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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...
Autores principales: | , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Nature Publishing Group UK
2019
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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. |
format | Online Article Text |
id | pubmed-6687745 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2019 |
publisher | Nature Publishing Group UK |
record_format | MEDLINE/PubMed |
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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