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A corticostriatal deficit promotes temporal distortion of automatic action in ageing

The acquisition of motor skills involves implementing action sequences that increase task efficiency while reducing cognitive loads. This learning capacity depends on specific cortico-basal ganglia circuits that are affected by normal ageing. Here, combining a series of novel behavioural tasks with...

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Autores principales: Matamales, Miriam, Skrbis, Zala, Bailey, Matthew R, Balsam, Peter D, Balleine, Bernard W, Götz, Jürgen, Bertran-Gonzalez, Jesus
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5677368/
https://www.ncbi.nlm.nih.gov/pubmed/29058672
http://dx.doi.org/10.7554/eLife.29908
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author Matamales, Miriam
Skrbis, Zala
Bailey, Matthew R
Balsam, Peter D
Balleine, Bernard W
Götz, Jürgen
Bertran-Gonzalez, Jesus
author_facet Matamales, Miriam
Skrbis, Zala
Bailey, Matthew R
Balsam, Peter D
Balleine, Bernard W
Götz, Jürgen
Bertran-Gonzalez, Jesus
author_sort Matamales, Miriam
collection PubMed
description The acquisition of motor skills involves implementing action sequences that increase task efficiency while reducing cognitive loads. This learning capacity depends on specific cortico-basal ganglia circuits that are affected by normal ageing. Here, combining a series of novel behavioural tasks with extensive neuronal mapping and targeted cell manipulations in mice, we explored how ageing of cortico-basal ganglia networks alters the microstructure of action throughout sequence learning. We found that, after extended training, aged mice produced shorter actions and displayed squeezed automatic behaviours characterised by ultrafast oligomeric action chunks that correlated with deficient reorganisation of corticostriatal activity. Chemogenetic disruption of a striatal subcircuit in young mice reproduced age-related within-sequence features, and the introduction of an action-related feedback cue temporarily restored normal sequence structure in aged mice. Our results reveal static properties of aged cortico-basal ganglia networks that introduce temporal limits to action automaticity, something that can compromise procedural learning in ageing.
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spelling pubmed-56773682017-11-13 A corticostriatal deficit promotes temporal distortion of automatic action in ageing Matamales, Miriam Skrbis, Zala Bailey, Matthew R Balsam, Peter D Balleine, Bernard W Götz, Jürgen Bertran-Gonzalez, Jesus eLife Neuroscience The acquisition of motor skills involves implementing action sequences that increase task efficiency while reducing cognitive loads. This learning capacity depends on specific cortico-basal ganglia circuits that are affected by normal ageing. Here, combining a series of novel behavioural tasks with extensive neuronal mapping and targeted cell manipulations in mice, we explored how ageing of cortico-basal ganglia networks alters the microstructure of action throughout sequence learning. We found that, after extended training, aged mice produced shorter actions and displayed squeezed automatic behaviours characterised by ultrafast oligomeric action chunks that correlated with deficient reorganisation of corticostriatal activity. Chemogenetic disruption of a striatal subcircuit in young mice reproduced age-related within-sequence features, and the introduction of an action-related feedback cue temporarily restored normal sequence structure in aged mice. Our results reveal static properties of aged cortico-basal ganglia networks that introduce temporal limits to action automaticity, something that can compromise procedural learning in ageing. eLife Sciences Publications, Ltd 2017-10-23 /pmc/articles/PMC5677368/ /pubmed/29058672 http://dx.doi.org/10.7554/eLife.29908 Text en © 2017, Matamales et al http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Matamales, Miriam
Skrbis, Zala
Bailey, Matthew R
Balsam, Peter D
Balleine, Bernard W
Götz, Jürgen
Bertran-Gonzalez, Jesus
A corticostriatal deficit promotes temporal distortion of automatic action in ageing
title A corticostriatal deficit promotes temporal distortion of automatic action in ageing
title_full A corticostriatal deficit promotes temporal distortion of automatic action in ageing
title_fullStr A corticostriatal deficit promotes temporal distortion of automatic action in ageing
title_full_unstemmed A corticostriatal deficit promotes temporal distortion of automatic action in ageing
title_short A corticostriatal deficit promotes temporal distortion of automatic action in ageing
title_sort corticostriatal deficit promotes temporal distortion of automatic action in ageing
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5677368/
https://www.ncbi.nlm.nih.gov/pubmed/29058672
http://dx.doi.org/10.7554/eLife.29908
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