A corticostriatal deficit promotes temporal distortion of automatic action in ageing

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Abstract

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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Miriam Matamales

Clem Jones Centre for Ageing Dementia Research, Queensland Brain Institute, University of Queensland, Brisbane, Australia

Competing interests
The authors declare that no competing interests exist.
Zala Skrbis

Clem Jones Centre for Ageing Dementia Research, Queensland Brain Institute, University of Queensland, Brisbane, Australia

Competing interests
The authors declare that no competing interests exist.
Matthew R Bailey

Psychology Department, Columbia University, New York, United States

Competing interests
The authors declare that no competing interests exist.
Peter D Balsam

Psychology Department, Barnard College, Columbia University, New York, United States

Competing interests
The authors declare that no competing interests exist.
Bernard W Balleine

Decision Neuroscience Laboratory, School of Psychology, University of New South Wales, Sydney, Australia

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-8618-7950
Jürgen Götz

Clem Jones Centre for Ageing Dementia Research, Queensland Brain Institute, University of Queensland, Brisbane, Australia

Competing interests
The authors declare that no competing interests exist.
Jesus Bertran-Gonzalez

Clem Jones Centre for Ageing Dementia Research, Queensland Brain Institute, University of Queensland, Brisbane, Australia

For correspondence
j.bertran@unsw.edu.au

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-3794-1782

Funding

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.

Ethics

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.

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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.