Striatal direct and indirect pathway neurons differentially control the encoding and updating of goal-directed learning

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Abstract

The posterior dorsomedial striatum (pDMS) is necessary for goal-directed action, however the role of the direct (dSPN) and indirect (iSPN) spiny projection neurons in the pDMS in such actions remains unclear. In this series of experiments, we examined the role of pDMS SPNs in goal-directed action in rats and found that, whereas dSPNs were critical for goal-directed learning and for energizing the learned response, iSPNs were involved in updating that learning to support response flexibility. Instrumental training elevated expression of the plasticity marker Zif268 in dSPNs only, and chemogenetic suppression of dSPN activity during training prevented goal-directed learning. Unilateral optogenetic inhibition of dSPNs induced an ipsilateral response bias in goal-directed action performance. In contrast, although initial goal-directed learning was unaffected by iSPN manipulations, optogenetic inhibition of iSPNs, but not dSPNs, impaired the updating of this learning and attenuated response flexibility after changes in the action-outcome contingency.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for all experiments reported in this manuscript in an online repository at https://figshare.com/s/23578523b81df00fa6e4

Article and author information

Author details

James Peak

Psychology, University of New South Wales, Sydney, Australia

Competing interests
The authors declare that no competing interests exist.
Billy Chieng

Psychology, University of New South Wales, Sydney, Australia

Competing interests
The authors declare that no competing interests exist.
Genevra Hart

Psychology, University of New South Wales, Sydney, Australia

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

School of Psychology, University of New South Wales, Sydney, Australia

For correspondence
bernard.balleine@unsw.edu.au

Competing interests
The authors declare that no competing interests exist.

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

Funding

Australian Research Council (DP150104878)

Bernard W Balleine

National Health and Medical Research Council (GNT1165346)

Bernard W Balleine

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: This study was performed in strict accordance All experiments conformed to the guidelines on the ethical use of animals maintained by the Australian code for the care and use of animals for scientific purposes, and all procedures were approved by the Animal Care and Ethics Committee at either the University of New South Wales (Protocl number 19/25A) or the University of Sydney (protocol number 5960/78). All surgery was performed under isofluorane anesthesia, and every effort was made to minimize suffering.

Copyright

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.