory input-driven neuronal firing patterns are replayed. Such replay is thought to be important for plasticity-related processes and consolidation of memory traces. It has previously been shown that the electrical stimulatio...

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Autores principales: Kovács, Krisztián A., O’Neill, Joseph, Schoenenberger, Philipp, Penttonen, Markku, Ranguel Guerrero, Damaris K., Csicsvari, Jozsef
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5070819/
https://www.ncbi.nlm.nih.gov/pubmed/27760158
http://dx.doi.org/10.1371/journal.pone.0164675
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author Kovács, Krisztián A.
O’Neill, Joseph
Schoenenberger, Philipp
Penttonen, Markku
Ranguel Guerrero, Damaris K.
Csicsvari, Jozsef
author_facet Kovács, Krisztián A.
O’Neill, Joseph
Schoenenberger, Philipp
Penttonen, Markku
Ranguel Guerrero, Damaris K.
Csicsvari, Jozsef
author_sort Kovács, Krisztián A.
collection PubMed
description During hippocampal sharp wave/ripple (SWR) events, previously occurring, sensory input-driven neuronal firing patterns are replayed. Such replay is thought to be important for plasticity-related processes and consolidation of memory traces. It has previously been shown that the electrical stimulation-induced disruption of SWR events interferes with learning in rodents in different experimental paradigms. On the other hand, the cognitive map theory posits that the plastic changes of the firing of hippocampal place cells constitute the electrophysiological counterpart of the spatial learning, observable at the behavioral level. Therefore, we tested whether intact SWR events occurring during the sleep/rest session after the first exploration of a novel environment are needed for the stabilization of the CA1 code, which process requires plasticity. We found that the newly-formed representation in the CA1 has the same level of stability with optogenetic SWR blockade as with a control manipulation that delivered the same amount of light into the brain. Therefore our results suggest that at least in the case of passive exploratory behavior, SWR-related plasticity is dispensable for the stability of CA1 ensembles.
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spelling pubmed-50708192016-10-27 Optogenetically Blocking Sharp Wave Ripple Events in Sleep Does Not Interfere with the Formation of Stable Spatial Representation in the CA1 Area of the Hippocampus Kovács, Krisztián A. O’Neill, Joseph Schoenenberger, Philipp Penttonen, Markku Ranguel Guerrero, Damaris K. Csicsvari, Jozsef PLoS One Research Article During hippocampal sharp wave/ripple (SWR) events, previously occurring, sensory input-driven neuronal firing patterns are replayed. Such replay is thought to be important for plasticity-related processes and consolidation of memory traces. It has previously been shown that the electrical stimulation-induced disruption of SWR events interferes with learning in rodents in different experimental paradigms. On the other hand, the cognitive map theory posits that the plastic changes of the firing of hippocampal place cells constitute the electrophysiological counterpart of the spatial learning, observable at the behavioral level. Therefore, we tested whether intact SWR events occurring during the sleep/rest session after the first exploration of a novel environment are needed for the stabilization of the CA1 code, which process requires plasticity. We found that the newly-formed representation in the CA1 has the same level of stability with optogenetic SWR blockade as with a control manipulation that delivered the same amount of light into the brain. Therefore our results suggest that at least in the case of passive exploratory behavior, SWR-related plasticity is dispensable for the stability of CA1 ensembles. Public Library of Science 2016-10-19 /pmc/articles/PMC5070819/ /pubmed/27760158 http://dx.doi.org/10.1371/journal.pone.0164675 Text en © 2016 Kovács et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Kovács, Krisztián A.
O’Neill, Joseph
Schoenenberger, Philipp
Penttonen, Markku
Ranguel Guerrero, Damaris K.
Csicsvari, Jozsef
Optogenetically Blocking Sharp Wave Ripple Events in Sleep Does Not Interfere with the Formation of Stable Spatial Representation in the CA1 Area of the Hippocampus
title Optogenetically Blocking Sharp Wave Ripple Events in Sleep Does Not Interfere with the Formation of Stable Spatial Representation in the CA1 Area of the Hippocampus
title_full Optogenetically Blocking Sharp Wave Ripple Events in Sleep Does Not Interfere with the Formation of Stable Spatial Representation in the CA1 Area of the Hippocampus
title_fullStr Optogenetically Blocking Sharp Wave Ripple Events in Sleep Does Not Interfere with the Formation of Stable Spatial Representation in the CA1 Area of the Hippocampus
title_full_unstemmed Optogenetically Blocking Sharp Wave Ripple Events in Sleep Does Not Interfere with the Formation of Stable Spatial Representation in the CA1 Area of the Hippocampus
title_short Optogenetically Blocking Sharp Wave Ripple Events in Sleep Does Not Interfere with the Formation of Stable Spatial Representation in the CA1 Area of the Hippocampus
title_sort optogenetically blocking sharp wave ripple events in sleep does not interfere with the formation of stable spatial representation in the ca1 area of the hippocampus
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5070819/
https://www.ncbi.nlm.nih.gov/pubmed/27760158
http://dx.doi.org/10.1371/journal.pone.0164675
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