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Prefrontal stimulation prior to motor sequence learning alters multivoxel patterns in the striatum and the hippocampus

Motor sequence learning (MSL) is supported by dynamical interactions between hippocampal and striatal networks that are thought to be orchestrated by the prefrontal cortex. In the present study, we tested whether individually-tailored theta-burst stimulation of the dorsolateral prefrontal cortex (DL...

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Autores principales: Gann, Mareike A., King, Bradley R., Dolfen, Nina, Veldman, Menno P., Davare, Marco, Swinnen, Stephan P., Mantini, Dante, Robertson, Edwin M., Albouy, Geneviève
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8523553/
https://www.ncbi.nlm.nih.gov/pubmed/34663890
http://dx.doi.org/10.1038/s41598-021-99926-1
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author Gann, Mareike A.
King, Bradley R.
Dolfen, Nina
Veldman, Menno P.
Davare, Marco
Swinnen, Stephan P.
Mantini, Dante
Robertson, Edwin M.
Albouy, Geneviève
author_facet Gann, Mareike A.
King, Bradley R.
Dolfen, Nina
Veldman, Menno P.
Davare, Marco
Swinnen, Stephan P.
Mantini, Dante
Robertson, Edwin M.
Albouy, Geneviève
author_sort Gann, Mareike A.
collection PubMed
description Motor sequence learning (MSL) is supported by dynamical interactions between hippocampal and striatal networks that are thought to be orchestrated by the prefrontal cortex. In the present study, we tested whether individually-tailored theta-burst stimulation of the dorsolateral prefrontal cortex (DLPFC) prior to MSL can modulate multivoxel response patterns in the stimulated cortical area, the hippocampus and the striatum. Response patterns were assessed with multivoxel correlation structure analyses of functional magnetic resonance imaging data acquired during task practice and during resting-state scans before and after learning/stimulation. Results revealed that, across stimulation conditions, MSL induced greater modulation of task-related DLPFC multivoxel patterns than random practice. A similar learning-related modulatory effect was observed on sensorimotor putamen patterns under inhibitory stimulation. Furthermore, MSL as well as inhibitory stimulation affected (posterior) hippocampal multivoxel patterns at post-intervention rest. Exploratory analyses showed that MSL-related brain patterns in the posterior hippocampus persisted into post-learning rest preferentially after inhibitory stimulation. These results collectively show that prefrontal stimulation can alter multivoxel brain patterns in deep brain regions that are critical for the MSL process. They also suggest that stimulation influenced early offline consolidation processes as evidenced by a stimulation-induced modulation of the reinstatement of task pattern into post-learning wakeful rest.
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spelling pubmed-85235532021-10-20 Prefrontal stimulation prior to motor sequence learning alters multivoxel patterns in the striatum and the hippocampus Gann, Mareike A. King, Bradley R. Dolfen, Nina Veldman, Menno P. Davare, Marco Swinnen, Stephan P. Mantini, Dante Robertson, Edwin M. Albouy, Geneviève Sci Rep Article Motor sequence learning (MSL) is supported by dynamical interactions between hippocampal and striatal networks that are thought to be orchestrated by the prefrontal cortex. In the present study, we tested whether individually-tailored theta-burst stimulation of the dorsolateral prefrontal cortex (DLPFC) prior to MSL can modulate multivoxel response patterns in the stimulated cortical area, the hippocampus and the striatum. Response patterns were assessed with multivoxel correlation structure analyses of functional magnetic resonance imaging data acquired during task practice and during resting-state scans before and after learning/stimulation. Results revealed that, across stimulation conditions, MSL induced greater modulation of task-related DLPFC multivoxel patterns than random practice. A similar learning-related modulatory effect was observed on sensorimotor putamen patterns under inhibitory stimulation. Furthermore, MSL as well as inhibitory stimulation affected (posterior) hippocampal multivoxel patterns at post-intervention rest. Exploratory analyses showed that MSL-related brain patterns in the posterior hippocampus persisted into post-learning rest preferentially after inhibitory stimulation. These results collectively show that prefrontal stimulation can alter multivoxel brain patterns in deep brain regions that are critical for the MSL process. They also suggest that stimulation influenced early offline consolidation processes as evidenced by a stimulation-induced modulation of the reinstatement of task pattern into post-learning wakeful rest. Nature Publishing Group UK 2021-10-18 /pmc/articles/PMC8523553/ /pubmed/34663890 http://dx.doi.org/10.1038/s41598-021-99926-1 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Gann, Mareike A.
King, Bradley R.
Dolfen, Nina
Veldman, Menno P.
Davare, Marco
Swinnen, Stephan P.
Mantini, Dante
Robertson, Edwin M.
Albouy, Geneviève
Prefrontal stimulation prior to motor sequence learning alters multivoxel patterns in the striatum and the hippocampus
title Prefrontal stimulation prior to motor sequence learning alters multivoxel patterns in the striatum and the hippocampus
title_full Prefrontal stimulation prior to motor sequence learning alters multivoxel patterns in the striatum and the hippocampus
title_fullStr Prefrontal stimulation prior to motor sequence learning alters multivoxel patterns in the striatum and the hippocampus
title_full_unstemmed Prefrontal stimulation prior to motor sequence learning alters multivoxel patterns in the striatum and the hippocampus
title_short Prefrontal stimulation prior to motor sequence learning alters multivoxel patterns in the striatum and the hippocampus
title_sort prefrontal stimulation prior to motor sequence learning alters multivoxel patterns in the striatum and the hippocampus
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8523553/
https://www.ncbi.nlm.nih.gov/pubmed/34663890
http://dx.doi.org/10.1038/s41598-021-99926-1
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