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Parvalbumin-expressing interneurons coordinate hippocampal network dynamics required for memory consolidation

Activity in hippocampal area CA1 is essential for consolidating episodic memories, but it is unclear how CA1 activity patterns drive memory formation. We find that in the hours following single-trial contextual fear conditioning (CFC), fast-spiking interneurons (which typically express parvalbumin (...

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Autores principales: Ognjanovski, Nicolette, Schaeffer, Samantha, Wu, Jiaxing, Mofakham, Sima, Maruyama, Daniel, Zochowski, Michal, Aton, Sara J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5384212/
https://www.ncbi.nlm.nih.gov/pubmed/28382952
http://dx.doi.org/10.1038/ncomms15039
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author Ognjanovski, Nicolette
Schaeffer, Samantha
Wu, Jiaxing
Mofakham, Sima
Maruyama, Daniel
Zochowski, Michal
Aton, Sara J.
author_facet Ognjanovski, Nicolette
Schaeffer, Samantha
Wu, Jiaxing
Mofakham, Sima
Maruyama, Daniel
Zochowski, Michal
Aton, Sara J.
author_sort Ognjanovski, Nicolette
collection PubMed
description Activity in hippocampal area CA1 is essential for consolidating episodic memories, but it is unclear how CA1 activity patterns drive memory formation. We find that in the hours following single-trial contextual fear conditioning (CFC), fast-spiking interneurons (which typically express parvalbumin (PV)) show greater firing coherence with CA1 network oscillations. Post-CFC inhibition of PV+ interneurons blocks fear memory consolidation. This effect is associated with loss of two network changes associated with normal consolidation: (1) augmented sleep-associated delta (0.5–4 Hz), theta (4–12 Hz) and ripple (150–250 Hz) oscillations; and (2) stabilization of CA1 neurons’ functional connectivity patterns. Rhythmic activation of PV+ interneurons increases CA1 network coherence and leads to a sustained increase in the strength and stability of functional connections between neurons. Our results suggest that immediately following learning, PV+ interneurons drive CA1 oscillations and reactivation of CA1 ensembles, which directly promotes network plasticity and long-term memory formation.
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spelling pubmed-53842122017-04-23 Parvalbumin-expressing interneurons coordinate hippocampal network dynamics required for memory consolidation Ognjanovski, Nicolette Schaeffer, Samantha Wu, Jiaxing Mofakham, Sima Maruyama, Daniel Zochowski, Michal Aton, Sara J. Nat Commun Article Activity in hippocampal area CA1 is essential for consolidating episodic memories, but it is unclear how CA1 activity patterns drive memory formation. We find that in the hours following single-trial contextual fear conditioning (CFC), fast-spiking interneurons (which typically express parvalbumin (PV)) show greater firing coherence with CA1 network oscillations. Post-CFC inhibition of PV+ interneurons blocks fear memory consolidation. This effect is associated with loss of two network changes associated with normal consolidation: (1) augmented sleep-associated delta (0.5–4 Hz), theta (4–12 Hz) and ripple (150–250 Hz) oscillations; and (2) stabilization of CA1 neurons’ functional connectivity patterns. Rhythmic activation of PV+ interneurons increases CA1 network coherence and leads to a sustained increase in the strength and stability of functional connections between neurons. Our results suggest that immediately following learning, PV+ interneurons drive CA1 oscillations and reactivation of CA1 ensembles, which directly promotes network plasticity and long-term memory formation. Nature Publishing Group 2017-04-06 /pmc/articles/PMC5384212/ /pubmed/28382952 http://dx.doi.org/10.1038/ncomms15039 Text en Copyright © 2017, The Author(s) http://creativecommons.org/licenses/by/4.0/ This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/
spellingShingle Article
Ognjanovski, Nicolette
Schaeffer, Samantha
Wu, Jiaxing
Mofakham, Sima
Maruyama, Daniel
Zochowski, Michal
Aton, Sara J.
Parvalbumin-expressing interneurons coordinate hippocampal network dynamics required for memory consolidation
title Parvalbumin-expressing interneurons coordinate hippocampal network dynamics required for memory consolidation
title_full Parvalbumin-expressing interneurons coordinate hippocampal network dynamics required for memory consolidation
title_fullStr Parvalbumin-expressing interneurons coordinate hippocampal network dynamics required for memory consolidation
title_full_unstemmed Parvalbumin-expressing interneurons coordinate hippocampal network dynamics required for memory consolidation
title_short Parvalbumin-expressing interneurons coordinate hippocampal network dynamics required for memory consolidation
title_sort parvalbumin-expressing interneurons coordinate hippocampal network dynamics required for memory consolidation
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5384212/
https://www.ncbi.nlm.nih.gov/pubmed/28382952
http://dx.doi.org/10.1038/ncomms15039
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