Mesostriatal dopamine is sensitive to changes in specific cue-reward contingencies

Author:

Garr Eric1ORCID,Cheng Yifeng1ORCID,Jeong Huijeong2ORCID,Brooke Sara3ORCID,Castell Laia1ORCID,Bal Aneesh1ORCID,Magnard Robin1ORCID,Namboodiri Vijay Mohan K.24ORCID,Janak Patricia H.135ORCID

Affiliation:

1. Department of Psychological & Brain Sciences, Krieger School of Arts & Sciences, Johns Hopkins University, Baltimore, MD 21218, USA.

2. Department of Neurology, University of California, San Francisco, CA 94158, USA.

3. Solomon H. Snyder Department of Neuroscience, Johns Hopkins School of Medicine, Baltimore, MD 21205, USA.

4. Weill Institute for Neurosciences, Kavli Institute for Fundamental Neuroscience, Center for Integrative Neuroscience, University of California, San Francisco, CA 94158, USA.

5. Kavli Neuroscience Discovery Institute, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.

Abstract

Learning causal relationships relies on understanding how often one event precedes another. To investigate how dopamine neuron activity and neurotransmitter release change when a retrospective relationship is degraded for a specific pair of events, we used outcome-selective Pavlovian contingency degradation in rats. Conditioned responding was attenuated for the cue-reward contingency that was degraded, as was dopamine neuron activity in the midbrain and dopamine release in the ventral striatum in response to the cue and subsequent reward. Contingency degradation also abolished the trial-by-trial history dependence of the dopamine responses at the time of trial outcome. This profile of changes in cue- and reward-evoked responding is not easily explained by a standard reinforcement learning model. An alternative model based on learning causal relationships was better able to capture dopamine responses during contingency degradation, as well as conditioned behavior following optogenetic manipulations of dopamine during noncontingent rewards. Our results suggest that mesostriatal dopamine encodes the contingencies between meaningful events during learning.

Publisher

American Association for the Advancement of Science (AAAS)

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