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CA1 hippocampal network activity changes during sleep-dependent memory consolidation

A period of sleep over the first few hours following single-trial contextual fear conditioning (CFC) is essential for hippocampally-mediated memory consolidation. Recent studies have uncovered intracellular mechanisms required for memory formation which are affected by post-conditioning sleep and sl...

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Autores principales: Ognjanovski, Nicolette, Maruyama, Daniel, Lashner, Nora, Zochowski, Michal, Aton, Sara J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4029013/
https://www.ncbi.nlm.nih.gov/pubmed/24860440
http://dx.doi.org/10.3389/fnsys.2014.00061
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author Ognjanovski, Nicolette
Maruyama, Daniel
Lashner, Nora
Zochowski, Michal
Aton, Sara J.
author_facet Ognjanovski, Nicolette
Maruyama, Daniel
Lashner, Nora
Zochowski, Michal
Aton, Sara J.
author_sort Ognjanovski, Nicolette
collection PubMed
description A period of sleep over the first few hours following single-trial contextual fear conditioning (CFC) is essential for hippocampally-mediated memory consolidation. Recent studies have uncovered intracellular mechanisms required for memory formation which are affected by post-conditioning sleep and sleep deprivation. However, almost nothing is known about the circuit-level activity changes during sleep that underlie activation of these intracellular pathways. Here we continuously recorded from the CA1 region of freely-behaving mice to characterize neuronal and network activity changes occurring during active memory consolidation. C57BL/6J mice were implanted with custom stereotrode recording arrays to monitor activity of individual CA1 neurons, local field potentials (LFPs), and electromyographic activity. Sleep architecture and state-specific CA1 activity patterns were assessed during a 24 h baseline recording period, and for 24 h following either single-trial CFC or Sham conditioning. We find that consolidation of CFC is not associated with significant sleep architecture changes, but is accompanied by long-lasting increases in CA1 neuronal firing, as well as increases in delta, theta, and gamma-frequency CA1 LFP activity. These changes occurred in both sleep and wakefulness, and may drive synaptic plasticity within the hippocampus during memory formation. We also find that functional connectivity within the CA1 network, assessed through functional clustering algorithm (FCA) analysis of spike timing relationships among recorded neurons, becomes more stable during consolidation of CFC. This increase in network stability was not present following Sham conditioning, was most evident during post-CFC slow wave sleep (SWS), and was negligible during post-CFC wakefulness. Thus in the interval between encoding and recall, SWS may stabilize the hippocampal contextual fear memory (CFM) trace by promoting CA1 network stability.
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spelling pubmed-40290132014-05-23 CA1 hippocampal network activity changes during sleep-dependent memory consolidation Ognjanovski, Nicolette Maruyama, Daniel Lashner, Nora Zochowski, Michal Aton, Sara J. Front Syst Neurosci Neuroscience A period of sleep over the first few hours following single-trial contextual fear conditioning (CFC) is essential for hippocampally-mediated memory consolidation. Recent studies have uncovered intracellular mechanisms required for memory formation which are affected by post-conditioning sleep and sleep deprivation. However, almost nothing is known about the circuit-level activity changes during sleep that underlie activation of these intracellular pathways. Here we continuously recorded from the CA1 region of freely-behaving mice to characterize neuronal and network activity changes occurring during active memory consolidation. C57BL/6J mice were implanted with custom stereotrode recording arrays to monitor activity of individual CA1 neurons, local field potentials (LFPs), and electromyographic activity. Sleep architecture and state-specific CA1 activity patterns were assessed during a 24 h baseline recording period, and for 24 h following either single-trial CFC or Sham conditioning. We find that consolidation of CFC is not associated with significant sleep architecture changes, but is accompanied by long-lasting increases in CA1 neuronal firing, as well as increases in delta, theta, and gamma-frequency CA1 LFP activity. These changes occurred in both sleep and wakefulness, and may drive synaptic plasticity within the hippocampus during memory formation. We also find that functional connectivity within the CA1 network, assessed through functional clustering algorithm (FCA) analysis of spike timing relationships among recorded neurons, becomes more stable during consolidation of CFC. This increase in network stability was not present following Sham conditioning, was most evident during post-CFC slow wave sleep (SWS), and was negligible during post-CFC wakefulness. Thus in the interval between encoding and recall, SWS may stabilize the hippocampal contextual fear memory (CFM) trace by promoting CA1 network stability. Frontiers Media S.A. 2014-04-17 /pmc/articles/PMC4029013/ /pubmed/24860440 http://dx.doi.org/10.3389/fnsys.2014.00061 Text en Copyright © 2014 Ognjanovski, Maruyama, Lashner, Zochowski and Aton. http://creativecommons.org/licenses/by/3.0/ 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) or licensor 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 Neuroscience
Ognjanovski, Nicolette
Maruyama, Daniel
Lashner, Nora
Zochowski, Michal
Aton, Sara J.
CA1 hippocampal network activity changes during sleep-dependent memory consolidation
title CA1 hippocampal network activity changes during sleep-dependent memory consolidation
title_full CA1 hippocampal network activity changes during sleep-dependent memory consolidation
title_fullStr CA1 hippocampal network activity changes during sleep-dependent memory consolidation
title_full_unstemmed CA1 hippocampal network activity changes during sleep-dependent memory consolidation
title_short CA1 hippocampal network activity changes during sleep-dependent memory consolidation
title_sort ca1 hippocampal network activity changes during sleep-dependent memory consolidation
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4029013/
https://www.ncbi.nlm.nih.gov/pubmed/24860440
http://dx.doi.org/10.3389/fnsys.2014.00061
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