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Task-evoked activity quenches neural correlations and variability across cortical areas

Many large-scale functional connectivity studies have emphasized the importance of communication through increased inter-region correlations during task states. In contrast, local circuit studies have demonstrated that task states primarily reduce correlations among pairs of neurons, likely enhancin...

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Autores principales: Ito, Takuya, Brincat, Scott L., Siegel, Markus, Mill, Ravi D., He, Biyu J., Miller, Earl K., Rotstein, Horacio G., Cole, Michael W.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7425988/
https://www.ncbi.nlm.nih.gov/pubmed/32745096
http://dx.doi.org/10.1371/journal.pcbi.1007983
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author Ito, Takuya
Brincat, Scott L.
Siegel, Markus
Mill, Ravi D.
He, Biyu J.
Miller, Earl K.
Rotstein, Horacio G.
Cole, Michael W.
author_facet Ito, Takuya
Brincat, Scott L.
Siegel, Markus
Mill, Ravi D.
He, Biyu J.
Miller, Earl K.
Rotstein, Horacio G.
Cole, Michael W.
author_sort Ito, Takuya
collection PubMed
description Many large-scale functional connectivity studies have emphasized the importance of communication through increased inter-region correlations during task states. In contrast, local circuit studies have demonstrated that task states primarily reduce correlations among pairs of neurons, likely enhancing their information coding by suppressing shared spontaneous activity. Here we sought to adjudicate between these conflicting perspectives, assessing whether co-active brain regions during task states tend to increase or decrease their correlations. We found that variability and correlations primarily decrease across a variety of cortical regions in two highly distinct data sets: non-human primate spiking data and human functional magnetic resonance imaging data. Moreover, this observed variability and correlation reduction was accompanied by an overall increase in dimensionality (reflecting less information redundancy) during task states, suggesting that decreased correlations increased information coding capacity. We further found in both spiking and neural mass computational models that task-evoked activity increased the stability around a stable attractor, globally quenching neural variability and correlations. Together, our results provide an integrative mechanistic account that encompasses measures of large-scale neural activity, variability, and correlations during resting and task states.
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spelling pubmed-74259882020-08-20 Task-evoked activity quenches neural correlations and variability across cortical areas Ito, Takuya Brincat, Scott L. Siegel, Markus Mill, Ravi D. He, Biyu J. Miller, Earl K. Rotstein, Horacio G. Cole, Michael W. PLoS Comput Biol Research Article Many large-scale functional connectivity studies have emphasized the importance of communication through increased inter-region correlations during task states. In contrast, local circuit studies have demonstrated that task states primarily reduce correlations among pairs of neurons, likely enhancing their information coding by suppressing shared spontaneous activity. Here we sought to adjudicate between these conflicting perspectives, assessing whether co-active brain regions during task states tend to increase or decrease their correlations. We found that variability and correlations primarily decrease across a variety of cortical regions in two highly distinct data sets: non-human primate spiking data and human functional magnetic resonance imaging data. Moreover, this observed variability and correlation reduction was accompanied by an overall increase in dimensionality (reflecting less information redundancy) during task states, suggesting that decreased correlations increased information coding capacity. We further found in both spiking and neural mass computational models that task-evoked activity increased the stability around a stable attractor, globally quenching neural variability and correlations. Together, our results provide an integrative mechanistic account that encompasses measures of large-scale neural activity, variability, and correlations during resting and task states. Public Library of Science 2020-08-03 /pmc/articles/PMC7425988/ /pubmed/32745096 http://dx.doi.org/10.1371/journal.pcbi.1007983 Text en © 2020 Ito et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Ito, Takuya
Brincat, Scott L.
Siegel, Markus
Mill, Ravi D.
He, Biyu J.
Miller, Earl K.
Rotstein, Horacio G.
Cole, Michael W.
Task-evoked activity quenches neural correlations and variability across cortical areas
title Task-evoked activity quenches neural correlations and variability across cortical areas
title_full Task-evoked activity quenches neural correlations and variability across cortical areas
title_fullStr Task-evoked activity quenches neural correlations and variability across cortical areas
title_full_unstemmed Task-evoked activity quenches neural correlations and variability across cortical areas
title_short Task-evoked activity quenches neural correlations and variability across cortical areas
title_sort task-evoked activity quenches neural correlations and variability across cortical areas
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7425988/
https://www.ncbi.nlm.nih.gov/pubmed/32745096
http://dx.doi.org/10.1371/journal.pcbi.1007983
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