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Extended Visual Sequence Learning Leaves a Local Trace in the Spontaneous EEG

We have previously demonstrated that, in rested subjects, extensive practice in a motor learning task increased both electroencephalographic (EEG) theta power in the areas involved in learning and improved the error rate in a motor test that shared similarities with the task. A nap normalized both E...

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Autores principales: Ricci, Serena, Tatti, Elisa, Nelson, Aaron B., Panday, Priya, Chen, Henry, Tononi, Giulio, Cirelli, Chiara, Ghilardi, M. Felice
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8322764/
https://www.ncbi.nlm.nih.gov/pubmed/34335178
http://dx.doi.org/10.3389/fnins.2021.707828
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author Ricci, Serena
Tatti, Elisa
Nelson, Aaron B.
Panday, Priya
Chen, Henry
Tononi, Giulio
Cirelli, Chiara
Ghilardi, M. Felice
author_facet Ricci, Serena
Tatti, Elisa
Nelson, Aaron B.
Panday, Priya
Chen, Henry
Tononi, Giulio
Cirelli, Chiara
Ghilardi, M. Felice
author_sort Ricci, Serena
collection PubMed
description We have previously demonstrated that, in rested subjects, extensive practice in a motor learning task increased both electroencephalographic (EEG) theta power in the areas involved in learning and improved the error rate in a motor test that shared similarities with the task. A nap normalized both EEG and performance changes. We now ascertain whether extensive visual declarative learning produces results similar to motor learning. Thus, during the morning, we recorded high-density EEG in well rested young healthy subjects that learned the order of different visual sequence task (VSEQ) for three one-hour blocks. Afterward, a group of subjects took a nap and another rested quietly. Between each VSEQ block, we recorded spontaneous EEG (sEEG) at rest and assessed performance in a motor test and a visual working memory test that shares similarities with VSEQ. We found that after the third block, VSEQ induced local theta power increases in the sEEG over a right temporo-parietal area that was engaged during the task. This local theta increase was preceded by increases in alpha and beta power over the same area and was paralleled by performance decline in the visual working memory test. Only after the nap, VSEQ learning rate improved and performance in the visual working memory test was restored, together with partial normalization of the local sEEG changes. These results suggest that intensive learning, like motor learning, produces local theta power increases, possibly reflecting local neuronal fatigue. Sleep may be necessary to resolve neuronal fatigue and its effects on learning and performance.
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spelling pubmed-83227642021-07-31 Extended Visual Sequence Learning Leaves a Local Trace in the Spontaneous EEG Ricci, Serena Tatti, Elisa Nelson, Aaron B. Panday, Priya Chen, Henry Tononi, Giulio Cirelli, Chiara Ghilardi, M. Felice Front Neurosci Neuroscience We have previously demonstrated that, in rested subjects, extensive practice in a motor learning task increased both electroencephalographic (EEG) theta power in the areas involved in learning and improved the error rate in a motor test that shared similarities with the task. A nap normalized both EEG and performance changes. We now ascertain whether extensive visual declarative learning produces results similar to motor learning. Thus, during the morning, we recorded high-density EEG in well rested young healthy subjects that learned the order of different visual sequence task (VSEQ) for three one-hour blocks. Afterward, a group of subjects took a nap and another rested quietly. Between each VSEQ block, we recorded spontaneous EEG (sEEG) at rest and assessed performance in a motor test and a visual working memory test that shares similarities with VSEQ. We found that after the third block, VSEQ induced local theta power increases in the sEEG over a right temporo-parietal area that was engaged during the task. This local theta increase was preceded by increases in alpha and beta power over the same area and was paralleled by performance decline in the visual working memory test. Only after the nap, VSEQ learning rate improved and performance in the visual working memory test was restored, together with partial normalization of the local sEEG changes. These results suggest that intensive learning, like motor learning, produces local theta power increases, possibly reflecting local neuronal fatigue. Sleep may be necessary to resolve neuronal fatigue and its effects on learning and performance. Frontiers Media S.A. 2021-07-16 /pmc/articles/PMC8322764/ /pubmed/34335178 http://dx.doi.org/10.3389/fnins.2021.707828 Text en Copyright © 2021 Ricci, Tatti, Nelson, Panday, Chen, Tononi, Cirelli and Ghilardi. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Ricci, Serena
Tatti, Elisa
Nelson, Aaron B.
Panday, Priya
Chen, Henry
Tononi, Giulio
Cirelli, Chiara
Ghilardi, M. Felice
Extended Visual Sequence Learning Leaves a Local Trace in the Spontaneous EEG
title Extended Visual Sequence Learning Leaves a Local Trace in the Spontaneous EEG
title_full Extended Visual Sequence Learning Leaves a Local Trace in the Spontaneous EEG
title_fullStr Extended Visual Sequence Learning Leaves a Local Trace in the Spontaneous EEG
title_full_unstemmed Extended Visual Sequence Learning Leaves a Local Trace in the Spontaneous EEG
title_short Extended Visual Sequence Learning Leaves a Local Trace in the Spontaneous EEG
title_sort extended visual sequence learning leaves a local trace in the spontaneous eeg
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8322764/
https://www.ncbi.nlm.nih.gov/pubmed/34335178
http://dx.doi.org/10.3389/fnins.2021.707828
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