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Curr Biol. 2019 Jan 7;29(1):93-103.e3. doi: 10.1016/j.cub.2018.11.050. Epub 2018 Dec 20.

Ventral Tegmental Dopamine Neurons Participate in Reward Identity Predictions.

Author information

1
Department of Psychological and Brain Sciences, Krieger School of Arts and Sciences, Johns Hopkins University, Baltimore, MD 21218, USA. Electronic address: rkeiflin@ucsb.edu.
2
Department of Psychological and Brain Sciences, Krieger School of Arts and Sciences, Johns Hopkins University, Baltimore, MD 21218, USA.
3
Department of Psychological and Brain Sciences, Krieger School of Arts and Sciences, Johns Hopkins University, Baltimore, MD 21218, USA; The Solomon H. Snyder Department of Neuroscience, Johns Hopkins School of Medicine, Johns Hopkins University, Baltimore, MD 21205, USA; Kavli Neuroscience Discovery Institute, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA. Electronic address: patricia.janak@jhu.edu.

Abstract

Dopamine (DA) neurons in the ventral tegmental area (VTA) and substantia nigra (SNc) encode reward prediction errors (RPEs) and are proposed to mediate error-driven learning. However, the learning strategy engaged by DA-RPEs remains controversial. RPEs might imbue predictive cues with pure value, independently of representations of their associated outcome. Alternatively, RPEs might promote learning about the sensory features (the identity) of the rewarding outcome. Here, we show that, although both VTA and SNc DA neuron activation reinforces instrumental responding, only VTA DA neuron activation during consumption of expected sucrose reward restores error-driven learning and promotes formation of a new cue→sucrose association. Critically, expression of VTA DA-dependent Pavlovian associations is abolished following sucrose devaluation, a signature of identity-based learning. These findings reveal that activation of VTA- or SNc-DA neurons engages largely dissociable learning processes with VTA-DA neurons capable of participating in outcome-specific predictive learning, and the role of SNc-DA neurons appears limited to reinforcement of instrumental responses.

KEYWORDS:

blocking; conditioning; dopamine; learning; model-based; model-free; optogenetics; reward-prediction error; substantia nigra; ventral tegmental area

PMID:
30581025
PMCID:
PMC6324975
[Available on 2020-01-07]
DOI:
10.1016/j.cub.2018.11.050

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