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 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.
Article and author information
Australian Research Council (DE160101275)
- Jesus Bertran-Gonzalez
Australian Research Council (DP130101932)
- Jürgen Götz
National Health and Medical Research Council (APP1037746)
- Jürgen Götz
National Health and Medical Research Council (APP1003150)
- Jürgen Götz
National Health and Medical Research Council (GNT1079561)
- Bernard W Balleine
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Animal experimentation: All procedures were approved by the University of Queensland Animal Ethics Committee (QBI/412/14/NHMRC and QBI/027/12/NHMRC) in accordance with the Animal Care and Protection Regulation (Queensland Government, 2012) and the Australian Code of Practice for the Care and Use of Animals for Scientific Purposes (National Health and Medical Research Council, 2013). All surgery was performed under isoflurane gas anesthesia and butorphanol analgesia, and every effort was made to minimize suffering.
- Geoffrey Schoenbaum, NIDA Intramural Research Program, United States
- Received: June 25, 2017
- Accepted: October 22, 2017
- Accepted Manuscript published: October 23, 2017 (version 1)
- Version of Record published: November 8, 2017 (version 2)
© 2017, Matamales et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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