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Information-processing dynamics in neural networks of macaque cerebral cortex reflect cognitive state and behavior

One of the essential functions of biological neural networks is the processing of information. This includes everything from processing sensory information to perceive the environment, up to processing motor information to interact with the environment. Due to methodological limitations, it has been...

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Autores principales: Varley, Thomas F., Sporns, Olaf, Schaffelhofer, Stefan, Scherberger, Hansjörg, Dann, Benjamin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9926243/
https://www.ncbi.nlm.nih.gov/pubmed/36603032
http://dx.doi.org/10.1073/pnas.2207677120
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author Varley, Thomas F.
Sporns, Olaf
Schaffelhofer, Stefan
Scherberger, Hansjörg
Dann, Benjamin
author_facet Varley, Thomas F.
Sporns, Olaf
Schaffelhofer, Stefan
Scherberger, Hansjörg
Dann, Benjamin
author_sort Varley, Thomas F.
collection PubMed
description One of the essential functions of biological neural networks is the processing of information. This includes everything from processing sensory information to perceive the environment, up to processing motor information to interact with the environment. Due to methodological limitations, it has been historically unclear how information processing changes during different cognitive or behavioral states and to what extent information is processed within or between the network of neurons in different brain areas. In this study, we leverage recent advances in the calculation of information dynamics to explore neural-level processing within and between the frontoparietal areas AIP, F5, and M1 during a delayed grasping task performed by three macaque monkeys. While information processing was high within all areas during all cognitive and behavioral states of the task, interareal processing varied widely: During visuomotor transformation, AIP and F5 formed a reciprocally connected processing unit, while no processing was present between areas during the memory period. Movement execution was processed globally across all areas with predominance of processing in the feedback direction. Furthermore, the fine-scale network structure reconfigured at the neuron level in response to different grasping conditions, despite no differences in the overall amount of information present. These results suggest that areas dynamically form higher-order processing units according to the cognitive or behavioral demand and that the information-processing network is hierarchically organized at the neuron level, with the coarse network structure determining the behavioral state and finer changes reflecting different conditions.
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spelling pubmed-99262432023-02-15 Information-processing dynamics in neural networks of macaque cerebral cortex reflect cognitive state and behavior Varley, Thomas F. Sporns, Olaf Schaffelhofer, Stefan Scherberger, Hansjörg Dann, Benjamin Proc Natl Acad Sci U S A Biological Sciences One of the essential functions of biological neural networks is the processing of information. This includes everything from processing sensory information to perceive the environment, up to processing motor information to interact with the environment. Due to methodological limitations, it has been historically unclear how information processing changes during different cognitive or behavioral states and to what extent information is processed within or between the network of neurons in different brain areas. In this study, we leverage recent advances in the calculation of information dynamics to explore neural-level processing within and between the frontoparietal areas AIP, F5, and M1 during a delayed grasping task performed by three macaque monkeys. While information processing was high within all areas during all cognitive and behavioral states of the task, interareal processing varied widely: During visuomotor transformation, AIP and F5 formed a reciprocally connected processing unit, while no processing was present between areas during the memory period. Movement execution was processed globally across all areas with predominance of processing in the feedback direction. Furthermore, the fine-scale network structure reconfigured at the neuron level in response to different grasping conditions, despite no differences in the overall amount of information present. These results suggest that areas dynamically form higher-order processing units according to the cognitive or behavioral demand and that the information-processing network is hierarchically organized at the neuron level, with the coarse network structure determining the behavioral state and finer changes reflecting different conditions. National Academy of Sciences 2023-01-05 2023-01-10 /pmc/articles/PMC9926243/ /pubmed/36603032 http://dx.doi.org/10.1073/pnas.2207677120 Text en Copyright © 2023 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Varley, Thomas F.
Sporns, Olaf
Schaffelhofer, Stefan
Scherberger, Hansjörg
Dann, Benjamin
Information-processing dynamics in neural networks of macaque cerebral cortex reflect cognitive state and behavior
title Information-processing dynamics in neural networks of macaque cerebral cortex reflect cognitive state and behavior
title_full Information-processing dynamics in neural networks of macaque cerebral cortex reflect cognitive state and behavior
title_fullStr Information-processing dynamics in neural networks of macaque cerebral cortex reflect cognitive state and behavior
title_full_unstemmed Information-processing dynamics in neural networks of macaque cerebral cortex reflect cognitive state and behavior
title_short Information-processing dynamics in neural networks of macaque cerebral cortex reflect cognitive state and behavior
title_sort information-processing dynamics in neural networks of macaque cerebral cortex reflect cognitive state and behavior
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9926243/
https://www.ncbi.nlm.nih.gov/pubmed/36603032
http://dx.doi.org/10.1073/pnas.2207677120
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