Neural substrates of parallel devaluation-sensitive and devaluation-insensitive Pavlovian learning in humans
Abstract
We aim to differentiate the brain regions involved in the learning and encoding of Pavlovian associations sensitive to changes in outcome value from those that are not sensitive to such changes by combining a learning task with outcome devaluation, eye-tracking, and functional magnetic resonance imaging in humans. Contrary to theoretical expectation, voxels correlating with reward prediction errors in the ventral striatum and subgenual cingulate appear to be sensitive to devaluation. Moreover, regions encoding state prediction errors appear to be devaluation insensitive. We can also distinguish regions encoding predictions about outcome taste identity from predictions about expected spatial location. Regions encoding predictions about taste identity seem devaluation sensitive while those encoding predictions about an outcome's spatial location seem devaluation insensitive. These findings suggest the existence of multiple and distinct associative mechanisms in the brain and help identify putative neural correlates for the parallel expression of both devaluation sensitive and insensitive conditioned behaviors.
Copyright and License
© The Author(s) 2023. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
Acknowledgement
We would like to thank Dr. Yoann Stussi and Dr. Vanessa Sennwald for helpful discussions. This work was supported by an Ambizione research grant (project PZPGP1 193120) to ERP and a National Institute on Drug Abuse (R01DA040011) grant to JPOD.
Copyright and License
E.R.P., J.P.O and W.M.P. conceptualized the work and the experimental design. E.R.P. and W.M.P. collected the data. E.R.P. and L.C. performed the analysis. E.R.P. and J.P.O wrote the original draft of the manuscript. All authors contributed to reviewing and editing of the manuscript.
Data Availability
The fMRI data generated in this study has been deposited in the YARETA database89 under accession code: https://doi.org/10.26037/yareta:dyhmmxkwkfbwvaq4yotxziszva. Source data are provided with this paper.
Code Availability
The code used to generate the figures and the results reported in this manuscript is available on the following repository: https://github.com/evapool/PavlovianPredictions/; Zenodo https://doi.org/10.5281/zenodo.10004873.
Conflict of Interest
The authors declare no competing interests.
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Additional details
- Swiss National Science Foundation
- PZPGP1 193120
- National Institutes of Health
- R01DA040011
- Caltech groups
- Tianqiao and Chrissy Chen Institute for Neuroscience