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Moment-by-moment tracking of naturalistic learning and its underlying hippocampo-cortical interactions

Humans form lasting memories of stimuli that were only encountered once. This naturally occurs when listening to a story, however it remains unclear how and when memories are stored and retrieved during story-listening. Here, we first confirm in behavioral experiments that participants can learn abo...

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Autores principales: Michelmann, Sebastian, Price, Amy R., Aubrey, Bobbi, Strauss, Camilla K., Doyle, Werner K., Friedman, Daniel, Dugan, Patricia C., Devinsky, Orrin, Devore, Sasha, Flinker, Adeen, Hasson, Uri, Norman, Kenneth A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8438040/
https://www.ncbi.nlm.nih.gov/pubmed/34518520
http://dx.doi.org/10.1038/s41467-021-25376-y
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author Michelmann, Sebastian
Price, Amy R.
Aubrey, Bobbi
Strauss, Camilla K.
Doyle, Werner K.
Friedman, Daniel
Dugan, Patricia C.
Devinsky, Orrin
Devore, Sasha
Flinker, Adeen
Hasson, Uri
Norman, Kenneth A.
author_facet Michelmann, Sebastian
Price, Amy R.
Aubrey, Bobbi
Strauss, Camilla K.
Doyle, Werner K.
Friedman, Daniel
Dugan, Patricia C.
Devinsky, Orrin
Devore, Sasha
Flinker, Adeen
Hasson, Uri
Norman, Kenneth A.
author_sort Michelmann, Sebastian
collection PubMed
description Humans form lasting memories of stimuli that were only encountered once. This naturally occurs when listening to a story, however it remains unclear how and when memories are stored and retrieved during story-listening. Here, we first confirm in behavioral experiments that participants can learn about the structure of a story after a single exposure and are able to recall upcoming words when the story is presented again. We then track mnemonic information in high frequency activity (70–200 Hz) as patients undergoing electrocorticographic recordings listen twice to the same story. We demonstrate predictive recall of upcoming information through neural responses in auditory processing regions. This neural measure correlates with behavioral measures of event segmentation and learning. Event boundaries are linked to information flow from cortex to hippocampus. When listening for a second time, information flow from hippocampus to cortex precedes moments of predictive recall. These results provide insight on a fine-grained temporal scale into how episodic memory encoding and retrieval work under naturalistic conditions.
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spelling pubmed-84380402021-10-04 Moment-by-moment tracking of naturalistic learning and its underlying hippocampo-cortical interactions Michelmann, Sebastian Price, Amy R. Aubrey, Bobbi Strauss, Camilla K. Doyle, Werner K. Friedman, Daniel Dugan, Patricia C. Devinsky, Orrin Devore, Sasha Flinker, Adeen Hasson, Uri Norman, Kenneth A. Nat Commun Article Humans form lasting memories of stimuli that were only encountered once. This naturally occurs when listening to a story, however it remains unclear how and when memories are stored and retrieved during story-listening. Here, we first confirm in behavioral experiments that participants can learn about the structure of a story after a single exposure and are able to recall upcoming words when the story is presented again. We then track mnemonic information in high frequency activity (70–200 Hz) as patients undergoing electrocorticographic recordings listen twice to the same story. We demonstrate predictive recall of upcoming information through neural responses in auditory processing regions. This neural measure correlates with behavioral measures of event segmentation and learning. Event boundaries are linked to information flow from cortex to hippocampus. When listening for a second time, information flow from hippocampus to cortex precedes moments of predictive recall. These results provide insight on a fine-grained temporal scale into how episodic memory encoding and retrieval work under naturalistic conditions. Nature Publishing Group UK 2021-09-13 /pmc/articles/PMC8438040/ /pubmed/34518520 http://dx.doi.org/10.1038/s41467-021-25376-y Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/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/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Michelmann, Sebastian
Price, Amy R.
Aubrey, Bobbi
Strauss, Camilla K.
Doyle, Werner K.
Friedman, Daniel
Dugan, Patricia C.
Devinsky, Orrin
Devore, Sasha
Flinker, Adeen
Hasson, Uri
Norman, Kenneth A.
Moment-by-moment tracking of naturalistic learning and its underlying hippocampo-cortical interactions
title Moment-by-moment tracking of naturalistic learning and its underlying hippocampo-cortical interactions
title_full Moment-by-moment tracking of naturalistic learning and its underlying hippocampo-cortical interactions
title_fullStr Moment-by-moment tracking of naturalistic learning and its underlying hippocampo-cortical interactions
title_full_unstemmed Moment-by-moment tracking of naturalistic learning and its underlying hippocampo-cortical interactions
title_short Moment-by-moment tracking of naturalistic learning and its underlying hippocampo-cortical interactions
title_sort moment-by-moment tracking of naturalistic learning and its underlying hippocampo-cortical interactions
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8438040/
https://www.ncbi.nlm.nih.gov/pubmed/34518520
http://dx.doi.org/10.1038/s41467-021-25376-y
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