Cargando…

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...

Descripción completa

Detalles Bibliográficos
Autores principales: Navarro Lobato, Irene, Aleman-Zapata, Adrian, Samanta, Anumita, Bogers, Milan, Narayanan, Shekhar, Rayan, Abdelrahman, Alonso, Alejandra, van der Meij, Jacqueline, Khamassi, Mehdi, Khan, Zafar U, Genzel, Lisa
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10229123/
https://www.ncbi.nlm.nih.gov/pubmed/37252780
http://dx.doi.org/10.7554/eLife.84911
_version_ 1785051172865835008
author Navarro Lobato, Irene
Aleman-Zapata, Adrian
Samanta, Anumita
Bogers, Milan
Narayanan, Shekhar
Rayan, Abdelrahman
Alonso, Alejandra
van der Meij, Jacqueline
Khamassi, Mehdi
Khan, Zafar U
Genzel, Lisa
author_facet Navarro Lobato, Irene
Aleman-Zapata, Adrian
Samanta, Anumita
Bogers, Milan
Narayanan, Shekhar
Rayan, Abdelrahman
Alonso, Alejandra
van der Meij, Jacqueline
Khamassi, Mehdi
Khan, Zafar U
Genzel, Lisa
author_sort Navarro Lobato, Irene
collection PubMed
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.
format Online
Article
Text
id pubmed-10229123
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher eLife Sciences Publications, Ltd
record_format MEDLINE/PubMed
spelling pubmed-102291232023-05-31 Increased cortical plasticity leads to memory interference and enhanced hippocampal-cortical interactions Navarro Lobato, Irene Aleman-Zapata, Adrian Samanta, Anumita Bogers, Milan Narayanan, Shekhar Rayan, Abdelrahman Alonso, Alejandra van der Meij, Jacqueline Khamassi, Mehdi Khan, Zafar U Genzel, Lisa eLife Neuroscience 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. eLife Sciences Publications, Ltd 2023-05-30 /pmc/articles/PMC10229123/ /pubmed/37252780 http://dx.doi.org/10.7554/eLife.84911 Text en © 2023, Navarro Lobato et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Navarro Lobato, Irene
Aleman-Zapata, Adrian
Samanta, Anumita
Bogers, Milan
Narayanan, Shekhar
Rayan, Abdelrahman
Alonso, Alejandra
van der Meij, Jacqueline
Khamassi, Mehdi
Khan, Zafar U
Genzel, Lisa
Increased cortical plasticity leads to memory interference and enhanced hippocampal-cortical interactions
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 Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10229123/
https://www.ncbi.nlm.nih.gov/pubmed/37252780
http://dx.doi.org/10.7554/eLife.84911
work_keys_str_mv AT navarrolobatoirene increasedcorticalplasticityleadstomemoryinterferenceandenhancedhippocampalcorticalinteractions
AT alemanzapataadrian increasedcorticalplasticityleadstomemoryinterferenceandenhancedhippocampalcorticalinteractions
AT samantaanumita increasedcorticalplasticityleadstomemoryinterferenceandenhancedhippocampalcorticalinteractions
AT bogersmilan increasedcorticalplasticityleadstomemoryinterferenceandenhancedhippocampalcorticalinteractions
AT narayananshekhar increasedcorticalplasticityleadstomemoryinterferenceandenhancedhippocampalcorticalinteractions
AT rayanabdelrahman increasedcorticalplasticityleadstomemoryinterferenceandenhancedhippocampalcorticalinteractions
AT alonsoalejandra increasedcorticalplasticityleadstomemoryinterferenceandenhancedhippocampalcorticalinteractions
AT vandermeijjacqueline increasedcorticalplasticityleadstomemoryinterferenceandenhancedhippocampalcorticalinteractions
AT khamassimehdi increasedcorticalplasticityleadstomemoryinterferenceandenhancedhippocampalcorticalinteractions
AT khanzafaru increasedcorticalplasticityleadstomemoryinterferenceandenhancedhippocampalcorticalinteractions
AT genzellisa increasedcorticalplasticityleadstomemoryinterferenceandenhancedhippocampalcorticalinteractions