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Bidirectional prefrontal-hippocampal dynamics organize information transfer during sleep in humans

How are memories transferred from short-term to long-term storage? Systems-level memory consolidation is thought to be dependent on the coordinated interplay of cortical slow waves, thalamo-cortical sleep spindles and hippocampal ripple oscillations. However, it is currently unclear how the selectiv...

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Autores principales: Helfrich, Randolph F., Lendner, Janna D., Mander, Bryce A., Guillen, Heriberto, Paff, Michelle, Mnatsakanyan, Lilit, Vadera, Sumeet, Walker, Matthew P., Lin, Jack J., Knight, Robert T.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6687745/
https://www.ncbi.nlm.nih.gov/pubmed/31395890
http://dx.doi.org/10.1038/s41467-019-11444-x
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author Helfrich, Randolph F.
Lendner, Janna D.
Mander, Bryce A.
Guillen, Heriberto
Paff, Michelle
Mnatsakanyan, Lilit
Vadera, Sumeet
Walker, Matthew P.
Lin, Jack J.
Knight, Robert T.
author_facet Helfrich, Randolph F.
Lendner, Janna D.
Mander, Bryce A.
Guillen, Heriberto
Paff, Michelle
Mnatsakanyan, Lilit
Vadera, Sumeet
Walker, Matthew P.
Lin, Jack J.
Knight, Robert T.
author_sort Helfrich, Randolph F.
collection PubMed
description How are memories transferred from short-term to long-term storage? Systems-level memory consolidation is thought to be dependent on the coordinated interplay of cortical slow waves, thalamo-cortical sleep spindles and hippocampal ripple oscillations. However, it is currently unclear how the selective interaction of these cardinal sleep oscillations is organized to support information reactivation and transfer. Here, using human intracranial recordings, we demonstrate that the prefrontal cortex plays a key role in organizing the ripple-mediated information transfer during non-rapid eye movement (NREM) sleep. We reveal a temporally precise form of coupling between prefrontal slow-wave and spindle oscillations, which actively dictates the hippocampal-neocortical dialogue and information transfer. Our results suggest a model of the human sleeping brain in which rapid bidirectional interactions, triggered by the prefrontal cortex, mediate hippocampal activation to optimally time subsequent information transfer to the neocortex during NREM sleep.
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spelling pubmed-66877452019-08-12 Bidirectional prefrontal-hippocampal dynamics organize information transfer during sleep in humans Helfrich, Randolph F. Lendner, Janna D. Mander, Bryce A. Guillen, Heriberto Paff, Michelle Mnatsakanyan, Lilit Vadera, Sumeet Walker, Matthew P. Lin, Jack J. Knight, Robert T. Nat Commun Article How are memories transferred from short-term to long-term storage? Systems-level memory consolidation is thought to be dependent on the coordinated interplay of cortical slow waves, thalamo-cortical sleep spindles and hippocampal ripple oscillations. However, it is currently unclear how the selective interaction of these cardinal sleep oscillations is organized to support information reactivation and transfer. Here, using human intracranial recordings, we demonstrate that the prefrontal cortex plays a key role in organizing the ripple-mediated information transfer during non-rapid eye movement (NREM) sleep. We reveal a temporally precise form of coupling between prefrontal slow-wave and spindle oscillations, which actively dictates the hippocampal-neocortical dialogue and information transfer. Our results suggest a model of the human sleeping brain in which rapid bidirectional interactions, triggered by the prefrontal cortex, mediate hippocampal activation to optimally time subsequent information transfer to the neocortex during NREM sleep. Nature Publishing Group UK 2019-08-08 /pmc/articles/PMC6687745/ /pubmed/31395890 http://dx.doi.org/10.1038/s41467-019-11444-x Text en © The Author(s) 2019 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Helfrich, Randolph F.
Lendner, Janna D.
Mander, Bryce A.
Guillen, Heriberto
Paff, Michelle
Mnatsakanyan, Lilit
Vadera, Sumeet
Walker, Matthew P.
Lin, Jack J.
Knight, Robert T.
Bidirectional prefrontal-hippocampal dynamics organize information transfer during sleep in humans
title Bidirectional prefrontal-hippocampal dynamics organize information transfer during sleep in humans
title_full Bidirectional prefrontal-hippocampal dynamics organize information transfer during sleep in humans
title_fullStr Bidirectional prefrontal-hippocampal dynamics organize information transfer during sleep in humans
title_full_unstemmed Bidirectional prefrontal-hippocampal dynamics organize information transfer during sleep in humans
title_short Bidirectional prefrontal-hippocampal dynamics organize information transfer during sleep in humans
title_sort bidirectional prefrontal-hippocampal dynamics organize information transfer during sleep in humans
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6687745/
https://www.ncbi.nlm.nih.gov/pubmed/31395890
http://dx.doi.org/10.1038/s41467-019-11444-x
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