Increased cortical plasticity leads to memory interference and enhanced hippocampal-cortical interactions

Our brain is continuously challenged by daily experiences. Thus, how to avoid systematic erasing of previously encoded memories? While it has been proposed that a dual-learning system with ‘slow’ learning in the cortex and ‘fast’ learning in the hippocampus could protect previous knowledge from inte...

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Main Authors: Irene Navarro Lobato, Adrian Aleman-Zapata, Anumita Samanta, Milan Bogers, Shekhar Narayanan, Abdelrahman Rayan, Alejandra Alonso, Jacqueline van der Meij, Mehdi Khamassi, Zafar U Khan, Lisa Genzel
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2023-05-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/84911
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author Irene Navarro Lobato
Adrian Aleman-Zapata
Anumita Samanta
Milan Bogers
Shekhar Narayanan
Abdelrahman Rayan
Alejandra Alonso
Jacqueline van der Meij
Mehdi Khamassi
Zafar U Khan
Lisa Genzel
author_facet Irene Navarro Lobato
Adrian Aleman-Zapata
Anumita Samanta
Milan Bogers
Shekhar Narayanan
Abdelrahman Rayan
Alejandra Alonso
Jacqueline van der Meij
Mehdi Khamassi
Zafar U Khan
Lisa Genzel
author_sort Irene Navarro Lobato
collection DOAJ
description Our brain is continuously challenged by daily experiences. Thus, how to avoid systematic erasing of previously encoded memories? While it has been proposed that a dual-learning system with ‘slow’ learning in the cortex and ‘fast’ learning in the hippocampus could protect previous knowledge from interference, this has never been observed in the living organism. Here, we report that increasing plasticity via the viral-induced overexpression of RGS14414 in the prelimbic cortex leads to better one-trial memory, but that this comes at the price of increased interference in semantic-like memory. Indeed, electrophysiological recordings showed that this manipulation also resulted in shorter NonREM-sleep bouts, smaller delta-waves and decreased neuronal firing rates. In contrast, hippocampal-cortical interactions in form of theta coherence during wake and REM-sleep as well as oscillatory coupling during NonREM-sleep were enhanced. Thus, we provide the first experimental evidence for the long-standing and unproven fundamental idea that high thresholds for plasticity in the cortex protect preexisting memories and modulating these thresholds affects both memory encoding and consolidation mechanisms.
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spelling doaj.art-83646e6390b64c1c8286f9c87d2e7ff52023-05-30T15:36:52ZengeLife Sciences Publications LtdeLife2050-084X2023-05-011210.7554/eLife.84911Increased cortical plasticity leads to memory interference and enhanced hippocampal-cortical interactionsIrene Navarro Lobato0Adrian Aleman-Zapata1https://orcid.org/0000-0002-9894-4370Anumita Samanta2Milan Bogers3Shekhar Narayanan4https://orcid.org/0000-0001-7609-2042Abdelrahman Rayan5https://orcid.org/0000-0002-0457-6379Alejandra Alonso6Jacqueline van der Meij7https://orcid.org/0000-0002-1083-8208Mehdi Khamassi8Zafar U Khan9Lisa Genzel10https://orcid.org/0000-0001-9537-7959Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Nijmegen, NetherlandsDonders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Nijmegen, NetherlandsDonders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Nijmegen, NetherlandsDonders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Nijmegen, NetherlandsDonders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Nijmegen, NetherlandsDonders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Nijmegen, NetherlandsDonders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Nijmegen, NetherlandsDonders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Nijmegen, NetherlandsInstitute of Intelligent Systems and Robotics, CNRS, Sorbonne Université, Paris, FranceLaboratory of Neurobiology, CIMES, University of Malaga, Malaga, SpainDonders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Nijmegen, NetherlandsOur brain is continuously challenged by daily experiences. Thus, how to avoid systematic erasing of previously encoded memories? While it has been proposed that a dual-learning system with ‘slow’ learning in the cortex and ‘fast’ learning in the hippocampus could protect previous knowledge from interference, this has never been observed in the living organism. Here, we report that increasing plasticity via the viral-induced overexpression of RGS14414 in the prelimbic cortex leads to better one-trial memory, but that this comes at the price of increased interference in semantic-like memory. Indeed, electrophysiological recordings showed that this manipulation also resulted in shorter NonREM-sleep bouts, smaller delta-waves and decreased neuronal firing rates. In contrast, hippocampal-cortical interactions in form of theta coherence during wake and REM-sleep as well as oscillatory coupling during NonREM-sleep were enhanced. Thus, we provide the first experimental evidence for the long-standing and unproven fundamental idea that high thresholds for plasticity in the cortex protect preexisting memories and modulating these thresholds affects both memory encoding and consolidation mechanisms.https://elifesciences.org/articles/84911sleepplasticitycortexhippocampusripples
spellingShingle Irene Navarro Lobato
Adrian Aleman-Zapata
Anumita Samanta
Milan Bogers
Shekhar Narayanan
Abdelrahman Rayan
Alejandra Alonso
Jacqueline van der Meij
Mehdi Khamassi
Zafar U Khan
Lisa Genzel
Increased cortical plasticity leads to memory interference and enhanced hippocampal-cortical interactions
eLife
sleep
plasticity
cortex
hippocampus
ripples
title Increased cortical plasticity leads to memory interference and enhanced hippocampal-cortical interactions
title_full Increased cortical plasticity leads to memory interference and enhanced hippocampal-cortical interactions
title_fullStr Increased cortical plasticity leads to memory interference and enhanced hippocampal-cortical interactions
title_full_unstemmed Increased cortical plasticity leads to memory interference and enhanced hippocampal-cortical interactions
title_short Increased cortical plasticity leads to memory interference and enhanced hippocampal-cortical interactions
title_sort increased cortical plasticity leads to memory interference and enhanced hippocampal cortical interactions
topic sleep
plasticity
cortex
hippocampus
ripples
url https://elifesciences.org/articles/84911
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