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Parallel processing relies on a distributed, low-dimensional cortico-cerebellar architecture

A characteristic feature of human cognition is our ability to ‘multi-task’—performing two or more tasks in parallel—particularly when one task is well learned. How the brain supports this capacity remains poorly understood. Most past studies have focussed on identifying the areas of the brain—typica...

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Autores principales: Müller, Eli J., Palesi, Fulvia, Hou, Kevin Y., Tan, Joshua, Close, Thomas, Gandini Wheeler-Kingschott, Claudia A. M., D’Angelo, Egidio, Calamante, Fernando, Shine, James M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MIT Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10312290/
https://www.ncbi.nlm.nih.gov/pubmed/37397895
http://dx.doi.org/10.1162/netn_a_00308
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author Müller, Eli J.
Palesi, Fulvia
Hou, Kevin Y.
Tan, Joshua
Close, Thomas
Gandini Wheeler-Kingschott, Claudia A. M.
D’Angelo, Egidio
Calamante, Fernando
Shine, James M.
author_facet Müller, Eli J.
Palesi, Fulvia
Hou, Kevin Y.
Tan, Joshua
Close, Thomas
Gandini Wheeler-Kingschott, Claudia A. M.
D’Angelo, Egidio
Calamante, Fernando
Shine, James M.
author_sort Müller, Eli J.
collection PubMed
description A characteristic feature of human cognition is our ability to ‘multi-task’—performing two or more tasks in parallel—particularly when one task is well learned. How the brain supports this capacity remains poorly understood. Most past studies have focussed on identifying the areas of the brain—typically the dorsolateral prefrontal cortex—that are required to navigate information-processing bottlenecks. In contrast, we take a systems neuroscience approach to test the hypothesis that the capacity to conduct effective parallel processing relies on a distributed architecture that interconnects the cerebral cortex with the cerebellum. The latter structure contains over half of the neurons in the adult human brain and is well suited to support the fast, effective, dynamic sequences required to perform tasks relatively automatically. By delegating stereotyped within-task computations to the cerebellum, the cerebral cortex can be freed up to focus on the more challenging aspects of performing the tasks in parallel. To test this hypothesis, we analysed task-based fMRI data from 50 participants who performed a task in which they either balanced an avatar on a screen (balance), performed serial-7 subtractions (calculation) or performed both in parallel (dual task). Using a set of approaches that include dimensionality reduction, structure-function coupling, and time-varying functional connectivity, we provide robust evidence in support of our hypothesis. We conclude that distributed interactions between the cerebral cortex and cerebellum are crucially involved in parallel processing in the human brain.
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spelling pubmed-103122902023-07-01 Parallel processing relies on a distributed, low-dimensional cortico-cerebellar architecture Müller, Eli J. Palesi, Fulvia Hou, Kevin Y. Tan, Joshua Close, Thomas Gandini Wheeler-Kingschott, Claudia A. M. D’Angelo, Egidio Calamante, Fernando Shine, James M. Netw Neurosci Research Article A characteristic feature of human cognition is our ability to ‘multi-task’—performing two or more tasks in parallel—particularly when one task is well learned. How the brain supports this capacity remains poorly understood. Most past studies have focussed on identifying the areas of the brain—typically the dorsolateral prefrontal cortex—that are required to navigate information-processing bottlenecks. In contrast, we take a systems neuroscience approach to test the hypothesis that the capacity to conduct effective parallel processing relies on a distributed architecture that interconnects the cerebral cortex with the cerebellum. The latter structure contains over half of the neurons in the adult human brain and is well suited to support the fast, effective, dynamic sequences required to perform tasks relatively automatically. By delegating stereotyped within-task computations to the cerebellum, the cerebral cortex can be freed up to focus on the more challenging aspects of performing the tasks in parallel. To test this hypothesis, we analysed task-based fMRI data from 50 participants who performed a task in which they either balanced an avatar on a screen (balance), performed serial-7 subtractions (calculation) or performed both in parallel (dual task). Using a set of approaches that include dimensionality reduction, structure-function coupling, and time-varying functional connectivity, we provide robust evidence in support of our hypothesis. We conclude that distributed interactions between the cerebral cortex and cerebellum are crucially involved in parallel processing in the human brain. MIT Press 2023-06-30 /pmc/articles/PMC10312290/ /pubmed/37397895 http://dx.doi.org/10.1162/netn_a_00308 Text en © 2023 Massachusetts Institute of Technology https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. For a full description of the license, please visit https://creativecommons.org/licenses/by/4.0/.
spellingShingle Research Article
Müller, Eli J.
Palesi, Fulvia
Hou, Kevin Y.
Tan, Joshua
Close, Thomas
Gandini Wheeler-Kingschott, Claudia A. M.
D’Angelo, Egidio
Calamante, Fernando
Shine, James M.
Parallel processing relies on a distributed, low-dimensional cortico-cerebellar architecture
title Parallel processing relies on a distributed, low-dimensional cortico-cerebellar architecture
title_full Parallel processing relies on a distributed, low-dimensional cortico-cerebellar architecture
title_fullStr Parallel processing relies on a distributed, low-dimensional cortico-cerebellar architecture
title_full_unstemmed Parallel processing relies on a distributed, low-dimensional cortico-cerebellar architecture
title_short Parallel processing relies on a distributed, low-dimensional cortico-cerebellar architecture
title_sort parallel processing relies on a distributed, low-dimensional cortico-cerebellar architecture
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10312290/
https://www.ncbi.nlm.nih.gov/pubmed/37397895
http://dx.doi.org/10.1162/netn_a_00308
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