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Dynamic reorganization of the cortico-basal ganglia-thalamo-cortical network during task learning

Adaptive behavior is coordinated by neuronal networks that are distributed across multiple brain regions such as in the cortico-basal ganglia-thalamo-cortical (CBGTC) network. Here, we ask how cross-regional interactions within such mesoscale circuits reorganize when an animal learns a new task. We...

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Detalles Bibliográficos
Autores principales: Sych, Yaroslav, Fomins, Aleksejs, Novelli, Leonardo, Helmchen, Fritjof
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cell Press 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9513804/
https://www.ncbi.nlm.nih.gov/pubmed/36130513
http://dx.doi.org/10.1016/j.celrep.2022.111394
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author Sych, Yaroslav
Fomins, Aleksejs
Novelli, Leonardo
Helmchen, Fritjof
author_facet Sych, Yaroslav
Fomins, Aleksejs
Novelli, Leonardo
Helmchen, Fritjof
author_sort Sych, Yaroslav
collection PubMed
description Adaptive behavior is coordinated by neuronal networks that are distributed across multiple brain regions such as in the cortico-basal ganglia-thalamo-cortical (CBGTC) network. Here, we ask how cross-regional interactions within such mesoscale circuits reorganize when an animal learns a new task. We apply multi-fiber photometry to chronically record simultaneous activity in 12 or 48 brain regions of mice trained in a tactile discrimination task. With improving task performance, most regions shift their peak activity from the time of reward-related action to the reward-predicting stimulus. By estimating cross-regional interactions using transfer entropy, we reveal that functional networks encompassing basal ganglia, thalamus, neocortex, and hippocampus grow and stabilize upon learning, especially at stimulus presentation time. The internal globus pallidus, ventromedial thalamus, and several regions in the frontal cortex emerge as salient hub regions. Our results highlight the learning-related dynamic reorganization that brain networks undergo when task-appropriate mesoscale network dynamics are established for goal-oriented behavior.
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spelling pubmed-95138042022-09-30 Dynamic reorganization of the cortico-basal ganglia-thalamo-cortical network during task learning Sych, Yaroslav Fomins, Aleksejs Novelli, Leonardo Helmchen, Fritjof Cell Rep Article Adaptive behavior is coordinated by neuronal networks that are distributed across multiple brain regions such as in the cortico-basal ganglia-thalamo-cortical (CBGTC) network. Here, we ask how cross-regional interactions within such mesoscale circuits reorganize when an animal learns a new task. We apply multi-fiber photometry to chronically record simultaneous activity in 12 or 48 brain regions of mice trained in a tactile discrimination task. With improving task performance, most regions shift their peak activity from the time of reward-related action to the reward-predicting stimulus. By estimating cross-regional interactions using transfer entropy, we reveal that functional networks encompassing basal ganglia, thalamus, neocortex, and hippocampus grow and stabilize upon learning, especially at stimulus presentation time. The internal globus pallidus, ventromedial thalamus, and several regions in the frontal cortex emerge as salient hub regions. Our results highlight the learning-related dynamic reorganization that brain networks undergo when task-appropriate mesoscale network dynamics are established for goal-oriented behavior. Cell Press 2022-09-20 /pmc/articles/PMC9513804/ /pubmed/36130513 http://dx.doi.org/10.1016/j.celrep.2022.111394 Text en © 2022 The Author(s) https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
spellingShingle Article
Sych, Yaroslav
Fomins, Aleksejs
Novelli, Leonardo
Helmchen, Fritjof
Dynamic reorganization of the cortico-basal ganglia-thalamo-cortical network during task learning
title Dynamic reorganization of the cortico-basal ganglia-thalamo-cortical network during task learning
title_full Dynamic reorganization of the cortico-basal ganglia-thalamo-cortical network during task learning
title_fullStr Dynamic reorganization of the cortico-basal ganglia-thalamo-cortical network during task learning
title_full_unstemmed Dynamic reorganization of the cortico-basal ganglia-thalamo-cortical network during task learning
title_short Dynamic reorganization of the cortico-basal ganglia-thalamo-cortical network during task learning
title_sort dynamic reorganization of the cortico-basal ganglia-thalamo-cortical network during task learning
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9513804/
https://www.ncbi.nlm.nih.gov/pubmed/36130513
http://dx.doi.org/10.1016/j.celrep.2022.111394
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