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Short-Term Classification Learning Promotes Rapid Global Improvements of Information Processing in Human Brain Functional Connectome

Classification learning is a preeminent human ability within the animal kingdom but the key mechanisms of brain networks regulating learning remain mostly elusive. Recent neuroimaging advancements have depicted human brain as a complex graph machinery where brain regions are nodes and coherent activ...

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Autores principales: Zippo, Antonio G., Castiglioni, Isabella, Lin, Jianyi, Borsa, Virginia M., Valente, Maurizio, Biella, Gabriele E. M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6971211/
https://www.ncbi.nlm.nih.gov/pubmed/32009918
http://dx.doi.org/10.3389/fnhum.2019.00462
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author Zippo, Antonio G.
Castiglioni, Isabella
Lin, Jianyi
Borsa, Virginia M.
Valente, Maurizio
Biella, Gabriele E. M.
author_facet Zippo, Antonio G.
Castiglioni, Isabella
Lin, Jianyi
Borsa, Virginia M.
Valente, Maurizio
Biella, Gabriele E. M.
author_sort Zippo, Antonio G.
collection PubMed
description Classification learning is a preeminent human ability within the animal kingdom but the key mechanisms of brain networks regulating learning remain mostly elusive. Recent neuroimaging advancements have depicted human brain as a complex graph machinery where brain regions are nodes and coherent activities among them represent the functional connections. While long-term motor memories have been found to alter functional connectivity in the resting human brain, a graph topological investigation of the short-time effects of learning are still not widely investigated. For instance, classification learning is known to orchestrate rapid modulation of diverse memory systems like short-term and visual working memories but how the brain functional connectome accommodates such modulations is unclear. We used publicly available repositories (openfmri.org) selecting three experiments, two focused on short-term classification learning along two consecutive runs where learning was promoted by trial-by-trial feedback errors, while a further experiment was used as supplementary control. We analyzed the functional connectivity extracted from BOLD fMRI signals, and estimated the graph information processing in the cerebral networks. The information processing capability, characterized by complex network statistics, significantly improved over runs, together with the subject classification accuracy. Instead, null-learning experiments, where feedbacks came with poor consistency, did not provoke any significant change in the functional connectivity over runs. We propose that learning induces fast modifications in the overall brain network dynamics, definitely ameliorating the short-term potential of the brain to process and integrate information, a dynamic consistently orchestrated by modulations of the functional connections among specific brain regions.
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spelling pubmed-69712112020-02-01 Short-Term Classification Learning Promotes Rapid Global Improvements of Information Processing in Human Brain Functional Connectome Zippo, Antonio G. Castiglioni, Isabella Lin, Jianyi Borsa, Virginia M. Valente, Maurizio Biella, Gabriele E. M. Front Hum Neurosci Neuroscience Classification learning is a preeminent human ability within the animal kingdom but the key mechanisms of brain networks regulating learning remain mostly elusive. Recent neuroimaging advancements have depicted human brain as a complex graph machinery where brain regions are nodes and coherent activities among them represent the functional connections. While long-term motor memories have been found to alter functional connectivity in the resting human brain, a graph topological investigation of the short-time effects of learning are still not widely investigated. For instance, classification learning is known to orchestrate rapid modulation of diverse memory systems like short-term and visual working memories but how the brain functional connectome accommodates such modulations is unclear. We used publicly available repositories (openfmri.org) selecting three experiments, two focused on short-term classification learning along two consecutive runs where learning was promoted by trial-by-trial feedback errors, while a further experiment was used as supplementary control. We analyzed the functional connectivity extracted from BOLD fMRI signals, and estimated the graph information processing in the cerebral networks. The information processing capability, characterized by complex network statistics, significantly improved over runs, together with the subject classification accuracy. Instead, null-learning experiments, where feedbacks came with poor consistency, did not provoke any significant change in the functional connectivity over runs. We propose that learning induces fast modifications in the overall brain network dynamics, definitely ameliorating the short-term potential of the brain to process and integrate information, a dynamic consistently orchestrated by modulations of the functional connections among specific brain regions. Frontiers Media S.A. 2020-01-14 /pmc/articles/PMC6971211/ /pubmed/32009918 http://dx.doi.org/10.3389/fnhum.2019.00462 Text en Copyright © 2020 Zippo, Castiglioni, Lin, Borsa, Valente and Biella. http://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
Zippo, Antonio G.
Castiglioni, Isabella
Lin, Jianyi
Borsa, Virginia M.
Valente, Maurizio
Biella, Gabriele E. M.
Short-Term Classification Learning Promotes Rapid Global Improvements of Information Processing in Human Brain Functional Connectome
title Short-Term Classification Learning Promotes Rapid Global Improvements of Information Processing in Human Brain Functional Connectome
title_full Short-Term Classification Learning Promotes Rapid Global Improvements of Information Processing in Human Brain Functional Connectome
title_fullStr Short-Term Classification Learning Promotes Rapid Global Improvements of Information Processing in Human Brain Functional Connectome
title_full_unstemmed Short-Term Classification Learning Promotes Rapid Global Improvements of Information Processing in Human Brain Functional Connectome
title_short Short-Term Classification Learning Promotes Rapid Global Improvements of Information Processing in Human Brain Functional Connectome
title_sort short-term classification learning promotes rapid global improvements of information processing in human brain functional connectome
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6971211/
https://www.ncbi.nlm.nih.gov/pubmed/32009918
http://dx.doi.org/10.3389/fnhum.2019.00462
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