Cargando…

Control of working memory maintenance by theta-gamma phase amplitude coupling of human hippocampal neurons

Retaining information in working memory (WM) is a demanding process that relies on cognitive control to protect memoranda-specific persistent activity from interference. How cognitive control regulates WM storage, however, remains unknown. We hypothesized that interactions of frontal control and hip...

Descripción completa

Detalles Bibliográficos
Autores principales: Daume, Jonathan, Kaminski, Jan, Schjetnan, Andrea G. P., Salimpour, Yousef, Khan, Umais, Reed, Chrystal, Anderson, William, Valiante, Taufik A., Mamelak, Adam N., Rutishauser, Ueli
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10104113/
https://www.ncbi.nlm.nih.gov/pubmed/37066145
http://dx.doi.org/10.1101/2023.04.05.535772
_version_ 1785025973436022784
author Daume, Jonathan
Kaminski, Jan
Schjetnan, Andrea G. P.
Salimpour, Yousef
Khan, Umais
Reed, Chrystal
Anderson, William
Valiante, Taufik A.
Mamelak, Adam N.
Rutishauser, Ueli
author_facet Daume, Jonathan
Kaminski, Jan
Schjetnan, Andrea G. P.
Salimpour, Yousef
Khan, Umais
Reed, Chrystal
Anderson, William
Valiante, Taufik A.
Mamelak, Adam N.
Rutishauser, Ueli
author_sort Daume, Jonathan
collection PubMed
description Retaining information in working memory (WM) is a demanding process that relies on cognitive control to protect memoranda-specific persistent activity from interference. How cognitive control regulates WM storage, however, remains unknown. We hypothesized that interactions of frontal control and hippocampal persistent activity are coordinated by theta-gamma phase amplitude coupling (TG-PAC). We recorded single neurons in the human medial temporal and frontal lobe while patients maintained multiple items in WM. In the hippocampus, TG-PAC was indicative of WM load and quality. We identified cells that selectively spiked during nonlinear interactions of theta phase and gamma amplitude. These PAC neurons were more strongly coordinated with frontal theta activity when cognitive control demand was high, and they introduced information-enhancing and behaviorally relevant noise correlations with persistently active neurons in the hippocampus. We show that TG-PAC integrates cognitive control and WM storage to improve the fidelity of WM representations and facilitate behavior.
format Online
Article
Text
id pubmed-10104113
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Cold Spring Harbor Laboratory
record_format MEDLINE/PubMed
spelling pubmed-101041132023-04-15 Control of working memory maintenance by theta-gamma phase amplitude coupling of human hippocampal neurons Daume, Jonathan Kaminski, Jan Schjetnan, Andrea G. P. Salimpour, Yousef Khan, Umais Reed, Chrystal Anderson, William Valiante, Taufik A. Mamelak, Adam N. Rutishauser, Ueli bioRxiv Article Retaining information in working memory (WM) is a demanding process that relies on cognitive control to protect memoranda-specific persistent activity from interference. How cognitive control regulates WM storage, however, remains unknown. We hypothesized that interactions of frontal control and hippocampal persistent activity are coordinated by theta-gamma phase amplitude coupling (TG-PAC). We recorded single neurons in the human medial temporal and frontal lobe while patients maintained multiple items in WM. In the hippocampus, TG-PAC was indicative of WM load and quality. We identified cells that selectively spiked during nonlinear interactions of theta phase and gamma amplitude. These PAC neurons were more strongly coordinated with frontal theta activity when cognitive control demand was high, and they introduced information-enhancing and behaviorally relevant noise correlations with persistently active neurons in the hippocampus. We show that TG-PAC integrates cognitive control and WM storage to improve the fidelity of WM representations and facilitate behavior. Cold Spring Harbor Laboratory 2023-04-07 /pmc/articles/PMC10104113/ /pubmed/37066145 http://dx.doi.org/10.1101/2023.04.05.535772 Text en https://creativecommons.org/licenses/by-nc/4.0/This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License (https://creativecommons.org/licenses/by-nc/4.0/) , which allows reusers to distribute, remix, adapt, and build upon the material in any medium or format for noncommercial purposes only, and only so long as attribution is given to the creator.
spellingShingle Article
Daume, Jonathan
Kaminski, Jan
Schjetnan, Andrea G. P.
Salimpour, Yousef
Khan, Umais
Reed, Chrystal
Anderson, William
Valiante, Taufik A.
Mamelak, Adam N.
Rutishauser, Ueli
Control of working memory maintenance by theta-gamma phase amplitude coupling of human hippocampal neurons
title Control of working memory maintenance by theta-gamma phase amplitude coupling of human hippocampal neurons
title_full Control of working memory maintenance by theta-gamma phase amplitude coupling of human hippocampal neurons
title_fullStr Control of working memory maintenance by theta-gamma phase amplitude coupling of human hippocampal neurons
title_full_unstemmed Control of working memory maintenance by theta-gamma phase amplitude coupling of human hippocampal neurons
title_short Control of working memory maintenance by theta-gamma phase amplitude coupling of human hippocampal neurons
title_sort control of working memory maintenance by theta-gamma phase amplitude coupling of human hippocampal neurons
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10104113/
https://www.ncbi.nlm.nih.gov/pubmed/37066145
http://dx.doi.org/10.1101/2023.04.05.535772
work_keys_str_mv AT daumejonathan controlofworkingmemorymaintenancebythetagammaphaseamplitudecouplingofhumanhippocampalneurons
AT kaminskijan controlofworkingmemorymaintenancebythetagammaphaseamplitudecouplingofhumanhippocampalneurons
AT schjetnanandreagp controlofworkingmemorymaintenancebythetagammaphaseamplitudecouplingofhumanhippocampalneurons
AT salimpouryousef controlofworkingmemorymaintenancebythetagammaphaseamplitudecouplingofhumanhippocampalneurons
AT khanumais controlofworkingmemorymaintenancebythetagammaphaseamplitudecouplingofhumanhippocampalneurons
AT reedchrystal controlofworkingmemorymaintenancebythetagammaphaseamplitudecouplingofhumanhippocampalneurons
AT andersonwilliam controlofworkingmemorymaintenancebythetagammaphaseamplitudecouplingofhumanhippocampalneurons
AT valiantetaufika controlofworkingmemorymaintenancebythetagammaphaseamplitudecouplingofhumanhippocampalneurons
AT mamelakadamn controlofworkingmemorymaintenancebythetagammaphaseamplitudecouplingofhumanhippocampalneurons
AT rutishauserueli controlofworkingmemorymaintenancebythetagammaphaseamplitudecouplingofhumanhippocampalneurons