Dopamine release in the nucleus accumbens core signals perceived saliency

A large body of work has aimed to define the precise information encoded by dopaminergic projections innervating the nucleus accumbens (NAc). Prevailing models are based on reward prediction error (RPE) theory, in which dopamine updates associations between rewards and predictive cues by encoding pe...

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Veröffentlicht in:Current biology 2021-11, Vol.31 (21), p.4748-4761.e8
Hauptverfasser: Kutlu, Munir Gunes, Zachry, Jennifer E., Melugin, Patrick R., Cajigas, Stephanie A., Chevee, Maxime F., Kelly, Shannon J., Kutlu, Banu, Tian, Lin, Siciliano, Cody A., Calipari, Erin S.
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Sprache:eng
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Zusammenfassung:A large body of work has aimed to define the precise information encoded by dopaminergic projections innervating the nucleus accumbens (NAc). Prevailing models are based on reward prediction error (RPE) theory, in which dopamine updates associations between rewards and predictive cues by encoding perceived errors between predictions and outcomes. However, RPE cannot describe multiple phenomena to which dopamine is inextricably linked, such as behavior driven by aversive and neutral stimuli. We combined a series of behavioral tasks with direct, subsecond dopamine monitoring in the NAc of mice, machine learning, computational modeling, and optogenetic manipulations to describe behavior and related dopamine release patterns across multiple contingencies reinforced by differentially valenced outcomes. We show that dopamine release only conforms to RPE predictions in a subset of learning scenarios but fits valence-independent perceived saliency encoding across conditions. Here, we provide an extended, comprehensive framework for accumbal dopamine release in behavioral control. •NAc core dopamine only mimics reward prediction error in select reward contexts•RPE does not model dopamine release during negative reinforcement•Dopamine signaling in the NAc core does not support valence-free prediction error•NAc core dopamine tracks valence-free perceived saliency in all conditions Kutlu et al. examine dopaminergic information encoding in the nucleus accumbens. This work revises the long-held theory of dopamine as a reward prediction molecule and provides a novel framework for dopamine as a perceived saliency signal. These results unite multiple theories of dopamine signaling and have broad implications for psychopathologies.
ISSN:0960-9822
1879-0445
1879-0445
DOI:10.1016/j.cub.2021.08.052